Toma o F ui De elopmen
and Me abolism
Mu iel Quine
1
*
, T inidad Angos o
2
, Fe nando J. Yus e-Lisbona
2
, Rémi Blancha d-G os
1
,
Se ane Bigo
1
, Juan-Pablo Ma inez
3
and S anley Lu s
1
1
G oupe de Reche che en Physiologie Végé ale, Ea h and Li e Ins i u e, Uni e si é Ca holique de Lou ain, Lou ain-la-Neu e,
Belgium,
2
Cen o de In es igación en Bio ecnología Ag oalimen a ia (BITAL), Uni e sidad de Alme ía, Alme ía, Spain,
3
Ins i u o de In es igaciones Ag opecua ias (INIA-La C uz), La C uz, Chile
Toma o (Solanum lycope sicum L.) belongs o he Solanaceae amily and is he second
mos impo an ui o ege able c op nex o po a o (Solanum ube osum L.). I is
cul i a ed o esh ui and p ocessed p oduc s. Toma oes con ain many heal h-
p omo ing compounds including i amins, ca o enoids, and phenolic compounds. In
addi ion o i s economic and nu i ional impo ance, oma oes ha e become he model o
he s udy o fleshy ui de elopmen . Toma o is a climac e ic ui and d ama ic me abolic
changes occu du ing i s ui de elopmen . In his e iew, we p o ide an o e iew o ou
cu en unde s anding o oma o ui me abolism. We begin by de ailing he gene ic and
ho monal con ol o ui de elopmen and ipening, a e which we documen he p ima y
me abolism o oma o ui s, wi h a special ocus on suga , o ganic acid, and amino acid
me abolism. Links be ween p ima y and seconda y me abolic pa hways a e u he
highligh ed by he impo ance o pigmen s, fla onoids, and ola iles o oma o ui
quali y. Finally, as oma o plan s a e sensi i e o se e al abio ic s esses, we b iefly
summa ize he e ec s o ad e se en i onmen al condi ions on oma o ui me abolism
and quali y.
Keywo ds: abio ic s ess, ui se , ui ipening, gene ic con ol, ho monal con ol, p ima y me abolism, seconda y
me abolism, Solanum lycope sicum
INTRODUCTION
Toma o (Solanum lycope sicum L.) is he second mos impo an ui o ege able c op nex o
po a o (Solanum ube osum L.), wi h app oxima ely 182.3 million ons o oma o ui s p oduced on
4.85 million ha each yea (FAOSTAT, 2019). Asia accoun s o 61.1% o global oma o p oduc ion,
while Eu ope, Ame ica, and A ica p oduced 13.5%, 13.4%, and 11.8% o he o al oma o yield,
espec i ely. Toma o yields a e highly a iable, anging om mo e han 508 ons pe ha in he
Ne he lands o ewe han 1.5 ons pe ha in Somalia in 2017 (FAOSTAT, 2019), wi h an a e age
global yield o 376 ons pe ha. Toma o consump ion is concen a ed in China, India, No h A ica,
he Middle Eas , he US, and B azil wi h oma o consump ion pe capi a, anging om 61.9 o 198.9
kg pe capi a (FAOSTAT, 2019). Toma o is a membe o he Solanaceae amily, which includes
se e al o he economically impo an c ops such as po a o, peppe (Capsicum annuum L.), and
eggplan (Solanum melongena L.), ep esen ing one o he mos aluable plan amilies o ege able
and ui c ops.
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15541
Edi ed by:
Robe Pe e Walke ,
Uni e si y o Pe ugia, I aly
Re iewed by:
Paolo Pesa esi,
Uni e si y o Milan, I aly
Giuseppe Colla,
Uni e si à degli S udi della Tuscia, I aly
*Co espondence:
Mu iel Quine
[email p o ec ed]
Special y sec ion:
This a icle was submi ed o
Plan Me abolism and Chemodi e si y,
a sec ion o he jou nal
F on ie s in Plan Science
Recei ed: 31 May 2019
Accep ed: 07 No embe 2019
Published: 29 No embe 2019
Ci a ion:
Quine M, Angos o T,
Yus e-Lisbona FJ, Blancha d-G os R,
Bigo S, Ma inez J-P and Lu S
(2019) Toma o F ui De elopmen
and Me abolism.
F on . Plan Sci. 10:1554.
doi: 10.3389/ pls.2019.01554
REVIEW
published: 29 No embe 2019
doi: 10.3389/ pls.2019.01554
Toma oes con ain many heal h-p omo ing compounds and
a e easily in eg a ed as a nu i ious pa o a balanced die (Ma í
e al., 2016). In addi ion o consuming he esh ui s, consume s
use oma oes in p ocessed p oduc s such as soups, juices, and
sauces (K auss e al., 2006;Li e al., 2018b). O e he las decade,
consume s ha e become mo e awa e o oods as a sou ce o
heal h benefi s and hei oles in p e en ion o se e al ch onic
diseases and dys unc ions (Pem and Jeewon, 2015). Al hough a
weal h o unc ional oods u s ha e been c ea ed o ulfil hese
equi emen s, i is impo an o no e ha he consump ion o
“con en ional oods”such as ui s and ege ables is mo e
e ec i e o his pu pose (Viuda-Ma os e al., 2014).
The nu i ional impo ance o oma oes is la gely explained by
hei a ious heal h-p omo ing compounds, including i amins,
ca o enoids, and phenolic compounds (Raiola e al., 2014;Liu e al.,
2016;Ma í e al., 2016;Li e al., 2018b). These bioac i e compounds
ha e a wide ange o physiological p ope ies, including an i-
inflamma o y, an i-alle genic, an imic obial, asodila o y,
an i h ombo ic, ca dio-p o ec i e, and an ioxidan e ec s (Raiola
e al., 2014). Toma oes a e ich in ca o enoids, ep esen ing he
main sou ce o lycopene in he human die (Viuda-Ma os e al.,
2014). Ca o enoids and polyphenolic compounds con ibu e o he
nu i ional alue o oma oes and imp o e hei unc ional a ibu es
and senso y quali ies, including as e, a oma, and ex u e (Raiola
e al., 2014;Tohge and Fe nie, 2015;Ma í e al., 2016). Toma oesalso
ha e hena u allyoccu ingan ioxidan s Vi amins CandE (Aga wal
and Rao, 2000;Ma í e al., 2016)aswellasla geamoun so
me aboli es, such as suc ose, hexoses, ci a e, mala e, and asco bic
acid (Li e al., 2018b).
Toma o ui quali y and me aboli e biosyn hesis a e a ec ed
by plan g owing condi ions (Diou e al., 2018). Toma o
p oduc ion is challenged by se e al p oblems a ound he wo ld,
including he sca ci y o wa e esou ces, soil saliniza ion, and
o he abio ic s esses (Fahad e al., 2017;Gha bi e al., 2017;Zhou
e al., 2019). In pa icula , in coun ies wi h a Medi e anean
clima e, including some egions in sou he n Eu ope and No h
and Sou h Ame ica, oma o cul i a ion is inc easingly con on ed
wi h limi ing condi ions such as d ough and salini y, which
ul ima ely educe he compe i i eness o oma o a me s in hese
a eas. This, in u n, impac s he in eg i y o he ecosys em,
con ibu ing o he eloca ion (abandonmen ) o u al sec o s.
In addi ion o i s economic and nu i ional impo ance,
oma oes ha e become he model o he s udy o fleshy ui
de elopmen (Ka lo ae al.,2014;Kim e al.,2018;Lie al.,2018b).
The en i e oma o genome has been sequenced, se ing as a ich
genomic esou ce, and bo h gene ic and physical maps and
molecula ma ke s a e a ailable o his species (The Toma o
Genome Conso ium, 2012;Su esh e al., 2014;Zhao e al., 2019).
Mo eo e , a ange o well-cha ac e ized monogenic mu an s,
TILLING popula ions, wild oma o species, ecombinan inb ed
lines and genome edi ing ools a e a ailable (Eshed and Zami ,
1994;Minoia e al., 2010;Pé ez-Ma ín e al., 2017;Li e al., 2018b;
Ma ín-Piza o and Posé, 2018;Toma o Gene ics Resou ce
Cen e , 2019;Ro han e al., 2019). Se e al da abases con ain
gene exp ession analysis da a (Fei e al., 2006;Su esh e al.,
2014;Zouine e al., 2017;Shinozaki e al., 2018b), while ecen
p og ess in oma o me abolomics has p o ided subs an ial
in o ma ion abou he p ima y and specialized me abolism o
his species and he pa hways in ol ed in molecula biosyn hesis
and u no e (Luo, 2015;Tieman e al., 2017;Zhu e al., 2018).
D ama ic me abolic changes occu du ing oma o ui
de elopmen (Ca a i and Fe nie, 2006). Toma o is a
climac e ic ui , meaning i unde goes a su ge in espi a ion
and e hylene p oduc ion a he onse o ipening (Li e al., 2019a).
As ipening p og esses, oma o ui s ansi om pa ially
pho osyn he ic o ue he e o ophic issues h ough he
pa allel di e en ia ion o chlo oplas s in o ch omoplas s and
he dominance o ca o enoids and lycopene in he cells o he
ipe ui s (Ca a i and Fe nie, 2006). The ipening p ocess has
e ol ed o make ui pala able o he o ganisms ha consume
hem and dispe se hei seeds. In doing so, ipening ac i a es
pa hways ha gene ally influence he le els o pigmen s, suga s,
acids, and a oma-associa ed ola iles o make he ui mo e
appealing, while simul aneously p omo ing issue so ening and
deg ada ion o pe mi easie seed elease (Ma as e al., 2009).
In his e iew, we p o ide an o e iew o ou cu en
unde s anding o oma o ui me abolism. We begin by
de ailing he gene ic and ho monal con ol o ui de elopmen
and ipening,a e whichwedocumen hep ima y me abolismo
oma o ui s, wi h a special ocus on suga , o ganic acid, and
amino acid me abolism. Links be ween p ima y and seconda y
me abolic pa hways a e u he highligh ed by he impo ance o
pigmen s, fla onoids, and ola iles o oma o ui quali y.
Finally, as oma o plan s a e sensi i e o se e al abio ic s esses,
we b iefly summa ize he e ec s o ad e se en i onmen al
condi ions on oma o ui me abolism and quali y.
GENETIC REGULATION OF THE
DEVELOPMENT AND RIPENING OF
TOMATO FRUIT
F ui Se and Ea ly F ui De elopmen
The gene ic egula ion o ui de elopmen begins in he flo al
me is em (FM), whe e he a chi ec u e and o ganiza ion o his
issue is de e mined, and con inues un il he la e de elopmen al
s ages be o e ui ipening (Gillaspy e al., 1993)(Figu es 1A,B).
A he ini ial s age o oma o ui de elopmen , he CLAVATA-
WUSCHEL (CLV-WUS) eedback loop con ols me is em
ac i i y and egula es FM size, which in u n de e mines he
final numbe o ca pels in flowe s and, hence, seed locules in
ui s (Rod íguez-Leal e al., 2017). The signaling pep ide CLV3
di ec ly in e ac s wi h leucine- ich epea ecep o kinases, such
as CLV1 o CLV2, o ac i a e a signaling cascade ha nega i ely
egula es he s em cell-p omo ing ansc ip ion ac o WUS
(Somssich e al., 2016). Loss-o - unc ion mu a ions in any o
he CLV genes will he e o e cause s em cell o e p oli e a ion,
esul ing in he de elopmen o ex a flo al o gans and la ge
ui s (Xu e al., 2015;Rod íguez-Leal e al., 2017); o example,
he join ac ion o he na u al mu a ions ascia ed ( as)andlocule
numbe (lc) ga e ise o la ge- ui ed cul i a s, in con as o he
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15542
bilocula ui s o oma o wild species and mos small- ui ed
a ie ies (Tanksley, 2004;Ba e o e al., 2006). The as mu a ion is
a 294-kb in e sion dis up ing he oma o CLV3 (SlCLV3)p omo e
(Xu e al., 2015), whe eas lc is associa ed wi h wo single-nucleo ide
polymo phisms in a pu a i e CA G box egula o y elemen
downs eam o WUS (SlWUS)(Muños e al., 2011; an de Knaap
e al., 2014).Fu he mo e,using o wa dgene icsandCRISPR/Cas9
genome edi ing echnology, Xu e al. (2015) iden ified he
a abinosyl ans e ase genes FASCIATED INFLORESCENCE
(FIN), FASCIATED AND BRANCHED2 (FAB2), and REDUCED
RESIDUAL ARABINOSE 3a (RRA3a) as new componen s o he
CLV-WUS pa hway. The SlCLV3 pep ide mus he e o e be ully
a abinosyla ed o main ain me is em size since he loss o an
a abinosyl ans e ase cascade causes flo al and ui ascia ion.
As he flowe de elops, he gynoecium is ini ia ed in he ou h
who l o e mina eFMac i i y.TheMADSbox ansc ip ion ac o
AGAMOUS (AG) is equi ed o o m he ca pel p imo dium
(Yano sky e al., 1990). Consequen ly, he down egula ion o
TOMATO AGAMOUS1 (TAG1), he oma o o holog o
A abidopsis haliana AG, gi es ise o al e a ions in ca pel
de elopmen and de e minacy by p oducing ui s ha con inue
ode elopinaninde e mina e ashion(Pnuelie al.,1994;Pane al.,
2010;Gimenez e al., 2016). Fu he mo e, in A abidopsis,AG u ns
o he s em cell main enance p og am h ough he ansc ip ional
ep ession o WUS ia wo di e en pa hways: di ec ly, by
p omo ing he ec ui men o Polycomb G oup (PcG) p o eins o
me hyla e his one H3K27 a he WUS locus (Liu e al., 2011); and
indi ec ly, by inducing he exp ession o a gene encoding he C2H2
zinc-finge p o ein KNUCKLES (KNU) (Sun e al., 2009). The
induc iono KNU exp ession by AG equi es a ime delay egula ed
by he epigene ic modifica ion o his ones a he KNU locus (Sun e
al., 2014). Recen ly, Bollie e al. (2018) demons a ed ha he AG-
KNU-WUS pa hway is conse ed in A abidopsis and oma o and
egula es he imed e mina ion o flo al s em cell ac i i y. In his
con ex , he oma o mini zinc-finge p o ein INHIBITOR OF
MERISTEM ACTIVITY (SlIMA) ec ui s SlKNU o o m a
ansc ip ional ep esso complex oge he wi h TOPLESS and
HISTONE DEACETYLASE19, which binds o he SlWUS locus
o ep ess i s ansc ip ion (Bollie e al., 2018). Addi ionally, i has
been hypo hesized ha lc is a weak gain-o - unc ion mu a ion ha
educes o blocks he binding o TAG1 o he SlWUS 3′ egula o y
egion, which impai s he abili y o TAG1 o ep ess SlWUS,
esul ing in he o ma ion o la ge ui s as a consequence o he
de elopmen o ex a ca pels ( an de Knaap e al., 2014).
The a ia ion in oma o ui mo phology no only depends on
CLV-WUS signaling pa hway- ela ed genes, bu also on OVATE and
SUN, which ha e a la ge e ec on ui shape (Figu e 1B). The o a e
null mu a ion gi es ise o changes in cell di ision pa e ns du ing he
ea lies s ages o gynoecium de elopmen , wi h mo e cells p oduced
in he p oximo-dis al di ec ion and ewe in he medio-la e al
FIGURE 1 | Gene ic and ho monal con ol o oma o ui de elopmen . (A) Main s ages o oma o ui de elopmen . (B) Genes in ol ed in he con ol o oma o
ui de elopmen ha a e men ioned in his a icle. (C) Main ho mones in ol ed in oma o ui de elopmen du ing ui se and ui g ow h (g een) and ui ipening
( ed). (D) Genes in ol ed in he ho monal egula ion o ui de elopmen ha a e men ioned in his a icle. The Figu e summa izes da a collec ed by Gillaspy e al.
(1993);S i as a a and Handa (2005);Ka lo a e al. (2014) and Ob ouche a (2014).
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15543
di ec ion,causing hede elopmen o elonga ed ui s(Kue al.,1999;
Liu e al., 2002;Rod íguez e al., 2011). In con as , he e ec o SUN
on ui shape is mos no iceable a flowe an hesis, when i begins o
inc easecelldi isionalong hep oximo-dis alaxisandcellelonga ion
immedia ely a e e iliza ion (Xiao e al., 2009;Wu e al., 2011; an
de Knaap e al., 2014). Thus, a p o ound shi in he exp ession o
genes in ol ed in cell di ision, cell wall de elopmen , and pa e ning
p ocesses was obse ed in he elonga ing ui issues o he sun
mu an (Cle enge e al., 2015). Mo eo e , he MADS box gene
ENHANCER OF J2 (EJ2) also seems o be in ol ed in de e mining
ui shape; ej2 knockou mu an s de elop sligh ly elonga ed ui s
oge he wi h se e al pleio opic e ec s, such as b anched
inflo escences and join less pedicels (Soyk e al., 2017).
Among he ui weigh egula o s,CELL NUMBER
REGULATOR (CNR)was ound ounde lie he w2.2
quan i a i e ai locus (QTL), ac ing ea ly du ing he
de elopmen o he gynoecium o inc ease o a y size (F a y e
al., 2000;Guo and Simmons, 2011) and enla ge he placen a and
columella ui issues (Cong e al., 2002;Gonzalo e al., 2009).
SlKLUH is he causal gene o he w3.2 QTL and encodes a
CYP450 o he 78A class (Chak aba i e al., 2013). One single-
nucleo ide polymo phism in he SlKLUH p omo e leads o i s
enhanced exp ession in me is ems and young flowe bud issues;
howe e , he inc eased ui weigh o hese mu an plan s
becomes e iden only a e e iliza ion. An inc eased numbe o
cell laye s in he pe ica p gi es ise o hea ie ui s wi h a ipening
delay, which has been hypo hesized o be he esul o he
ex ension o he cell p oli e a ion s age (Chak aba i e al.,
2013). S udies in A abidopsis ha e sugges ed ha KLUH is
in ol ed in gene a ing a mobile g ow h-p omo ing signal,
al hough i s exac molecula and biochemical na u e is ye o be
deciphe ed (Anas asiou e al., 2007;Adamski e al., 2009). Cell
expansion in he pe ica p is esponsible o he d ama ic inc ease
in ui size om a 1- o 2-mm gynoecium o a 5- o 10-cm oma o
ui (Gillaspy e al., 1993;Xiao e al., 2009). The CELL SIZE
REGULATOR (CSR) gene con ols pe ica p cell size and unde lies
he w11.3 QTL (Huang and an de Knaap, 2011;Mu e al., 2017).
CSR exp ession is es ic ed o ui s, s a ing abou 5 days a e
pollina ion and dec easing a he onse o ipening. Along wi h he
inc eased cell size, coexp ession s udies sugges ha CSR is also
in ol ed in shoo de elopmen and phloem/xylem his ogenesis;
howe e , he molecula unc ion o CSR in con olling hese
de elopmen al p ocesses emains unclea (Mu e al., 2017).
F ui Ripening
A he end o ui de elopmen , when seeds a e ma u e and eady o
dispe sal, oma o ui s unde go ipening, a complex de elopmen al
p og am in ol ing he coo dina ed egula ion o nume ous
physiological and biochemical changes ha de e mine fla o ,
colo , ex u e, and a oma. These changes in ol e he up- o
down egula ion o nume ous genes in a ious me abolic pa hways
(Alba e al., 2005;Fujisawa e al., 2011;Oso io e al., 2011). Mul iple
s udies o he de elopmen and ma u a ion o oma o ui s ha e
acili a ed he iden ifica ion o specific genes ha pa icipa e in
ipening (V ebalo e al., 2002;Manning e al., 2006;Gio annoni,
2007;Wang e al., 2009;Chung e al., 2010;Nashile i z e al., 2010;
Ka lo a e al., 2011;Pesa esi e al., 2014)(Figu e 1B).
Toma oes a e classified as climac e ic ui s, exhibi ing a peak o
espi a ion and e hylene p oduc ion a he s a o ipening
(Alexande and G ie son, 2002). The biosyn hesis and pe cep ion
o e hylene a e highly egula ed, in ol ing genes conse ed in
a ious plan axa (Seymou e al., 2013). Some ansc ip ion
ac o s modula e e hylene biosyn hesis and signal ansduc ion
du ing ui ipening, among which i is wo h highligh ing
RIPENING INHIBITOR (RIN) (V ebalo e al., 2002),
COLORLESS NON-RIPENING (CNR) (Manning e al., 2006),
and NON-RIPENING (NOR) (Yuan e al., 2016). RIN ac s as he
main egula o o ui ipening, di ec ly con olling he exp ession
o a ge genes in ol ed in a wide ange o ipening- ela ed e en s
(Fujisawa e al., 2011;Qin e al., 2012). RIN encodes a SEPALLATA
(SEP)-class MADS-box ansc ip ion ac o (V ebalo e al., 2002),
which was p e iously conside ed o be an essen ial egula o o he
induc ion o ipening (V ebalo e al., 2002); howe e , i s ole in
ui ipening was ecen ly eassessed ollowing he publica ion o
s udies showing ha RIN, al hough necessa y o comple e ipening,
is no equi ed o he ini ia ion o his p ocess (I o e al., 2017). The
in mu an was ound o be caused by he dele ion o a genomic
DNA agmen be ween RIN and MACROCALYX (MC), o ming
he chime ic gene RIN-MC (V ebalo e al., 2002). MC a ec s
inflo escence de e minacy and sepal de elopmen (V ebalo e al.,
2002), and he in mu an was ound o be a gain-o - unc ion
mu an ha p oduced a p o ein ha ac i ely ep esses ipening (I o
e al., 2008;Li e al., 2018a). RIN binds o he deme hyla ed
p omo e egions o se e al genes, such as he e hylene
biosyn hesis genes SlACS2 (1-AMINOCYCLOPROPANE-1-
CARBOXYLIC ACID SYNTHASE 2), SlACS4,SlACO1 (ACC
OXIDASE 1), he e hylene ecep o NEVER RIPE (NR), and
o he s whose p oduc s a e in ol ed in ui so ening and he
ansc ip ional egula ion o cell wall hyd olases
[POLYGALACTURONASE (PG), b-GALACTOSIDASE4 (TBG4),
ENDO-(1,4)-b-MANNANASE4 (MAN4), and a-EXPANSIN1
(EXP1)] (Klee and Tieman, 2002;I o e al., 2008;Fujisawa e al.,
2011;Ma el e al., 2011;Shima e al., 2013;I o e al., 2017).
RIN also posi i ely s imula es he exp ession o CNR (Ca don
e al.,1999;Manning e al., 2006). The cn mu a ionis he esul o a
spon aneous epigene ic change ha inc eases cy osine me hyla ion
in he p omo e o a SQUAMOSA p omo e -binding p o ein-
encoding gene, which s ongly dec eases gene exp ession and
p oduces colo less ui s wi h an al e ed pe ica p ex u e
(Manning e al., 2006). Du ing ipening, he CNR p omo e is
p og essi ely deme hyla ed, bu in cn mu an s, he p omo e
emains hype me hyla ed, p e en ing RIN om binding o i
(Zhong e al., 2013). In addi ion, CNR was in ol ed in he posi i e
egula ion o many ipening- ela ed genes, including PG,
PECTINESTERASE (PE), XYLOGLUCAN
ENDOTRANSGLYCOSYLASE (XET), PHYTOENE SYNTHASE1
(PSY1), LIPOXYGENASE (LOX), and ACO1 (E iksson e al., 2004).
The no mu an exhibi s abno mal ipening as a esul o a 2-
bp dele ion in he NOR coding sequence, leading o he ea ly
e mina ion o p o ein ansla ion (Tigchelaa e al., 1973;Ma el
e al., 2011;Oso io e al., 2011). NOR encodes a NAC amily
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15544
ansc ip ion ac o ha egula es ui ipening h ough a
cu en ly unclea mechanism, while mu a ions in his gene
inhibi mul iple me abolic p ocesses and p olong ui shel li e
(Kuma e al., 2018). A s udy o he ole o NOR and RIN in
oma o ui ipening confi med ha he no mu a ion had a
mo e global e ec on e hylene/ ipening- ela ed gene exp ession
han in, sugges ing ha NOR migh e en ac ups eam o RIN in
he ansc ip ional ne wo k con olling oma o ui ipening
(Oso io e al., 2011). In addi ion o NOR, h ee o he NAC amily
genes, SlNAC1,SlNAC4,andNOR-like1,a eknown obe
in ol ed in he egula ion o oma o ui ipening (Ma e al.,
2014;Zhu e al., 2014;Meng e al., 2016).
O he ipening ac o s, such as he MADS box TOMATO
AGAMOUS-LIKE1 (TAGL1) (V ebalo e al., 2002;Giménez
e al., 2010), oma o APETALA2 (SlAP2a) (Ka lo a e al., 2011),
and he oma o homeodomain leucine zippe homeobox p o ein
SlHB1 (Lin e al., 2008), exe cise hei egula o y unc ions by
in e ac ingwi hRIN(Fujisawae al.,2011;Qine al.,2012;Seymou
e al., 2013). TAGL1 (also e e ed o as ARLEQUIN in some
publica ions), a PLENA lineage gene o hologous o A abidopsis
SHATTERPROOF1/2, con ols many aspec s o oma o ui
ipening (V ebalo e al., 2009;Ga ceau e al., 2017), including
he di ec ac i a ion o he exp ession o he e hylene biosyn hesis
gene ACS2 (I kin e al., 2009). Toma o ui s p oduced by TAGL1-
silenced plan s had de ec s in ipening wi hou hei flo al o gan
specifica ion being a ec ed (V ebalo e al., 2009;Giménez e al.,
2010;Pan e al., 2010). Plan s wi h educed TAGL1 exp ession
p oduced ui s wi h a na ow pe ica p and educed fi mness a he
b eake s age, which emained yellow and p oduced significan ly
less e hylene han he con ol ui s (V ebalo e al., 2009). The
MADS box p o eins TAGL1 and wo homologs o FRUITFULL
(FUL1/TDR4 and FUL2/MBP7) unc ion as co egula o s o RIN
(Lesebe g e al., 2008;I kin e al., 2009;V ebalo e al., 2009;
Giménez e al., 2010;Ma el e al., 2011;Beme e al., 2012;Shima
e al., 2013;Wang e al., 2014). Fujisawa e al. (2014) demons a ed
ha RIN, TAGL1, and he FUL homologs o m a DNA-binding
complex, p obably a e ame , which is belie ed o egula e oma o
ui ipening. The RIN and CNR egula o s ha e been shown o
unc ion ups eam o SlAP2a and o posi i ely egula e i s exp ession
(Ka lo ae al.,2014),whe easSlHB1con olse hyleneme abolismby
binding o he egula o y egions o ACO1 (Lin e al., 2008). On he
o he hand, ansc ip omic s udies ha e shown ha SlAP2a
pa icipa es in he con ol o ui ipening as a nega i e egula o o
se e al p ocesses in ol ed in e hylene biosyn hesis, and signaling
pa hways, as well as in he di e en ia ion o ch omoplas s (Chung
e al., 2010;Ka lo a e al., 2011).
HORMONAL REGULATION OF THE
DEVELOPMENT AND RIPENING OF
TOMATO FRUIT
F ui Se and Ea ly F ui De elopmen
F ui se and ui de elopmen a e complex p ocesses ha equi e
he coo dina ion o di e en phy oho mones (McA ee e al., 2013;
Shinozaki e al., 2018b;Li e al., 2019b)(Figu es 1C, D). F om
flowe ini ia ion o e iliza ion, he mo phogenesis and g ow h o
ca pels and o ules equi e he spa ial and empo al biosyn hesis
and ac ion o auxins, cy okinins (CKs), and gibbe ellins (GAs)
(Azzi e al., 2015). Sho ly be o e an hesis, when he o a y has
eached i s ma u e size, abscisic acid (ABA) and e hylene wo k o
s op g ow h wi hin he o a y o main ain a empo ally p o ec ed
and do man s a e (Gillaspy e al., 1993;Azzi e al., 2015). A e he
success ul pollina ion and e iliza ion o he o ules, o a y g ow h
esumes and he ui and seeds de elop concomi an ly (Azzi e al.,
2015). These changes a e associa ed wi h a dec ease in ABA and
e hyleneconcen a ionsandaninc easeinauxin,GAs,andCKs(de
Jonge al.,2009;McA eee al.,2013;Shinozakie al.,2015;Shinozaki
e al., 2018a). GAs p oduced by pollen may inc ease auxin
p oduc ion in he o a y, which in u n may ac as a signal o ui
se and he subsequen ac i a ion o cell di ision (Gillaspy e al.,
1993;de Jong e al., 2009). Ac i e ui g ow h in ol ing pe ica p cell
di ision and elonga ion is p omo ed by he biosyn hesis o auxin in
he de eloping seeds and GAs in he pe ica p (Ob ouche a, 2014).
Auxins and GAs appea o be he p edominan ho mones equi ed
o oma o ui ini ia ion in esponse o e iliza ion, since he
exogenous applica ion o bo h ho mones leads o ui ini ia ion
andpa henoca picde elopmen (deJong e al.,2009).CKs, e hylene,
ABA, b assinos e oids, and polyamines (PAs) ha e also been shown
o play a ole in ui o ma ion, bu his is cu en ly less well
documen ed (S i as a a and Handa, 2005;McA ee e al., 2013;
Azzi e al., 2015;Shinozaki e al., 2015;Liu e al., 2018;Shinozaki
e al., 2018a).
In oma o, ea ly ui de elopmen is go e ned by healloca ion
o auxin o issues and cells, which ini ia es signal ansduc ion
pa hways(Azzie al.,2015).The PIN-FORMED(PIN)auxine flux
anspo p o eins we e shown o be in ol ed in ui se and ea ly
oma o ui de elopmen (Moune e al., 2012;Pa ison and
Ca alá, 2012). Silencing SlPIN4 esul ed in he p oduc ion o
small pa henoca pic ui s exhibi ing p ecocious de elopmen
(Moune e al., 2012). The auxin signaling pa hway in ol es an
auxin ecep o called TRANSPORT INHIBITOR RESPONSE1
(TIR1) (Azzi e al., 2015). In he p esence o auxin, TIR1 ec ui s
he ansc ip ional ep esso s AUXIN/INDOLE-3-ACETIC ACID
(Aux/IAA) and igge s hei deg ada ion by he 26S p o easome
(Azzi e al., 2015), eleasing he Aux/IAA-bound auxin esponse
ac o s (ARFs) and ini ia ing he auxin esponse h ough auxin-
esponsi e elemen -media ed gene ansc ip ion(Azzie al.,2015).
In oma o, he misexp ession o TIR1 and specific membe s o he
Aux/IAA and ARF gene amily al e s he no mal flowe - o- ui
ansi ion and esul s in pa henoca pic ui p oduc ion (de Jong
e al., 2009;Ren e al., 2011;Moune e al., 2012;Azzi e al., 2015).
Howe e ,Aux/IAA andARFgenesmayha eopposing unc ions o
TIR ega ding ui se ; he ansc ip abundance o SlIAA9 and
SlARF7 dec eased in SlTIR1-o e exp essing plan s, which esul ed
in he o ma ion o seedless ui (Ren and Wang, 2016;Golden al-
Cohen e al., 2017). The silencing o he Aux/IAA ansc ip ional
ep esso SlIAA17 esul ed in la ge ui s wi h hicke pe ica p
issues, a pheno ype caused by enhanced cell expansion (Su e al.,
2014). Ren and Wang (2016) showed ha SlTIR was egula ed by
GAs, auxins, ABA, and e hylene, sugges ing ha TIR may be a key
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15545

media o o hec oss alkbe weenauxinando he phy oho mones.
The SlARF7/SllAA9 complex also media es c oss alk be ween
auxin and GA pa hways o egula e ui ini ia ion h ough hei
in e ac ion wi h he GA-signaling ep esso SlDELLA (Hu e al.,
2018). SlARF7/SllAA9 complex and SlDELLA an agonis ically
egula e genes in ol ed in auxin and GA me abolism while hey
addi i ely co egula e genes in ol ed in ui g ow h (Hu
e al., 2018).
Indeed, auxins do no ac alone o igge ui de elopmen
and ui se ; hese p ocesses a e pa ly media ed by GAs, as pa
o a complex ho monal c oss- alk wi h auxin (de Jong e al., 2009;
McA ee e al., 2013;Azzi e al., 2015). Pollina ion igge s he
up egula ion o ansc ip s encoding GA 20-oxidases (GA20ox),
which biosyn hesize ac i e GA1 and GA4 (Azzi e al., 2015). I
was sugges ed ha he exp ession o mo e han one GA20ox gene
is equi ed o con ol ui se in oma o because he silencing o
indi idual GA20ox genes did no s ongly a ec ui se o
de elopmen (Xiao e al., 2006;Olimpie i e al., 2011;Azzi
e al., 2015). Despi e his, he he e ologous o e exp ession o
ci us CgGA20ox1 in oma o esul ed in an ele a ed GA4 con en
and pa henoca pic ui de elopmen , demons a ing he
influence o GA and GA20ox ac i i y on ui se and
de elopmen (Ga cía-Hu ado e al., 2012). The GA signal
ansduc ion pa hway equi es he ecogni ion o GA by i s
ecep o , GA INSENSITIVE DWARF1 (GID1) (Azzi e al.,
2015). The GID1-GA complex in e ac s wi h he nuclea
ep esso DELLA o a ge i o ubiqui in-dependen
p o eoly ic deg ada ion by he 26S p o easome (Azzi e al.,
2015). This emo es he ep ession o he GA- esponsi e genes,
which a e hen able o ini ia e GA signal ansduc ion. Consis en
wi h his, he silencing o he SlDELLA gene in oma o esul ed in
small, acul a i e pa henoca pic ui s wi h an elonga ed shape
(Ma í e al., 2007). The p oce a (p o) mu an , which ca ies a
poin mu a ion in he GRAS egion o SlDELLA, has also e y
s ong pa henoca pic capaci y and shows enhanced g ow h o
p ean hesis o a ies (Jones, 1987;Ca e a e al., 2012;Shinozaki
e al., 2018c). The pa henoca pic capaci y o p o is mainly
associa ed wi h changes in he exp ession o genes in ol ed in
GA and auxin pa hways (Ca e a e al., 2012). A new SlDELLA
mu an con aining a single nucleo ide subs i u ion, p oce a2
(p o2), has been ecen ly iden ified and shows a po en ial o
high ui yield in bo h op imal and un a o able g owing
condi ions due o i s acul a i e pa henoca pic capaci y
(Shinozaki e al., 2018c). Pa henoca py is indeed an a ac i e
ai o ui p oduc ion (Shinozaki e al., 2018c).
As men ioned p e iously, o he phy oho mones a e in ol ed
in ui se and g ow h. A numbe o ABA-deficien mu an s ha e
p o ided aluable insigh s in o he ole o ABA in ui g ow h
(Azzi e al., 2015). Pheno ypic cha ac e iza ion o he ABA
biosyn hesis no /flcdouble mu an showed ha i s small ui s
had conside ably educed ABA le els and smalle cell sizes,
especially wi hin he pe ica p (Ni sch e al., 2012). I was
sugges ed ha ABA s imula es ui g ow h by es ic ing he
le el o e hylene in no mal ui s (Azzi e al., 2015), which may
indeed induce ui se as oma o plan s ea ed wi h he e hylene
ac ion inhibi o 1-me hylcyclop opene (1-MCP) p oduce
pa henoca pic ui s (Shinozaki e al., 2015). In he same way,
oma o plan s ca ying ei he o wo allelic mu a ions in
ETHYLENE RECEPTOR1 (Sle 1-1 o Sle 1-2) we e insensi i e
o e hylene, esul ing in pa henoca py (Shinozaki e al., 2015;
Shinozaki e al., 2018a). E hylene is in ol ed in he senescence o
unpollina ed o a ies and p e en s ui se by down egula ing
GA accumula ion, ac ing downs eam o auxin and ups eam o
GA in he con ol o ui se (Shinozaki e al., 2018a). Exogenous
CK applica ion induces pa henoca pic ui s (Ma suo e al.,
2012;Ding e al., 2013), sugges ing a ole o CKs du ing
oma o ui ini ia ion. Cy okinins induce pa henoca py in
oma o pa ially h ough modula ion o GA and auxin
me abolisms (Ding e al., 2013). Mo eo e , ansc ip omic and
me abolomics udies showed ha al hough CKs mainly con olcell
di ision du ing oma o ui de elopmen , hey also play a c i ical
ole in ui -se and ea ly g ow h o oma o ui s (Ma io i e al.,
2011;Ma suo e al., 2012). A key ole o PAs du ing ui se was
also sugges ed, wi h oma o genes encoding enzymes in ol ed in
PA biosyn hesis, such as a ginine/o ni hine deca boxylase (ADC/
ODC) and spe mine syn hase (SPMS), sugges ed o be pa icula ly
impo an du ing he p ocess o ui se ing (Liu e al., 2018).
F ui Ripening
F ui ipening has been widely s udied in oma o, wi h e hylene
known o play a key ole in his p ocess (Oso io e al., 2013;
Seymou e al., 2013;Liu e al., 2015;Bo ghesi e al., 2016;
Shinozaki e al., 2018b;Li e al., 2019a)(Figu es 1C, D). Two
sys ems o e hylene biosyn hesis ha e been p oposed in climac e ic
ui s (McMu chie e al., 1972): Sys em 1 is esponsible o
p oducing basal e hylene le els du ing ui g ow h and is
e hylene au oinhibi o y, while sys em 2 ope a es du ing
climac e ic ipening and is au oca aly ic (Liu e al., 2015). A he
onse o ipening, an inc ease in e hylene is obse ed in ma u e
g een oma oes, esul inginane en ual100- o300- oldinc easein
he e hylene concen a ion du ing ui ipening (Ka lo a e al.,
2014;Li e al., 2019a). E hylene ini ia es a cascade o changes, which
culmina e in he ans o ma ion o he ha d, unpala able g een
oma o in o an a ac i e, b igh ly colo ed succulen and nu i ious
ui (Gio annoni, 2004;Li e al., 2019a).
E hylene signaling can be egula ed a se e al le els, including
e hylene biosyn hesis and i s pe cep ion (Ka lo a e al., 2014;
Ma a e al., 2018;Li e al., 2019a). E hylene biosyn hesis in ol es
mul iple aminocyclop opane-1-ca boxylic acid (ACC) syn hase
and ACC oxidase enzymes and genes (Oso io e al., 2013;
Ka lo a e al., 2014;Kou e al., 2016;Li e al., 2019a). Fou een
pu a i e ACS genes and six ACO genes ha e been iden ified in
he oma o genome (Liu e al., 2015). Among hem, i has been
p oposed ha SlACS2,SlACS4,SlACO1,SlACO2, and SlACO4
play impo an oles in e hylene p oduc ion du ing oma o ui
ma u a ion (Ca a and Gio annoni, 2008;Liu e al., 2015). Some
ansc ip ion ac o s a e known o ac ups eam o he e hylene
biosyn hesisgenes o egula e ui ipening,includingRIN,SlHB-1,
and he NAC ansc ip ion ac o s SNAC4 and SNAC9 (Liu e al.,
2015;Kou e al., 2016).
E hylene pe cep ion is media ed h ough e hylene ecep o s
encoded by ETHYLENE RESPONSE (ETR) genes, which ac i a e
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15546
a signal ansduc ion cascade h ough he elease o he block on
ETHYLENE INSENSITIVE2 (EIN2) exe ed by CONSTITUTIVE
TRIPLE RESPONSE1 (CTR1)(Ka lo a e al., 2014;Liu e al.,
2015;Ma a e al., 2018;Li e al., 2019a). Se en ETR genes and
ou CTR1 homologs ha e been iden ified in oma o hus a , all
o which con ol e hylene sensi i i y by balancing he u no e o
he componen s o he e hylene signaling pa hway, combining
posi i e and nega i e eedback (Liu e al., 2015;Ma a e al., 2018).
This elease hen ac i a es he EIN3/EIN3-like (EIL) p ima y
ansc ip ion ac o genes, esul ing in he exp ession o
seconda y ansc ip ion ac o genes encoding he e hylene
esponse ac o s (ERFs) (Ka lo a e al., 2014;Liu e al., 2015;
Ma a e al., 2018). The final esul o his signaling pa hway is he
ansc ip ional egula ion o he a ge genes by he EILs o ERFs
(Ka lo a e al., 2014). Some o he ERF genes ha e been
cha ac e ized in oma o, including SlERF1,SlERF.B3,and
SlERF6 (Li e al., 2007;Liu e al., 2013;Ka lo a e al., 2014),
bu many o hei unc ions and e hylene- esponsi e a ge genes
emain unknown (Li e al., 2019a). Six EIL genes ha e been
iden ified in oma o, al hough SlEIL5 and SlEIL6 may no be
in ol ed in oma o ipening (Liu e al., 2015). Se e al genes ha
egula e oma o ipening h ough he ansduc ion o e hylene
signals ha e been iden ified (Ka lo a e al., 2014), including he
e hylene ecep o genes NR,ETR6, and GREEN-RIPE (G )(Yen
e al., 1995;Ba y and Gio annoni, 2006;Ke any e al., 2007).
Two o he p o eins, RESPONSE TO ANTAGONIST1 (RAN1) and
TETRATRICOPEPTIDE REPEAT1 (TRP1), also play impo an
oles a he ecep o le els (Liu e al., 2015).
Ripening is also influenced by he balance o o he ho mones,
including ABA, auxin, and he b assinos e oids (Seymou e al.,
2013;Ka lo a e al., 2014;Liu e al., 2015;Shinozaki e al., 2018b;
Li e al., 2019a;Shin e al., 2019). ABA is known o p omo e
ipening, whe eas auxin seems o ha e an an agonis ic e ec (Liu
e al., 2015). ABA is a key in e media e egula o o oma o ui
ipening, and i s le els change acco ding o ui de elopmen
s ages (Zhang e al., 2009;Bo ghesi e al., 2016). In oma o, he
supp ession o he gene ha ca alyzes he fi s s ep in ABA
biosyn hesis [9-cis-epoxy ca o enoid dioxygenase (NCED1)]
esul s in he down egula ion o some ipening- ela ed cell wall
genes, such as hose encoding polygalac u onase and pec in
me hyles e ase, p omo ing an inc ease in fi mness and a longe
shel li e (Sun e al., 2012). ABA in e ac s wi h e hylene signaling;
he exp ession o genes in ol ed in e hylene biosyn hesis a e
induced by exogenous ABA (Liu e al., 2015).
Low le els o auxins a e also equi ed a he onse o ipening,
and auxin signaling declines a his s age (Gillaspy e al., 1993;
Ka lo a e al., 2014;Shin e al., 2019); howe e , i seems ha he
a io be ween indole ace ic acid (IAA) and i s conjuga ed o ms is
mo e impo an han he le el o ee IAA o he egula ion o
oma o ipening (Ka lo a e al., 2014). Indeed, he dec ease o
ee IAA a he onse o ipening is associa ed wi h an inc ease in
i s conjuga ed o m, IAA-Asp (Bu a and Spaulding, 1994;
Ka lo a e al., 2014). SlSAUR69 is in ol ed in he dec ease o
auxin le els and/o signaling in he pe ica p issue a he onse o
ui ipening ia he ep ession o pola auxin anspo (Shin e
al., 2019). ARF genes a e also in ol ed in ui ipening; he
down egula ion o SlARF4 o SlARF2 esul ed in ui s wi h
d ama ic ipening de ec s (Jones e al., 2002;Ka lo a e al.,
2014;Hao e al., 2015). Auxin–e hylene in e ac ions a e c ucial
o he ui ipening p ocess, al hough he molecula basis o he
egula o y ne wo k is s ill ela i ely unclea (Li e al., 2017;Shin
e al., 2019). An an agonis ic e ec be ween auxin and e hylene
has been obse ed du ing he ipening o oma oes (Li e al.,
2017), wi h e hylene inhibi ing auxin anspo , me abolism,
and signaling p ocesses, while auxin ep esses he exp ession o
genes in ol ed in e hylene biosyn hesis and signaling
(Chaabouni e al., 2009;Liu e al., 2015;Li e al., 2016a;Li
e al., 2017). Mo eo e , bo h auxin and e hylene di e en ially
egula e CK me abolism and signaling p ocesses du ing oma o
ipening (Li e al., 2017).
B assinos e oids migh also be in ol ed in oma o ipening, as
exogenous applica ions o his ho mone can p omo e ipening
and e hylene p oduc ion in oma oes (Ka lo a e al., 2014). PAs
a e also ac i ely in ol ed in climac e ic ui ipening (Liu e al.,
2018); o example, pu escine le els p og essi ely inc ease
du ing ui ma u a ion and peak in ipe oma oes, while
spe mine and spe midine le els dec ease g adually un il he
ui s a e ully ipe (Tsaniklidis e al., 2016;Liu e al., 2018).
Mo eo e , al hough he exp ession le els o SPMS,ADC, and
ODC we e minimal du ing he ui ipening p ocess, he SPDS
genes may play an impo an ole du ing oma o ui ipening
(Liu e al., 2018).
Phy oho mones also play a key ole in he egula ion o
oma o ui me abolism and quali y (Van Meuleb oek e al.,
2015;C uz e al., 2018;Li e al., 2019b). The ho mones discussed
abo e all con ibu e o he me abolism o oma o ui s, al hough
ABA and e hylene play he mos impo an oles (Li e al.,
2019b). ABA had a g ea e e ec on he egula ion o he
p ima y me abolism, while e hylene plays an impo an ole in
he ansi ion o p ima y o seconda y me abolism in oma oes
(Li e al., 2019b). Rega ding seconda y me abolism, e hylene and
auxins we e desc ibed as he mos impo an egula o s o
ca o enoid biosyn hesis du ing oma o ui ipening (Van
Meuleb oek e al., 2015;C uz e al., 2018).
PRIMARY METABOLISM IN TOMATO
FRUIT
De elopmen o he oma o fleshy ui occu s in h ee dis inc
phases : i) cell di ision phase occu s in he ea ly days ollowing
e iliza ion un il 10 DAA ii) cell expansion ( om 10 DAA o 40
DAA) and iii) ui ipening and ma u a ion (Figu e 1A). Du ing
his e olu ion, oma o ui s ollows a ansi ion om pa ially
pho osyn he ic o comple e he e o ophic me abolism. Typical
mo phophysiological s eps a e conside ed and include imma u e,
ma u e g een, b eake , pink and ed ipe ui s. Al hough he ui
ipening is an impo an s ep de e mining he ui quali y and
nu i ional alues, ecen wo ks p o ided e idences ha he ea ly
ui de elopmen also assumes key oles o acquisi ion o quali y
ai s, including he accumula ion o suga s and o ganic acids
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15547
(Ca a i and Fe nie, 2006;Beau oi e al., 2014;Biais e al., 2014;
Bauche e al., 2017). Pos genomic app oaches including analyses
o ui ansc ip omes, p o eomes, and me abolomes as well as
mul ile el s udies in eg a ing enzyme p ofiling gene a ed a la gese
o use ul da a imp o ing ou knowledge on he egula ion o
me aboli es u no e du ing oma o ui de elopmen (Moune
e al., 2009;Cen eno e al., 2011;Van de Poel e al., 2012;Van
Meuleb oeke al.,2015).Hie a chicalclus e ingpe o medbyBiais
e al. (2014) e ealed igh associa ions be ween enzyme ac i i ies
and de elopmen al phase and concluded ha me aboli es a e mo e
sensi i e o g ow h condi ions han enzyme ac i i ies. A global
o e iew o he main eco ded changes in me aboli es eco ded
du ing ui ansi ion omg een o edma u e ui sisp o idedin
Figu e 2.
Ca bohyd a e Me abolism
Imma u e G een F ui Pho osyn hesis
Suga s a e closely ela ed o ui yield and quali y. In oma o
ui s, suga s p o ide swee ness and a e impo an o he
gene a ion o u go p essu e o p omo e cell expansion
(Kanayama, 2017). Suga s also ac as signal molecules
con olling ui de elopmen and me abolism. G een ui s
emain able o pe o m pho osyn hesis which can p oduce up
o 20% o he ui pho osyn he a es, he emaining pa being
impo ed by sou ce lea es (Pesa esi e al., 2014). The ligh
ha es ing elec on ans e and CO
2
fixa ion p o eins a e
conse ed in hei ac i e s a e in g een ui issues (Ma as e
al., 2011). F ui chlo oplas s con ain su ficien amoun s o
plas ocyanin, e edoxins, Rieske p o eins, cy och ome and
cy och ome b
559
and ibulose-1,5-biphospha e ca boxylase
ac i i y is de ec ed in he ui s (He he ing on e al., 1998). The
iose phospha e and glucose phospha e anspo e s a e ac i e in
he oma o chlo oplas s. Unexpec edly, genes associa ed wi h
pho osyn hesis a e highly exp essed in he locule which is in ac
he main si e o espi a ion (Lemai e-Chamley e al., 2005).
Ne e heless, he impo ance o g een ui pho osyn hesis is
s ill a ma e o deba e. Acco ding o Ca a a e al. (2001), oma o
ui s do no show signs o CO
2
fixa ion, e en i pho ochemical
FIGURE 2 | Global o e iew o me abolic changes occu ing du ing he ansi ion om g een expanding ui o ipening p ocesses ( om 30 DAA o 60 DAA) in
oma o ui . Names o me aboli es in ed, g een and black indica e inc ease, dec ease o no changes, espec i ely. Me aboli es a e analyzed mainly in pe ica ps. The
Figu e summa izes da a collec ed by Ca a i and Fe nie (2006);Gilbe (2009);Moune e al. (2009);Cen eno e al. (2011);Beau oi e al. (2014);Biais e al. (2014),
Van Meuleb oek e al. (2015),Van de Poel e al. (2012), and Zhao e al. (2018).
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15548
ac i i y is de ec able and an e ec i e elec on anspo obse ed.
Xu e al. (1997) epo ed ha a small ui ( esh weigh lowe han
10 g) is able o pe o m a g oss pho osyn hesis equi alen o a 3-
cm
2
lea blade bu ha his ac i i y apidly dec eases he ea e : in
hea ie ui s, g oss pho osyn hesis dec eases o negligible alues.
These au ho s e en assume ha he aim o he pho osyn he ic
p ocess in ma u ing ui is mainly o dele e CO
2
p oduced by
espi a ion a he han con ibu ing o pho osyn ha e p oduc ion.
Kahlau and Bock (2008) showed ha RNA, ansla ion and
p o ein accumula ion down egula ion was obse ed o all
plas id-encoded pho osyn hesis genes al eady in he g een ui .
He he ing on e al. (1998) howe e demons a ed ha all uss
issues, including ui s, a e qui e ac i e pho osyn he ically. These
au ho s in e es ingly demons a ed ha he ela i e con ibu ion
o he ui e sus he lea pho osyn hesis o ui pho osyn ha e
accumula ion end o na ow unde low ligh in ensi ies.
A ui specific an isense inhibi ion o he chlo oplas ic uc ose
1,6-biphospha ase (FBPase) led o an ob ious dec ease in final
weigh o ipe ui s (Obiadalla-Ali e al., 2004) while, con e sely,
oma o lines wi h a ui specific educ ion in he exp ession o
glu ama e-1-semialdehyde amino ans e ase (GSA) and hus a lowe
le el o chlo ophyll and pho osyn he ic a e, emained una ec ed in
e ms o ui weigh (Ly o chenko e al., 2011). N agkas e al. (2019)
ecen ly demons a ed ha phosyn he ically ac i e ui s able o
espond o ligh may igge asco ba e syn hesis while non-
pho osyn he ic ed ma u ing ui s a e unable o p oduce his
an ioxidan in esponse o ligh .
Auxin plays an impo an ole o de e mining final ui s age
h ough he con ol o cell di ision and cell expansion. Auxin-
esponsi e ac o s (ARF) can ei he ac i a e o ep ess ansc ip ion
o auxin- esponsi e genes. Combined me abolomics and
ansc ip omic s udies o plan s deficien in he exp ession o he
oma o Aux/IAA ansc ip ion ac o IAA9 sugges a ole o
pho osyn hesis in he ini ia ion o ui de elopmen (Wang
e al., 2009). Down egula ion o SlARF4 enhanced ui fi mness
and inc eased chlo ophyll con en in g een ui s in ela ion o an
inc eased numbe o chlo oplas s (Guillon e al., 2008). SlARF4
also has a di ec impac on ui suga me abolism: he SlARF4
unde exp ession oma o lines accumula ed mo e s a ch a ea ly
s ages o ui de elopmen associa ed wi h an imp o ed
pho ochemical e ficiency (Saga e al., 2013). Mo eo e , SlARF4
is highly exp essed in he pe ica p issues o imma u e ui s and
unde goes decline a he onse o ipening. Down- egula ed
oma oes also p esen a highe s a ch con en han he wild ype
in de eloping ui s which is di ec ly ela ed o up- egula ion o
se e al genes and enzyme ac i i ies in ol ed in s a ch biosyn hesis
(Saga e al., 2013).
Plas id numbe s and chlo ophyll con en in ui s a e posi i ely
co ela ed wi h pho osyn hesis and pho osyn ha e accumula ion
and bo h a e influenced by nume ous en i onmen al and gene ic
ac o s. In oma o ui s, he GOLDEN2-LIKE (GLK) ansc ip ion
ac o induces he exp ession o nume ous genes ela ed o
chlo oplas di e en ia ion and pho osyn hesis (Powell e al.,
2012). The genome o S. lycope sicum possesses wo copies o
his gene: SlGLK1 is p edominan ly exp essed in he lea es while
SlGLK2 is exp essed in he ui s, especially in he a ea o pedicel
junc ion (Nguyen e al., 2014). A la i udinal g adien o SlGLK2
exp ession induces a ypical une en colo a ion in ipe ui SlGLK2
is p e e en ially exp essed in he shoulde o he ui (Saga e al.,
2013). Sl-GLK2 belongs o he GARP sub amily o he myb
ansc ip ion ac o and is encoded by he UNIFORM (U) gene
(Powell e al., 2012). The umu a ion has been widely selec ed in
mode n oma o a ie ies which consequen ly exhibi a uni o m
ipening a ac i e o consume s and sui able o indus ial
p ocessing. This mu an con ains less suga and chlo oplas s
p esen a lowe numbe o hylakoid g ana. Acco ding o
Nadakudu i e al. (2014),someclassIKNOTTED1-LIKE
HOMEOBOX gene (TKN2 and TKN4)alsoinfluence chlo oplas
de elopmen in oma o ui s and ac ups eam o SlGLK2. A
dominan gain-o - unc ionmu a ion o TKN2 induces ec opic ui
chlo oplas de elopmen ha esembles SlGLK2 o e exp ession.
Mo e ecen ly, Lupi e al. (2019) demons a ed ha SlGLK2
exp ession is pa ly egula ed by a phy och ome-media ed ligh
pe cep ion. Auxin appea s as a nega i e egula o o SlGLK2
exp ession and SlGLK2 enhances cy okinin esponsi eness. This
s udy also demons a ed ha SlGLK2 enhances ocophe ol and
o al soluble solid h ough amylase s imula ion, so ha selec ion o
he umu a ion in comme cial a ie ies p obably inad e en ly
comp omise ipe ui quali y.
Suga Unloading in F ui s
Suga unloading in oma o ui is a con olled p ocess and i s
pa e n is no cons an du ing he ui de elopmen . In g een
de eloping ui s, suga is mainly unloaded ia he symplasm.
Nume ous plasmodesma a and cell connec ions a e p esen a
his s age (Ruan and Pa ick, 1995) bu hen a e p og essi ely
los . Du ing his ea ly phase o de elopmen , only a small
amoun o suc ose is unloaded by he apoplas ic in e ase and
anspo ed in o he ui cells by hexose anspo e s (Nguyen-
Quoc and Foye , 2001;Beckles e al., 2012). Al hough i has been
demons a ed ha suc ose unloads in oma o pe ica p un il 35
DAA, a p ecocious ole o apoplas ic in e ase has howe e
been pos ula ed on he basis o kine ics p ope ies explaining a
mode a e QTL o B ix index (F idman e al., 2004).
Suga Me abolism A he Cell Di ision S age
In g owing ui s, suc ose ep esen s less han 1% DW while
uc ose and glucose a e he main accumula ed soluble suga s (25
and 22% DW; Gilbe , 2009). Glucose and uc ose con en
s ongly inc eased du ing ea ly ui de elopmen al phase.
Mos s udies un il ecen yea ha e ocused on he ipe s age
bu omics analysis need o be conduc ed h oughou ui
de elopmen since se e al in e ac ions may occu be ween he
di e en s ages (Kanayama, 2017). In g een ui s, hexose
phospha es a e mainly used o s a ch syn hesis un il 13 DPA.
S a ch accumula ion in pe ica p and columella issues a his
ea ly s age is a key ac o de e mining he final soluble solid
con en o ma u e ui s (Ca a i and Fe nie, 2006).
The sink s eng h o a de eloping ui depends on bo h sink
ac i i y and sink size, he la e being a unc ion o bo h he
numbe and he size o he ui cells. Acco ding o Ka aoka e al.
(2009), gibbe ellic acid jus a e an hesis can p omo e an
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 15549
cul i a -dependen (A kinson e al., 2011;Sánchez‐Rod ígueze al.,
2012). In con as o salini y and d ough , hea mainly dec eased
he concen a ion o pigmen s and asco bic acid in oma oes (Li
e al., 2012;He nández e al., 2015) and inc eased CO
2
le els
dec eased ca o enoid, polyphenol and fla onoid concen a ions
bu inc eased asco bic acid concen a ion in oma oes (Mama ha
e al., 2014). All hese compounds play an impo an ole in he
final nu i ional and comme cial quali y o oma o and depend on
gene ic, en i onmen al, ag onomic and pos -ha es ac o s (Flo es
e al., 2016). Se e al s udies based on he influence o hese ac o s
on ui composi ion ha e been ca ied ou wi h he aim o
inc easing oma o quali y (Flo es e al., 2016).
In addi ion o he en i onmen al condi ions o which plan s
a e subjec ed du ing hei g ow h, pos -ha es condi ions may
also a ec ui quali y and me abolism. The impac o low
empe a u e s o age on oma o quali y has been ex ensi ely
in es iga ed (Se illano e al., 2009;Luengwilai e al., 2012;
C uz-Mendí il e al., 2015;Wang e al., 2015;Ra o e al., 2018;
Zhang e al., 2019). Among o he s, ea ly ha es ing and cold
s o age nega i ely a ec oma o fla o and dec ease he le els o
a oma compounds (Wang e al., 2015;Ra o e al., 2018). Indeed,
me abolomics da a showed ha 7 amino acids, 27 o ganic acids,
16 o suga s and 22 o he compounds had a significan ly di e en
con en in cold-s o ed oma oes and ansc ip omics da a
showed 1735 di e en ially exp essed genes due o cold s o age
(Zhang e al., 2019). Some p e- ea men s ha e been p oposed o
imp o e oma o ui esis ance o cold s ess such as ozone
exposi ion, high CO
2
ea men , UV-C ho mesis, oxalic acid
applica ion and hea ea men (Mo e i e al., 2010;
Luengwilai e al., 2012;Ma os e al., 2014;Cha les e al., 2015;
C uz-Mendí il e al., 2015;Li e al., 2016b;Sangwanangkul e al.,
2017;Ra o e al., 2018). These ea men s p o ide p o ec ion
om chilling in pa by al e ing le els o ui me aboli es
(Luengwilai e al., 2012;Wang e al., 2015;Sangwanangkul
e al., 2017).
CONCLUSIONS
In his e iew, we ocused on he oma o ui de elopmen and
me abolism.Toma ohaslongbeen hemodel o hes udyo fleshy
ui s and he eme gence o “omics”app oaches (phenomics,
genomics, ansc ip omics, p o eomics, and me abolomics) has
la gely con ibu ed o imp o e ou unde s anding o he gene ic,
ho monal and me abolic ne wo ks ha go e n oma o ui
de elopmen and me abolism. Toma oes a e climac e ic ui s
wi h high le el o heal h-p omo ing compounds. As impo an as
yield imp o emen and s ess esis ance, enhancemen o oma o
ui quali y has gained ex ensi e a en ion. Imp o emen o
oma o fla o and quali y is a challenge o he coming yea s.
The sequencing o oma o genome and genome-wide associa ion
s udies p o ide gene ic insigh s in o he gene ic con ol o
oma o fla o and gi es a oadmap o fla o imp o emen .
Mo eo e , se e al echniques can now be exploi ed o b eeding
supe io oma o a ie ies in he con ex o cu en changing
clima ic condi ions.
AUTHOR CONTRIBUTIONS
MQ and SL designed he ou line o he manusc ip . MQ, SL, FY-L,
TA, and J-PM con ibu ed o w i ing and e isions o he
manusc ip . SB and RB-G con ibu ed o figu e design and
e isions o he manusc ip . All au ho s ead and app o ed he
final manusc ip .
FUNDING
This wo k was suppo ed by unding om he Belgium “Fonds
Na ional de la Reche che Scien ifique (FRS-FNRS)”(g an no.
CDR J.0136.19).
ACKNOWLEDGMENTS
The au ho s a e g a e ul o Jenni e Mach o language
imp o emen . RB-G is g a e ul o he FSR (Fonds special de
eche ché) o he awa d o a esea ch ellowship. This wo k was
published wi h he suppo o he Uni e si y Founda ion
o Belgium.
REFERENCES
Adamski, N. M., Anas asiou, E., E iksson, S., O’Neill, C. M., and Lenha d, M.
(2009). Local ma e nal con ol o seed size by KLUH/CYP78A5-dependen
g ow h signaling. PNAS 106, 20115–20120. doi: 10.1073/pnas.0907024106
Ada o, A., Mandel, T., Min z-O on, S., Venge , I., Le y, D., Ya i , M., e al. (2009).
F ui -su ace fla onoid accumula ion in oma o is con olled by a SlMYB12-
egula ed ansc ip ional ne wo k. PloS Gene . 5, e1000777. doi: 10.1371/
jou nal.pgen.1000777
Aga wal, S., and Rao, A. V. (2000). Toma o lycopene and i s ole in human heal h
and ch onic diseases. CMAJ 163, 739–744.
Alba, R., Pay on, P., Fei, Z., McQuinn, R., Debbie, P., Ma in, G. B., e al. (2005).
T ansc ip ome and selec ed me aboli e analyses e eal mul iple poin s o
e hylene con ol du ing oma o ui de elopmen . Plan Cell 17, 2954–2965.
doi: 10.1105/ pc.105.036053
Albe , E., G icou , J., Be in, N., Bonne oi, J., Pa ey on, S., Tamby, J.-P., e al.
(2016a). Geno ype by wa e ing egime in e ac ion in cul i a ed oma o: lessons
om linkage mapping and gene exp ession. Theo . Appl. Gene . 129, 395–418.
doi: 10.1007/s00122-015-2635-5
Albe , E., Segu a, V., G icou , J., Bonne oi, J., De i o , L., and Causse, M.
(2016b). Associa ion mapping e eals he gene ic a chi ec u e o oma o
esponse o wa e defici : ocus on majo ui quali y ai s. J. Exp. Bo . 67,
6413–6430. doi: 10.1093/jxb/e w411
Alexande , L., and G ie son, D. (2002). E hylene biosyn hesis and ac ion in
oma o: a model o climac e ic ui ipening. J. Exp. Bo . 53, 2039–2055.
doi: 10.1093/jxb/e 072
Alseekh, S., Tohge, T., Wendenbe g, R., Scossa, F., Om anian, N., Li, J., e al. (2015).
Iden ifica ion and mode o inhe i ance o quan i a i e ai loci o seconda y
me aboli e abundance in oma o. Plan Cell 27, 485–512. doi: 10.1105/ pc.114.132266
Alseekh, S., Tong, H., Scossa, F., B o man, Y., Vig oux, F., Tohge, T., e al. (2017).
Canaliza ion o oma o ui me abolism. Plan Cell 29, 2753–2765. doi: 10.1105/
pc.17.00367
Amemiya, T., Kanayama, Y., Yamaki, S., Yamada, K., and Shi a ake, K. (2006).
F ui -specific V-ATPase supp ession in an isense- ansgenic oma o educes
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155416

ui g ow h and seed o ma ion. Plan a 223, 1272–1280. doi: 10.1007/s00425-
005-0176-x
Anas asiou, E., Kenz, S., Ge s ung, M., MacLean, D., Timme , J., Fleck, C., e al.
(2007). Con ol o plan o gan size by KLUH/CYP78A5-dependen
in e cellula signaling. De . Cell 13, 843–856. doi: 10.1016/j.de cel.2007.10.001
A kinson, N. J., Dew, T. P., O fila, C., and U win, P. E. (2011). Influence o
combined bio ic and abio ic s ess on nu i ional quali y pa ame e s in oma o
(Solanum lycope sicum). J. Ag ic. Food Chem. 59, 9673–9682. doi: 10.1021/
j 202081
Azzi, L., Deluche, C., Gé audan , F., F angne, N., Delmas, F., He nould, M., e al.
(2015). F ui g ow h- ela ed genes in oma o. J. Exp. Bo . 66, 1075–1086. doi:
10.1093/jxb/e u527
Baldwin, E. A., Sco , J. W., Shewmake , C. K., and Schuch, W. (2000). Fla o i ia
and oma o a oma: biochemis y and possible mechanisms o con ol o
impo an a oma componen s. Ho Science 35, 1013–1022. doi: 10.21273/
ho sci.35.6.1013
Balles e , A.-R., Tikuno , Y., Mol ho , J., G andillo, S., Viquez-Zamo a, M., de
Vos, R., e al. (2016). Iden ifica ion o loci a ec ing accumula ion o seconda y
me aboli es in oma o ui o a Solanum lycope sicum × Solanum chmielewskii
in og ession line popula ion. F on . Plan Sci. 7, 1428. doi: 10.3389/ pls.2016.
01428
Ba e o, L. S., Cong, B., Wu, F., and Tanksley, S. D. (2006). De elopmen al
cha ac e iza ion o he ascia ed locus and mapping o A abidopsis candida e
genes in ol ed in he con ol o flo al me is em size and ca pel numbe in
oma o. Genome 49, 991–1006. doi: 10.1139/g06-059
Ba y, C. S., and Gio annoni, J. J. (2006). Ripening in he oma o G een- ipe mu an
is inhibi ed by ec opic exp ession o a p o ein ha dis up s e hylene signaling.
P oc. Na l. Acad. Sci. U.S.A. 103, 7923–7928. doi: 10.1073/pnas.0602319103
Bas ías, A., López-Climen , M., Valcá cel, M., Rosello, S., Gómez-Cadenas, A., and
Casa e o, J. A. (2011). Modula ion o o ganic acids and suga con en in
oma o ui s by an abscisic acid- egula ed ansc ip ion ac o . Physiol. Plan .
141, 215–226. doi: 10.1111/j.1399-3054.2010.01435.x
Bauche , G., G enie , S., Samson, N., Segu a, V., Kende, A., Beekwilde , J., e al.
(2017). Iden ifica ion o majo loci and genomic egions con olling acid and
ola ile con en in oma o ui : implica ions o fla o imp o emen . New
Phy ol. 215, 624–641. doi: 10.1111/nph.14615
Beau oi , B. P., Colombié, S., Monie , A., And ieu, M.-H., Biais, B., Béna d, C.,
e al. (2014). Model-assis ed analysis o suga me abolism h oughou oma o
ui de elopmen e eals enzyme and ca ie p ope ies in ela ion o acuole
expansion. Plan Cell 26, 3224–3242. doi: 10.1105/ pc.114.127761
Beckles, D. M., Hong, N., S amo a, L., and Luengwilai, K. (2012). Biochemical
ac o s con ibu ing o oma o ui suga con en : a e iew. F ui s 67, 49–64.
doi: 10.1051/ ui s/2011066
Beme , M., Ka lo a, R., Balles e , A. R., Tikuno , Y. M., Bo y, A. G., Wol e s-A s,
M., e al. (2012). The oma o FRUITFULL homologs TDR4/FUL1 and MBP7/
FUL2 egula e e hylene-independen aspec s o ui ipening. Plan Cell 24,
4437–4451. doi: 10.1105/ pc.112.103283
Biais, B., Béna d, C., Beau oi , B., Colombié, S., P odhomme, D., Ména d, G., e al.
(2014). Rema kable ep oducibili y o enzyme ac i i y p ofiles in oma o ui s
g own unde con as ing en i onmen s p o ides a oadmap o s udies o ui
me abolism. Plan Physiol. 164, 1204–1221. doi: 10.1104/pp.113.231241
Bino, R. J., Ric de Vos, C. H., Liebe man, M., Hall, R. D., Bo y, A., Jonke , H. H.,
e al. (2005). The ligh -hype esponsi e high pigmen -2dg mu a ion o oma o:
al e a ions in he ui me abolome. New Phy ol. 166, 427–438. doi: 10.1111/
j.1469-8137.2005.01362.x
Bollie , N., Sica d, A., Leblond, J., La asse, D., Gonzalez, N., Gé audan , F., e al.
(2018). A -MINI ZINC FINGER2 and Sl-INHIBITOR OF MERISTEM
ACTIVITY, a conse ed missing link in he egula ion o flo al me is em
e mina ion in A abidopsis and oma o. Plan Cell 30, 83–100. doi: 10.1105/
pc.17.00653
Bo ghesi, E., Fe an e, A., Go dillo, B., Rod íguez-Pulido, F. J., Coce a, G.,
T i ellini, A., e al. (2016). Compa a i e physiology du ing ipening in
oma o ich-an hocyanins ui s. Plan G ow h Regul. 80, 207–214. doi:
10.1007/s10725-016-0158-y
Bo y, A., Schijlen, E., and Hall, R. D. (2007). Me abolic enginee ing o fla onoids
in oma o (Solanum lycope sicum): he po en ial o me abolomics.
Me abolomics 3, 399. doi: 10.1007/s11306-007-0074-2
Bo y, A. G., Gómez-Roldán, V., and Hall, R. D. (2010). “S a egies o Op imize he
Fla onoid Con en o Toma o F ui ,”in Recen Ad ances in Polyphenol
Resea ch eds V. La anzio, C. San os‐Buelga, M. T. Esc ibano‐Bailon and V.
La anzio (Ox o d, UK: Blackwell Publishing L d.), p. 138–162. doi: 10.1002/
9781444323375.ch5
Bu a, J. G., and Spaulding, D. W. (1994). Changes in indole-3-ace ic acid and abscisic
acid le els du ing oma o (Lycope sicon esculen um Mill.) ui de elopmen and
ipening. J. Plan G ow h Regul. 13, 163. doi: 10.1007/BF00196382
Bu e y, R. G., Te anishi, R., Fla h, R. A., and Ling, L. C. (1989). “F esh Toma o
Vola iles,”in Fla o Chemis y ACS Symposium Se ies (Wasing on, DC:
Ame ican Chemical Socie y), p. 213–222. doi: 10.1021/bk-1989-0388.ch017
Ca a, B., and Gio annoni, J. J. (2008). Molecula biology o e hylene du ing
oma o ui de elopmen and ma u a ion. Plan Sci. 175, 106–113. doi:
10.1016/j.plan sci.2008.03.021
Ca don, G., Höhmann, S., Klein, J., Ne esheim, K., Saedle , H., and Huijse , P. (1999).
Molecula cha ac e isa ion o he A abidopsis SBP-box genes. Gene 237, 91–104.
doi: 10.1016/S0378-1119(99)00308-X
Ca a a, S., Pa dosi, A., Solda ini, G. F., Tognoni, F., and Guidi, L. (2001).
Pho osyn he ic ac i i y o ipening oma o ui . Pho osyn he ica 39, 75–78.
doi: 10.1023/A:1012495903093
Ca a i, F., and Fe nie, A. R. (2006). Me abolic egula ion unde lying oma o ui
de elopmen . J. Exp. Bo . 57, 1883–1897. doi: 10.1093/jxb/e j020
Ca a i, F., Asis, R., and Fe nie, A. R. (2007). The me abolic shi s unde lying
oma o ui de elopmen . Plan Bio echnol. 24, 45–55. doi: 10.5511/
plan bio echnology.24.45
Ca e a, E., Ruiz-Ri e o, O., Pe es, L. E., A a es, A., and Ga cia-Ma inez, J. L.
(2012). Cha ac e iza ion o he p oce a oma o mu an shows no el unc ions
o he SlDELLA p o ein in he con ol o flowe mo phology, cell di ision and
expansion, and he auxin-signaling pa hway du ing ui -se and de elopmen .
Plan Physiol. 160, 1581–1596. doi: 10.1104/pp.112.204552
Cen eno, D. C., Oso io, S., Nunes-Nesi, A., Be olo, A. L. F., Ca nei o, R. T.,
A aújo, W. L., e al. (2011). Mala e plays a c ucial ole in s a ch me abolism,
ipening, and soluble solid con en o oma o ui and a ec s pos ha es
so ening. Plan Cell 23, 162–184. doi: 10.1105/ pc.109.072231
Chaabouni, S., Jones,B., Delalande, C., Wang, H., Li, Z., Mila, I., e al. (2009).Sl-IAA3,
a oma o Aux/IAA a he c oss oads o auxin and e hylene signalling in ol ed
in di e en ial g ow h. J. Exp. Bo . 60, 1349–1362. doi: 10.1093/jxb/e p009
Chak aba i, M., Zhang, N., Sau age, C., Muños, S., Blanca, J., Cañiza es, J., e al.
(2013). A cy och ome P450 egula es a domes ica ion ai in cul i a ed oma o.
P oc. Na l. Acad. Sci. U. S. A. 110, 17125–17130. doi: 10.1073/pnas.1307313110
Cha les, M. T., Rolland, D., Roussel, D., Me isie , M. J., Cha lebois, D., and A ul, J.
(2015). Assessmen o changes in o ganic acid and suga p ofiles o oma o
ui s induced by u -c ho mesis. Ac a Ho ic. 1079, 159–164. doi: 10.17660/
Ac aHo ic.2015.1079.16
Chung, M.-Y., V ebalo , J., Alba, R., Lee, J., McQuinn, R., Chung, J.-D., e al.
(2010). A oma o (Solanum lycope sicum) APETALA2/ERF gene, SlAP2a, is a
nega i e egula o o ui ipening. Plan J. 64, 936–947. doi: 10.1111/j.1365-
313X.2010.04384.x
Cle enge , J. P., Van Hou en, J., Blackwood, M., Rod íguez, G. R., Jikuma u, Y.,
Kamiya, Y., e al. (2015). Ne wo k analyses e eal shi s in ansc ip p ofiles
and me aboli es ha accompany he exp ession o sun and an elonga ed
oma o ui . Plan Physiol. 168, 1164–1178. doi: 10.1104/pp.15.00379
Cong, B., Liu, J., and Tanksley, S. D. (2002). Na u al alleles a a oma o ui size
quan i a i e ai locus di e by he e och onic egula o y mu a ions. PNAS 99,
13606–13611. doi: 10.1073/pnas.172520999
C uz, A. B., Bianche i, R. E., Al es, F. R. R., Pu ga o, E., Pe es, L. E. P., Rossi, M.,
e al. (2018). Ligh , e hylene and auxin signaling in e ac ion egula es
ca o enoid biosyn hesis du ing oma o ui ipening. F on . Plan Sci. 9,
1370. doi: 10.3389/ pls.2018.01370
C uz-Mendí il, A., López-Valenzuela, J. A., Calde ón-Vázquez, C. L., Vega-
Ga cía,M.O.,Reyes-Mo eno,C.,andValdez-O iz,A.(2015).
T ansc ip ional changes associa ed wi h chilling ole ance and suscep ibili y
in ‘Mic o-Tom’ oma o ui using RNA-Seq. Pos ha es Biol. Technol. 99,
141–151. doi: 10.1016/j.pos ha bio.2014.08.009
D’Amb osio, C., S igliani, A. L., and Gio io, G. (2018). CRISPR/Cas9 edi ing o
ca o enoid genes in oma o. T ansgenic Res. 27, 367–378. doi: 10.1007/s11248-
018-0079-9
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155417
Da ies, J. N., and Hobson, G. E. (1981). The cons i uen s o oma o ui – he
influence o en i onmen , nu i ion, and geno ype. C i . Re . Food Sci. Nu .
15, 205–280. doi: 10.1080/10408398109527317
de Jong, M., Ma iani, C., and V iezen, W. H. (2009). The ole o auxin and
gibbe ellin in oma o ui se . J. Exp. Bo . 60, 1523–1532. doi: 10.1093/jxb/
e p094
Ding, J., Chen, B., Xia, X., Mao, W., Shi, K., Zhou, Y., e al. (2013). Cy okinin-
induced pa henoca pic ui de elopmen in oma o is pa ly dependen on
enhanced gibbe ellin and auxin biosyn hesis. PloS One 8 (7), e70080. doi:
10.1371/jou nal.pone.0070080
Diou , I. A., De i o , L., Bi on, F., Pascual, L., and Causse, M. (2018). Wa e defici
and salini y s ess e eal many specific q l o plan g ow h and ui quali y
ai s in oma o. F on . Plan Sci. 9, 279. doi: 10.3389/ pls.2018.00279
E iksson, E. M., Bo y, A., Manning, K., Ha ison, L., And ews, J., Sil a, J. D., e al.
(2004). E ec o he colo less non- ipening mu a ion on cell wall biochemis y
and gene exp ession du ing oma o ui de elopmen and ipening. Plan
Physiol. 136, 4184–4197. doi: 10.1104/pp.104.045765
Eshed, Y., and Zami , D. (1994). In og essions om Lycope sicon pennellii can
imp o e he soluble-solids yield o oma o hyb ids. Theo e . Appl. Gene . 88,
891–897. doi: 10.1007/BF01254002
Fahad, S., Bajwa, A. A., Nazi , U., Anjum, S. A., Fa ooq, A., Zohaib, A., e al.
(2017). C op p oduc ion unde d ough and hea s ess: plan esponses and
managemen op ions. F on . in Plan Sci. 8, 1147. doi: 10.3389/ pls.2017.01147
FAOSTAT (2019). A ailable a : h p://www. ao.o g/ aos a /en/#home [Accessed
Ap il 15, 2019].
Fei, Z., Tang, X., Alba, R., and Gio annoni, J. (2006). Toma o Exp ession Da abase
(TED): a sui e o da a p esen a ion and analysis ools. Nucleic Acids Res. 34,
D766–D770. doi: 10.1093/na /gkj110
Feng, C. Y., Han, J. X., Han, X. X., and Jiang, J. (2015). Genome wide iden ifica ion,
phylogeny, and exp ession analysis o he SWEET gene amily in oma o. Gene
573, 261–272. doi: 10.1016/j.gene.2015.07.055
Flo es, P., He nández, V., Hellín, P., Fenoll, J., Ca a, J., Mes e, T., e al. (2016).
Me aboli e p ofile o he oma o dwa cul i a Mic o-Tom and compa a i e
esponse o saline and nu i ional s esses wi h ega d o a comme cial cul i a .
J. Sci. Food Ag ic. 96, 1562–1570. doi: 10.1002/js a.7256
F a y, A., Nesbi , T. C., G andillo, S., Knaap, E., Cong, B., Liu, J., e al. (2000).
w2.2: a quan i a i e ai locus key o he e olu ion o oma o ui size. Science
289, 85–88. doi: 10.1126/science.289.5476.85
F ase , P. D., T uesdale, M. R., Bi d, C. R., Schuch, W., and B amley, P. M. (1994).
Ca o enoid biosyn hesis du ing oma o ui de elopmen (e idence o issue-
specific gene exp ession). Plan Physiol. 105, 405–413. doi: 10.1104/
pp.105.1.405
F idman, E., Ca a i, F., Liu, Y.-S., Fe nie, A. R., and Zami , D. (2004). Zooming in
on a quan i a i e ai o oma o yield using in e specific in og essions.
Science 305, 1786–1789. doi: 10.1126/science.1101666
F iedman, M. (2002). Toma o glycoalkaloids: ole in he plan and in he die . J.
Ag ic. Food Chem. 50, 5751–5780. doi: 10.1021/j 020560c
F iedman, M. (2015). Chemis y and an ica cinogenic mechanisms o
glycoalkaloids p oduced by eggplan s, po a oes, and oma oes. J. Ag ic. Food
Chem. 63, 3323–3337. doi: 10.1021/acs.ja c.5b00818
Fujisawa, M., Shima, Y., Higuchi, N., Nakano, T., Koyama, Y., Kasumi, T., e al.
(2011). Di ec a ge s o he oma o- ipening egula o RIN iden ified by
ansc ip ome and ch oma in immunop ecipi a ion analyses. Plan a 235,
1107–1122. doi: 10.1007/s00425-011-1561-2
Ga cía-Hu ado, N., Ca e a, E., Ruiz-Ri e o, O., López-G esa, M. P., Hedden, P.,
Gong, F., e al. (2012). The cha ac e iza ion o ansgenic oma o
o e exp essing gibbe ellin 20-oxidase e eals induc ion o pa henoca pic
ui g ow h, highe yield, and al e a ion o he gibbe ellin biosyn he ic
pa hway. J. Exp. Bo . 63, 5803–5813. doi: 10.1093/jxb/e s229
Ga ceau, D. C., Ba son, M. K., and Pan, I. L. (2017). Va ia ions on a heme in ui
de elopmen : he PLE lineage o MADS-box genes in oma o (TAGL1) and
o he species. Plan a 246, 313–321. doi: 10.1007/s00425-017-2725-5
Ge szbe g, A., and Hna uszko-Konka, K. (2017). Toma o ole ance o abio ic
s ess: a e iew o mos o en enginee ed a ge sequences. Plan G ow h Regul.
83, 175–198. doi: 10.1007/s10725-017-0251-x
Gha bi, E., Ma ínez, J.-P., Benahmed, H., Lepoin , G., Vanpee, B., Quine , M.,
e al. (2017). Inhibi ion o e hylene syn hesis educes sal - ole ance in oma o
wild ela i e species Solanum chilense.J. Plan Physiol. 210, 24–37. doi:
10.1016/j.jplph.2016.12.001
Gilbe , L. (2009l). É ude de la biosyn hèse de l’asco ba e e des mé abolismes
associés chez la Toma e : ôle de la L-galac ono-1,4-lac one déshyd ogénase e
de la GDP-D-mannose-3’,5’-épimé ase. A ailable a : h p://www. heses. /
2009BOR21668 [Accessed May 29, 2019].
Gillaspy, G., Ben-Da id, H., and G uissem, W. (1993). F ui s: a de elopmen al
pe spec i e. Plan Cell 5, 1439–1451. doi: 10.1105/ pc.5.10.1439
Giménez, E., Pineda, B., Capel, J., An ón, M. T., A a és, A., Pé ez-Ma ín, F., e al.
(2010). Func ional analysis o he a lequin mu an co obo a es he essen ial
ole o he ARLEQUIN/TAGL1 gene du ing ep oduc i e de elopmen o
oma o. PloS One 5, e14427. doi: 10.1371/jou nal.pone.0014427
Gimenez, E., Cas añeda, L., Pineda, B., Pan, I. L., Mo eno, V., Angos o, T., e al.
(2016). TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-
LIKE1 MADS-box genes ha e edundan and di e gen unc ions equi ed
o oma o ep oduc i e de elopmen . Plan Mol. Biol. 91, 513–531. doi:
10.1007/s11103-016-0485-4
Gio annoni, J. J. (2004). Gene ic egula ion o ui de elopmen and ipening.
Plan Cell 16, S170–S180. doi: 10.1105/ pc.019158
Gio annoni, J. J. (2007). F ui ipening mu an s yield insigh s in o ipening
con ol. Cu . Opin. in Plan Biol. 10, 283–289. doi: 10.1016/j.pbi.2007.04.008
Golden al-Cohen, S., Is aeli, A., O i, N., and Yasuo , H. (2017). Auxin esponse
dynamics du ing wild- ype and en i e flowe de elopmen in oma o. Plan
Cell Physiol. 58, 1661–1672. doi: 10.1093/pcp/pcx102
Gonzalo, M. J., B ewe , M. T., Ande son, C., Sulli an, D., G ay, S., and an de , K.
E. (2009). Toma o ui shape analysis using mo phome ic and mo phology
a ibu es implemen ed in oma o analyze so wa e p og am. J. Am. Soc.
Ho ic. Sci. 134, 77–87. doi: 10.21273/JASHS.134.1.77
Guillon, F., Philippe, S., Bouche , B., De aux, M.-F., F asse, P., Jones, B., e al.
(2008). Down- egula ion o an Auxin Response Fac o in he oma o induces
modifica ion o fine pec in s uc u e and issue a chi ec u e. J. Exp. Bo . 59,
273–288. doi: 10.1093/jxb/e m323
Guo, M., and Simmons, C. R. (2011). Cell numbe coun s –The w2.2 and CNR
genes and implica ions o con olling plan ui and o gan size. Plan Sci. 181,
1–7. doi: 10.1016/j.plan sci.2011.03.010
Gu , A., and Zami , D. (2004). Unused na u al a ia ion can li yield ba ie s in
plan b eeding. PloS Biol. 2, e245. doi: 10.1371/jou nal.pbio.0020245
Hao, Y., Hu, G., B ei el, D., Liu, M., Mila, I., F asse, P., e al. (2015). Auxin
esponse ac o SlARF2 is an essen ial componen o he egula o y mechanism
con olling ui ipening in oma o. PloS Gene . 11, e1005649. doi: 10.1371/
jou nal.pgen.1005649
He nández, V., Hellín, P., Fenoll, J., and Flo es, P. (2015). Inc eased empe a u e
p oduces changes in he bioac i e composi ion o oma o, depending on i s
de elopmen al s age. J. Ag ic. Food Chem. 63, 2378–2382. doi: 10.1021/j 505507h
He he ing on, S. E., Smillie, R. M., and Da ies, W. J. (1998). Pho osyn he ic
ac i i ies o ege a i e and ui ing issues o oma o. J. Exp. Bo . 49, 1173–1181.
doi: 10.1093/jxb/49.324.1173
Hu, J., Is aeli, A., O i, N., and Sun, T. P. (2018). The in e ac ion be ween DELLA
and ARF/IAA media es c oss alk be ween gibbe ellin and auxin signaling o
con ol ui ini ia ion in oma o. Plan Cell 30, 1710–1728. doi: 10.1105/
pc.18.00363
Huang, Z., and an de Knaap, E. (2011). Toma o ui weigh 11.3 maps close o
ascia ed on he bo om o ch omosome 11. Theo . Appl. Gene . 123, 465–474.
doi: 10.1007/s00122-011-1599-3
Huang, Y.-X., Go o, Y., Nonaka, S., Fukuda, N., Ezu a, H., and Ma suku a, C.
(2015). O e exp ession o he phosphoenolpy u a e ca boxykinase gene
(SlPEPCK)p omo essolublesuga accumula ionin ui andpos -
ge mina ion g ow h o oma o (Solanum lycope sicum L.). Plan Bio echnol.
32, 281–289. doi: 10.5511/plan bio echnology.15.1019a
Ikeda, H., Shibuya, T., Imanishi, S., Aso, H., Nishiyama, M., and Kanayama, Y.
(2016). Dynamic me abolic egula ion by a ch omosome segmen om a wild
ela i e du ing ui de elopmen in a oma o in og ession line, IL8-3. Plan
Cell Physiol. 57, 1257–1270. doi: 10.1093/pcp/pcw075
I kin, M., Seybold, H., B ei el, D., Rogache , I., Mei , S., and Aha oni, A. (2009).
TOMATO AGAMOUS-LIKE 1 is a componen o he ui ipening
egula o y ne wo k. Plan J. 60, 1081–1095. doi: 10.1111/j.1365-
313X.2009.04064.x
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155418
I o, Y., Ki agawa, M., Ihashi, N., Yabe, K., Kimba a, J., Yasuda, J., e al. (2008).
DNA-binding specifici y, ansc ip ional ac i a ion po en ial, and he in
mu a ion e ec o he oma o ui - ipening egula o RIN. Plan J. 55, 212–
223. doi: 10.1111/j.1365-313X.2008.03491.x
I o, Y., Nishizawa-Yokoi, A., Endo, M., Mikami, M., Shima, Y., Nakamu a, N.,
e al. (2017). Re-e alua ion o he in mu a ion and he ole o RIN in he
induc ion o oma o ipening. Na . Plan s 3, 866. doi: 10.1038/s41477-017-
0041-5
Jiang, F., Lopez, A., Jeon, S., de F ei as, S. T., Yu, Q., Wu, Z., e al. (2019).
Disassembly o he ui cell wall by he ipening-associa ed polygalac u onase
and expansin influences oma o c acking. Ho ic. Res. 6, 17. doi: 10.1038/
s41438-018-0105-3
Jones, B., F asse, P., Olmos, E., Zegzou i, H., Li, Z. G., La ché, A., e al. (2002).
Down- egula ion o DR12, an auxin- esponse- ac o homolog, in he oma o
esul s in a pleio opic pheno ype including da k g een and blo chy ipening
ui . Plan J. 32, 603–613. doi: 10.1046/j.1365-313X.2002.01450.x
Jones, M. G. (1987). Gibbe ellins and he p oce a mu an o oma o. Plan a 172,
280–284. doi: 10.1007/BF00394598
Kahlau, S., and Bock, E. (2008). Plas id ansc ip omics o oma o ui
de elopmen and chlo oplas -ch omoplas di e en ia ion: ch omoplas gene
exp ession la gely se es he p oduc ion o a single p o ein. Plan Cell 20, 856–
874. doi: 10.1105/ pc.107.055202
Kanayama, Y. (2017). Suga me abolism and ui de elopmen in he oma o.
Ho i. J. 86, 417–425. doi: 10.2503/ho j.OKD-IR01
Ka lo a, R., Rosin, F. M., Bussche -Lange, J., Pa apuno a, V., Do, P. T., Fe nie, A.
R., e al. (2011). T ansc ip ome and me aboli e p ofiling show ha
APETALA2a is a majo egula o o oma o ui ipening. Plan Cell 23,
923–941. doi: 10.1105/ pc.110.081273
Ka lo a, R., Chapman, N., Da id, K., Angenen , G. C., Seymou , G. B., and de
Maagd, R. A. (2014). T ansc ip ional con ol o fleshy ui de elopmen and
ipening. J. Exp. Bo . 65, 4527–4541. doi: 10.1093/jxb/e u316
Ka aoka, K., Yashi o, Y., Habu, T., Sunamo o, K., and Ki ajima, A. (2009). The
addi ion o gibbe ellic acid o auxin solu ions inc eases suga accumula ion and
sink s eng h in de eloping auxin-induced pa henoca pic oma o ui s. Sci.
Ho ic. 123, 228–233. doi: 10.1016/j.scien a.2009.09.001
Ke any, B. M., Tieman, D. M., Taylo , M. G., Cin, V. D., and Klee, H. J. (2007).
E hylene ecep o deg ada ion con ols he iming o ipening in oma o ui .
Plan J. 51, 458–467. doi: 10.1111/j.1365-313X.2007.03170.x
Kim, J. Y., Kim, S.-K., Jung, J., Jeong, M.-J., and Ryu, C.-M. (2018). Explo ing he
sound-modula ed delay in oma o ipening h ough exp ession analysis o coding
and non-coding RNAs. Ann. Bo . 122, 1231–1244. doi: 10.1093/aob/mcy134
Klä ing, H.-P., Klopo ek, Y., K umbein, A., and Schwa z, D. (2015). The e ec o
educing he hea ing se poin on he pho osyn hesis, g ow h, yield and ui
quali y in g eenhouse oma o p oduc ion. Ag ic. Fo . Me eo ol. 214–215, 178–
188. doi: 10.1016/j.ag o me .2015.08.250
Klee, H. J., and Gio annoni, J. J. (2011). Gene ics and con ol o oma o ui
ipening and quali y a ibu es. Annu. Re . Gene . 45, 41–59. doi: 10.1146/
annu e -gene -110410-132507
Klee, H., and Tieman, D. (2002). The oma o e hylene ecep o gene amily: Fo m
and unc ion. Physiol. Plan . 115, 336–341. doi: 10.1034/j.1399-
3054.2002.1150302.x
Klee, H. J. (2010). Imp o ing he fla o o esh ui s: genomics, biochemis y, and
bio echnology. New Phy ol. 187, 44–56. doi: 10.1111/j.1469-8137.2010.03281.x
Kou, X., Liu, C., Han, L., Wang, S., and Xue, Z. (2016). NAC ansc ip ion ac o s
play an impo an ole in e hylene biosyn hesis, ecep ion and signaling o
oma o ui ipening. Mol. Gene . Genomics 291, 1205–1217. doi: 10.1007/
s00438-016-1177-0
K auss, S., Schni zle , W. H., G assmann, J., and Woi ke, M. (2006). The influence
o di e en elec ical conduc i i y alues in a simplified eci cula ing soilless
sys em on inne and ou e ui quali y cha ac e is ics o oma o. J. Ag ic. Food
Chem. 54, 441–448. doi: 10.1021/j 051930a
Ku, H.-M., Doganla , S., Chen, K.-Y., and Tanksley, S. D. (1999). The gene ic basis
o pea -shaped oma o ui . Theo . Appl. Gene . 99, 844–850. doi: 10.1007/
s001220051304
Kuma , R., Tamboli, V., Sha ma, R., and S eelakshmi, Y. (2018). NAC-NOR
mu a ions in oma o Penja accessions a enua e mul iple me abolic p ocesses
and p olong he ui shel li e. Food Chem. 259, 234–244. doi: 10.1016/
j. oodchem.2018.03.135
Lecou ieux, F., Lecou ieux, D., Vignaul , C., and Del o , S. (2010). A suga -
inducible p o ein kinase, sk1, egula es hexose anspo and suga
accumula ion in g ape ine cells. Plan Physiol. 152, 1096–1106. doi: 10.1104/
pp.109.149138
Lemai e-Chamley, M., Pe i , J., Ga cia, V., Jus , D., Balde , P., Ge main, V., e al.
(2005). Changes in ansc ip ional p ofiles a e associa ed wi h ea ly ui issue
specializa ion in oma o. Plan Physiol. 139, 750–769. doi: 10.1104/
pp.105.063719
Lesebe g, C. H., Eissle , C. L., Wang, X., Johns, M. A., Du all, M. R., and Mao, L.
(2008). In e ac ion s udy o MADS-domain p o eins in oma o. J. Exp. Bo . 59,
2253–2265. doi: 10.1093/jxb/e n094
Le in, I., Gilboa, N., Yeselson, E., Shen, S., and Scha e , A. A. (2000). Fg , a majo
locus ha modula es he uc ose o glucose a io in ma u e oma o ui s.
Theo . Appl. Gene . 100, 256–262. doi: 10.1007/s001220050034
Li, Y., Zhu, B., Xu, W., Zhu, H., Chen, A., Xie, Y., e al. (2007). LeERF1 posi i ely
modula ed e hylene iple esponse on e iola ed seedling, plan de elopmen
and ui ipening and so ening in oma o. Plan Cell Rep. 26, 1999–2008. doi:
10.1007/s00299-007-0394-8
Li, Z., Palme , W. M., Ma in, A. P., Wang, R., Rains o d, F., Jin, Y., e al. (2012).
High in e ase ac i i y in oma o ep oduc i e o gans co ela es wi h enhanced
suc ose impo in o, and hea ole ance o , young ui . J. Exp. Bo . 63, 1155–
1166. doi: 10.1093/jxb/e 329
Li, J., Tao, X., Li, L., Mao, L., Luo, Z., Khan, Z. U., e al. (2016a). Comp ehensi e
RNA-Seq Analysis on he Regula ion o Toma o Ripening by Exogenous
Auxin. PloS One 11, e0156453. doi: 10.1371/jou nal.pone.0156453
Li, P., Yin, F., Song, L., and Zheng, X. (2016b). Alle ia ion o chilling inju y in
oma o ui by exogenous applica ion o oxalic acid. Food Chem. 202, 125–132.
doi: 10.1016/j. oodchem.2016.01.142
Li, J., Tao, X., Bu, J., Ying, T., Mao, L., and Luo, Z. (2017). Global ansc ip ome
p ofiling analysis o e hylene-auxin in e ac ion du ing oma o ui ipening.
Pos ha es Biol. Technol. 130, 28–38. doi: 10.1016/j.pos ha bio.2017.03.021
Li, S., Xu, H., Ju, Z., Cao, D., Zhu, H., Fu, D., e al. (2018a). The RIN-MC usion o
mads-box ansc ip ion ac o s has ansc ip ional ac i i y and modula es
exp ession o many ipening genes. Plan Physiol. 176, 891–909. doi:
10.1104/pp.17.01449
Li, Y., Wang, H., Zhang, Y., and Ma in, C. (2018b). Can he wo ld’s a o i e ui ,
oma o, p o ide an e ec i e biosyn he ic chassis o high- alue me aboli es?.
Plan Cell Rep. 37, 1443–1450. doi: 10.1007/s00299-018-2283-8
Li, S., Chen, K., and G ie son, D. (2019a). A c i ical e alua ion o he ole o
e hylene and MADS ansc ip ion ac o s in he ne wo k con olling fleshy
ui ipening. New Phy ol. 221, 1724–1741. doi: 10.1111/nph.15545
Li, Y., Lu, Y., Li, L., Chu, Z., Zhang, H., Li, H., e al. (2019b). Impai men o
ho mone pa hways esul s in a gene al dis u bance o ui p ima y me abolism
in oma o. Food Chem. 274, 170–179. doi: 10.1016/j. oodchem.2018.08.026
Lin, Z., Hong, Y., Yin, M., Li, C., Zhang, K., and G ie son, D. (2008). A oma o
HD-Zip homeobox p o ein, LeHB-1, plays an impo an ole in flo al
o ganogenesis and ipening. Plan J. 55, 301–310. doi: 10.1111/j.1365-
313X.2008.03505.x
Liu, J., Eck, J. V., Cong, B., and Tanksley, S. D. (2002). A new class o egula o y
genes unde lying he cause o pea -shaped oma o ui . PNAS 99, 13302–
13306. doi: 10.1073/pnas.162485999
Liu, X., Kim, Y. J., Mülle , R., Yumul, R. E., Liu, C., Pan, Y., e al. (2011).
AGAMOUS e mina es flo al s em cell main enance in a abidopsis by di ec ly
ep essing WUSCHEL h ough ec ui men o polycomb g oup p o eins. Plan
Cell 23, 3654–3670. doi: 10.1105/ pc.111.091538
Liu, M., Pi ello, J., Kesa i, R., Mila, I., Rous an, J.-P., Li, Z., e al. (2013). A
dominan ep esso e sion o he oma o Sl-ERF.B3 gene con e s e hylene
hype sensi i i y ia eedback egula ion o e hylene signaling and esponse
componen s. Plan J. 76, 406–419. doi: 10.1111/ pj.12305
Liu, M., Pi ello, J., Che in, C., Rous an, J.-P., and Bouzayen, M. (2015). E hylene
con ol o ui ipening: e isi ing he complex ne wo k o ansc ip ional
egula ion. Plan Physiol. 169, 2380–2390. doi: 10.1104/pp.15.01361
Liu, Z., Alseekh, S., B o man, Y., Zheng, Y., Fei, Z., Tieman, D. M., e al. (2016).
Iden ifica ion o a Solanum pennellii Ch omosome 4 F ui Fla o and
Nu i ional Quali y-Associa ed Me aboli e QTL. F on . Plan Sci. 7, 1671.
doi: 10.3389/ pls.2016.01671
Liu, T., Huang, B., Chen, L., Xian, Z., Song, S., Chen, R., e al. (2018). Genome-
wide iden ifica ion, phylogene ic analysis, and exp ession p ofiling o
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155419
polyamine syn hesis gene amily membe s in oma o. Gene 661, 1–10. doi:
10.1016/j.gene.2018.03.084
Luengwilai, K., Sal ei , M., and Beckles, D. M. (2012). Me aboli e con en o
ha es ed Mic o-Tom oma o (Solanum lycope sicum L.) ui is al e ed by
chilling and p o ec i e hea -shock ea men s as shown by GC–MS me abolic
p ofiling. Pos ha es Biol. Technol. 63, 116–122. doi: 10.1016/j.pos ha bio.
2011.05.014
Luo, J. (2015). Me aboli e-based genome-wide associa ion s udies in plan s. Cu .
Opin. Plan Biol. 24, 31–38. doi: 10.1016/j.pbi.2015.01.006
Lupi, A. C. D., Lia, B. S., G amegna, G., T ench, B., Al es, G. R. R., Dema co, D., e al.
(2019). Solanum lycope sicum GOLDEN2-LIKE 2 ansc ip ion ac o a ec s ui
quali y in a ligh - and auxin-dependen manne . PloS One 14, e212224. doi:
10.1371/jou nal.pone.0212224
Ly o chenko, A., Eickmeie , I., Pons, C., Oso io, S., Szecowka, M., Lehmbe g, K.,
e al. (2011). Toma o ui pho osyn hesis is seemingly unimpo an in p ima y
me abolism and ipening bu plays a conside able ole in seed de elopmen .
Plan Physiol. 157, 1650–1663. doi: 10.1104/pp.111.186874
Ma, N., Feng, H., Meng, X., Li, D., Yang, D., Wu, C., e al. (2014). O e exp ession
o oma o SlNAC1 ansc ip ion ac o al e s ui pigmen a ion and so ening.
BMC Plan Biol. 14, 351. doi: 10.1186/s12870-014-0351-y
Mama ha, H., S ini asa Rao, N. K., Laxman, R. H., Shi ashanka a, K. S., Bha , R.
M., and Pa i h a, K. C. (2014). Impac o ele a ed CO2 on g ow h, physiology,
yield, and quali y o oma o (Lycope sicon esculen um Mill) c . A ka Ashish.
Pho osyn he ica 52, 519–528. doi: 10.1007/s11099-014-0059-0
Manning, K., Tö , M., Poole, M., Hong, Y., Thompson, A. J., King, G. J., e al.
(2006). A na u ally occu ing epigene ic mu a ion in a gene encoding an SBP-
box ansc ip ion ac o inhibi s oma o ui ipening. Na . Gene . 38, 948–
952. doi: 10.1038/ng1841
Ma io i, L., Piccia elli, P., Lomba di, L., and Cecca elli, N. (2011). F ui -se and
ea ly ui g ow h in oma o a e associa ed wi h inc eases in indoleace ic acid,
cy okinin, and bioac i e gibbe ellin con en s. J. Plan G ow h Regul. 30, 405.
doi: 10.1007/s00344-011-9204-1
Ma sic, N. K., Vodnik, D., Mikulic-Pe ko sek, M., Vebe ic, R., and Si celj, H.
(2018). Pho osyn he ic ai s o plan s and he biochemical p ofile o oma o
ui s a e influenced by g a ing, salini y s ess, and g owing season. J. Ag ic.
Food Chem. 66, 5439–5450. doi: 10.1021/acs.ja c.8b00169
Ma í, C., O záez, D., Ellul, P., Mo eno, V., Ca bonell, J., and G anell, A. (2007).
Silencing o DELLA induces acul a i e pa henoca py in oma o ui s. Plan J.
52, 865–876. doi: 10.1111/j.1365-313X.2007.03282.x
Ma í, R., Roselló, S., and Cebolla-Co nejo, J. (2016). Toma o as a sou ce o
ca o enoids and polyphenols a ge ed o cance p e en ion. Cance s (Basel) 8,
E58. doi: 10.3390/cance s8060058
Ma ín-Piza o, C., and Posé, D. (2018). Genome edi ing as a ool o ui
ipening manipula ion. F on . Plan Sci. 9, 1415. doi: 10.3389/ pls.2018.01415
Ma el, C., V ebalo , J., Ta elmeye , P., and Gio annoni, J. J. (2011). The oma o
MADS-box ansc ip ion ac o RIPENING INHIBITOR in e ac s wi h
p omo e s in ol ed in nume ous ipening p ocesses in a COLORLESS
NONRIPENING-dependen manne . Plan Physiol. 157, 1568–1579. doi:
10.1104/pp.111.181107
Ma a, C. I., Fab e, B., Pa sons, H. T., He og, M. L. A. T. M., Van Raemdonck, G.,
Bagge man, G., e al. (2018). E hylene ecep o s, c s and ein2 a ge p o ein
iden ifica ion and quan ifica ion h ough pa allel eac ion moni o ing du ing
oma o ui ipening. F on . Plan Sci. 9, 1626. doi: 10.3389/ pls.2018.01626
Ma as, A. J., Gappe , N. E., Chung, M.-Y., Gio annoni, J. J., and Rose, J. K. (2009).
Biology and gene ic enginee ing o ui ma u a ion o enhanced quali y and
shel -li e. Cu . Opin. in Bio echnol. 20, 197–203. doi: 10.1016/j.copbio.2009.
02.015
Ma as, A. J., Yea s, T. H., Buda, G. J., Zheng, Y., Cha e jee, S., Tohge, T., e al.
(2011). Tissue- and cell- ype specific ansc ip ome p ofiling o expanding
oma o ui p o ides insigh s in o me abolic and egula o y specializa ion and
cu icle o ma ion. Plan Cell 23, 3893–3910. doi: 10.1105/ pc.111.091173
Ma hieu, S., Cin, V. D., Fei, Z., Li, H., Bliss, P., Taylo , M. G., e al. (2009). Fla ou
compounds in oma o ui s: iden ifica ion o loci and po en ial pa hways
a ec ing ola ile composi ion. J. Exp. Bo . 60, 325–337. doi: 10.1093/jxb/e n294
Ma suo, S., Kikuchi, K., Fukuda, M., Honda, I., and Imanishi, S. (2012). Roles and
egula ion o cy okinins in oma o ui de elopmen . J. Exp. Bo . 63, 5569–
5579. doi: 10.1093/jxb/e s207
Ma os, L. M., Mo e i, C. L., Jan, S., Sa gen , S. A., Lima, C. E. P., and Fon enelle,
M. R. (2014). “Chap e 19 - Clima e changes and po en ial impac s on quali y
o ui and ege able c ops,”in Eme ging Technologies and Managemen o
C op S ess Tole ance. Eds.P. Ahmad, and S. Rasool (San Diego:Academic
P ess), p. 467–486. doi: 10.1016/B978-0-12-800876-8.00019-9
McA ee, P., Ka im, S., Scha e , R. J., and Da id, K. (2013). A dynamic in e play
be ween phy oho mones is equi ed o ui de elopmen , ma u a ion, and
ipening. F on . Plan Sci. 4, 79. doi: 10.3389/ pls.2013.00079
McMu chie, E. J., McGlasson, W. B., and Eaks, I. L. (1972). T ea men o ui wi h
p opylene gi es in o ma ion abou he biogenesis o e hylene. Na u e 237, 235–
236. doi: 10.1038/237235a0
Meng, C., Yang, D., Ma, X., Zhao, W., Liang, X., Ma, N., e al. (2016). Supp ession
o oma o SlNAC1 ansc ip ion ac o delays ui ipening. J. Plan Physiol.
193, 88–96. doi: 10.1016/j.jplph.2016.01.014
Minoia, S., Pe ozza, A., D’Ono io, O., Pi on, F., Mosca, G., Sozio, G., e al. (2010).
A new mu an gene ic esou ce o oma o c op imp o emen by TILLING
echnology. BMC Res. No es 3, 69. doi: 10.1186/1756-0500-3-69
Min z-O on, S., Mandel, T., Rogache , I., Feldbe g, L., Lo an, O., Ya i , M., e al.
(2008). Gene exp ession and me abolism in oma o ui su ace issues. Plan
Physiol. 147, 823–851. doi: 10.1104/pp.108.116004
Mi on, D., and Scha e , A. A. (1991). Suc ose phospha e syn hase, suc ose
syn hase, and in e ase ac i i ies in de eloping ui o Lycope sicon
esculen um Mill. and he suc ose accumula ing Lycope sicon hi su um
Humb. and Bonpl. Plan Physiol. 95, 623–627. doi: 10.1104/pp.95.2.623
Mo e i, C. L., Ma os, L. M., Calbo, A. G., and Sa gen , S. A. (2010). Clima e
changes and po en ial impac s on pos ha es quali y o ui and ege able
c ops: a e iew. Food Res. In . 43, 1824–1832. doi: 10.1016/j. ood es.2009.10.013
Moune , F., Moing, A., Ga cia, V., Pe i , J., Maucou , M., Debo de, C., e al.
(2009). Gene and me aboli e egula o y ne wo k analysis o ea ly de eloping
ui issues highligh s new candida e genes o he con ol o oma o ui
composi ion and de elopmen . Plan Physiol. 149, 1505–1528. doi: 10.1104/
pp.108.133967
Moune , F., Moing, A., Kowalczyk, M., Roh mann, J., Pe i , J., Ga cia, V., e al.
(2012). Down- egula ion o a single auxin e flux anspo p o ein in oma o
induces p ecocious ui de elopmen . J. Exp. Bo . 63, 4901–4917. doi: 10.1093/
jxb/e s167
Mu, Q., Huang, Z., Chak aba i, M., Illa-Be engue , E., Liu, X., Wang, Y., e al.
(2017). F ui weigh is con olled by cell size egula o encoding a no el p o ein
ha is exp essed in ma u ing oma o ui s. PloS Gene . 13, e1006930. doi:
10.1371/jou nal.pgen.1006930
Muños, S., Ranc, N., Bo on, E., Bé a d, A., Rolland, S., Du é, P., e al. (2011).
Inc ease in oma o locule numbe is con olled by wo single-nucleo ide
polymo phisms loca ed nea WUSCHEL. Plan Physiol. 156, 2244–2254. doi:
10.1104/pp.111.173997
Mu shed, R., Lopez-Lau i, F., and Sallanon, H. (2013). E ec o wa e s ess on
an ioxidan sys ems and oxida i e pa ame e s in ui s o oma o (Solanum
lycope sicon L, c . Mic o- om). Physiol. Mol. Biol. Plan s 19, 363–378. doi:
10.1007/s12298-013-0173-7
Nadakudu i, S. S., Holdswo h, W. L., Klein, C. L., and Ba y, C. S. (2014). KNOX
genes influence a g adien o ui chlo oplas de elopmen h ough egula ion
o GOLDEN2-LIKE exp ession in oma o. Plan J. 78, 1022–1033. doi: 10.1111/
pj.12529
Nashile i z, S., Melamed-Bessudo, C., Izko ich, Y., Rogache , I., Oso io, S., I kin,
M., e al. (2010). An o ange ipening mu an links plas id NAD(P)H
dehyd ogenase complex ac i i y o cen al and specialized me abolism
du ing oma o ui ma u a ion. Plan Cell 22, 1977–1997. doi: 10.1105/
pc.110.074716
Nguyen, C. V., V ebalo , J., Gappe , N. E., Zheng, Y., Zhong, S., Fei, Z., e al. (2014).
Toma o GOLDEN2-LIKE ansc ip ion ac o s e eal molecula g adien s ha
unc ion du ing ui de elopmen and ipening. Plan Cell 26, 585–601. doi:
10.1105/ pc.113.118794
Nguyen-Quoc, B., and Foye , C. H. (2001). A ole o “ u ile cycles”in ol ing
in e ase and suc ose syn hase in suc ose me abolism o oma o ui . J. Exp.
Bo . 52, 881–889. doi: 10.1093/jexbo /52.358.881
Ni sch, L., Kohlen, W., Oplaa , C., Cha nikho a, T., C is escu, S., Michieli, P., e al.
(2012). ABA-deficiency esul s in educed plan and ui size in oma o. J.
Plan Physiol. 169, 878–883. doi: 10.1016/j.jplph.2012.02.004
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155420
N agkas, N., Wol e ing, E., Nicole, C., Lab ie, C., and Ma celis, L. F. M. (2019). Ligh
egula ion o i amin C in oma o ui is media ed h ough pho osyn hesis.
En i on. Exp. Bo . 158, 180–188. doi: 10.1016/j.en expbo .2018.12.002
Obiadalla-Ali, H., Fe nie, A. R., Ly o chenko, A., Kossmann, J., and Lloyd, J. R.
(2004). Inhibi ion o chlo oplas ic uc ose 1,6-bisphospha ase in oma o ui s
leads o dec eased ui size, bu only small changes in ca bohyd a e
me abolism. Plan a 219, 533–540. doi: 10.1007/s00425-004-1257-y
Ob ouche a, N. V. (2014). Ho monal egula ion du ing plan ui de elopmen .
Russian J. De . Biol. 45, 11–21. doi: 10.1134/S1062360414010068
Odanaka, S., Benne , A. B., and Kanayama, Y. (2002). Dis inc physiological oles
o uc okinase isozymes e ealed by gene-specific supp ession o F k1 and
F k2 exp ession in Toma o. Plan Physiol. 129, 1119–1126. doi: 10.1104/
pp.000703
Olimpie i, I., Caccia, R., Pica ella, M. E., Pucci, A., San angelo, E., So essi, G. P.,
e al. (2011). Cons i u i e co-supp ession o he GA 20-oxidase1 gene in
oma o leads o se e e de ec s in ege a i e and ep oduc i e de elopmen .
Plan Sci. 180, 496–503. doi: 10.1016/j.plan sci.2010.11.004
Oso io, S., Alba, R., Damasceno, C. M. B., Lopez-Casado, G., Lohse, M., Zano , M.
I., e al. (2011). Sys ems biology o oma o ui de elopmen : combined
ansc ip , p o ein, and me aboli e analysis o oma o ansc ip ion ac o
(no , in)andE hylene Recep o (N ) mu an s e eals no el egula o y
in e ac ions. Plan Physiol. 157, 405–425. doi: 10.1104/pp.111.175463
Oso io, S., Scossa, F., and Fe nie, A. (2013). Molecula egula ion o ui ipening.
F on . Plan Sci. 4, 198. doi: 10.3389/ pls.2013.00198
Pan, I. L., McQuinn, R., Gio annoni, J. J., and I ish, V. F. (2010). Func ional
di e sifica ion o AGAMOUS lineage genes in egula ing oma o flowe and
ui de elopmen . J. Exp. Bo . 61, 1795–1806. doi: 10.1093/jxb/e q046
Pa anè, C., T ingali, S., and So ino, O. (2011). E ec s o defici i iga ion on
biomass, yield, wa e p oduc i i y and ui quali y o p ocessing oma o unde
semi-a id Medi e anean clima e condi ions. Sci. Ho ic. 129, 590–596. doi:
10.1016/j.scien a.2011.04.030
Pa ison, R. J., and Ca alá, C. (2012). E alua ing auxin dis ibu ion in oma o
(Solanum lycope sicum) h ough an analysis o he PIN and AUX/LAX gene
amilies. Plan J. 70, 585–598. doi: 10.1111/j.1365-313X.2011.04895.x
Pem, D., and Jeewon, R. (2015). F ui and ege able in ake: benefi s and p og ess
o nu i ioneduca ion in e en ions- na a i e e iew a icle. I an J. Public
Heal h 44, 1309–1321.
Pé ez-Ma ín, F., Yus e-Lisbona, F. J., Pineda, B., Anga i a-Díaz, M. P., Ga cía-
Sogo, B., An ón, T., e al. (2017). A collec ion o enhance ap inse ional
mu an s o unc ional genomics in oma o. Plan Bio echnol. J. 15, 1439–1452.
doi: 10.1111/pbi.12728
Pesa esi, P., Mizzo i, C., Colombo, M., and Masie o, S. (2014). Gene ic egula ion
and s uc u al changes du ing oma o ui de elopmen and ipening. F on .
Plan Sci. 5, 124. doi: 10.3389/ pls.2014.00124
Pnueli, L., Ha e en, D., Rounsley, S. D., Yano sky, M. F., and Li schi z, E. (1994).
Isola ion o he oma o AGAMOUS gene TAG1 and analysis o i s homeo ic ole
in ansgenic plan s. Plan Cell 6, 163–173. doi: 10.1105/ pc.6.2.163
Powell, A. L. T., Nguyen, C. V., Hill, T., Chen, K. L., Figue oa-Balde as, R., Ak as,
H., e al. (2012). Uni o m ipening encodes a Golden 2-like ansc ip ion ac o
egula ing oma o ui chlo oplas de elopmen . Science 336, 1711–1715. doi:
10.1126/science.1222218
Qin, G., Wang, Y., Cao, B., Wang, W., and Tian, S. (2012). Un a eling he
egula o y ne wo k o he MADS box ansc ip ion ac o RIN in ui ipening.
Plan J. 70, 243–255. doi: 10.1111/j.1365-313X.2011.04861.x
Ra o, A., Baiamon e, I., Na do, N., Nicoli, S., Mone a, E., Pepa aio, M., e al.
(2018). Impac o ea ly ha es ing and wo cold s o age echnologies on ea ing
quali y o ed ipe oma oes. Eu . Food Res. Technol. 244, 805–818. doi:
10.1007/s00217-017-2996-x
Raiola, A., Rigano, M. M., Calafio e, R., F uscian e, L., and Ba one, A. (2014).
Enhancing he heal h-p omo ing e ec s o oma o ui o bio o ified ood.
Media o s Inflamma ion 2014. doi: 10.1155/2014/139873
Rambla, J. L., Tikuno , Y. M., Mon o e, A. J., Bo y, A. G., and G anell, A. (2014).
The expanded oma o ui ola ile landscape. J. Exp. Bo . 65, 4613–4623. doi:
10.1093/jxb/e u128
Ren, Z., and Wang, X. (2016). SlTIR1 is in ol ed in c oss alk o phy oho mones,
egula es auxin-induced oo g ow h and s imula es s enospe moca pic
ui o ma ion in oma o. Plan Sci. 253, 13–20. doi: 10.1016/j.plan sci.2016.
09.005
Ren, Z., Li, Z., Miao, Q., Yang, Y., Deng, W., and Hao, Y. (2011). The auxin
ecep o homologue in Solanum lycope sicum s imula es oma o ui se and
lea mo phogenesis. J. Exp. Bo . 62, 2815–2826. doi: 10.1093/jxb/e q455
Rod íguez, G. R., Muños, S., Ande son, C., Sim, S.-C., Michel, A., Causse, M., e al.
(2011). Dis ibu ion o SUN, OVATE, LC, and FAS in he oma o ge mplasm
and he ela ionship o ui shape di e si y. Plan Physiol. 156, 275–285. doi:
10.1104/pp.110.167577
Rod íguez-Leal, D., Lemmon, Z. H., Man, J., Ba le , M. E., and Lippman, Z. B.
(2017). Enginee ing quan i a i e ai a ia ion o c op imp o emen by
genome edi ing. Cell 171, 470–480.e8. doi: 10.1016/j.cell.2017.08.030
Ro han, C., Diou , I., and Causse, M. (2019). T ai disco e y and edi ing in oma o.
Plan J. 97, 73–90. doi: 10.1111/ pj.14152
Rounis, V., Ska mou sos, K., Tsaniklidis, G., Nikoloudakis, N., Delis, C.,
Ka apanos, I., e al. (2015). Seeded and pa henoca pic che y oma o ui s
exhibi simila suc ose, glucose, and uc ose le els, despi e dissimila i ies in
UGPase and SPS gene exp ession and enzyme ac i i y. J. Plan G ow h Regul.
34, 47–56. doi: 10.1007/s00344-014-9441-1
Ruan, Y.-L., and Pa ick, J. W. (1995). The cellula pa hway o pos phloem suga
anspo in de eloping oma o ui . Plan a 196, 434–444. doi: 10.1007/
BF00203641
Sánchez-Rod íguez, E., Ley a, R., Cons án-Aguila , C., Rome o, L., and Ruiz, J. M.
(2012a). G a ing unde wa e s ess in oma o che y: imp o ing he ui yield
and quali y. Ann. Appl. Biol. 161, 302–312. doi: 10.1111/j.1744-
7348.2012.00574.x
Sánchez-Rod íguez, E., Ruiz, J. M., Fe e es, F., and Mo eno, D. A. (2012b). Phenolic
p ofiles o che y oma oes as influenced by hyd ic s ess and oo s ock
echnique. Food Chem. 134, 775–782. doi: 10.1016/j. oodchem.2012.02.180
Saga , M., Che in, C., Mila, I., Hao, Y., Rous an, J.-P., Benichou, M., e al. (2013).
SlARF4, an auxin esponse ac o in ol ed in he con ol o suga me abolism
du ing oma o ui de elopmen . Plan Physiol. 161, 1362–1374. doi: 10.1104/
pp.113.213843
Sago , G. H. M., Be be ich, T., Tanaka, S., Nishiyama, M., Kanayama, Y., Kojima,
S., e al. (2016). A no el s a egy o p oduce swee e oma o ui s wi h high
suga con en s by ui -specific exp ession o a single bZIP ansc ip ion ac o
gene. Plan Bio echnol. J. 14, 1116–1126. doi: 10.1111/pbi.12480
Sai o, T., Fukuda, N., Ma suku a, C., and Nishimu a, S. (2009). E ec s o salini y
on dis ibu ion o pho osyn ha es and ca bohyd a e me abolism in oma o
g own using nu ien film echnique. J. Jpn. Soc Ho ic. Sci. 78, 90–96. doi:
10.2503/jjshs1.78.90
Saliba-Colombani, V., Causse, M., Langlois, D., Philouze, J., and Bu e , M. (2001).
Gene ic analysis o o ganolep ic quali y in esh ma ke oma o. 1. Mapping
QTLs o physical and chemical ai s. Theo . Appl. Gene . 102, 259–272. doi:
10.1007/s001220051643
Sangwanangkul, P., Bae, Y.-S., Lee, J.-S., Choi, H.-J., Choi, J.-W., and Pa k, M.-H.
(2017). Sho - e m p e ea men wi h high CO2 al e s o ganic acids and
imp o es che y oma o quali y du ing s o age. Ho ic. En i on. Bio echnol.
58, 127–135. doi: 10.1007/s13580-017-0198-x
Scha e , A. A., Pe eiko , M., Mi on, D., Fogelman, M., Spiegelman, M., Bnei-
Moshe, Z., e al. (1998). Modifica ion o ca bohyd a e con en in de eloping
oma o ui . Ho Science 34, 1024–1027.
Schaue , N., Zami , D., and Fe nie, A. R. (2005). Me abolic p ofiling o lea es and
ui o wild species oma o: a su ey o he Solanum lycope sicum complex. J.
Exp. Bo . 56, 297–307. doi: 10.1093/jxb/e i057
Schijlen, E. G. W. M., Beekwilde , J., Hall, R. D., and an de Mee , I. M. (2008).
Boos ing beneficial phy ochemicals in ege able c op plan s. CAB Re .:
Pe spec .InAg ic.Ve .Sci.Nu .Na u alResou .3, 21. doi: 10.1079/
PAVSNNR20083025
Schni zle , W. H., and K auss, S. (2010). Quali y and heal h p omo ing
compounds o oma o ui (Lycope sicum esculen um Mill) unde salini y.
Ac a Ho ic. 856, 21–30. doi: 10.17660/Ac aHo ic.2010.856.2
Schou en, R. E., Wol e ing, E. J., and Tijskens, L. M. M. (2016). Suga and acid
in e con e sion in oma o ui s based on biopsy sampling o locule gel and
pe ica p issue. Pos ha es Biol. Technol. 111, 83–92. doi: 10.1016/
j.pos ha bio.2015.07.032
Sch oede ,J.I.,Delhaize,E.,F omme ,W.B.,e al.(2013).Usingmem b ane
anspo e s o imp o e c ops o sus ainable ood p oduc ion. Na u e 497, 60–66.
Se illano, L., Sanchez-Balles a, M. T., Romoja o, F., and Flo es, F. B. (2009).
Physiological, ho monal and molecula mechanisms egula ing chilling inju y
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155421

in ho icul u al species. Pos ha es echnologies applied o educe i s impac .
J. Sci. Food Ag ic. 89, 555–573. doi: 10.1002/js a.3468
Seymou , G. B., Chapman, N. H., Chew, B. L., and Rose, J. K. C. (2013). Regula ion
o ipening and oppo uni ies o con ol in oma o and o he ui s. Plan
Bio echnol. J. 11, 269–278. doi: 10.1111/j.1467-7652.2012.00738.x
Shammai, A., Pe eiko , M., Yeselson, Y., Faigenboim, A., Moy-Komemi, M., e al.
(2018). Na u al gene ic a ia ion o exp ession o a SWEET anspo e
among wild species o Solanum lycope sicum ( oma o) de e mines he
hexose composi ion o ipening oma o ui . Plan J. 96, 343–357. doi:
10.1111/ pj.14035
Shao, G., Wang, M., Liu, N., Yuan, M., Kuma , P., and She, D.-L. (2014). G ow h
and comp ehensi e quali y index o oma o unde ain shel e s in eesponse o
di e en i iga ion and d ainage ea men s. Sci. Wo ld J. doi: 10.1155/2014/
457937
Shima, Y., Ki agawa, M., Fujisawa, M., Nakano, T., Ka o, H., Kimba a, J., e al.
(2013). Toma o FRUITFULL homologues ac in ui ipening ia o ming
MADS-box ansc ip ion ac o complexes wi h RIN. Plan Mol. Biol. 82, 427–
438. doi: 10.1007/s11103-013-0071-y
Shin, J.-H., Mila, I., Liu, M., Rod igues, M. A., Ve noux, T., Pi ello, J., e al. (2019).
The RIN- egula ed Small Auxin-Up RNA SAUR69 is in ol ed in he un ipe-
o- ipe phase ansi ion o oma o ui ia enhancemen o he sensi i i y o
e hylene. New Phy ol. 222, 820–836. doi: 10.1111/nph.15618
Shinozaki, Y., Hao, S., Kojima, M., Sakakiba a, H., Ozeki-Iida, Y., Zheng, Y., e al.
(2015). E hylene supp esses oma o (Solanum lycope sicum) ui se h ough
modifica ion o gibbe ellin me abolism. Plan J. 83, 237–251. doi: 10.1111/
pj.12882
Shinozaki, Y., Ezu a, H., and A iizumi, T. (2018a). The ole o e hylene in he
egula ion o o a y senescence and ui se in oma o (Solanum lycope sicum).
Plan Signaling Beha . 13, e1146844. doi: 10.1080/15592324.2016.1146844
Shinozaki, Y., Nicolas, P., Fe nandez-Pozo, N., Ma, Q., E anich, D. J., Shi, Y., e al.
(2018b). High- esolu ion spa io empo al ansc ip ome mapping o oma o
ui de elopmen and ipening. Na . Commun. 9, 364. doi: 10.1038/s41467-
017-02782-9
Shinozaki, Y., Ezu a, K., Hu, J., Okabe, Y., Béna d, C., P odhomme, D., e al.
(2018c). Iden ifica ion and unc ional s udy o a mild allele o SlDELLA gene
con e ing he po en ial o imp o ed yield in oma o. Sci. Rep. 8, 12043. doi:
10.1038/s41598-018-30502-w
Snowden, C. J., Thomas, B., Bax e , C. J., Smi h, J. A. C., and Swee lo e, L. J.
(2015). A onoplas Glu/Asp/GABA exchange ha a ec s oma o ui amino
acid composi ion. Plan J. 81, 651–660. doi: 10.1111/ pj.12766
Somssich, M., Je, B. I., Simon, R., and Jackson, D. (2016). CLAVATA-WUSCHEL
signaling in he shoo me is em. De elopmen 143, 3238–3248. doi: 10.1242/
de .133645
So equie a, A., Fe a o, G., Boggio, S. B., and Valle, E. M. (2010). F ee amino acid
p oduc ion du ing oma o ui ipening: a ocus on L-glu ama e. Amino Acids
38, 1523–1532. doi: 10.1007/s00726-009-0373-1
Soyk, S., Lemmon, Z. H., O ed, M., Fishe , J., Libe a o e, K. L., Pa k, S. J., e al.
(2017). Bypassing nega i e epis asis on yield in oma o imposed by a
domes ica ion gene. Cell 169, 1142–1155.e12. doi: 10.1016/j.cell.2017.04.032
S i as a a, A., and Handa, A. K. (2005). Ho monal egula ion o oma o ui
de elopmen : A Molecula pe spec i e. J. Plan G ow h Regul. 24, 67–82. doi:
10.1007/s00344-005-0015-0
Su, L., Bassa, C., Aud an, C., Mila, I., Chenicle , C., Che alie , C., e al. (2014). The
auxin Sl-IAA17 ansc ip ional ep esso con ols ui size ia he egula ion
o endo eduplica ion- ela ed cell expansion. Plan Cell Physiol. 55, 1969–1976.
doi: 10.1093/pcp/pcu124
Sun, B., Xu, Y., Ng, K.-H., and I o, T. (2009). A iming mechanism o s em cell
main enance and di e en ia ion in he A abidopsis flo al me is em. Genes De .
23, 1791–1804. doi: 10.1101/gad.1800409
Sun, L., Sun, Y., Zhang, M., Wang, L., Ren, J., Cui, M., e al. (2012). Supp ession o
9-cis-epoxyca o enoid dioxygenase, which encodes a key enzyme in abscisic
acid biosyn hesis, zl e s ui ex u e in ansgenic oma o. Plan Physiol. 158,
283–298. doi: 10.1104/pp.111.186866
Sun, B., Looi, L.-S., Guo, S., He, Z., Gan, E.-S., Huang, J., e al. (2014). Timing
mechanism dependen on cell di ision is in oked by polycomb e ic ion in
plan s em cells. Science 343, 1248559. doi: 10.1126/science.1248559
Su esh, B. V., Roy, R., Sahu, K., Mis a, G., and Cha opadhyay, D. (2014). Toma o
genomic esou ces da abase: an in eg a ed eposi o y o use ul oma o genomic
in o ma ion o basic and applied esea ch. PloS One 9, e86387. doi: 10.1371/
jou nal.pone.0086387
Tadmo , Y., F idman, E., Gu , A., La ko , O., Las ochkin, E., Ra id, U., e al.
(2002). Iden ifica ion o malodo ous, a wild species allele a ec ing oma o
a oma ha was aelec ed agains du ing domes ica ion. J. Ag ic. Food Chem. 50,
2005–2009. doi: 10.1021/j 011237x
Tamasi, G., Pa dini, A., Bonechi, C., Dona i, A., Pessina, F., Ma colongo, P., e al.
(2019). Cha ac e iza ion o nu aceu ical componen s in oma o pulp, skin and
locula gel. Eu . Food Res. Technol. 245, 907–918. doi: 10.1007/s00217-019-
03235-x
Tanksley, S. D. (2004). The gene ic, de elopmen al, and molecula bases o ui
size and shape a ia ion in oma o. Plan Cell 16, S181–S189. doi: 10.1105/
pc.018119
The Toma o Genome Conso ium (2012). The oma o genome sequence p o ides
insigh s in o fleshy ui e olu ion. Na u e 485, 635–641. doi: 10.1038/
na u e11119
Tieman, D. M., Zeigle , M., Schmelz, E. A., Taylo , M. G., Bliss, P., Ki s , M., e al.
(2006). Iden ifica ion o loci a ec ing fla ou ola ile emissions in oma o
ui s. J. Exp. Bo . 57, 887–896. doi: 10.1093/jxb/e j074
Tieman, D., Zhu, G., Resende, M. F. R., Lin, T., Nguyen, C., Bies, D., e al. (2017). A
chemical gene ic oadmap o imp o ed oma o fla o . Science 355, 391–394.
doi: 10.1126/science.aal1556
Tigchelaa , E. C., Tomes, M., Ke , M., and Ba man, R. (1973). A new ui
ipening mu an , non- ipening (no ).Rep. Toma o Gene . Coop 23, 33.
Tohge, T., and Fe nie, A. R. (2015). Me abolomics-inspi ed insigh in o
de elopmen al, en i onmen al and gene ic aspec s o oma o ui chemical
composi ion and quali y. Plan Cell Physiol. 56, 1681–1696. doi: 10.1093/pcp/
pc 093
Tohge, T., de Souza, L. P., and Fe nie, A. R. (2017). Cu en unde s anding o he
pa hways o fla onoid biosyn hesis in model and c op plan s. J. Exp. Bo . 68,
4013–4028. doi: 10.1093/jxb/e x177
Toma o Gene ics Resou ce Cen e (2019). A ailable a : h ps:// g c.ucda is.edu/
[Accessed Ap il 16, 2019].
Tsaniklidis, G., Ko si as, A., Tsa ou os, A., Roussos, P. A., Ai alakis, G., Ka inakis,
P., e al. (2016). Spa ial and empo al dis ibu ion o genes in ol ed in
polyamine me abolism du ing oma o ui de elopmen . Plan Physiol.
Biochem. 100, 27–36. doi: 10.1016/j.plaphy.2016.01.001
Van de Poel, B., Bulens, I., Ma koula, A., He og, M. L. A. T. M., D eesen, R.,
Wi z, M., e al. (2012). Ta ge ed sys ems biology p ofiling o oma o ui
e eals coo dina ion o he yang cycle and a dis inc egula ion o e hylene
biosyn hesis du ing pos climac e ic ipening. Plan Physiol. 160, 1498–1514.
doi: 10.1104/pp.112.206086
an de Knaap, E., Chak aba i, M., Chu, Y. H., Cle enge , J. P., Illa-Be engue , E.,
Huang, Z., e al. (2014). Wha lies beyond he eye: he molecula mechanisms
egula ing oma o ui weigh and shape. F on . Plan Sci. 5, 227. doi: 10.3389/
pls.2014.00227
Van Meuleb oek, L., Bussche, J. V., De Cle cq, N., S eppe, K., and Vanhaecke, L.
(2015). A me abolomics app oach o un a el he egula ing ole o
phy oho mones owa ds ca o enoid me abolism in oma o ui .
Me abolomics 11, 667–683. doi: 10.1007/s11306-014-0728-9
Viuda-Ma os, M., Sanchez-Zapa a, E., Sayas-Ba be á, E., Send a, E., Pé ez-
Ál a ez, J. A., and Fe nández-López, J. (2014). Toma o and oma o
byp oduc s. Human heal h benefi s o lycopene and i s applica ion o mea
p oduc s: a e iew. C i . Re . In Food Sci. Nu . 54, 1032–1049. doi: 10.1080/
10408398.2011.623799
Vogel, J. T., Tieman, D. M., Sims, C. A., Odabasi, A. Z., Cla k, D. G., and Klee, H. J.
(2010). Ca o enoid con en impac s fla o accep abili y in oma o (Solanum
lycope sicum). J. Sci. Food Ag ic. 90, 2233–2240. doi: 10.1002/js a.4076
V ebalo , J., Ruezinsky, D., Padmanabhan, V., Whi e, R., Med ano, D., D ake, R.,
e al. (2002). A MADS-box gene necessa y o ui ipening a he oma o
ipening-inhibi o ( in) locus. Science 296, 343–346. doi: 10.1126/
science.1068181
V ebalo , J., Pan, I. L., A oyo, A. J. M., McQuinn, R., Chung, M., Poole, M., e al.
(2009). Fleshy ui expansion and ipening a e egula ed by he oma o
SHATTERPROOF Gene TAGL1.Plan Cell 21, 3041–3062. doi: 10.1105/
pc.109.066936
Wang, H., Schaue , N., Usadel, B., F asse, P., Zouine, M., He nould, M., e al.
(2009). Regula o y ea u es unde lying pollina ion-dependen and
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155422
-independen oma o ui se e ealed by ansc ip and p ima y me aboli e
p ofiling. Plan Cell 21, 1428–1452. doi: 10.1105/ pc.108.060830
Wang, S., Lu, G., Hou, Z., Luo, Z., Wang, T., Li, H., e al. (2014). Membe s o he
oma o FRUITFULL MADS-box amily egula e s yle abscission and ui
ipening. J. Exp. Bo . 65, 3005–3014. doi: 10.1093/jxb/e u137
Wang, L., Baldwin, E. A., Zhao, W., Plo o, A., Sun, X., Wang, Z., e al. (2015).
Supp ession o ola ile p oduc ion in oma o ui exposed o chilling
empe a u e and alle ia ion o chilling inju y by a p e-chilling hea ea men .
LWT - Food Sci. Technol. 62, 115–121. doi: 10.1016/j.lw .2014.12.062
Wang,Y.,Luo,Z.,Lu,C.,Zhou,R.,Zhang,H.,Zhao,L.,e al.(2019).
T ansc ip ome p ofiles e eal new egula o y ac o s o an hocyanin
accumula ion in a no el pu ple-colo ed che y oma o cul i a Jinling Moyu.
Plan G ow h Regul. 87, 9–18. doi: 10.1007/s10725-018-0444-y
Wei, Z., Du, T., Li, X., Fang, L., and Liu, F. (2018). In e ac i e e ec s o ele a ed
CO2 and N e iliza ion on yield and quali y o oma o g own unde educed
i iga ion egimes. F on . Plan Sci. 9, 328. doi: 10.3389/ pls.2018.00328
Wu, S., Xiao, H., Cab e a, A., Meulia, T., and an de Knaap, E. (2011). SUN
egula es ege a i e and ep oduc i e o gan shape by changing cell di ision
pa e ns. Plan Physiol. 157, 1175–1186. doi: 10.1104/pp.111.181065
Xiao, J., Li, H., Zhang, J., Chen, R., Zhang, Y., Ouyang, B., e al. (2006). Dissec ion
o GA 20-oxidase membe s a ec ing oma o mo phology by RNAi-media ed
silencing. Plan G ow h Regul. 50, 179–189. doi: 10.1007/s10725-006-9117-3
Xiao,H.,Rado ich,C.,Wel y,N.,Hsu,J.,Li,D.,Meulia,T.,e al.(2009).In eg a iono
oma o ep oduc i e de elopmen al landma ks and exp ession p ofiles, and he
e ec o SUN on ui shape. BMC Plan Biol. 9, 49. doi: 10.1186/1471-2229-9-49
Xu, H. L., Gau hie , L., Desja din, Y., and Gosselin, A. (1997). Pho osyn hesis in
lea es, ui s, s em and pe ioles o g eenhouse-g own oma o plan s.
Pho osyn he ica 33, 113–123. doi: 10.1023/A:1022135507700
Xu, C., Libe a o e, K. L., MacAlis e , C. A., Huang, Z., Chu, Y.-H., Jiang, K., e al.
(2015). A cascade o a abinosyl ans e ases con ols shoo me is em size in
oma o. Na . Gene . 47, 784–792. doi: 10.1038/ng.3309
Yáñez, M., Cáce es, S., O ellana, S., Bas ías, A., Ve dugo, I., Ruiz-La a, S., e al.
(2009). An abio ic s ess- esponsi e bZIP ansc ip ion ac o om wild and
cul i a ed oma oes egula es s ess- ela ed genes. Plan Cell Rep. 28, 1497–
1507. doi: 10.1007/s00299-009-0749-4
Yano sky, M. F., Ma, H., Bowman, J. L., D ews, G. N., Feldmann, K. A., and
Meye owi z, E. M. (1990). The p o ein encoded by he A abidopsis homeo ic
gene agamous esembles ansc ip ion ac o s. Na u e 346, 35–39. doi: 10.1038/
346035a0
Yelle, S., Che ela , R. T., Do ais, M., DeVe na, J. W., and Benne , A. B. (1991).
Sink me abolism in oma o ui : IV. Gene ic and biochemical analysis o
suc ose accumula ion. Plan Physiol. 95, 1026–1035. doi: 10.1104/pp.95.4.1026
Yen, H. C., Lee, S., Tanksley, S. D., Lanahan, M. B., Klee, H. J., and Gio annoni, J. J.
(1995). The oma o Ne e - ipe locus egula es e hylene-inducible gene
exp ession and is linked o a homolog o he A abidopsis ETR1 gene. Plan
Physiol. 107, 1343–1353. doi: 10.1104/pp.107.4.1343
Yen, H. C., Shel on, B. A., Howa d, L. R., Lee, S., V ebalo , J., and Gio annoni, J. J.
(1997). The oma o high-pigmen (hp) locus maps o ch omosome 2 and
influences plas ome copy numbe and ui quali y. Theo . Appl. Gene . 95,
1069–1079. doi: 10.1007/s001220050664
Yuan, X.-Y., Wang, R.-H., Zhao, X.-D., Luo, Y.-B., and Fu, D.-Q. (2016). Role o
he oma o Non-Ripening mu a ion in egula ing ui quali y elucida ed using
iTRAQ p o ein p ofile analysis. PloS One 11, e0164335. doi: 10.1371/
jou nal.pone.0164335
Zano , M. I., Rambla, J.-L., Chaïb, J., S eppa, A., Medina, A., G anell, A., e al. (2009).
Me abolic cha ac e iza ion o loci a ec ing senso y a ibu es in oma o allows an
assessmen o he influence o he le els o p ima y me aboli es and ola ile
o ganic con en s. J. Exp. Bo . 60, 2139–2154. doi: 10.1093/jxb/e p086
Zhang, M., Yuan, B., and Leng, P. (2009). The ole o ABA in igge ing e hylene
biosyn hesis and ipening o oma o ui . J. Exp. Bo . 60, 1579–1588. doi:
10.1093/jxb/e p026
Zhang, Y., Bu elli, E., Alseekh, S., Tohge, T., Rallapalli, G., Luo, J., e al. (2015).
Mul i-le el enginee ing acili a es he p oduc ion o phenylp opanoid
compounds in oma o. Na . Commun. 6, 8635. doi: 10.1038/ncomms9635
Zhang, W.-F., Gong, Z.-H., Wu, M.-B., Chan, H., Yuan, Y.-J., Tang, N., e al.
(2019). In eg a i e compa a i e analyses o me aboli e and ansc ip p ofiles
unco e s complex egula o y ne wo k in oma o (Solanum lycope sicum L.)
ui unde going chilling inju y. Sci. Rep. 9, 4470. doi: 10.1038/s41598-019-
41065-9
Zhao, X., Yuan, X., Chen, S., Meng, L., and Fu, D. (2018). Role o he oma o
TAGL1 gene in egula ing ui me aboli es elucida ed using RNA sequence
and me abolomics analyses. PloS One 13, e0199083. doi: 10.1371/
jou nal.pone.0199083
Zhao, J., Sau age, C., Zhao, J., Bi on, F., Bauche , G., Liu, D., e al. (2019).
Me a-analysis o genome-wide associa ion s udies p o ides insigh s in o
gene ic con ol o oma o fla o . Na . Commun. 10, 1534. doi: 10.1038/s41467-
019-09462-w
Zheng, J., Huang, G., Jia, D., Wang, J., Mo a, M., Pe ei a, L. S., e al. (2013).
Responses o d ip i iga ed oma o (Solanum lycope sicum L.) yield, quali y and
wa e p oduc i i y o a ious soil ma ic po en ial h esholds in an a id egion
o No hwes China. Ag ic. Wa e Manage. 129, 181–193. doi: 10.1016/
j.agwa .2013.08.001
Zhong, S., Fei, Z., Chen, Y.-R., Zheng, Y., Huang, M., V ebalo , J., e al. (2013).
Single-base esolu ion me hylomes o oma o ui de elopmen e eal
epigenome modifica ions associa ed wi h ipening. Na . Bio echnol. 31, 154–
159. doi: 10.1038/nb .2462
Zhou, R., Kong, L., Wu, Z., Rosenq is , E., Wang, Y., Zhao, L., e al. (2019).
Physiological esponse o oma oes a d ough , hea and hei combina ion
ollowed by eco e y. Physiol. Plan 165, 144–154. doi: 10.1111/ppl.12764
Zhu, M., Chen, G., Zhou, S., Tu, Y., Wang, Y., Dong, T., e al. (2014). A new
oma o NAC (NAM/ATAF1/2/CUC2) ansc ip ion ac o , SlNAC4, unc ions
as a posi i e egula o o ui ipening and ca o enoid accumula ion. Plan Cell
Physiol. 55, 119–135. doi: 10.1093/pcp/pc 162
Zhu, G., Wang, S., Huang, Z., Zhang, S., Liao, Q., Zhang, C., e al. (2018). Rewi ing
o he ui me abolome in oma o b eeding. Cell 172, 249–261.e12. doi:
10.1016/j.cell.2017.12.019
Zouine, M., Maza, E., Dja i, A., Lau e nie , M., F asse, P., Smouni, A., e al. (2017).
TomExp ess, a unified oma o RNA-Seq pla o m o isualiza ion o
exp ession da a, clus e ing and co ela ion ne wo ks. Plan J. 92, 727–735.
doi: 10.1111/ pj.13711
Zushi, K., and Ma suzoe, N. (2015). Me abolic p ofile o o ganolep ic and heal h-
p omo ing quali ies in wo oma o cul i a s subjec ed o sal s ess and hei
in e ac ions using co ela ion ne wo k analysis. Sci. Ho ic. 184, 8–17. doi:
10.1016/j.scien a.2014.12.030
Conflic o In e es : The au ho s decla e ha he esea ch was conduc ed in he
absence o any comme cial o financial ela ionships ha could be cons ued as a
po en ial conflic o in e es .
Copy igh © 2019 Quine , Angos o, Yus e-Lisbona, Blancha d-G os, Bigo , Ma inez
and Lu s. This is an open-access a icle dis ibu ed unde he e ms o he C ea i e
Commons A ibu ion License (CC BY). The use, dis ibu ion o ep oduc ion in o he
o ums is pe mi ed, p o ided he o iginal au ho (s) and he copy igh owne (s) a e
c edi ed and ha he o iginal publica ion in his jou nal is ci ed, in acco dance wi h
accep ed academic p ac ice. No use, dis ibu ion o ep oduc ion is pe mi ed which
does no comply wi h hese e ms.
Quine e al. Toma o F ui Me abolism
F on ie s in Plan Science | www. on ie sin.o g No embe 2019 | Volume 10 | A icle 155423