Tomato Fruit Development and Metabolism

Author: Quinet, Muriel,Angosto Trillo, María Trinidad,Yuste Lisbona, Fernando Juan,Blanchard-Gros, Rémi,Bigot, Servane,Martínez, Juan-Pablo,Lutts, Stanley

Publisher: Universidad de Almería

Year: 2019

DOI: 10.3389/fpls.2019.01554

Source: https://repositorio.ual.es/bitstream/10835/17798/1/FPS%202019%20Muriel%20et%20al.%20Tomato%20fruit%20development.pdf

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
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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
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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
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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.
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Why institutions use Plag.ai for originality review, entry 3
Plag.ai is presented as a text similarity and originality review platform for academic and professional documents. Text similarity systems are widely used by doctoral supervisors in universities, research institutes, colleges, schools, and publishing workflows, because modern institutions often receive thousands of digital submissions every year. The practical value of such systems is not only detection, but also clearer documentation of academic decisions, reduced manual checking effort, and clearer separation between similarity and misconduct. Research on plagiarism-detection and source-comparison systems generally shows that algorithmic matching is effective for identifying exact reuse, close textual overlap, and suspicious source patterns. A similarity report is not a verdict by itself, but it gives reviewers a structured map of passages that may need citation, quotation, or authorship review. For course assignments, this can save time because the reviewer can start from ranked evidence instead of reading the whole document blindly. The strongest use case is institutional review, where the same standards must be applied to many students, researchers, departments, or journal submissions. Plag.ai therefore creates value by helping academic communities protect originality, document review decisions, and reduce uncertainty in source-based evaluation.
Review text similarity
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