Ag icul u al Wa e Managemen 278 (2023) 108176
A ailable online 18 Janua y 2023
0378-3774/© 2023 The Au ho s. Published by Else ie B.V. This is an open access a icle unde he CC BY-NC-ND license (h p://c ea i ecommons.o g/licenses/by-
nc-nd/4.0/).
Could buckwhea and spel be al e na i es o whea unde u u e
en i onmen al condi ions? S udy o hei physiological esponse o d ough
Xabie Sim´
on Ma ínez-Go˜
ni
*
, Jon Mi anda-Apodaca, Usue P´
e ez-L´
opez
Uni e si y o he Basque Coun y (UPV/EHU), Facul y o Science and Technology, Depa men o Plan Biology and Ecology, Ba io Sa iena, 48940 Leioa, Biscay, Spain
ARTICLE INFO
Handling Edi o J.E. Fe n´
andez
Keywo ds:
Al e na i e c ops
An ioxidan me abolism
Gas exchange
Pho ochemis y
S oma a
Wa e use e iciency
ABSTRACT
D ough is one o he mos ha m ul abio ic s esses o plan s. Fu u e d ough episodes a e expec ed o inc ease,
nega i ely a ec ing globally cul i a ed c ops as whea (T i icum aes i um). Toge he wi h he c op dependency,
u u e global ood secu i y is a isk. Thus, inding al e na i e c ops o whea capable o esis ing d ough ep-
isodes is essen ial o ensu e ood supply. Spel (T i icum spel a) and buckwhea (Fagopy um esculen um) a e wo
unde u ilized al e na i e c ops, whose d ough esis ance mechanisms emain unknown. We hypo hesize ha
bo h species will ha e d ough a oidance cha ac e is ics and will ha e a be e d ough esponse han whea . We
g ew whea , spel and buckwhea in a g eenhouse. D ough ea men s a ed 28 days a e sowing. When whea
and spel eached 40 % ield capaci y (FC), d ough was kep o 1-week, while in buckwhea he d ough was
kep o 4-weeks a 20 % FC. E en i pa ially inhibi ed by d ough , buckwhea showed an ex emely highe o al
biomass, as well as an ex emely highe wa e use e iciency (WUE) han whea and spel . Pho osyn he ic pa-
ame e s we e ex emely educed in spel , whe eas hose we e less a ec ed in whea . The educ ion in osmo ic
po en ial and he use o osmo ic adjus men o spel in combina ion wi h he inc eases in he an ioxidan
me abolism indica e he p e alence o d ough ole ance mechanisms. The lack o e ec on an ioxidan me a-
bolism in whea , along wi h he educ ions in s oma al conduc ance and wa e po en ial indica e he use o
d ough a oidance mechanisms. Buckwhea showed d ough a oidance mechanisms, and i s physiological pa-
ame e s we e almos no a ec ed by ex eme d ough . O e all, spel showed s ong damages unde mild
d ough , whe eas buckwhea managed o cope wi h ex eme d ough by educing i s wa e equi emen s and
inc easing WUE in o de o ensu e i s pho osyn he ic ac i i y. Thus, buckwhea appea s o be a po en ial
al e na i e o whea o ex eme d ough condi ions, while spel is no .
1. In oduc ion
Due o hei nu i ional alue, ce eals a e he main sou ce o ood o
bo h, humans and li es ock (FAOSTAT, 2019). In ac , app oxima ely 40
% o he daily calo ies consumed wo ldwide come om ice, whea and
maize, wi h whea (T i icum aes i um) accoun ing o he 20 % o global
consump ion (FAOSTAT, 2019). Ne e heless, he global dependency on
such a small numbe o c ops has pu global ood secu i y a isk, since
u u e d ough episodes will nega i ely impac he p oduc ion o hese
ce eals (Knox e al., 2012). No only ha , bu unde he u u e clima ic
scena ios, d ough episodes a e expec ed o inc ease, no only in num-
be , bu also in in ensi y (IPCC, 2014). The e o e, i is c ucial o ind
al e na i e c ops o educe dependency and ensu e ood supply unde
he u u e d ough episodes.
D ough is one o he mos de imen al and limi ing abio ic s esses
o c ops, which causes dec eases in pho osyn hesis, ege a i e g ow h,
numbe o lowe s and pollen ge mina ion (Ba nab´
as e al., 2007; G ay
and B ady, 2016). In addi ion, d ough s ess con ibu es o an o e -
p oduc ion and accumula ion o eac i e oxygen species (ROS), which
e en ually esul s in damages o he cell memb ane, inhibi ion o
pho ochemical eac ions and damages o he pho osyn he ic appa a us
(Li e al., 2014). Main d ough esis ance mechanisms a e known o be
d ough a oidance and d ough ole ance (Fang and Xiong, 2015).
D ough a oidance is de ined as he abili y o plan s o main ain issue
wa e con en ega dless o wa e sca ci y (Del in e al., 2021). Among
hem, wa e -sa e plan s a e he ones ha a oid d ough damage by
educing wa e loss ia s oma al closu e, inc easing wa e use e iciency
(WUE), inhibi ing shoo g ow h and/o inc easing wa e up ake by
inc easing oo g ow h (Gilbe e al., 2011; Kooye s, 2015). On he
con a y, wa e -spende a ie ies use he a ailable wa e o maximize
* Co esponding au ho .
E-mail add ess: [email p o ec ed] (X.S. Ma ínez-Go˜
ni).
Con en s lis s a ailable a ScienceDi ec
Ag icul u al Wa e Managemen
jou nal homepage: www.else ie .com/loca e/agwa
h ps://doi.o g/10.1016/j.agwa .2023.108176
Recei ed 23 Sep embe 2022; Recei ed in e ised o m 6 Janua y 2023; Accep ed 16 Janua y 2023
Ag icul u al Wa e Managemen 278 (2023) 108176
2
p oduc i i y wi hou p o ec ing lea u go , while hey could also in-
c ease oo dep h and e iciency o main ain high wa e s a us (Del in
e al., 2021). On he o he hand, d ough ole ance is p ima ily based on
he use o osmo ic adjus men (OA) and ROS-sca enging sys ems o
educe oxida i e damage (Fang and Xiong, 2015; Kooye s, 2015). A
ecen me a-analysis published by Li e al. (2021)) showed ha wild and
old cul i a ed whea a ie ies use d ough a oidance mechanisms, while
mode n whea a ie ies imp o ed du ing he las decades mos ly ely on
d ough ole ance s a egies. No only ha , bu unde se e e d ough
s ess mode n whea a ie ies showed lowe yields han olde a ie ies
(Li e al., 2021). Thus, inding al e na i e c ops o whea wi h imp o ed
d ough a oidance mechanisms seems o ha e he po en ial o inc ease
ood supply and educe c op dependency.
Al e na i e c ops could be de ined as c ops whose cul i a ion is no
widesp ead h ough he wo ld, o c ops ha a e widely cul i a ed in a
speci ic egion o he plane . Spel (T i icum spel a) is conside ed o be a
good nou ishmen sou ce, as well as an ances al ela i e o whea
whose cul i a ion was especially high du ing he Roman Empi e
(Campbell, 1997; Salamon e al., 2020). Du ing he las yea s, spel has
egained in e es among he consume s, a me s and b eede s due o i s
high nu i ional alue and numbe o ances al genes (Al a ez, 2021).
On he o he hand, buckwhea (Fagopy um esculen um) is an unde u il-
ized pseudo-ce eal wi h a high nu i ional con en , whose cul i a ion is
mainly ocused on some a eas o Asia and Eas e n Eu ope (Fa ooq e al.,
2016). Despi e he conside able in e es hey ha e been a ac ing in he
ecen yea s, e y li le is known abou he esponse o spel and buck-
whea o d ough s ess. In ac , some p elimina y wo k was ca ied ou
in he ea ly 1990s analysing d ough esponse and eco e y o spel , bu
i was ocused p ima ily on ille p oduc ion (Cabeza e al., 1993).
Simila ly, ew esea ch ha e s udied in de ail he physiological esponse
o d ough o buckwhea (Delp´
e ´
ee e al., 2003; Ge m e al., 2013;
Aube e al., 2020). The e o e, a huge lack o knowledge exis s
ega ding he d ough esis ance mechanisms o hese al e na i e c ops.
Unde u u e clima ic condi ions, we will be acing inc eases in
d ough in ensi y and episodes, which will educe c op p oduc ion.
Using al e na i e c ops wi h an imp o ed d ough a oidance mecha-
nisms as an al e na i e o whea , one o he main consumed c ops, could
ha e he po en ial o educe global c op dependency and ensu e ood
p oduc ion. The e o e, he aim o his esea ch was o cha ac e ize he
d ough esponse o he al e na i e c ops spel and buckwhea o
d ough , and de e mine whe he hey could be a sui able al e na i e o
whea . Since hese species ha e no been used as much as whea in
b eeding p og ams, we belie e ha hey will conse e d ough a oid-
ance mechanisms and will p ese e a highe plas ici y o cope wi h
d ough . Thus, we hypo hesize ha 1) spel will ha e d ough a oidance
cha ac e is ics; 2) buckwhea will show d ough a oidance cha ac e -
is ics; and 3) spel and buckwhea will ha e a be e d ough esponse
han whea , and hus, hey will be sui able al e na i es o whea in he
u u e.
2. Ma e ials and me hods
2.1. Plan ma e ial and g ow h condi ions
Seeds o T. aes i um a . Flo ence Au o a (whea ), T. spel a a .
F anckenko n (spel ) and F. esculen um a . Ko a (buckwhea ) we e
ob ained om he Basque Ins i u e o Ag icul u al Resea ch and
De elopmen (NEIKER, Basque Coun y, Spain). A o al o 32 plan s pe
species we e g own in 16 po s o 3 L wi h a 3:1 mix u e o pe li e:
e miculi e. The expe imen was conduc ed in a g eenhouse loca ed a
43◦19’46.9"N, 2◦58’07.6"W unde an a e age empe a u e o 24.6/21
◦C and a ela i e humidi y o 68/77 % o day/nigh . Na u al ligh was
supplemen ed wi h 2 VANQ Lamps (VQ-GLTW030) o 30 W each.
Po s we e wa e ed h ee imes pe week o keep ield capaci y (FC)
wi h Hoagland’s solu ion (Hoagland and A non, 1938) (well-wa e ed
ea men , WW), as well as o a ed h ee imes pe week o a oid
in a-g eenhouse en i onmen al g adien s. 28 days a e sowing (DAS),
d ough was imposed by wi hholding i iga ion in hal o he po s. Plan
heal h was moni o ed measu ing chlo ophyll con en wi h a Minol a
SPAD 502 Plus (Konica Minol a Op ics, Japan) and chlo ophyll luo-
escence using a Fluo Pen FP 110 (Pho on Sys ems Ins umen s, The
Czech Republic). When whea and spel eached 40 % ±5 FC, his s ess
was kep o 1-week (mild d ough ea men , MD). Howe e , unlike in
whea and spel , when buckwhea eached 40 % FC, we obse ed li le o
no e ec o d ough on he measu ed pa ame e s, as well as a lack o
damages in he ae ial issues o he d ough ea men plan s. The e o e,
we decided o inc ease d ough in ensi y in buckwhea : FC was educed
o 20 % ±5, and kep o 4-weeks (ex eme d ough ea men , ED).
All he in i o measu emen s and plan ma e ial ha es ing we e
pe o med a he end o he d ough ea men : 59 DAS in whea and
spel (31 days o d ough ) and 68 DAS in buckwhea (40 days o
d ough ).
2.2. Soil and lea wa e pa ame e s
Cumula i e anspi a ion o eigh po s pe species and ea men was
calcula ed by weighing po s h ee imes pe week be o e and a e wa-
e ing. Rela i e soil wa e con en (RSWC) was de e mined as RSWC =
100 (SFW – SDW)/(SFW
i
– SDW), whe e SFW, SDW and SFW
i
we e he
soil esh weigh , soil d y weigh and he ini ial soil esh weigh ,
espec i ely.
Lea wa e po en ial (Ψ
w
) o ou lea es pe species and ea men
was measu ed using he Scholande p essu e-equilib a ion echnique
(Scholande e al., 1965) six h a e dawn. Due o i s high Ψ
w
alue, i
was no possible o quan i y he Ψ
w
using p essu e chambe s me hod in
buckwhea , as p e iously epo ed by Delp´
e ´
ee e al. (2003). Lea os-
mo ic po en ial (Ψ
o
) o he same ou lea es was measu ed by analysing
he eezing poin o sap o lea segmen s using an OSMOMAT 030
c yoscopic osmome e (Gono ec GMBH, Be lin, Ge many) and calcu-
la ed as Ψ
o
=M ×T ×R, whe e M was he concen a ion (osmol⋅kg
−1
), T
was he empe a u e o he sample (298 K) and R was he mola gas
cons an (0.00832 L⋅MPa⋅K
−1
⋅mol
−1
). The osmo ic po en ial a ull
u go (Ψ
o
100
) was measu ed simila o Ψ
o
. Full u go o lea es was
ob ained by cu ing ou lea es pe species and ea men s and incu-
ba ing hem in deionized wa e a 4 ◦C in da k o 24 h. P essu e po-
en ial (Ψ
p
) was calcula ed as he di e ence be ween Ψ
w
and Ψ
o
. Cell
wall elas ici y (
ε
) was calcula ed as
ε
=(Ψ
p
100
– Ψ
p
)/(100 – RLWC) ×100.
Rela i e lea wa e con en (RLWC) was calcula ed as he RLWC =
(FW – DW)/(TW – FW) ×100, whe e FW, DW and TW we e he lea esh
weigh , d y weigh and u gid weigh , espec i ely. Fou lea es pe
species and ea men we e used in whea and spel , and eigh lea es pe
ea men in buckwhea . Dehyd a ion (DH) o plan s unde d ough
ea men s was calcula ed as he di e ence o Ψ
o
and Ψ
o
100
be ween
ea men s. Osmo ic adjus men (OA) was calcula ed as he di e ence o
Ψ
o
100
o plan s unde d ough and con ol condi ions.
2.3. Gas exchange and pho ochemical pa ame e s
Gas exchange pa ame e s o six ully de eloped lea es pe species
and ea men we e measu ed using a Li-Co 6400 (Li-Co Inc., Lincoln,
NE, USA). Measu emen s o whea and spel we e made on he lea
p eceding he Flag Lea , while in buckwhea he measu emen was made
on he i h ully de eloped lea coun ing om he op. The empe a u e
o he cu e e was held a 24 ◦C a a ela i e humidi y o 60 %. Mea-
su emen s we e made h ee h a e dawn unde a pho osyn he ic lux
densi y o 400 µmol m
−2
s
−1
, p o ided by a ed/blue LED ligh sou ce
(model LI 6400–40, Li-Co Inc.). In e cellula CO
2
concen a ion (Ci),
s oma al conduc ance (gs), ne pho osyn he ic CO
2
assimila ion (A) and
ins an aneous anspi a ion (E) we e calcula ed acco ding o on
Caemme e and Fa quha (1981). The ca boxyla ion capaci y (A/Ci)
was calcula ed as he a io be ween A and Ci.
Quan um yield o PSII (Φ
PSII
=(F
m
’ – F
s
)/F
m
’) was de e mined wi h
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
3
an in eg a ed lea luo escence chambe (Li-6400–40; Li-Co Inc.) by
measu ing F
s
, he a iable luo escence a s eady s a e, and F
m
’, he
maximum ligh -adap ed luo escence (Schindle and Lich en hale ,
1996). Elec on anspo a e (ETR) was de e mined as ETR =Φ
PSII
×
PPFD ×0.85 ×0.5, whe e PPFD e e s o he Pho osyn he ic Pho on Flux
Densi y, and he a io o elec on anspo a e o ne pho osyn he ic
CO
2
assimila ion (ETR/A) was calcula ed as he a io be ween ETR and
A.
2.4. An ioxidan pa ame e s
Lea es o wo plan s pe po we e pooled as one biological eplica e
o an ioxidan enzyme ac i i y measu emen s. Fou eplica es pe
species and ea men we e used. Ac i i ies o supe oxide dismu ase
(SOD), ca alase (CAT), glu a hione educ ase (GR) and asco ba e
pe oxidase (APX) we e measu ed as desc ibed in P´
e ez-L´
opez e al.
(2009) wi h li le modi ica ions.
B ie ly, SOD, CAT and GR we e ex ac ed in a bu e composed by 50
mM T is-HCl (pH 7.8), 0.1 mM e hylenediamine e aace ic acid (EDTA),
0.2 % T i on X-100, 0.1 mM phenylme hylsul onyl luo ide (PMSF) and
2 mM di hio ei ol. Supe na an om samples we e il e ed o e She-
padex G-25 columns equilib a ed wi h 50 mM T is–HCl (pH 7.8), 0.1
mM EDTA and 0.2 % T i on X-100. CAT was measu ed a 240 nm as
desc ibed by Aebi (1984). GR ac i i y was measu ed a 340 nm ac-
co ding o Edwa ds e al. (1990). Ac i i y o SOD was measu ed a 550
nm as desc ibed by McCo d and F ido ich (1969). APX was ex ac ed in
a mix u e o 50 mM KH
2
PO
4
and K
2
HPO
4
(pH 7.8) con aining 0.1 mM
EDTA, 0.2 % T i on X-100, 5 mM cys eine, 2 mM asco ba e (AsA) and
0.1 mM PMSF. APX ac i i y was measu ed a 290 nm in acco dance wi h
Hossain and Asada (1984). All enzyme ac i i ies we e exp essed on a
p o ein basis, which was measu ed acco ding o he B ad o d (1976)
me hod.
2.5. G ow h pa ame e s and in o ma ics measu emen s
Lea es, s ems and oo s o ou plan s pe species and ea men we e
ha es ed in whea and spel , and eigh plan s pe ea men in buck-
whea . Plan o gans we e o en-d ied o 72 h o d y-weigh (DW)
measu emen s. WUE was calcula ed by di iding plan DW and cumu-
la i e anspi a ion.
Pho os o he ha es ed lea es we e aken o measu ing lea a ea
(LA) wi h he open-sou ce so wa e Fiji (Fiji Is Jus ImageJ; Schindelin
e al., 2012) p io o o en-d ying hem. S oma al densi y (SD) was
measu ed by ob aining lea imp in s om adaxial and abaxial su aces as
explained by Casado-Ga cía e al. (2020). Pho os o s oma a we e aken
using a Nikon ECLIPSE 50i luo escence mic oscope (Nikon co po a ion,
Japan) wi h a Leica DFC 420 C came a (Leica Mic osys ems, Ge many).
Th ee pho os o he adaxial and h ee pho os o he abaxial su aces o
ou plan s pe species and ea men we e used. Measu emen s we e
made wi h LabelS oma ool (Casado-Ga cía e al., 2020).
B ie ly explained, pho os we e loaded in o LabelS oma and he scale
and a ea o be analysed we e es ablished. Au oma ic s oma a de ec ion
was pe o med using he de aul pa ame e s. Each pho o was e iewed
indi idually and, i necessa y, unde ec ed s oma a we e added
manually.
2.6. S a is ical analysis and igu es
All igu es we e pe o med using G aphPad P ism e sion 8.2.1 o
Windows (G aphPad So wa e, San Diego, Cali o nia USA, www.
g aphpad.com). S a is ical analysis was done using SPSS e sion 27.0 o
Windows (IBM Co p, A monk, NY). The e ec o wa e ea men (WW,
MD and ED), species (whea , spel and buckwhea ) and hei in e ac ion
we e de e mined by wo-way ANOVA. A e wa ds, da a was compa ed
using Duncan’s Pos -Hoc es . P alues <0.05 we e conside ed s a is-
ically signi ican .
3. Resul s
3.1. G ow h pa ame e s
Buckwhea showed inc eased g ow h unde WW, especially o
abo eg ound o gans, which we e 12 imes bigge han in whea and
spel (Fig. 1A–D). Likewise, he biomass accumula ion o buckwhea
unde ED was signi ican ly educed by app oxima ely 45 % o all o -
gans, while among whea and spel we only ound lea DW o be
signi ican ly educed in spel (Fig. 1A). As occu ed wi h he g ow h,
buckwhea showed signi ican ly highe shoo / oo a io and LA (Fig. 1E-
F), which we e signi ican ly educed unde ED. On he con a y, among
whea and spel , we only ound LA o be signi ican ly educed by
d ough in spel (Fig. 1F).
Buckwhea had a WUE o 4.3 g DW kg
−1
H
2
O unde con ol condi-
ions, while o whea and spel hese alues we e o 1.76 and 1.64 g DW
kg
−1
H
2
O, signi ican ly smalle (Fig. 2). Nei he whea no spel WUE
was a ec ed by MD, whe eas buckwhea showed a signi ican ly highe
WUE, wi h alues 24 % highe han unde WW and 2.7 imes bigge han
in whea and spel (Fig. 2).
3.2. Wa e ela ions
We obse ed a p og essi e dec ease in RSWC o whea and spel ,
eaching 40 % ±5 a e 47–49 DAS, while his alue was eached a
35–36 DAS in buckwhea (Fig. 3). Simila ly, 20 % ±5 RSWC was
eached in buckwhea a 39–40 DAS.
Spel showed a signi ican ly highe cumula i e anspi a ion unde
con ol condi ions (Fig. 4), which was signi ican ly educed in a 41 %
a e he MD ea men . Buckwhea had he lowes alue o cumula i e
anspi a ion, and was signi ican ly educed by 17 %. Unde 20 % FC,
buckwhea managed o keep ex emely lowe cumula i e anspi a ion
a es pe week, showing a 50–60 % educ ion om s a o end o he
d ough ea men .
Bo h, whea and spel , showed signi ican ly lowe Ψ
w
unde MD
ea men (Table 1). No only ha , bu spel showed a signi ican
educ ion in Ψ
o
, eaching a alue o −2.607 MPa, while Ψ
o
was no
a ec ed in whea no in buckwhea .
ε
showed an opposi e end in whea
and spel when exposed o d ough : i inc eased om 8.667 MPa o
14.705 MPa in whea , whe eas i dec eased om 37.520 MPa o
5.348 MPa in spel . The RLWC was signi ican ly educed by 10.5 % in
spel , while i emained simila o con ol condi ions in whea and
buckwhea . Also, spel showed a DH le el o 0.937 MPa, which was
signi ican ly highe han he DH alues o whea (0.491 MPa) and
buckwhea (0 MPa). In he same way, spel showed an OA h ee imes
highe han he es o he species. Thus, i appea s ha he wa e pa-
ame e s o buckwhea we e no a ec ed by ED, while unde MD he
same pa ame e s o spel and whea we e highly and sligh ly a ec ed,
espec i ely.
3.3. Gas exchange pa ame e s
Spel showed signi ican ly highe alues o gs and E unde con ol
condi ions han whea and buckwhea (Fig. 5A-B), and hus, was he
mos a ec ed by he d ough ea men . MD induced an ex eme
educ ion o 75 % gs in spel , which was u ned in o a 72 % educ ion o
E. In whea , d ough signi ican ly educed gs and E by 58 % and 56 %. On
he con a y, al hough signi ican , he educ ions in buckwhea we e
only o 39 % and 36 %. Also, al hough he alues o Φ
PSII
we e simila o
he h ee species, spel was he only species o ha e i signi ican ly
educed (Fig. 5C). D ough signi ican ly educed A by hal in whea and
by 92 % in spel , while i had no signi ican e ec on buckwhea
(Fig. 5D). Ci was no a ec ed in whea by he d ough ea men , while
in spel i was signi ican ly inc eased (Fig. 5E). Ne e heless, despi e he
lack o e ec in Ci in whea and i s accumula ion in spel , A/Ci was
signi ican ly educed in bo h species, wi h his educ ion being caused
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
4
by A (Fig. 5D-F). In buckwhea , al hough Ci was sligh ly dec eased, A/Ci
emained unchanged unde he ED ea men (Fig. 5E-F). E en hough
he h ee species had simila alues o ETR unde con ol condi ions,
ETR o spel was signi ican ly educed by 73 % and ETR/A was signi i-
can ly inc eased by 254 % unde MD (Fig. 5G). Simila ly, ETR/A alues
we e signi ican ly inc eased in whea by 110 %, mainly d i en by A
dec ease (Fig. 5G-H). On he con a y, ED showed no in luence on ETR
no ETR/A in buckwhea . O e all, i seems ha he pho osyn he ic pa-
ame e s o spel a e ex emely damaged by MD, while he same pa-
ame e s a e less a ec ed in whea and no a ec ed a all in buckwhea
unde ED.
Buckwhea showed signi ican ly highe abaxial SD han whea and
spel unde WW, while his alue was signi ican ly lowe o he adaxial
SD (Fig. 6). Howe e , he sum o he abaxial and he adaxial SD did no
di e among he h ee species unde con ol condi ions. On he con-
a y, unde he d ough ea men s, whea and spel showed no di -
e ences nei he in he SD o bo h sides o he lea es no in he o al SD,
while in buckwhea he e was a signi ican inc ease in he adaxial,
abaxial and o al SD (Fig. 6).
Fig. 1. E ec o well-wa e ed (WW), mild d ough (MD) and ex eme d ough (ED) condi ions in whea , spel and buckwhea in A) lea d y-weigh (DW), B) s em
DW, C) oo DW, D) o al DW, E) shoo / oo a io and F) lea a ea (LA). Each ba ep esen s mean ±s anda d e o (S.E.) o a leas 4 eplica es. The applied d ough
ea men s a e ep esen ed as well-wa e ed (WW, ligh blue ba s), mild d ough (MD, ligh o ange ba s) and ex eme d ough (ED, ligh ed ba s). Blue ci cles, o ange
iangles and ed squa es a e used o ep esen single eplica es unde WW, MD and ED, espec i ely. Di e en le e s a e used o ep esen alues signi ican ly
di e en be ween ea men s and species (P<0.05). Resul s o a wo-way ANOVA o species (Sp), ea men (T ea ) and hei in e ac ion a e ep esen ed as ns (non-
signi ican ), *(P<0.05), ** (P<0.01) and ***(P<0.001).
Fig. 2. E ec o WW, MD and ED condi ions in wa e use e iciency (WUE) in
whea , spel and buckwhea . Each ba ep esen s mean ±S.E. o a leas 4
eplica es. G ow h condi ions and s a is ical analysis a e explained in Fig. 1.
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
5
3.4. An ioxidan me abolism
We ound no e ec o d ough ea men s on he an ioxidan me a-
bolism enzymes in whea no buckwhea (Fig. 7A–D). APX ac i i y was
signi ican ly inc eased 160 % in spel unde MD, while we did no ind
any ema kable e ec on SOD, CAT and GR (Fig. 7A–D).
4. Discussion
The global dependency o a ew numbe o c ops, along wi h he
inc eases in numbe and in ensi y o he d ough episodes h ea ens
global ood secu i y (IPCC, 2014). Mode n whea a ie ies ha e shown
dec eases in p oduc ion when exposed o se e e d ough s ess (Li e al.,
2021), and hus, i is essen ial o ind al e na i e c ops o whea wi h he
abili y o esis d ough s ess. He e, we ha e cha ac e ized he d ough
esponse o whea and wo al e na i e species: spel and buckwhea . Ou
esea ch p o ides da a which demons a es ha 1) spel ac i a es
d ough ole ance mechanisms in he p esence o a mild in ensi y
d ough , e en hough hese mechanisms a e no enough o wi hs and a
mild d ough ea men ; 2) buckwhea ac i a es d ough a oidance
mechanisms and manages o cope wi h an ex eme d ough ea men
be e han whea does wi h a mild d ough ; and 3) buckwhea may ha e
he po en ial o be used as an al e na i e c op o whea unde ex eme
d ough condi ions.
Among all he c ops, buckwhea s ood ou in e ms o g ow h, since
unde con ol condi ions i showed an a e age biomass accumula ion 7
and 12 imes highe han spel and whea , espec i ely (Fig. 1A-F). In
o de o es whe he he di e ences in o al biomass among species
we e explained due o he di e ences in g ow h days, we analysed he
ela i e g ow h a e (RGR, Sup. Fig. 1), which showed ha he e we e
ba ely any di e ences. Gi en he excep ionally highe biomass accu-
mula ion o buckwhea , he epo ed g ow h educ ion o his species
unde ex eme d ough was no pa icula ly su p ising. E en hough he
o e all g ow h o buckwhea was inhibi ed, we obse ed a dec ease in
he shoo / oo a io when exposed o d ough , suppo ing p e ious
hypo hesis on buckwhea g ow h esponse o d ough (Aube e al.,
2020). In spi e o e e y hing, buckwhea was he species wi h highe
biomass unde bo h wa e ea men s, sugges ing an imp o ed use o
wa e esou ces.
As a ma e o ac , we ound buckwhea o ha e highe le els o WUE
unde well-wa e ed condi ions, as well as main aining highe le els o
WUE unde d ough . This is a highly alued ai in c op b eeding p o-
g ams (Richa ds e al., 2002; Condon e al., 2004), and hus, exploi a ion
o he high WUE o buckwhea o ge imp o ed d ough - esis an c ops
could be wo hwhile. In addi ion o ha ing a lowe WUE, whea and
spel showed no a ia ion in his pa ame e when exposed o d ough
s ess, which indica es he abili y o buckwhea o con ol wa e
Fig. 3. RSWC o e ime o well-wa e ed (WW), mild d ough (MD) and
ex eme d ough (ED) ea men s in whea , spel and buckwhea . Solid lines a e
used o ep esen WW ea men s, dashed lines ep esen MD ea men s and
do ed lines ep esen ED. Ci cles, iangles and squa es ep esen esul s o
whea , spel and buckwhea , espec i ely. Each poin ep esen s he mean ±S.
E. o 8 eplica es.
Fig. 4. E ec o d ough in cumula i e anspi a ion when A) achie ing 40 % FC in whea , spel and buckwhea and B) achie ing 20 % FC and i s e olu ion o e 4-
weeks in buckwhea . Each ba ep esen s mean ±S.E. o 8 eplica es. G ow h condi ions and s a is ical analysis a e explained in Fig. 1.
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
6
esou ces mo e e icien ly han whea and spel . The be e use o wa e
esou ces in buckwhea could be explained by inc eases in wa e up ake
and/o educ ions in wa e loss, which a e wo adap i e s a egies ha
mi iga e d ough impac (Blum, 2005). In his case, i was essen ially
explained by a s ic egula ion o cumula i e anspi a ion, since
buckwhea managed o es ic anspi a ion o e ime when exposed o
ex eme d ough . The highe p opo ion o abaxial s oma a in ela ion o
adaxial s oma a in buckwhea could be es ic ing cumula i e anspi-
a ion, educing he e apo a i e demand and hus, causing educ ions in
o al anspi a ion. Besides, buckwhea showed a signi ican dec ease in
shoo / oo a io, which con ibu es o he be e use o wa e esou ces
by inc easing wa e up ake unde d ough .
The dec ease o Ψ
w
unde wa e sca ci y is also a mechanism ha
plan s ac i a e o inc ease wa e up ake, and hus, i has been associa ed
wi h an imp o ed d ough esponse (Rob edo e al., 2007). E en hough
we we e unable o quan i y Ψ
w
o buckwhea (see 2. Ma e ials and
Me hods), we ound ha whea and spel had simila educ ions in Ψ
w
unde mild d ough . Al hough dehyd a ion (passi e mechanism) was he
main d i ing o ce in esponse o d ough in whea and spel , he deg ee
o dehyd a ion in spel was double han in whea . On he con a y,
buckwhea showed no signs o dehyd a ion, which oge he wi h he
RLWC esul s, indica e ha i was capable o main aining an op imal
wa e s a us inside he plan e en i i was unde an ex eme d ough
ea men . Wa e sca ci y p omo es wa e low ou side he cells, and
hus, dehyd a ion commonly causes dec eases in Ψ
p
(Chen e al., 2020),
as occu ed in whea . The accumula ion o di e en osmoly es inside he
cells (OA) could also p omo e dec eases in Ψ
w
, which inc eases he
u go o he cells (Nemesk´
e i and Helyes, 2019). This would explain he
obse ed educ ions in Ψ
o
and inc eases in Ψ
p
o spel . Ne e heless, he
ac i a ion o hese mechanisms we e no enough o spel o main ain
RLWC and o e come he impac o mild d ough s ess on he pho o-
syn he ic pa ame e s.
Ac ually, he pho osyn he ic p ocesses o spel we e he mos
damaged ones by he d ough ea men . Mild d ough induced an
ex eme s oma al closu e and anspi a ion dec ease on his species,
while in whea hese educ ions we e mo e conse a i e. S oma al
closu e is a sho - e m s a egy o p e en wa e loss in mos plan
species, bu could esul in limi a ions o pho osyn hesis unde wa e
sca ci y i i is main ained o long pe iods (Diaz-Espejo e al., 2007;
Silim e al., 2009). Howe e , in buckwhea we only ound a sligh
closu e o s oma a and dec ease in anspi a ion unde ex eme d ough ,
wi h no signi ican e ec on A. These esul s a e in con adic ion wi h
p e ious esul s, which epo ed educ ions highe han 80 % in E, gs
and/o A unde wa e s ess (Delp´
e ´
ee e al., 2003; Ge m e al., 2013;
Aube e al., 2020). Ne e heless, i should be no ed ha , as well as
using dis inc a ie ies and d ough in ensi ies, he d ough ea men s
we e combined wi h di e en le els o ligh (Delp´
e ´
ee e al., 2003) o
UV-B adia ion (Ge m e al., 2013), which could explain he epo ed
di e ences (Masojídek e al., 1991; I am e al., 2020; Wasaya e al.,
2021). Despi e he educ ion in gs, nei he whea no spel showed
a ia ions in SD in esponse o d ough , while buckwhea inc eased i in
bo h sides o he lea es. Howe e , he inc ease in SD could be he esul
o a concen a ing e ec o s oma a due o he educ ion in LA. Unlike in
buckwhea , pho osyn hesis in spel and whea was inhibi ed when
exposed o d ough . This inhibi ion o A induced dec eases in A/Ci in
whea and spel , sugges ing non-s oma al limi a ions (Mi anda-Apodaca
e al., 2018). Howe e , while we ound spel o ha e an ex emely
educed Φ
PSII
, indica ing a down- egula ion o s uc u al al e a ion o
he pho osyn he ic appa a us (Foye e al., 2017), we did no obse e he
same end in whea . This di e en pho ochemical sensi i i y be ween
bo h T i icum species unde d ough could explain he be e beha iou
o A in whea . In addi ion, he dec eases in A induced ETR/A o be
signi ican ly inc eased in whea and spel , sugges ing a de ia ion o
elec ons o o he p ocesses ha a e no he pho osyn hesis.
In he p esen s udy, we ound spel o signi ican ly inc ease he
ac i i y o he APX an ioxidan enzyme, indica ing a de ia ion o elec-
ons om pho osyn hesis o Mehle eac ion (C uz de Ca alho, 2008).
On he con a y, we ound no e ec o d ough ea men s on an ioxi-
dan me abolism o whea and buckwhea . Up egula ion o an ioxidan
me abolism, along wi h he use o OA a e wo key mechanisms used by
he d ough ole an species o cope wi h d ough s ess (Kooye s, 2015).
On he con a y, d ough a oidance species mainly ocus on main aining
no mal physiological p ocesses by inc easing WUE and/o modi ying
g ow h a es o a oid he ha m ul e ec s caused by d ough (Fang and
Xiong, 2015; Del in e al., 2021). Wild whea and old cul i a s ha e been
epo ed o use p ima ily d ough a oidance mechanisms, while mode n
a ie ies mainly ely on d ough ole ance mechanisms (Li e al., 2021).
Because o he ew b eeding p og ams conduc ed wi h spel and i s close
ela ion wi h whea , we ini ially hypo hesized ha i would mainly use
d ough a oidance s a egies. Unexpec edly, spel signi ican ly
inc eased OA and he ROS-sca enging enzyme APX, indica ing he
p e alence o d ough ole ance mechanisms (Kooye s, 2015). On he
con a y, ou esul s showed ha whea based i s esponse o mild
d ough on d ough a oidance mechanisms. These con adic o y esul s
a e no necessa ily incompa ible, conside ing ha d ough esis ance
s a egies a e no mu ually exclusi e and could al e na ely occu in he
same species depending on he in ensi y o he d ough (Sha uko
e al., 2017). In ac , whea has been epo ed o use d ough a oidance,
d ough ole ance and e en d ough escape mechanisms (Izanloo e al.,
2008; Dol e us, 2014; Fang e al., 2017; Sha uko e al., 2017). Con-
ce ning buckwhea , al hough we ound i s g ow h o be inhibi ed by
ex eme d ough , mos o he analysed pa ame e s we e li le o no
a ec ed. Buckwhea showed low alues o gs and E unde con ol con-
di ions, which we e sligh ly educed unde ex eme d ough . Low gs and
E alues ha e been ela ed wi h less wa e loss du ing d ough , and a e
in e es ing ai s o be aken in o conside a ion when sea ching d ough
esis an c ops (Med ano e al., 2002). This would explain he obse ed
educ ions in cumula i e anspi a ion o e ime and consequen
Table 1
E ec o WW, MD and ED condi ions in wa e po en ial (Ψ
w
), osmo ic po en ial (Ψ
o
), p essu e po en ial (Ψ
p
), cell wall elas ici y (
ε
), ela i e lea wa e con en (RLWC),
dehyd a ion (DH) and osmo ic adjus men (OA). G ow h condi ions and s a is ical analysis a e explained in Fig. 1. Fo each species and ea men , mean ±S.E. o a
leas 4 eplica es a e showed. Di e en le e s a e used o ep esen alues signi ican ly di e en among species and ea men (P<0.05).
Species T ea men Ψ
w
(MPa) Ψ
o
(MPa) Ψ
p
(MPa)
ε
(MPa) RLWC ( %) DH (MPa) OA (MPa)
Whea WW -0.805 ±0.125
a
-1.832 ±0.123
b
1.027 ±0.172
a
8.667 96.84 ±0.807
ab
MD -1.530 ±0.107
b
-1.890 ±0.153
b
0.360 ±0.195
b
14.705 92.93 ±0.828
b
0.491 ±0.102
b
0.099
Spel WW -1.030 ±0.150
a
-1.336 ±0.037
c
0.306 ±0.156
b
37.520 97.17 ±0.768
ab
MD -1.637 ±0.068
b
-2.607 ±0.143
a
0.971 ±0.211
a
5.348 86.92 ±5.931
c
0.937 ±0.045
a
0.304
Buckwhea WW – -0.782 ±0.011
d
– – 98.34 ±1.074
ab
ED – -0.869 ±0.079
d
– – 99.778 ±0.119
a
-0.008 ±0.015
c
0.116
ANOVA Ψ
w
Ψ
o
Ψ
p
RLWC
Species ns *** ns ns
T ea men *** *** ns **
In e ac ion ns *** *** ns
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
7
inc eases in WUE by he end o he ex eme d ough ea men . Thus,
buckwhea appea s o be a d ough -a oiding species, as p e ious
esea ch ha e also sugges ed (Aube e al., 2020), and mo e speci ically,
a wa e -sa ing species.
O e all, buckwhea showed a highe biomass p oduc ion as well as
inc eased le els o WUE unde con ol condi ions. In addi ion, i
managed o cope wi h he imposed ex eme d ough ea men by
inc easing e en mo e i s WUE and main aining i s pho osyn he ic pa-
ame e s. Gi en he pe spec i e o he inc eases in he numbe o
d ough e en s, high WUE is conside ed o be a desi able ai o c ops
in o de o educe he use o wa e esou ces. Likewise, al hough we
ound he g ow h o whea and spel o be li le o no a ec ed by he mild
d ough , i s nega i e impac on he es o he analysed pa ame e s
makes us belie e ha a d ough ea men as ex eme as he one applied
o buckwhea would ha e esul ed in a highe educ ion o g ow h –o
e en dea h–. The e o e, ou esul s show he clea po en ial o buck-
whea o e spel o be an al e na i e c op o whea unde he u u e
clima ic condi ions. Howe e , i should be no ed ha his esea ch has
analysed he e ec o d ough on he ege a i e g ow h, whose e ec s
do no necessa ily ha e o be simila h ough he ep oduc i e pe iod. I
has p e iously been epo ed ha d ough has a signi ican impac on
g ain yield when imposed a ege a i e s age o whea , al hough his
impac could be g ea e a ep oduc i e s age (Ta a e al., 2015; Abid
e al., 2017; Li e al., 2019; Ul a e al., 2021). The e o e, u u e esea ch
should also ocus on he analysis o he ep oduc i e pe iod, o e i y
whe he he po en ial o buckwhea o be an al e na i e c op o whea is
Fig. 5. E ec o WW, MD and ED condi ions in whea , spel and buckwhea o A) s oma al conduc ance (gs), B) anspi a ion a e (E), C) quan um yield o PSII
(Φ
PSII
), D) ne pho osyn he ic CO
2
assimila ion (A), E) in e cellula CO
2
concen a ion (Ci), F) ca boxyla ion capaci y (A/Ci), G) elec on anspo a e (ETR) and H)
he a io o elec on anspo a e o ne CO
2
pho osyn he ic assimila ion (ETR/A). Each ba ep esen s mean ±S.E. o 6 eplica es. G ow h condi ions and s a is ical
analysis a e explained in Fig. 1.
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
8
no limi ed o he be e esponse a ege a i e g ow h, bu also o an
imp o ed g ain yield.
5. Conclusions
Inc eases in d ough episodes and hei in ensi y will be one o he
main ac o s o cause a educ ion in he p oduc ion o con en ional
c ops, including whea (T i icum aes i um). The e o e, i is essen ial o
ind al e na i e c ops ha a e capable o wi hs anding u u e d ough
episodes in o de o ensu e ood supply. In his esea ch we ha e g own
whea , spel and buckwhea in a g eenhouse and e alua ed he esponse
o whea and spel (T i icum spel a) o mild d ough (MD), and o
buckwhea (Fagopy um esculen um) o ex eme d ough (ED). Unde
well-wa e ed condi ions, we ound no signi ican di e ences among
whea and spel , al hough buckwhea showed signi ican ly highe
biomass accumula ion and wa e use e iciency (WUE). Unde MD, we
ound spel o ely on d ough ole an mechanisms, inc easing an iox-
idan me abolism and osmo ic adjus men , while whea elied on
d ough a oidance mechanisms. Ne e heless, spel was no able o
o e come he MD, showing ex eme educ ions on he quan um yield o
PSII (Φ
PSII
) and ne pho osyn he ic assimila ion (A). Thus, i showed
damages on i s pho osyn he ic machine y. On he con a y, e en hough
he s oma al conduc ance (gs), anspi a ion (E) and A we e educed in
whea , his educ ion was no as ex eme as in spel , and i showed no
damage o he pho osyn he ic machine y no inc eases in he an ioxi-
dan me abolism. On he o he hand, al hough i s d y-weigh (DW) was
educed, buckwhea was capable o coping wi h he ED by inc easing
e en mo e i s WUE and main aining i s pho osyn he ic pa ame e s.
Taking in o conside a ion ha buckwhea was able o wi hs and ED,
while unde MD whea was sligh ly damaged and spel was ex emely
damaged, ou esul s show ha buckwhea may ha e he po en ial o be
an al e na i e c op o whea in he u u e.
Funding
This esea ch was inancially suppo ed by he g an GRUPO IT1682-
22 om Depa amen o de Educaci´
on del Gobie no Vasco. X. S. Ma ínez-
Go˜
ni is he ecipien o a g an om Depa amen o de Uni e sidades e
In es igaci´
on del Gobie no Vasco (Spain).
Decla a ion o Compe ing In e es
The au ho s decla e ha hey ha e no known compe ing inancial
in e es s o pe sonal ela ionships ha could ha e appea ed o in luence
he wo k epo ed in his pape .
Fig. 6. E ec o WW, MD and ED condi ions in he s oma al densi y (SD) o
whea , spel and buckwhea . Blue, o ange and ed ba s ep esen adaxial s o-
ma a, while ligh blue, ligh o ange and ligh ed ba s ep esen abaxial s oma a
o WW, MD and ED ea men s, espec i ely. The le e s abo e he ho izon al
lines ep esen he s a is ical compa ison o o al s oma a among species as
explained in Fig. 1. Simila ly, he le e s abo e S.E. ba s ep esen he s a is ical
compa ison o adaxial s oma a among species as well as he abaxial s oma a
among species unde d ough .
Fig. 7. E ec o WW, MD and ED condi ions in whea , spel and buckwhea o A) supe oxide dismu ase (SOD), B) ca alase (CAT), C) asco ba e pe oxidase (APX)
ac i i y and D) glu a hione educ ase (GR). Each ba ep esen s mean ±S.E. o a leas 3 eplica es. G ow h condi ions and s a is ical analysis a e explained in Fig. 1.
X.S. Ma ínez-Go˜
ni e al.
Ag icul u al Wa e Managemen 278 (2023) 108176
9
Da a A ailabili y
Da a will be made a ailable on eques .
Appendix A. Suppo ing in o ma ion
Supplemen a y da a associa ed wi h his a icle can be ound in he
online e sion a doi:10.1016/j.agwa .2023.108176.
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