Academic Edi o s: Dayong Zhang
and Ped o Diaz-Vi ancos
Recei ed: 19 Feb ua y 2025
Re ised: 29 Ma ch 2025
Accep ed: 7 Ap il 2025
Published: 8 Ap il 2025
Ci a ion: San os, T.S.d.; Co eia,
M.R.S.; Sena, L.S.; San ana, L.P.d.S.;
Sil a, G.B.G.d.; Lima, K.S.; Du a,
E.V.d.S.; Adas, M.E.; Ribei o,
M.C.B.d.O.; Ribei o, J.E.d.S.; e al. The
Combina ion o Salicylic Acid,
Nico inamide, and P oline Mi iga es
he Damage Caused by Sal S ess in
Nas u ium (T opaeolum majus). Plan s
2025,14, 1156. h ps://doi.o g/
10.3390/plan s14081156
Copy igh : © 2025 by he au ho s.
Licensee MDPI, Basel, Swi ze land.
This a icle is an open access a icle
dis ibu ed unde he e ms and
condi ions o he C ea i e Commons
A ibu ion (CC BY) license
(h ps://c ea i ecommons.o g/
licenses/by/4.0/).
A icle
The Combina ion o Salicylic Acid, Nico inamide, and P oline
Mi iga es he Damage Caused by Sal S ess in Nas u ium
(T opaeolum majus)
Thainan Sip iano dos San os 1, Ma cos Robe o San os Co eia 1, Luma San os Sena 1,
Lau a Pe ei a dos San os San ana 1, Geo anna Buique Gualbe o da Sil a 1, Keilane Sil a Lima 1,
Elienay Vinícius da Sil a Du a 1, My iam El Adas 1, Ma ia Ca olina Bo ges de Oli ei a Ribei o 1,
João E e hon da Sil a Ribei o 2, Rogé io Fe ei a Ribas 1, Elania F ei e da Sil a 2,3,
Al edo Emilio Rubio-Casal
3
, Au élio Paes Ba os Júnio
2
, Xuguang Tang
4
, Thie es Geo ge F ei e da Sil a
5
,
Alexand e Maniçoba da Rosa Fe az Ja dim 6,* and Toshik Ia ley da Sil a 1,*
1Cen e o Ag a ian, En i onmen al, and Biological Sciences, Uni e sidade Fede al do Recônca o da Bahia,
C uz das Almas 44380-000, BA, B azil; [email p o ec ed] (T.S.d.S.);
ma cos_ [email p o ec ed] (M.R.S.C.); [email p o ec ed] (L.S.S.);
[email p o ec ed] (L.P.d.S.S.); [email p o ec ed] (G.B.G.d.S.);
[email p o ec ed] (K.S.L.); [email p o ec ed] (E.V.d.S.D.);
[email p o ec ed] (M.E.A.); [email p o ec ed] (M.C.B.d.O.R.);
[email p o ec ed] (R.F.R.)
2Depa men o Ag icul u al and Fo es y Sciences, Fede al Ru al Uni e si y o he Semi-A id,
Mosso ó 59625-900, RN, B azil; [email p o ec ed] (J.E.d.S.R.);
[email p o ec ed] (E.F.d.S.); [email p o ec ed] (A.P.B.J.)
3
Depa men o Plan Biology and Ecology, Uni e si y o Se ille, A . Reina Me cedes, s/n, 41012 Se illa, Spain;
[email p o ec ed]
4Ins i u e o Remo e Sensing and Geosciences, Hangzhou No mal Uni e si y, Hangzhou 311121, China;
[email p o ec ed]
5
Depa men o Ag icul u al Enginee ing, Fede al Ru al Uni e si y o Pe nambuco, Dom Manoel de Medei os
A enue, s/n, Dois I mãos, Reci e 52171-900, PE, B azil; [email p o ec ed]
6
Depa men o Biodi e si y, Ins i u e o Biosciences, São Paulo S a e Uni e si y—UNESP, Rio Cla o 13506-900,
SP, B azil
*Co espondence: [email p o ec ed] (A.M.d.R.F.J.); [email p o ec ed] (T.I.d.S.)
Abs ac : Salini y ep esen s a signi ican challenge o ag icul u e, especially in semi-a id
egions, a ec ing he g ow h and p oduc i i y o plan s such as nas u ium (T opaeolum
majus), which is alued o i s o namen al, medicinal, and ood uses. Sal s ess dis up s
biochemical, physiological, and ana omical p ocesses, limi ing plan de elopmen . This
s udy in es iga ed he applica ion o a enua o s, including salicylic acid, nico inamide,
and p oline, o mi iga e he e ec s o sal s ess on nas u ium cul i a ed in a hyd oponic
sys em. The ea men s in ol ed di e en combina ions o hese compounds unde saline
condi ions (40 mM NaCl). The a enua o s educed he nega i e impac s o sal s ess,
p omo ing imp o emen s in gas exchange, such as inc eased ne pho osyn hesis, wa e -use
e iciency, and s oma al conduc ance. Addi ionally, he ea men s enhanced ege a i e
and ep oduc i e g ow h, inc easing he d y biomass o lea es, s ems, and lowe s, as well
as he numbe o lowe s and lowe buds. The combina ion o salicylic acid, nico inamide,
and p oline s ood ou by p o iding g ea e e iciency in ca bon assimila ion, s abili y o
pho osyn he ic pigmen s, and highe ole ance o sal s ess. These indings ein o ce he po-
en ial o using a enua o s o op imize he cul i a ion o nas u ium in saline en i onmen s,
p omo ing highe p oduc i i y and plan quali y.
Keywo ds: abio ic s ess; edible lowe s; plan ho mones; i amin B3; amino acids; gas
exchange; ino ganic and o ganic solu es
Plan s 2025,14, 1156 h ps://doi.o g/10.3390/plan s14081156
Plan s 2025,14, 1156 2 o 21
1. In oduc ion
Nas u ium (T opaeolum majus L., T opaeolaceae), also known in B azil as “capuch-
inha”, “nas ú io”, and “chaguinha”, is a non-con en ional ood plan , g own as an o na-
men al, medicinal, and edible plan , and widely cul i a ed wo ldwide due o i s adap abili y
and di e se applica ions [
1
]. I s lowe s exhibi a dis inc i e peppe y la o , a hallma k
o he species, which has made hem one o he mos comme cially alued edible lowe s
globally [
2
]. The lea es and lowe s o nas u ium a e highly e sa ile, equen ly used in
salads, sandwiches, and as deco a i e elemen s in dishes and desse s, enhancing bo h he
aes he ic appeal and unc ional alue o culina y c ea ions [
3
]. The plan is cha ac e ized
by ounded lea es, ib an lowe s in shades o yellow, o ange, and ed, o en ado ned
wi h da k in e nal ma kings, and g eenish ui s. All pa s o he plan a e conside ed
edible, wi h he excep ion o he oo s [
4
]. Fu he mo e, nas u ium is ich in a y acids,
glucosinola es, la onoids, and e acyclic i e penes, and in B azil i is widely employed
o he ea men o ulce s, colds, celluli is, and anemia [5,6].
The quali y o nas u ium plan s is s ongly in luenced by en i onmen al condi ions [
1
].
Unde abio ic s ess, he plan s o en expe ience educed g ow h and diminished isual
quali y o hei lowe s [
7
]. This impac is pa icula ly p onounced in a id and semi-a id
egions, whe e s esso s such as d ough and salini y a e he p ima y limi ing ac o s o he
cul i a ion o edible lowe s [
6
,
8
]. Unde hese condi ions, wa e de ici and salini y dis up
essen ial physiological p ocesses, such as pho osyn hesis, and impai oo de elopmen ,
leading o educed p oduc i i y and o e all plan quali y [2].
Salini y, cha ac e ized by he accumula ion o soluble sal s such as sodium (Na
+
) and
chlo ide (Cl
−
), is a signi ican en i onmen al challenge ha h ea ens ag icul u al sus ain-
abili y. In addi ion o ad e sely a ec ing c op g ow h and p oduc i i y, salini y deg ades
soil s uc u e, educes wa e in il a ion, diminishes biodi e si y, and con amina es wa e
esou ces [
9
]. The use o high-salini y wa e exace ba es hese e ec s by subjec ing plan s o
combined osmo ic and ionic s esses. These s esses lead o a ma ked decline in ege a i e
g ow h due o educed wa e and nu ien up ake, s uc u al cell diso ganiza ion, and
excessi e p oduc ion o eac i e oxygen species (ROS), which cause oxida i e damage [
10
].
Soil salini y impac s app oxima ely 800 million hec a es globally, accoun ing o a ound
20% o i iga ed ag icul u al land, pa icula ly in a id, semi-a id, and coas al a eas, due
o poo i iga ion and d ainage p ac ices, limi ed ain all, high e apo a ion a es, and he
use o saline wa e o i iga ion [
8
,
11
]. Excess Na
+
dis up s cellula me abolism and ionic
balance, making i ha m ul o plan s. Fo T. majus, salini y le els abo e 1 dS m
−1
ha e been
shown o inhibi oo ing and seedling g ow h [
12
], al hough low sal concen a ions may
enhance biomass p oduc ion [13].
In ligh o he challenges posed by soil saliniza ion and inc easing wa e sca ci y, he
adop ion o sus ainable ag icul u al p ac ices is essen ial. In his con ex , hyd oponics
eme ges as a p omising al e na i e, o e ing g ea e wa e -use e iciency and enabling
cul i a ion in egions wi h limi ed o low-quali y wa e esou ces [
14
]. The exogenous
applica ion o s ess alle ia o s has p o en o be a p omising s a egy o mi iga ing he
dele e ious e ec s o salini y s ess in nas u ium plan s [
6
,
8
,
15
–
18
]. These compounds play
a c i ical ole in modula ing a ious physiological and biochemical p ocesses, enhancing
he plan s’ ole ance o ad e se salini y condi ions [
19
]. Among he mos commonly used
alle ia o s a e phy oho mones, i amins, and amino acids, whose posi i e e ec s a e
widely documen ed in he li e a u e.
Salicylic acid (SA) is a well-s udied phy oho mone wi h p o en e ec s in mi iga ing
damage caused by salini y s ess [
17
]. I s exogenous applica ion educes oxida i e s ess,
Plan s 2025,14, 1156 3 o 21
egula es ion up ake, p omo es wa e balance, and posi i ely in luences s oma al beha io ,
gas exchange, chlo ophyll luo escence, and osmo egula ion [
20
]. Nico inamide (nico i-
namide o niacin) unc ions as a g ow h egula o , in luencing physiological p ocesses
such as enzyme, nucleic acid, and p o ein biosyn hesis, while also se ing as a c i ical
coenzyme [
21
]. P oline, an amino acid in ol ed in p ima y me abolism, plays a cen al ole
unde s ess condi ions [
18
]. As one o he mos accumula ed compa ible solu es in plan s
exposed o salini y, wa e de ici , o ex eme empe a u es, p oline con ibu es o cellula
p o ec ion and he main enance o me abolic p ocesses [22].
The inno a i e aspec s o his esea ch lie in i s pionee ing explo a ion o he com-
bined use o salicylic acid, p oline, and nico inamide o mi iga e salini y-induced damage
in hyd oponically g own nas u ium plan s. Unlike p e ious s udies ha ha e ocused indi-
idually on hese compounds, his s udy e alua es hei syne gis ic e ec s on physiological
and biochemical p ocesses, including gas exchange, pho osyn he ic pigmen s, o ganic and
ino ganic solu es, and o e all plan g ow h. The no el y also ex ends o assessing he
iabili y o hyd oponic cul i a ion as a sus ainable al e na i e o g owing nas u ium
unde saline condi ions, p o iding aluable insigh s in o enhancing plan ole ance and
p oduc i i y in challenging en i onmen s.
The selec ion o SA, nico inamide, and p oline as s ess alle ia o s was based on hei
complemen a y oles in enhancing plan esilience unde sal s ess h ough dis inc mech-
anisms. SA is known o educing oxida i e s ess, egula ing ion up ake, imp o ing wa e
balance, and enhancing pho osyn he ic e iciency. Nico inamide ac s as a g ow h egula o ,
in luencing enzyme, nucleic acid, and p o ein biosyn hesis, while also se ing as a c ucial
coenzyme. P oline unc ions as an osmop o ec an , con ibu ing o osmo ic balance, mem-
b ane s abiliza ion, and ROS sca enging. Thei combined applica ion o e s a syne gis ic
e ec , add essing mul iple s ess ac o s simul aneously, which is pa icula ly ele an
unde saline condi ions whe e plan s ace osmo ic, ionic, and oxida i e s ess. Addi ionally,
while hese alle ia o s ha e been indi idually s udied, hei join applica ion in hyd oponi-
cally g own nas u ium unde salini y condi ions is an inno a i e app oach ha aims o
enhance plan ole ance and p oduc i i y mo e e ec i ely han indi idual applica ion.
Al hough p og ess has been made in unde s anding he physiological and biochemical
esponses o nas u ium o sal s ess, signi ican gaps emain, pa icula ly conce ning he
use o a enua o s such as salicylic acid, nico inamide, and p oline. These compounds
ha e shown p omising po en ial in mi iga ing he nega i e e ec s o salini y by egula ing
ion up ake, main aining wa e balance, s abilizing memb anes, modula ing an ioxidan
me abolism, and imp o ing pho osyn he ic e iciency. Howe e , s udies so a ha e mainly
ocused on he isola ed applica ion o hese a enua o s, wi hou adequa ely explo ing he
combined e ec s ha could p o ide a mo e obus app oach o enhancing nas u ium’s
ole ance o sal s ess. In es iga ing he join use o hese compounds in hyd oponic
sys ems exposed o salini y ep esen s an inno a i e s a egy ha could signi ican ly
imp o e he p oduc i i y and quali y o nas u ium g own unde ad e se condi ions.
Despi e ad ances in unde s anding he ole o s ess alle ia o s, s udies on hei use
in nas u ium plan s cul i a ed unde salini y s ess in hyd oponic sys ems emain sca ce.
This s udy is a pionee ing e o in explo ing he combined use o salicylic acid, p oline, and
nico inamide o mi iga e salini y-induced damage in hyd oponically g own nas u ium
plan s. Acco dingly, he p esen esea ch aimed o e alua e he e ec s o salicylic acid,
nico inamide, and p oline applica ion on gas exchange, pho osyn he ic pigmen s, o ganic
and ino ganic solu es, and he g ow h o T opaeolum majus cul i a ed in a hyd oponic
sys em unde salini y condi ions.
Plan s 2025,14, 1156 4 o 21
2. Resul s
2.1. E ec o Sal S ess on Gas Exchange
Sal s ess and he applica ion o a enua o s in luenced gas exchange in T. majus
(Figu e 1). The isola ed applica ion o nico inamide (T4) educed s oma al conduc ance (gs;
Figu e 1a), ne pho osyn hesis (A; Figu e 1b), anspi a ion a e (E; Figu e 1c), in e cellula
CO
2
concen a ion (Ci; Figu e 1d), in insic ca boxyla ion e iciency (iCE; Figu e 1e), and he
a io o in e cellula o ex e nal CO
2
concen a ion (Ci/Ca; Figu e 1h). On he o he hand,
he combina ion o nico inamide wi h salicylic acid (T7) and wi h salicylic acid and p oline
(T8) inc eased s oma al conduc ance (0.13 and 0.14 mol H
2
O m
−2
s
−1
, espec i ely) and
he anspi a ion a e (3.58 and 3.55 mmol H
2
O m
−2
s
−1
, espec i ely). Addi ionally, he
combined applica ion o all h ee a enua o s inc eased he in e cellula CO
2
concen a ion
(278.33
µ
mol CO
2
mol
−1
ai ) and he Ci/Ca a io (0.63), sugges ing a possible imp o emen
in he plan ’s adap i e capaci y unde sal s ess condi ions.
Plan s 2025, 14, x FOR PEER REVIEW 4 o 21
o ganic and ino ganic solu es, and he g ow h o T opaeolum majus cul i a ed in a hyd o-
ponic sys em unde salini y condi ions.
2. Resul s
2.1. E ec o Sal S ess on Gas Exchange
Sal s ess and he applica ion o a enua o s in luenced gas exchange in T. majus (Fig-
u e 1). The isola ed applica ion o nico inamide (T4) educed s oma al conduc ance (gs;
Figu e 1a), ne pho osyn hesis (A; Figu e 1b), anspi a ion a e (E; Figu e 1c), in e cellula
CO
2
concen a ion (Ci; Figu e 1d), in insic ca boxyla ion e iciency (iCE; Figu e 1e), and
he a io o in e cellula o ex e nal CO
2
concen a ion (Ci/Ca; Figu e 1h). On he o he
hand, he combina ion o nico inamide wi h salicylic acid (T7) and wi h salicylic acid and
p oline (T8) inc eased s oma al conduc ance (0.13 and 0.14 mol H
2
O m
−2
s
−1
, espec i ely)
and he anspi a ion a e (3.58 and 3.55 mmol H
2
O m
−2
s
−1
, espec i ely). Addi ionally, he
combined applica ion o all h ee a enua o s inc eased he in e cellula CO
2
concen a ion
(278.33 µmol CO
2
mol
−1
ai ) and he Ci/Ca a io (0.63), sugges ing a possible imp o emen
in he plan ’s adap i e capaci y unde sal s ess condi ions.
Figu e 1. Con .
Plan s 2025,14, 1156 5 o 21
Plan s 2025, 14, x FOR PEER REVIEW 5 o 21
Figu e 1. (a) S oma al conduc ance (gs), (b) ne pho osyn hesis (A), (c) anspi a ion a e (E), (d)
in e cellula CO
2
concen a ion (Ci), (e) in insic ca boxyla ion e iciency (iCE), ( ) ins an aneous
wa e -use e iciency (WUE), (g) in insic wa e -use e iciency (iWUE), and (h) Ci/Ca a io o T opae-
olum majus subjec ed o sal s ess and he applica ion o salicylic acid (SA), nico inamide (NAM),
and p oline (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM NaCl; T2 = 40 mM NaCl + P o; T3 = 40 mM
NaCl + SA; T4 = 40 mM NaCl + NAM; T5 = 40 mM NaCl + P o + SA; T6 = 40 mM NaCl + P o + NAM;
T7 = 40 mM NaCl + SA + NAM; and T8 = 40 mM NaCl + P o + SA + NAM. Means ollowed by he
same le e do no di e acco ding o he Sco –Kno es (p ≤ 0.05). Ba s a e means ± s anda d e o
(n = 4).
Unde sal s ess, in he absence o a enua o s (T1), and wi h he applica ion o nic-
o inamide combined wi h salicylic acid (T7) and wi h all h ee a enua o s (T8), an in-
c ease in ne pho osyn hesis (A, Figu e 1b) was obse ed, eaching 10.54, 10.15, and 10.40
µmol CO
2
m
−2
s
−1
, espec i ely. In insic ca boxyla ion e iciency (iCE) imp o ed wi h he
applica ion o salicylic acid combined wi h p oline (T5) and wi h nico inamide (T7), bo h
esul ing in 0.044. Wa e -use e iciency (WUE; Figu e 1 ) was ele a ed unde salini y wi h-
ou a enua o s (T1) and wi h he applica ion o salicylic acid (T3), wi h alues o 4.00 and
3.76 µmol CO
2
/mmol H
2
O m
−2
s
−1
, espec i ely. Addi ionally, in insic wa e -use e iciency
(iWUE; Figu e 1g) inc eased unde salini y condi ions wi h he applica ion o nico ina-
mide (109.7 µmol CO
2
/mol H
2
O m
−2
s
−1
).
2.2. Impac o Sal S ess on Pho osyn he ic Pigmen s
The applica ion o a enua o s o nas u ium plan s cul i a ed unde salini y condi-
ions in luenced he le els o pho osyn he ic pigmen s (Figu e 2). Sal s ess educed he
con en s o chlo ophyll a (Figu e 2a), chlo ophyll b (Figu e 2b), o al chlo ophyll (Figu e
2c), and ca o enoids (Figu e 2d). Howe e , he applica ion o salicylic acid (T3) and he
combina ion o all h ee a enua o s (T8) con ibu ed o a mo e s able main enance o chlo-
ophyll indices unde salini y. On he o he hand, he combined applica ion o p oline
wi h salicylic acid (T5) esul ed in a educ ion in chlo ophyll a (6.73 µg g
−1
d y mass),
chlo ophyll b (6.11 µg g
−1
DM), o al chlo ophyll (13.48 µg g
−1
DM), and ca o enoids (6.40
µg g
−1
DM). Addi ionally, he combina ion o p oline wi h nico inamide (T6) also educed
chlo ophyll b (6.20 µg g
−1
DM) and ca o enoid le els (6.35 µg g
−1
DM), ein o cing he
nega i e e ec s o hese in e ac ions on pho osyn he ic pigmen s.
Figu e 1. (a) S oma al conduc ance (gs), (b) ne pho osyn hesis (A), (c) anspi a ion a e (E), (d) in e -
cellula CO
2
concen a ion (Ci), (e) in insic ca boxyla ion e iciency (iCE), ( ) ins an aneous wa e -use
e iciency (WUE), (g) in insic wa e -use e iciency (iWUE), and (h)Ci/Ca a io o T opaeolum majus
subjec ed o sal s ess and he applica ion o salicylic acid (SA), nico inamide (NAM), and p o-
line (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM NaCl; T2 = 40 mM NaCl + P o; T3 = 40 mM
NaCl + SA
; T4 = 40 mM NaCl + NAM; T5 = 40 mM NaCl + P o + SA; T6 = 40 mM NaCl + P o + NAM;
T7 = 40 mM NaCl + SA + NAM
; and T8 = 40 mM NaCl + P o + SA + NAM. Means ollowed by he
same le e do no di e acco ding o he Sco –Kno es (p
≤
0.05). Ba s a e means
±
s anda d e o
(n= 4).
Unde sal s ess, in he absence o a enua o s (T1), and wi h he applica ion o
nico inamide combined wi h salicylic acid (T7) and wi h all h ee a enua o s (T8), an
inc ease in ne pho osyn hesis (A, Figu e 1b) was obse ed, eaching 10.54, 10.15, and
10.40
µ
mol CO
2
m
−2
s
−1
, espec i ely. In insic ca boxyla ion e iciency (iCE) imp o ed
wi h he applica ion o salicylic acid combined wi h p oline (T5) and wi h nico inamide (T7),
bo h esul ing in 0.044. Wa e -use e iciency (WUE; Figu e 1 ) was ele a ed unde salini y
wi hou a enua o s (T1) and wi h he applica ion o salicylic acid (T3), wi h alues o 4.00
and 3.76
µ
mol CO
2
/mmol H
2
O m
−2
s
−1
, espec i ely. Addi ionally, in insic wa e -use
e iciency (iWUE; Figu e 1g) inc eased unde salini y condi ions wi h he applica ion o
nico inamide (109.7 µmol CO2/mol H2O m−2s−1).
2.2. Impac o Sal S ess on Pho osyn he ic Pigmen s
The applica ion o a enua o s o nas u ium plan s cul i a ed unde salini y condi ions
in luenced he le els o pho osyn he ic pigmen s (Figu e 2). Sal s ess educed he con en s
o chlo ophyll a (Figu e 2a), chlo ophyll b (Figu e 2b), o al chlo ophyll (Figu e 2c), and
ca o enoids (Figu e 2d). Howe e , he applica ion o salicylic acid (T3) and he combina ion
o all h ee a enua o s (T8) con ibu ed o a mo e s able main enance o chlo ophyll indices
unde salini y. On he o he hand, he combined applica ion o p oline wi h salicylic
acid (T5) esul ed in a educ ion in chlo ophyll a (6.73
µ
g g
−1
d y mass), chlo ophyll b
(6.11
µ
g g
−1
DM), o al chlo ophyll (13.48
µ
g g
−1
DM), and ca o enoids (6.40
µ
g g
−1
DM).
Addi ionally, he combina ion o p oline wi h nico inamide (T6) also educed chlo ophyll b
(6.20
µ
g g
−1
DM) and ca o enoid le els (6.35
µ
g g
−1
DM), ein o cing he nega i e e ec s
o hese in e ac ions on pho osyn he ic pigmen s.
Plan s 2025,14, 1156 6 o 21
Plan s 2025, 14, x FOR PEER REVIEW 6 o 21
Figu e 2. (a) Chlo ophyll a, (b) chlo ophyll b, (c) o al chlo ophyll, and (d) ca o enoids o T opaeolum
majus subjec ed o sal s ess and he applica ion o salicylic acid (SA), nico inamide (NAM), and
p oline (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM NaCl; T2 = 40 mM NaCl + P o; T3 = 40 mM
NaCl + SA; T4 = 40 mM NaCl + NAM; T5 = 40 mM NaCl + P o + SA; T6 = 40 mM NaCl + P o + NAM;
T7 = 40 mM NaCl + SA + NAM; and T8 = 40 mM NaCl + P o + SA + NAM. Means ollowed by he
same le e do no di e acco ding o he Sco –Kno es (p ≤ 0.05). Ba s a e means ± s anda d e o
(n = 4).
2.3. Ino ganic Solu es o Lea es and Flowe s
The applica ion o sal s ess a enua o s in luenced he le els o ino ganic solu es in
he lea es and lowe s o nas u ium (Figu e 3). Unde sal s ess condi ions, he e was an
inc ease in Na
+
, Cl
−
, and he Na
+
/K
+
a io in he lea es (Figu e 3a,e,g), di e ing om he
con ol (T0). The ea men wi h salicylic acid (T3) esul ed in he highes accumula ion o
hese ions, wi h alues o 99.8 mg g
−1
DM, 24.0 µg g
−1
DM, and 3.2, espec i ely. In he
lowe s, sal s ess also led o an inc ease in Na
+
le els (Figu e 3b). The ea men wi h
salicylic acid (T3) esul ed in he highes Na
+
accumula ion in he lowe s, eaching 9.4 mg
g
−1
DM. Con e sely, he applica ion o p oline alone (T2) and i s combina ions wi h sali-
cylic acid (T5) o wi h salicylic acid and nico inamide (T8) main ained Na
+
le els in he
lowe s simila o he con ol (T0), wi h alues o 6.68, 6.23, 6.34, and 6.52 mg g
−1
DM,
espec i ely.
Figu e 2. (a) Chlo ophyll a, (b) chlo ophyll b, (c) o al chlo ophyll, and (d) ca o enoids o T opaeolum
majus subjec ed o sal s ess and he applica ion o salicylic acid (SA), nico inamide (NAM), and
p oline (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM NaCl; T2 = 40 mM NaCl + P o; T3 = 40 mM
NaCl + SA; T4 = 40 mM NaCl + NAM; T5 = 40 mM NaCl + P o + SA; T6 = 40 mM NaCl + P o + NAM;
T7 = 40 mM NaCl + SA + NAM; and T8 = 40 mM NaCl + P o + SA + NAM. Means ollowed by he
same le e do no di e acco ding o he Sco –Kno es (p
≤
0.05). Ba s a e means
±
s anda d e o
(n= 4).
2.3. Ino ganic Solu es o Lea es and Flowe s
The applica ion o sal s ess a enua o s in luenced he le els o ino ganic solu es in
he lea es and lowe s o nas u ium (Figu e 3). Unde sal s ess condi ions, he e was an
inc ease in Na
+
, Cl
−
, and he Na
+
/K
+
a io in he lea es (Figu e 3a,e,g), di e ing om he
con ol (T0). The ea men wi h salicylic acid (T3) esul ed in he highes accumula ion
o hese ions, wi h alues o 99.8 mg g
−1
DM, 24.0
µ
g g
−1
DM, and 3.2, espec i ely. In
he lowe s, sal s ess also led o an inc ease in Na
+
le els (Figu e 3b). The ea men
wi h salicylic acid (T3) esul ed in he highes Na
+
accumula ion in he lowe s, eaching
9.4 mg g
−1
DM. Con e sely, he applica ion o p oline alone (T2) and i s combina ions
wi h salicylic acid (T5) o wi h salicylic acid and nico inamide (T8) main ained Na
+
le els
in he lowe s simila o he con ol (T0), wi h alues o 6.68, 6.23, 6.34, and 6.52 mg g
−1
DM, espec i ely.
Unde sal s ess condi ions, he applica ion o salicylic acid alone (T3) and in combina-
ion wi h all h ee a enua o s (T8) esul ed in he lowes K
+
le els in he lea es (Figu e 3c),
wi h alues o 31.4 and 31.8 mg g
−1
DM, espec i ely, while he con ol (T0) showed he
highes accumula ion, eaching 58.1 mg g
−1
DM. Salini y also a ec ed he le els o K
+
and
Cl
−
in he lowe s (Figu e 3d, ). The combina ion o p oline wi h nico inamide (T6) signi i-
can ly inc eased K
+
and Cl
−
le els, egis e ing alues o 58.1 mg g
−1
DM and 16.0
µ
g g
−1
DM, espec i ely. In con as , he combina ion o p oline wi h salicylic acid (T5) educed K
+
accumula ion in he lowe s, wi h a alue o 29.7 mg g
−1
DM. Addi ionally, he applica ion
o nico inamide alone (T4), combined wi h salicylic acid (T7), and he combina ion o p o-
Plan s 2025,14, 1156 7 o 21
line wi h salicylic acid (T5) educed Cl
−
le els in he lowe s, showing alues o 12.5, 12.9,
and 12.4
µ
g g
−1
DM, espec i ely. Rega ding he Na
+
/K
+
a io in he lea es (Figu e 3h),
he combina ions o p oline wi h nico inamide (T6) and all h ee a enua o s (T8) unde sal
s ess esul ed in he lowes alues (0.15, 0.14, and 0.14, espec i ely), simila o he con ol
(T0). Con e sely, nico inamide alone (T4) and combined wi h salicylic acid (T7) showed
he highes Na+/K+ a ios, wi h alues o 0.23 and 0.24, espec i ely.
Plan s 2025, 14, x FOR PEER REVIEW 7 o 21
Figu e 3. (a,b) Sodium (Na
+
), (c,d) po assium (K
+
), (e, ) chlo ide (Cl
−
), and (g,h) Na
+
/K
+
a io in lea es
and lowe s, espec i ely, o T opaeolum majus subjec ed o sal s ess and he applica ion o salicylic
acid (SA), nico inamide (NAM), and p oline (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM NaCl; T2
= 40 mM NaCl + P o; T3 = 40 mM NaCl + SA; T4 = 40 mM NaCl + NAM; T5 = 40 mM NaCl + P o +
SA; T6 = 40 mM NaCl + P o + NAM; T7 = 40 mM NaCl + SA + NAM; and T8 = 40 mM NaCl + P o +
SA + NAM. Means ollowed by he same le e do no di e acco ding o he Sco –Kno es (p ≤
0.05). Ba s a e means ± s anda d e o (n = 4).
Figu e 3. (a,b) Sodium (Na
+
), (c,d) po assium (K
+
), (e, ) chlo ide (Cl
−
), and (g,h) Na
+
/K
+
a io in
lea es and lowe s, espec i ely, o T opaeolum majus subjec ed o sal s ess and he applica ion o
Plan s 2025,14, 1156 8 o 21
acid (SA), nico inamide (NAM), and p oline (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM NaCl;
T2 = 40 mM NaCl + P o; T3 = 40 mM NaCl + SA; T4 = 40 mM NaCl + NAM;
T5 = 40 mM
NaCl
+ P o + SA; T6 = 40 mM NaCl + P o + NAM; T7 = 40 mM NaCl + SA + NAM; and
T8 = 40 mM
NaCl + P o + SA + NAM
. Means ollowed by he same le e do no di e acco ding o he Sco –
Kno es (p≤0.05). Ba s a e means ±s anda d e o (n= 4).
2.4. O ganic Solu es o Lea es and Flowe s
Unde sal s ess condi ions, he applica ion o a enua o s in luenced he le els o
o ganic solu es in nas u ium lowe s (Figu e 4). The le els o soluble ca bohyd a es, ee
amino acids, and soluble p o eins in he lea es we e no a ec ed by he ea men s. Soluble
ca bohyd a e le els (Figu e 4a) we e educed by he applica ion o nico inamide alone (T4),
in combina ion wi h salicylic acid (T7), and in he in e ac ion among all h ee a enua o s
(T8), showing alues o 4.54, 4.55, and 4.58
µ
mol g
−1
DM, espec i ely. Con e sely, he
combina ion o p oline wi h salicylic acid (T5) esul ed in he highes le els o soluble ca bo-
hyd a es, equi alen o hose obse ed in he con ol (T0) and in he sal -s essed ea men
wi hou a enua o s (T1), wi h alues o 4.95, 5.01, and 5.00 µmol g−1DM, espec i ely.
Plan s 2025, 14, x FOR PEER REVIEW 9 o 22
Figu e 4. (a) Soluble ca bohyd a es, (b) ee amino acids, (c) soluble p o eins, (d) ee p oline in
lowe s, and (e) ee p oline in lea es o T opaeolum majus subjec ed o sal s ess and he applica ion
o salicylic acid (SA), nico inamide (NAM), and p oline (P o). T0 = con ol (0 mM NaCl); T1 = 40 mM
NaCl; T2 = 40 mM NaCl + P o; T3 = 40 mM NaCl + SA; T4 = 40 mM NaCl + NAM; T5 = 40 mM NaCl
+ P o + SA; T6 = 40 mM NaCl + P o + NAM; T7 = 40 mM NaCl + SA + NAM; and T8 = 40 mM NaCl
+ P o + SA + NAM. Means ollowed by he same le e do no di e acco ding o he Sco –Kno es
(p ≤ 0.05). Ba s a e means ± s anda d e o (n = 4).
Salini y educed he con en s o ee amino acids in he lowe s o nas u ium (Figu e
4b). The con ol (T0) showed he highes accumula ion, wi h 15.74 µmol g
−1
DM. Unde
salini y condi ions, he highes con en s o ee amino acids we e obse ed in ea men s
wi hou a enua o s (T1) and wi h he applica ion o nico inamide alone (T4), combined
wi h p oline (T6), salicylic acid (T7), and wi h bo h a enua o s (T8), wi h alues o 14.7
(T1), 14.7 (T4), 14.8 (T6), 14.1 (T7), and 14.7 µmol g
−1
DM (T8), espec i ely. The applica ion
o nico inamide combined wi h salicylic acid (T7) inc eased he le els o soluble p o eins
in he lowe s, eaching 5.30 mg g
−1
DM (Figu e 4c). In con as , unde salini y wi hou
Figu e 4. (a) Soluble ca bohyd a es, (b) ee amino acids, (c) soluble p o eins, (d) ee p oline in
lowe s, and (e) ee p oline in lea es o T opaeolum majus subjec ed o sal s ess and he applica ion
Plan s 2025,14, 1156 9 o 21
o salicylic acid (SA), nico inamide (NAM), and p oline (P o). T0 = con ol (0 mM NaCl);
T1 = 40 mM
NaCl; T2 = 40 mM NaCl + P o; T3 = 40 mM NaCl + SA; T4 = 40 mM NaCl + NAM;
T5 = 40 mM
NaCl + P o + SA; T6 = 40 mM NaCl + P o + NAM; T7 = 40 mM NaCl + SA + NAM; and
T8 = 40 mM
NaCl + P o + SA + NAM
. Means ollowed by he same le e do no di e acco ding o he Sco –
Kno es (p≤0.05). Ba s a e means ±s anda d e o (n= 4).
Salini y educed he con en s o ee amino acids in he lowe s o nas u ium
(Figu e 4b)
. The con ol (T0) showed he highes accumula ion, wi h 15.74
µ
mol g
−1
DM. Unde salini y condi ions, he highes con en s o ee amino acids we e obse ed in
ea men s wi hou a enua o s (T1) and wi h he applica ion o nico inamide alone (T4),
combined wi h p oline (T6), salicylic acid (T7), and wi h bo h a enua o s (T8), wi h alues
o 14.7 (T1), 14.7 (T4), 14.8 (T6), 14.1 (T7), and 14.7
µ
mol g
−1
DM (T8), espec i ely. The
applica ion o nico inamide combined wi h salicylic acid (T7) inc eased he le els o soluble
p o eins in he lowe s, eaching 5.30 mg g
−1
DM (Figu e 4c). In con as , unde salini y
wi hou a enua o s (T1) and wi h he applica ion o p oline alone (T2), he le els o soluble
p o eins dec eased o 2.84 and 2.87 mg g−1DM, espec i ely.
F ee p oline le els in he lowe s (Figu e 4d) we e inc eased by he applica ion o
salicylic acid alone (T3) and in combina ion wi h nico inamide (T7), eaching alues o 1.87
and 1.89
µ
mol g
−1
DM, espec i ely. On he o he hand, he lowes ee p oline le el was
obse ed unde salini y wi hou a enua o s (T1), wi h 1.60
µ
mol g
−1
DM. F ee p oline
le els in he lea es (Figu e 4e) we e also in luenced by salini y and he applica ion o
a enua o s. All ea men s wi h a enua o s inc eased ee p oline le els compa ed o he
con ol (T0) and he sal -s essed ea men wi hou a enua o s (T1), which showed he
lowes alues a 1.16 and 1.25
µ
mol g
−1
DM, espec i ely. Howe e , he ea men s wi h
a enua o s did no di e signi ican ly om each o he .
2.5. G ow h and Biomass P oduc ion
The applica ion o a enua o s o nas u ium plan s cul i a ed unde sal s ess in lu-
enced g ow h and biomass p oduc ion (Figu e 5). The alles plan s we e obse ed wi h he
applica ion o salicylic acid (T3), eaching 51.1 cm, while he applica ion o p oline alone
(T2) esul ed in he sho es plan s a 34.7 cm (Figu e 5a). Sal s ess educed he numbe
o lea es compa ed o he con ol, highligh ing he nega i e impac s o his condi ion.
Howe e , he combined applica ion o nico inamide wi h salicylic acid (T7) esul ed in he
highes numbe o lea es (225.5) in sal -s essed plan s, indica ing a posi i e e ec o his
ea men in mi iga ing he damages caused by salini y (Figu e 5b).
Salini y and he applica ion o a enua o s in luenced he numbe o lowe s in nas-
u ium (Figu e 2c). The applica ion o salicylic acid (T3) and he combina ion o p oline
wi h nico inamide (T6) inc eased he numbe o lowe s, eco ding alues o 25.5 and 23.25,
espec i ely. The numbe o lowe buds (Figu e 5d) was also a ec ed, wi h he highes
alue obse ed in he ea men wi h nico inamide alone (T4), which eached 23.75 unde
sal s ess. Con e sely, he applica ion o p oline alone (T2) and i s combina ion wi h
salicylic acid (T5) esul ed in educ ions in he numbe o lowe buds, wi h alues o 10.25
and 10.75, espec i ely.
The d y mass o he s ems (Figu e 5e), lea es (Figu e 5 ), and lowe s (Figu e 5g) was
a ec ed by sal s ess and he applica ion o a enua o s. Unde salini y condi ions, he
combina ion o p oline wi h salicylic acid (T5) esul ed in he g ea es educ ion in s em d y
mass, eco ding 10.44 g. Con e sely, he highes alues o lea es d y mass we e obse ed
in he con ol (T0) and in he sal -s essed ea men wi hou a enua o s (T1), wi h 11.38
and 11.93 g, espec i ely. The applica ion o p oline alone (T2), combined wi h salicylic
acid (T5), and nico inamide alone (T4) educed he lea es’ d y mass unde sal s ess, wi h
alues o 6.92, 7.04, and 7.29 g, espec i ely. Rega ding lowe d y mass, he applica ion
Plan s 2025,14, 1156 16 o 21
o 15 min wi h 2 h in e als du ing bo h he day ime (6:00 a.m. o 6:00 p.m.) and nigh ime
(6:00 p.m. o 6:00 a.m.).
4.2. G ow h Condi ions
In he p esen s udy, he seeds o T. majus a . ‘AnãSo ida’ (ISLA Semen es, Po o
Aleg e, RS, B azil) we e sown in phenolic oam wi h 5 mm pe o a ions, p e iously s e -
ilized in a 5% sodium hypochlo i e solu ion, and main ained unde adequa e humidi y
condi ions o ge mina ion. The expe imen began wi h he sowing o one seed pe phenolic
oam cell. Eigh days a e sowing (DAS), he seedlings we e ans e ed o he nu se y
and kep in a nu ien solu ion (NS) o mula ed based on he ecommenda ions o Fu lani
e al. [
51
] a 50% concen a ion o ou days. A 12 DAS, he seedlings we e ans e ed
o he loa ing hyd oponic sys em and subjec ed o he p e-de ined salini y ea men s.
The nu ien solu ion was p epa ed ollowing an adap a ion o he ecommenda ions by
Fu lani e al. [
51
] a 100% concen a ion, and salini y was adjus ed o 40 mM by adding
sodium chlo ide (NaCl). P elimina y es s (unpublished da a) we e conduc ed unde he
same expe imen al condi ions p io o se ing up he expe imen desc ibed in his pape
o de e mine an NaCl concen a ion ha would cause mode a e sal s ess in he plan s.
The concen a ion o 40 mM NaCl was ound o be he mos sui able acco ding o hese
p elimina y es s.
Nine days a e ansplan a ion (DAT), olia applica ion o he a enua o s salicylic
acid (SA—1 mM, Sigma Ald ich, São Paulo, B azil), p oline (P o—10 mM, Syn h, Diadema,
SP, B azil), and nico inamide (NAM—300 mg L
−1
, Syn h, Diadema, SP, B azil) was ini ia ed.
The olia ea men was pe o med weekly, always in he ea ly mo ning, using manual
sp aye s equipped wi h d op egula o s. To enhance he adhesion o he a enua o s o he
lea su ace, Tween 20 (0.05%) was added o each solu ion applied. A o al o 550 mL o
each ea men was applied o each plan un il he end o he expe imen , wi h his amoun
being di ided in o six applica ions h oughou he cul i a ion pe iod. A 15 DAT, saline
wa e eplenishmen s (40 mM NaCl) we e ini ia ed, excep o he con ol ea men . These
eplenishmen s we e pe o med e e y i e days, always in he la e a e noon. A he same
in e als, measu emen s o he elec ical conduc i i y (EC) and pH o he nu ien solu ion
we e pe o med.
4.3. Va iables Analyzed
4.3.1. Gas Exchange
Gas exchange a iables we e measu ed using an in a ed gas analyze (IRGA, LICOR,
Lincoln, NE, USA). Measu emen s we e conduc ed be ween 8:00 and 10:00 a.m. unde
con olled condi ions, wi h a i icial ligh se o 1000
µ
mol pho ons m
−2
s
−1
, ambien CO
2
concen a ion, and empe a u e. The e alua ed a iables included s oma al conduc ance
(gs, mol H
2
O m
−2
s
−1
), ne pho osyn hesis a e (A,
µ
mol CO
2
m
−2
s
−1
), anspi a ion a e
(E, mmol H
2
O m
−2
s
−1
), in e cellula CO
2
concen a ion (Ci,
µ
mol CO
2
mol ai
−1
), ins an-
aneous wa e -use e iciency (WUE = A/E), in insic wa e -use e iciency (
iWUE = A/gs
),
and Ci/Ca a io. These measu emen s we e pe o med on ully expanded lea es om he
middle hi d o he plan s.
4.3.2. Pho osyn he ic Pigmen s
Fo he de e mina ion o he chlo ophyll a, chlo ophyll b, and ca o enoid con en s,
20 mg o lyophilized ma e ial was used. The ma e ial was ans e ed o es ubes, whe e
lea ex ac s we e collec ed, and 3 mL o 80% ace one was added. The ubes we e s o ed
unde e ige a ion (4
◦
C) in he da k o 24 h o ensu e pigmen s abili y. The samples we e
cen i uged a 14,000
×
g o 15 min, and he supe na an s we e collec ed. The con en s
o chlo ophylls and ca o enoids we e de e mined by spec opho ome y, wi h eadings
Plan s 2025,14, 1156 17 o 21
pe o med a wa eleng hs o 664.1 nm, 648.6 nm, and 470 nm, ollowing he me hodology
desc ibed by Lich en hale and Buschmann [
52
]. Addi ionally, o al chlo ophyll was
calcula ed as he sum o chlo ophyll a and b.
4.3.3. Ino ganic Solu es
To p epa e he samples o ino ganic solu e analysis, lowe s and lea es p e iously
d ied in an o en we e used. A e d ying, he ma e ial was g ound, and 0.1 g o each
sample was weighed and ans e ed o es ubes. Subsequen ly, 10 mL o deionized wa e
was added o each ube. The samples we e hen placed in a he mos a ic ba h a 100
◦
C
o 1 h. A e hea ing, he solu ions we e il e ed and p epa ed o subsequen analyses.
The con en s o Na
+
and K
+
we e de e mined using a lame pho ome e (model Q498M2,
QUIMIS, Diadema, SP, B azil) acco ding o he me hod desc ibed by Sil a e al. [
53
]. The Cl
−
con en was de e mined by spec opho ome y using a spec opho ome e (model 2000 UV,
BEL PHOTONICS, Pi acicaba, SP, B azil) based on he me hodology o Sil a e al. [54].
4.3.4. O ganic Solu es
Fo he de e mina ion o o ganic solu es, h ee lea es and h ee lowe s we e collec ed,
sepa a ely s o ed in bags, and subjec ed o lyophiliza ion. A e he lyophiliza ion p ocess,
he samples unde wen a wo-s ep ex ac ion p o ocol. Ini ially, 0.1 g o he lyophilized
ma e ial was weighed in o mic ocen i uge ubes (Eppendo ), and 1.5 mL o 80% e hanol
was added. The samples we e cen i uged a 14,000
×
g o 15 min, and he supe na an s
we e collec ed. Subsequen ly, 1.5 mL o 80% e hanol was added again o he esidue, and
he same p ocedu e was epea ed.
The quan i ica ion o soluble ca bohyd a es was pe o med acco ding o he me hod
desc ibed by Dubois e al. [
55
], using 0.5 mL o he ex ac and he phenol–sul u ic acid
me hod, wi h colo ime ic eading a 490 nm and D-(+)-glucose as he s anda d. The
de e mina ion o ee p oline was based on he me hod o Ba es e al. [
56
], using 0.5 mL o
he ex ac and ninhyd in eagen , wi h a colo ime ic eading a 520 nm and pu e p oline
as he s anda d.
F ee amino acids we e quan i ied acco ding o he me hod o Yemm and Cocking [
57
],
using 0.5 mL o he ex ac and ninhyd in eagen , wi h a colo ime ic eading a 570 nm
and pu e L-leucine as he s anda d. Soluble p o eins we e de e mined using he B ad o d
me hod [
58
], employing 0.1 mL o he ex ac and he dye-binding me hod, wi h a eading
a 595 nm and bo ine se um albumin as he s anda d.
4.3.5. G ow h and P oduc ion
The biome ic analyses included measu ing plan heigh (PH), coun ing he numbe
o lea es, he numbe o lowe s, and he numbe o lowe buds. The p oduc ion analyses
in ol ed de e mining he d y mass o he s em, lea es, oo s, and lowe s. All collec ions
we e ca ied ou a he end o he expe imen al cycle, 51 days a e ansplan a ion (DAT).
To ob ain he da a, he plan s we e ha es ed and sepa a ed in o hei di e en componen s.
The ma e ials we e s o ed in pape bags and hen d ied in a o ced-ai ci cula ion o en a
65 ◦C o 72 h o de e mine he d y masses.
4.4. S a is ical Analysis
The da a ob ained we e subjec ed o analysis o a iance (ANOVA) using he F- es . All
da a we e es ed o no mali y (Shapi o–Wilk es ) and homogenei y o a iance (Ba le ’s
es ). T ea men means we e compa ed using he Sco –Kno es (p
≤
0.05). All s a is ical
analyses we e pe o med using he R so wa e e sion 4.3.1 [59].
Plan s 2025,14, 1156 18 o 21
5. Conclusions
The combina ion o nico inamide, salicylic acid, and p oline posi i ely in luenced
T opaeolum majus by imp o ing physiological and biochemical esponses unde sal s ess,
including enhanced gas exchange pa ame e s such as s oma al conduc ance, anspi a ion,
and in e cellula CO
2
concen a ion. This ea men also s abilized pho osyn he ic pigmen s,
p omo ed osmo ic balance by inc easing p oline and soluble suga le els, and educed he
de imen al e ec s o ion accumula ion and oxida i e s ess. Addi ionally, he combina ion
enhanced he s abili y o chlo oplas s and p o ec ed cellula s uc u es, esul ing in be e
o e all plan g ow h and biomass alloca ion, pa icula ly in ep oduc i e issues.
Au ho Con ibu ions: T.S.d.S., M.R.S.C., and T.I.d.S.: in es iga ion, w i ing—o iginal d a ; T.S.d.S.,
A.E.R.-C., and X.T.: isualiza ion and supe ision; T.I.d.S. and A.M.d.R.F.J.: unding acquisi ion,
alida ion, supe ision, w i ing— e iew and edi ing; J.E.d.S.R., E.F.d.S., A.E.R.-C., and R.F.R.: in-
es iga ion, w i ing—o iginal d a ; T.S.d.S., L.S.S., L.P.d.S.S., G.B.G.d.S., K.S.L., E.V.d.S.D., M.E.A.,
and M.C.B.d.O.R.: esou ces, in es iga ion, alida ion, me hodology, isualiza ion, w i ing; E.F.d.S.,
A.P.B.J., X.T., and T.G.F.d.S.: w i ing— e iew and edi ing. All au ho s ha e ead and ag eed o he
published e sion o he manusc ip .
Funding: This wo k was suppo ed by he Coo denação de Ape eiçoamen o de Pessoal de Ní el
Supe io —B azil (CAPES – Financing code 001), Conselho Nacional de Desen ol imen o Cien í ico
e Tecnológico (CNPq – Financing code 001), Fundação de Ampa o àPesquisa do Es ado da Bahia
(FAPESB), Ins i u o de Ciência, Ino ação e Tecnologia do Es ado da Bahia—Recu sos Híd icos
e Desen ol imen o Sus en á el (INCITE Economia Ve de), and Ins i u o Nacional de Ciência e
Tecnologia em Ag icul u a Sus en á el no Semiá ido T opical (INCT Ag iS).
Da a A ailabili y S a emen : All da a p oduced and/o analyzed in his s udy a e included in he
manusc ip . The co esponding au ho s a e a ailable o p o ide addi ional da a and ma e ials upon
easonable eques .
Acknowledgmen s: The au ho s hank he CAPES, CNPq, FAPESB, INCITE Economia Ve de, and
INCT Ag iS by suppo and unding. A.M.d.R.F.J. acknowledges suppo om he São Paulo Resea ch
Founda ion (FAPESP-2023/05323–4).
Con lic s o In e es : The au ho s decla e no con lic s o in e es .
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Disclaime /Publishe ’s No e: The s a emen s, opinions and da a con ained in all publica ions a e solely hose o he indi idual
au ho (s) and con ibu o (s) and no o MDPI and/o he edi o (s). MDPI and/o he edi o (s) disclaim esponsibili y o any inju y o
people o p ope y esul ing om any ideas, me hods, ins uc ions o p oduc s e e ed o in he con en .
