© The Authors, 2023, Published by the Universidad del Zulia*Corresponding author: sarahbenkadja8@gmail.com
Keywords:
Membrane damage
Glyphosate
Reactive oxygen species
Tolerance
Lipid Peroxidation, Proline Content and Soluble Sugars as indicators of Oxidative Stress
Tolerance in Some Advanced Durum Wheat Lines (Triticum durum Desf.).
Peroxidación lipídica, contenido en prolina libre y azúcares solubles como indicadores de tolerancia
al estrés oxidativo en algunas líneas avanzadas de trigo duro (Triticum durum Desf.).
Peroxidação lipídica, teor de prolina livre e açúcares solúveis como indicadores de tolerância ao
estresse oxidativo em algumas linhagens avançadas de trigo-duro (Triticum durum Desf.).
Abdelmalek Oulmi
1
Sarah Benkadja
2*
Ali Guendouz
3
Benalia Frih
1
Amor Mehanni
4
Samir Selloum
4
Rev. Fac. Agron. (LUZ). 2023, 40(2): e234018
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v40.n2.08
Crop Production
Associate editor: Professor Andreina García de González
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
1
Department of Biology and Plant Ecology, Valorization
of Natural Biological Resources Laboratory, Farhat Abbas
University Setif 1, Algeria.
2
Department of Agronomy, Valorization of Natural
Biological Resources Laboratory, Farhat Abbas University
of Setif, Algeria.
3
National Institute of Agronomic Research of Algeria
(INRAA), Setif Unit, Algeria.
4
Technical Institute of Field Crops, Setif, Algeria.
Received: 18-03-2023
Accepted: 28-04-2023
Published: 23-05-2023
Abstract
Oxidative stress induced by glyphosate is a complex phenomenon caused
by an imbalance between reactive oxygen species (ROS) and antioxidants
in plants cells. The present research was carried out at the eld crops
institute, Agricultural Experimental Station of Setif (ITGC-AES), to assess
the response of some durum wheat (Triticum Durum Desf.) lines exposed
to oxidative stress induced by glyphosate herbicide. In the heading stage,
a solution of 5 Mm of glyphosate was sprayed on ag leaves, and each
measurement was taken 48 hours after the glyphosate application. Lipid
peroxidation, free proline and soluble sugars were determined. The results
indicated that oxidative stress increased the content of lipid peroxidation,
proline, and soluble sugars in ag leaves. Analysis of variance revealed
signicantdierencesamongthegenotypestested,theincreaseinthelevel
of lipid peroxidation is much higher in advanced lines G5 and G3, in which
lipid peroxidation and membrane damage are greater. Oxidative damage also
increased the proline content in lines G3 and G4, and soluble sugars in line
G5, which were showing a high tolerance to the oxidative stress induced.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2023, 40(2): e234018. Abril-Junio. ISSN 2477-9407.2-5 |
Resumen
El estrés oxidativo inducido por el glifosato es un fenómeno
complejo causado por un desequilibrio entre las especies de oxígeno
reactivo (ROS) y los antioxidantes en las células de las plantas. La
presente investigación se llevó a cabo en el instituto de cultivos de
campo, Estación Experimental Agrícola de Setif (ITGC-AES), para
evaluar la respuesta de lineas de trigo duro (Triticum Durum Desf.)
expuestas al estrés oxidativo inducido por el herbicida glifosato. En
la etapa de encabezamiento, se pulverizó una solución de 5 Mm de
glifosato en las hojas bandera, y cada medición se tomó 48 horas
después de la aplicación del glifosado. Se determinó la peroxidación
de lípidos, prolina libre y azúcares solubles. Los resultados indicaron
que el estrés oxidativo aumentó el contenido de Peroxidación
lipídica, prolina y azúcares solubles en las hojas bandera. El análisis
de la varianza reveló diferencias signicativas entre los genotipos
probados, el aumento del nivel de Peroxidación lipídica es mucho
mayor en las líneas avanzadas G5 y G3, en las que la peroxidación de
lípidos y el daño de la membrana son mayores. Los daños oxidativos
también aumentaron el contenido de prolina en las líneas G3 y G4, y
azúcares solubles en la línea G5, que mostraban una alta tolerancia al
estrés oxidativo inducido.
Palabras clave: daño de membrana, glifosato, especies de oxígeno
reactivo, tolerancia.
Resumo
O estresse oxidativo induzido pelo glifosato é um fenômeno
complexo causado por um desequilíbrio entre espécies reativas de
oxigênio (ROS) e antioxidantes nas células vegetais. A presente
pesquisa foi realizada no instituto de culturas de campo, Estação
Experimental Agrícola de Setif (ITGC-AES), para avaliar a resposta
de algum trigo duro (Triticum Durum Desf.) linhas expostas ao estresse
oxidativo induzido pelo herbicida glifosato. Na fase de pontuação,
uma solução de 5 mm de glifosato foi pulverizada sobre as folhas
de bandeira, e cada medição foi tomada 48 horas após a aplicação
do glyphosate. A peroxidação lipídica, a prolina livre e os açúcares
solúveis foram determinados. Os resultados indicaram que o estresse
oxidativo aumentou o teor de Peroxidação lipídica, prolina e açúcares
solúveis nas folhas de bandeira. A análise da variância revelou
diferenças signicativas entreos genótipos testados, o aumento do
nível de Peroxidação lipídica é muito maior nas linhas avançadas
G5 e G3, nas quais a peroxidação lipídica e danos à membrana são
maiores. Os danos oxidativos também aumentaram o teor de prolina
nas linhas G3 e G4, e açúcares solúveis na linha G5, que estavam
mostrando uma alta tolerância ao estresse oxidativo induzido.
Palavras-chave: danos à membrana, glifosato, espécies reativas de
oxigênio, tolerância
Introduction
Cereal cultivation is very ancient in Algeria due to its utilization
as human and animal food (Ladoui et al., 2020). Among cereals,
durum wheat (Triticum durum Desf.) is an important cereal crop
in the Mediterranean basin that has been cultivated for centuries
under widely varying climatic conditions (Ben M’Barek et al.,
2022). It is cultivated worldwide over almost 17 million ha, with a
global production of 38.1 million tons in 2019 (Xynias et al., 2020).
Glyphosate (N-(phosphonomethyl)-glycine) is one of the most
extensively used herbicide substances in modern agriculture because
of its broad spectrum of weed control (Sergiev et al.,2020).Itaects
not only weeds but crop plants as well, leading to oxidative stress and
disturbed cellular homeostasis in plants (Gomes et al., 2014; Zhao
et al., 2020). Thus, glyphosate might stimulate the development of
reactive oxygen species (ROS), resulting in oxidative stress (Spormann
et al., 2019). Chaki et al. (2020) stated that high concentrations of
reactive species in plants disturb redox homeostasis, which could
trigger damage to membrane lipids, proteins, and nucleic acids.
Lipid peroxidation can be described generally as a process under
which oxidants such as free radicals or non-radical species attack
lipids containing carbon-carbon double bonds (Ayala et al., 2014).
The degree of lipid peroxidation is evaluated by the malondialdehyde
content. It is one of the nal products of lipid peroxidation and is
frequently used as an indicator of oxidative stress since it reects
the degree of oxidative degradation of membranes (Sharma et al.,
2016; Spormann et al., 2019). Similarly, Singh and Rathore (2017)
noticed that the accumulation of malondialdehyde content in pea
plants revealed lipid peroxidation. Plants evolved mechanisms to deal
with oxidative stress caused by the accumulation of reactive oxygen
species (ROS). Hence, plants accumulate certain solutes known
as osmolytes to limit cellular damage and maintain the osmotic
dierencesbetweenthecell’ssurroundingmembraneandthecytosol
(Sharma et al., 2019). Among the frequent osmolytes that play an
important role in osmoregulation are proline and sugar. Proline is an
aminoacidthatplaysabenecialroleinplantsexposedtostressful
conditions, i.e., as a metal chelator, an antioxidative defense molecule
and a signaling molecule. Furthermore, a positive correlation between
the accumulation of proline and improving stress tolerance in plants
has been revealed (Elewa et al., 2017; Hosseinifard et al., 2022).
According to Rajametov et al. (2021), Proline protects the cell from
damage caused by lipid peroxidation and detoxies the membrane
due to reactive oxygen species. In addition, several studies have
reported that proline plays various roles during stressful conditions,
which can improve protein stability and protect membrane integrity
by binding to hydrogen bonds. Furthermore, proline may protect cells
by increasing water uptake potential and facilitating the activation of
enzymes Hosseinifard et al., 2022). Similar, to proline, soluble sugars
serve as an osmoprotectant, aid in maintaining cell homeostasis, and
reactiveoxygenspeciesdetoxication,andactasasignalingmolecule
under stressful conditions (Chauhan et al., 2022). Furthermore,
sugars play an active role in the regulation of photosynthesis, osmotic
homeostasis, and membrane stabilization. The present research aimed
to determine the oxidative stress tolerance of some durum wheat lines
by assessing the degree of lipid peroxidation, proline content, and
soluble sugars accumulation.
Material and methods
Plant material and growth conditions
This study was carried out during the 2021–2022 cropping season
at the Agricultural Experimental Station of Setif (Algeria), (ITGC-
AES, 36° 12’N and 05° 24’E and 1.081 masl), Algeria. Six advanced
lines and four varieties are included in the genetic material, three
of which are local varieties (table 1). All genotypes were sown in
randomized complete block design with three replications, each plot
consisted of six row with 2.5 m long, spaced 20 cm between rows.
At the heading stage, in each plot, we sprayed four leaves from each
genotype with a 5 mM glyphosate solution. All measurements were
performed 48 hours after glyphosate treatments.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Oulmi et al. Rev. Fac. Agron. (LUZ). 2023 40(2): e234018
3-5 |
Table 1. The pedigrees of the durum wheat genotypes tested.
Genotype Pedigrees
G1
RASCON_37/GREEN_2/9/USDA595/3/D67.3/RABI//
CRA/4/ALO/5/…
G2
MINIMUS_6/PLATA_16//IMMER/3/SOOTY_9/
RASCON_37/9/…
G3 CMH77.774/CORM//SOOTY-9/RASCON-37/3/SOMAT-4
G4 CNDO/PRIMADUR//HAI-OU-17/3/SNITAN/4/SOMAT-3/
G5
CNDO/VEE//CELTA/3/PATA_2/6/ARAM_7//CREX/
ALLA/5/ENTE/...
G6
SILVER 14/MOEWE//BISU_l/PATKA_3/3/PORRON_4/
YUAN_l/9/...
Jupare C 2001 STINKPOT//ALTAR-84/ALONDRA
Bousselam Heider/Martes/Huevos de Oro. ICD-414
Boutaleb GTA dur /Ofanto
Oued el bared Hedba3/Ofanto
Lipid peroxidation
Oxidative damage to lipids was evaluated by quantifying the
content of malondialdehyde (MDA) in leaf samples. Leaf samples (200
mg)weregroundtonepowderinliquidnitrogenusingamortarand
pestle and homogenized with 3 ml of a 50 mM potassium phosphate
buer(pH7.5).An equivalentvolumeof0.5%thiobarbituric acid
was added, the mixture was placed in a boiling water bath for 30
min and centrifuged at 3000 × g for 10 min, and the absorbance was
measured at 532 and 600 nm (Zhang et al., 2013). The MDA content
was calculated as described by Bao et al. (2009): [MDA] (nmol.g
-1
FW)=[(Abs532–Abs600)xVt/εxFW]x1000.
Proline content and soluble sugars
For the quantication of proline content (PC) in fresh leaves,
the method given by Monneveux and Nemmar (1986) was used.
The proline is extracted at 85 °C with methanol and stained by
ninhydrin in the presence of acetic acid, orthophosphoric acid, and
toluene. The measurement of the red color obtained is carried out on
aspectrophotometerat528nm.SolubleSugarswerequantiedvia
the anthrone reagent according to Staub (1963).
Results and discussion
Lipid peroxidation assay
Malondialdehyde (MDA) level is a product of lipid peroxidation;
it’s commonly used as a biomarker of oxidative stress (Morales
and Munné-Boschb, 2019). The data presented in table 2 showed
a signicant increase in levels of MDA content after glyphosate
treatments. The maximum increase in MDA was observed in line G5
(65.8 nmol.g
-1
FW), followed by line G3 (52.83 nmol.g
-1
FW). The
signicantincreaseinMDAcontentindicatesastrongimbalanceof
the biomembrane lipid peroxidation in the herbicide-treated plants
(Shopova et al., 2021). However, we recorded a slight increase of
MDA content in genotypes Jupare C 2001, Boutaleb, and Oued el
bared with 21.09, 26.32, and 26.96 nmol.g
-1
FW respectively, with an
average of 35.24; genotypes with a lower level of lipid peroxidation
are considered more tolerant to oxidative damage. Both lines G5 and
G3 show a high positive deviation of MDA levels above the average
(gure1),indicatingahighdegradationoflipidsinthecellmembrane,
which is an indicator of severe oxidative stress. While genotypes
with a negative deviation have low oxidative damage and stable cell
membranes. Gomes et al. (2017) stated that oxidative stress caused
by herbicides increases lipid peroxidation (MDA concentration) in
plants. However, Shopova et al. (2021) observed that glyphosate
caused typical adverse alterations in wheat growth; glyphosate-
suppressed plant growth is a consequence of the accumulation
of ROS, which induce degradation in cellular biomembranes as
evidenced by the increased amount of MDA. It’s also known that
lipid peroxidation could have damaged the chloroplast by inhibiting
the synthesis of chlorophyll and thus photosynthesis (Langaro et al.,
2020). Membrane lipid peroxidation has often been used as a tool
to determine the degree of plant sensitivity to oxidative damage.
Tulkova and Kabashnikova (2021) found that lipid peroxidation
refers to a series of free radical reactions in unsaturated fatty acids
and that an increase in lipid peroxidation activity under prolonged
stress indicates a decline in the scavenging ability within plant cells.
KarabulutandCanakcı(2021)analyzedtheeectsoftheherbicide
glyphosate in maize and wheat varieties and observed that plants
produce antioxidant defense systems, including enzymatic and non-
enzymatic methods, as a result of ROS accumulation. Thus, as the
amount of ROS increases, the level of MDA begins to accumulate.
Furthermore, lipid peroxidation products induce a loss of membrane
integrity that ultimately leads to unadorned cytotoxicity, and could
resultinunrestrainedcellulargrowthorevenapoptosis.Ourndings
support several reports that also found an increased amount of MDA
content after glyphosate treatment in barley (Spormann et al., 2019),
tomato (Soares et al., 2019), and peas (Sergiev et al., 2020). Similarly,
Bouchemal et al. (2016) revealed that the oxidative stress mediated
by paraquat herbicide increased the level of lipid peroxidation in
wheat genotypes.
Figure 1. Deviation from the mean values of malondialdehyde
under oxidative stress in genotypes tested.
Proline content and soluble sugars accumulation
Based on the results in table 2, an increase in the accumulation
of free proline was observed in leaves treated with glyphosate;
the highest accumulations were observed for the lines G3 (54.17
µmol.g
-1
FW), and G4 (42.81 µmol.g
-1
FW). While, line G6 showed
the lowest value (19 µmol.g
-1
FW), with an overall mean of 33.61. It
is believed that this increase is due to oxidative damage induced by
glyphosate. Furthermore, Sergiev et al. (2020) reported that oxidative
damagecausedbyglyphosateapplicationincreasedsignicantlythe
proline content in pea plants; a similar response was also observed
in wheat (Shopova et al., 2021). Rapid accumulation of free proline
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2023, 40(2): e234018. Abril-Junio. ISSN 2477-9407.4-5 |
is a response to oxidative stress, with lines G4 and G3 showing
a high positive deviation from the average, which are considered
themost tolerant under oxidativestress (gure 2). Proline serves
as an important molecule in oxidative stress resistance (Kishor et
al., 2022). Thus, it plays a role against oxidative damage due to its
ability to eliminate ROS from the cell or activate an antioxidant
defense mechanism (Langaro et al.,2020). According to Gomes
et al. (2017), increased cellular ROS concentrations commonly
stimulate proline biosynthesis. Proline can also act as a mediator
of osmotic adjustment and protection of the plasma membrane as
a source of carbon and nitrogen (Hemaprabha et al., 2013). Many
studies have supported the idea that proline plays a diverse role
during oxidative stress, including improving photosynthesis and
interact with several molecules of signaling, such as nitric oxide and
phytohormones, to activate the stress signaling molecules (Hanif
et al., 2021; Rajametovet al., 2021). Like the proline content, the
levelofsolublesugarswasalsosignicantlyaectedbyglyphosate
treatments. Values of soluble sugars varied from 39.44 ug.g
-1
for line
G4 to 178.04 ug.g
-1
for line G5, with an overall average of 114.82.
The most stressed line, G5, has responded by increasing the total
amount of sugars in their cells, which is an indicator of adaptation
to oxidative damage (gure 3). Soluble sugars are an important
osmolytes, which limit cellular damage due to oxidative stress;
levels of sugar might also accumulate due to starch degradation
under stress conditions (Sharma et al.,2019).Our ndingsarein
agreement with Fernández-Escalada et al. (2019), who showed
that soluble sugars increased in Palmer amaranth treated with
glyphosate. Soluble sugar aids in maintaining the cellular redox
homeostasis, reactive oxygen species detoxication, and protect
photosynthesis systems (Chauhan et al., 2022).
Figure 2. Deviation from the mean values of free proline under
oxidative stress in genotypes tested.
Table 2. Change in Malondialdehyde content, proline content and soluble sugar in genotypes tested.
Genotypes Non-glyphosate conditions Glyphosate application
MDA
nmol.g
-1
FW
PC
µmol.g
-1
FW
SS
ug.g
-1
MDA
nmol.g
-1
FW
PC
µmol g-
1
FW
SS
μg·g-
1
G1 6
c
10.10
bc
63.24
bcd
34.77
bc
27.2
bc
100.6
bc
G2 5.74
c
7.81
bcde
77.86
abc
31.22
bc
25.85
bc
134.81
abc
G3 10.83
bc
14.48
a
66.48
bc
52.83
ab
54.17
a
127.3
abc
G4 8.12
bc
5.64
de
25.91
e
29.54
bc
42.81
ab
39.44
d
G5 20.9
a
10.65
ab
104.84
a
65.8
a
30.58
bc
178.81
a
G6 13.54
abc
4.07
e
69.94
bc
32.45
bc
19
c
103.59
bc
Jupare C 2001 5.29
c
11.28
ab
86.29
ab
21.09
c
39.78
ab
152.45
ab
Boussalam 11.22
bc
10.36
bc
76.54
bc
31.41
bc
35.25
bc
132.86
abc
Boutaleb 15.03
ab
6.54 39.31
de
26.32
c
27.79
bc
98.49
bc
Oued el bared 12.83
abc
9.07
bcd
56.51
cd
26.96
c
33.69
bc
79.84
cd
Mean 10.95 9 25.29 35.24 33.61 114.82
Min 5.29 4.07 25.91 21.09 19 39,44
Max 20.9 14.48 104.84 65.8 54.17 178.81
LSD 8.53 4.03 20.05 23.45 18.26 55.7
Eectgenotypes * ** ** * ** **
MDA:Malondialdehyde,PC:Prolinecontent,SS:Solublesugars,(*/**)signicantdierencesat0.05and0.01,respectively.
Figure 3. Deviation from the mean values of soluble sugars
under oxidative stress in genotypes tested.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Oulmi et al. Rev. Fac. Agron. (LUZ). 2023 40(2): e234018
5-5 |
ROS accumulation is directly correlated with sugar accumulation
to adapt to the ill eects of oxidative stress. In addition, sugar
accumulation prevents the oxidation of cell membranes under
waterdeciency,maintainstheturgidityofleaves,andpreventsthe
dehydration of membranes and proteins (Sami et al., 2016). Sensitive
genotypes of crop plants adapt fewer osmoprotectants with low
concentrations than tolerant genotypes under stress.
Conclusion
Oxidative stress induced by glyphosate is a complex phenomenon
thatnegativelyaectsplantgrowth.Ourndingsrevealedavariable
response to oxidative stress in the genotypes tested. The lipid
peroxidation assay revealed that both lines G3 and G5 recorded the
highest MDA content, which are the susceptible lines, and genotype
Jupare C 2001 is the most tolerant one. It also revealed that the
genotypes tested responded to oxidative damage by accumulating
proline and soluble sugars. Lines G3, G4, and G5 accumulated more
proline and sugars, which suggests they are the most adapted and
stable lines to oxidative stress.
Literature cited
Ayala, A., Muñoz, M.F., and Argüelles, S. (2014). Lipid Peroxidation: Production,
Metabolism, and Signaling Mechanisms of Malondialdehyde and
4-Hydroxy-2-Nonenal. Oxidative medicine and cellular longevity,
360438. https://doi.org/10.1155/2014/360438.
Bao, A.K., Wang, S.M., Wu, G.Q., Xi, J.J., Zhang, J.L., Wang, C.M. (2009).
Overexpression of the Arabidopsis H+-PPase enhanced resistance to
salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant
Science, 176, 232–240. https://doi.org/10.1016/j.plantsci.2008.10.009.
Ben M’Barek, S., Laribi, M., Kouki, H., Castillo, D., Araar, C., Nefzaoui, M.,
Ammar, K., Saint-Pierre, C., Yahyaoui, A.H. (2022). Phenotyping
Mediterranean Durum Wheat Landraces for Resistance to Zymoseptoria
tritici in Tunisia. Genes, 13, 355. https://doi.org/10.3390/genes13020355
Bouchemal, K., Bouldjadj, R., Belbekri, M.N., Ykhlef, N., and Djekoun, A. (2016).
Dierencesinantioxidantenzymeactivitiesandoxidativemarkersinten
wheat (Triticumdurum Desf.) genotypes in response to drought, heat and
paraquat stress. Archives of Agronomy and Soil Science, (63) 5. https://
doi.org/10.1080/03650340.2016.1235267.
Chaki, M., Begara-Morales, J.C., Barroso, J.B. (2020). Oxidative Stress in Plants.
Antioxidants, 9, 481. https://doi.org/10.3390/antiox9060481.
Chauhan, J., Srivastava, J.P., KumarSinghal, R., Soufan, W., KumarDadarwal, B.
(2022). Alterations of Oxidative Stress Indicators, Antioxidant Enzymes,
Soluble Sugars, and Amino Acids in Mustard [Brassica juncea (L.) Czern
and Coss.] in Response to Varying Sowing Time, and Field Temperature.
Frontiers in plant science,13: 875009. https://doi.org/10.3389/
fpls.2022.875009.
Elewa, T.A., Sadak, M.S., Saad, A.M. (2017). Proline treatment improves
physiological responses in quinoa plants under drought stress. Bioscience
Research, 14:21–33.
Fernández-Escalada, M., González, A., Monreal, M., Royuela, M., and Zabalza,
A. (2019). Physiological performance of glyphosate and imazamox
mixtures on Amaranthuspalmeri sensitive and resistant to glyphosate.
Scientic Reports, 9,18225. https://doi.org/10.1038/s41598-019-54642-9.
Gomes, M.P., Le Manach, S.G., Hénault-Ethier, L., Labrecque, M., and Juneau,
P. (2017). Glyphosate-Dependent Inhibition of Photosynthesis in
Willow. Frontiers in plant science, 8, 207. https://doi.org/10.3389/
fpls.2017.00207.
Gomes, M.P., Smedbol, E., Chalifour, A., Hénault-Ethier, L., Labrecque, M.,
Lepage, L., Lucotte, M., and Juneau, P. (2014). Alteration of plant
physiology by glyphosate and its by-product aminomethylphosphonic
acid: an overview. Journal of Experimental Botany, (65)17. https://doi.
org/10.1093/jxb/eru269.
Hanif, S., Saleem, M.F., Sarwar, M., Irshad, M., Shakoor, A., Wahid, M.A.,
Zaman Khan, H. (2021). Biochemically triggered heat and drought
stress tolerance in rice by proline application. Journal of Plant Growth
Regulation, 40, 305–312. https://doi.org/10.1007/s00344-020-10095-3.
Hemaprabha, G., Swapna, S., Leena Lavanya, D., Sajitha, B., Venkataramana
S. (2013). Evaluation of drought tolerance potential of elite genotypes
and progenies of sugarcane (Saccharum sp. hybrids). Sugar technology,
(15)1, 9-16.https://doi.org/10.1007/s12355-012-0182-9.
Hosseinifard, M., Stefaniak, S., GhorbaniJavid, M., Soltani, E., Wojtyla, L.,
and Garnczarska, M. (2022). Contribution of Exogenous Proline to
Abiotic Stresses Tolerance in Plants: A Review. International journal of
Molecular science, 23(9), 5186. https://doi.org/10.3390/ijms23095186.
Karabulut, F., and Canakcı, S. (2021). Eects of Glyphosate Herbicide on
Photosynthetic Pigments and Antioxidant Enzyme Activities in Corn
(Zea mays L.) And Wheat (Triticuma estivum L.) Varieties. Journal
of Physical Chemistry and Functional Materials, 4(2), 61-66. https://doi.
org/10.54565/jphcfum.1004433.
Kavi Kishor, P.B., Suravajhala, P., Rathnagiri, P., and Sreenivasulu, N.
(2022). Intriguing Role of Proline in Redox Potential Conferring High
Temperature Stress Tolerance. Frontiers Plant Science, 13, 867531.
https://doi.org/10.3389/fpls.2022.867531.
Ladoui, K., Mefti, M., and Benkherbache, N. (2020). Selection of drought tolerant
genotypes of barley (Hordeum vulgare L.) through stress tolerance
indices. Agrobiologia, 10, 1805-12. http://agrobiologia.net/online/
selection-de-genotypes-dorge-hordeum-vulgare-l-tolerants-au-stress-
hydrique-par-les-indices-de-tolerance-a-la-secheresse/
Langaro, A., Agostinetto, D., Ruchel, Q., Rodrigues Garcia, J., and TessariPerboni,
L. (2020). Oxidative stress caused by the use of preemergent herbicides
in rice crops. Revista CiênciaAgronômica, (48)2, 358-364. https://doi.
org/10.5935/1806-6690.20170041.
Monneveux, P., Nemmar, M. (1986). Contribution to the study of drought
resistance in soft wheat (Triticum aestivum L.) and durum wheat (Triticum
durum Desf.): study of the accumulation of proline during the during the
development cycle. Agronomy, 6 (6), 583-590. https://doi.org/10.1051/
agro:19860611
Morales, M., and Munné-Bosch, S. (2019). Malondialdehyde: Facts and
Artifacts. Plant Physiology, 180(3), 1246–1250. https://doi.org/10.1104/
pp.19.00405.
Rajametov, S.N., Yang, E.Y., Cho, M.C., Chae, S.Y., Jeong, H.B. (2021). Heat-
tolerant hot pepper exhibits constant photosynthesis via increased
transpiration rate, high proline content and fast recovery in heat stress
condition. Scientic Report, 12; 11(1), 14328. .https://doi.org/10.1038/
s41598-021-93697-5.
Sami, F., Yusuf, M., Faizan, M., Faraz, A., Hayat, S. (2016). Role of sugars under
abiotic stress. Plant Physiology et Biochemistry, 109, 54-61. https://doi.
org/10.1016/j.plaphy.2016.09.005
Sergiev,I.,Todorova,D.,Shopova,E.,Brankova,L.,Jankauskienė,J.,Jurkonienė,
S.,Gavelienė,V.,andMockeviciute.,R.(2020).Assessmentofsynthetic
auxin type compounds as potential modulators of herbicide action in
Pisum sativum L. Biologia,75,1845–1853. https://doi.org/10.3390/
agronomy10060793.
Sharma, A., Shahzad, B., Kumar, V., Kohli, S.K., Sidhu, G.P.S., Shreeya Bali,
A., Handa, N., Kapoor, D., Bhardwaj, R., and Zheng, B. (2019).
Phytohormones Regulate Accumulation of Osmolytes Under Abiotic
Stress. Biomolecules, 9(7), 285. https://doi.org/10.3390/biom9070285.
Sharma, P., Jha, A.B., Dubey, R.S. (2016). Oxidative stress and antioxidative
defense systems in plants growing under abiotic stresses. Handbook of
Plant and Crop Stress, p 109–158. https://doi.org/10.3390/antiox9080681.
Shopova, E., Brankova, L., Katerova, Z., Dimitrova, L., Todorova, D., Sergiev,
I., and Talaat, N.B. (2021). Salicylic Acid Pretreatment Modulates Wheat
Responses to Glyphosate. Crops, 1(2), 88–96. https://doi.org/10.3390/
crops1020009.
Singh, R., Rathore, D. (2017). Oxidative stress defence responses of wheat
(Triticuma estivum L.) and chilli (Capsicum annum L.) cultivars grown
under textile euent fertilization, Plant Physiology and Biochemistry.
123, 342-358. https://doi.org/10.1016/j.plaphy.2017.12.027.
Soares, C., Pereira, R., Spormann, S., Fidalgo, F. (2019). Is soil contamination by
a glyphosate commercial formulation truly harmless to non-target plants-
Evaluation of oxidative damage and antioxidant responses in tomato.
Environnemental Pollution., 247, 256–265. https://doi.org/10.1016/j.
envpol.2019.01.063.
Spormann, S., Soares, C., Fidalgo, F. (2019). Salicylic acid alleviates glyphosate-
induced oxidative stress in Hordeum vulgare L. Journal of Environmental
Management, 241, 226–23. https://doi.org/10.3390/crops1020009.
Staub, A.M. (1963). Extraction, identication and assays of carbohydrates in
organ extracts and bacterial bodies. In: Laboratory techniques, volumes 1
and 2, Masson, Paris, 1307-1366.
Tulkova, E., Kabashinikova, L. (2021). Malondialdehyde content in the leaves of
smallleaved linden tiliacordata and Norway maple acer platanoides under
the inuenceofvolatile organic compounds.Plant Biosystems, 156(2),
619-627 https://doi.org/10.1080/11263504.2021.1897701.
Xynias, I., Mylonas, I., Korpetis, G., Ninou, E., Tsaballa, A., Avdikos, I., and
Mavromatis, G. (2020). Durum Wheat Breeding in the Mediterranean
Region: Current Status and Future Prospects. Agronomy, 10, 432. https://
doi.org/10.3390/agronomy10030432.
Zhang,L.,Chen,L.,Zhang,H.,Ren,Z.,andLuo,P.(2013).Eectsofparaquat-
inducedoxidativestressonantioxidantsandchlorophylluorescencein
Stay-green wheat (Triticum aestivum L.) Flag leaves. Bangladesh Journal
of Botany, 42(2), 239-245. https://doi.org/10.3329/bjb.v42i2.18025.
Zhao, L., Xie, L., Huang, J., Su, Y., and Zhang, C. (2020). Proper Glyphosate
Application at Post-anthesis Lowers Grain Moisture Content at Harvest
and Reallocates Non-structural Carbohydrates in Maize. Frontiers in
plant sciences, 11: 580883. https://doi.org/10.3389/fpls.2020.580883.