© The Authors, 2023, Published by the Universidad del Zulia
*Corresponding author: sarahbenkadja8@gmail.com
Sarah Benkadja
1
*
Abdelmalek Oulmi
2
Benalia Frih
2
Hocine Bendada
3
Ali Guendouz
4
Amar Benmahammed
2
Rev. Fac. Agron. (LUZ). 2023, 40(1): e234007
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v40.n1.07
Crop Production
Associate editor: Professor Andreina García de González
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
Keywords:
Electrolyte leakage
Chlorophyll loss
Tolerant
Sensitivity
Evaluation of chlorophyll content and membrane stability under oxidative stress induced
by g
lyphosate herbicide as i
ndicators
of drought tolerance in some advanced durum
wheat (Triticum durum L.) lines: in vitro study
Evaluación del contenido de clorola y la estabilidad de la membrana bajo estrés oxidativo inducido
por el herbicida glifosato como indicadores de tolerancia a la sequía en algunas líneas avanzadas
de trigo duro (Triticum durum L.): estudio in vitro
Avaliação do teor de clorola e da estabilidade da membrana sob estresse oxidativo induzido pelo
herbicida glifosato como indicadores de tolerância à seca em algumas linhagens avançadas de
trigo duro (Triticum durum L.): estudo in vitro
1
Department of Agronomy, VRBN Laboratory, Faculty of
Nature and Life Sciences, Farhat Abbas University of Setif,
Algeria.
2
Department of Biology and Plant Ecology, VRBN
Laboratory, Faculty of Nature and Life Sciences, Farhat
Abbas University of Setif, Algeria.
3
Department of Agricultural Sciences, Relizane University,
Relizane, Algeria.
4
National Agronomic Research Institute of Algeria (INRAA),
Setif Research Unit, Algeria.
Received: 16-11-2022
Accepted: 26-01-2023
Published: 04-02-2023
Abstract
Oxidative stress caused by glyphosate is a complex chemical and
physiological phenomenon and develops as a result of overproduction and
accumulation of reactive oxygen species (ROS). This study was carried out
in vitro at the National Institute of Agronomic Research of Algeria (INRAA)
Setif, to select the most susceptible durum wheat (Triticum durum L.) under
oxidative stress induced by glyphosate herbicide by evaluating chlorophyll
content degradation and cell membrane leakage. Genotypes showed
signicant variations in almost all the studied traits. The chlorophyll loss ratio
ranged from 26.42 % for the genotype G5 to 48.75 % for the local variety
Boutaleb, glyphosate sensitivity index values were found to be between
0.65-1.2, the advanced line G5 was found to be the most tolerant under
oxidative stress with the lowest chlorophyll loss ratio and lowest Glyphosate
sensitivity index. Furthermore, the advanced line G4 recorded the highest
electrolyte leakage (80.16 %) while G6 showed the lowest estimate (50.77
%). Therefore, advanced lines G5 and G6 appear the most suitable for the
growing conditions.
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(1): e234007. Enero-Marzo. ISSN 2477-9407.
2-5 |
Resumen
El estrés oxidativo causado por el glifosato es un fenómeno
químico y siológico complejo y se desarrolla como resultado
de la sobre producción y acumulación de especies reactivas del
oxígeno (ROS). Este estudio se llevó a cabo in vitro
en el Instituto
Nacional de Investigación Agronómica de Argelia (INRAA) Setif,
para seleccionar el trigo duro (Triticum durum L.) más susceptible
bajo estrés oxidativo inducido por el herbicida glifosato mediante
la evaluación de la degradación del contenido de clorola y la
fuga de la membrana celular. Los genotipos mostraron variaciones
signicativas en casi todos los rasgos estudiados. El índice de pérdida
de clorola osciló entre el 26,42 % del genotipo G5 y el 48,75 % de
la variedad local Boutaleb, y los valores del índice de sensibilidad al
glifosato se situaron entre 0,65 y 1,2. La línea avanzada G5 resultó
ser la más tolerante al estrés oxidativo, con el menor índice de pérdida
de clorola y el menor índice de sensibilidad al glifosato. Además,
la línea avanzada G4 registró la mayor pérdida de electrolitos (80,16
%), mientras que G6 mostró la estimación más baja (50,77 %). Por lo
tanto, las líneas avanzadas G5 y G6 parecen las más adecuadas para
las condiciones de crecimiento.
Palabras clave: fuga de electrolitos, pérdida de clorofila,
tolerancia, sensibilidad.
Resumo
Estresse oxidativo causado pelo glifosato é um fenômeno
químico e siológico complexo e se desenvolve como resultado da
superprodução e acúmulo de espécies reativas de oxigênio (ROS).
Este estudo foi realizado in vitro no Instituto Nacional de Pesquisas
Agronômicas da Argélia (INRAA) Setif, para selecionar o trigo duro
mais suscetível (Triticum durum L.) sob estresse oxidativo induzido
pelo herbicida glifosato, avaliando a degradação do teor de clorola e
o vazamento da membrana celular. Os genótipos mostraram variações
signicativas em quase todos os traços estudados. A taxa de perda
de clorola variou de 26,42 % para o genótipo G5 a 48,75 % para
a variedade local Boutaleb, os valores do índice de sensibilidade
ao glifosato foram encontrados entre 0,65-1,2, a linha avançada G5
foi encontrada como a mais tolerante sob estresse oxidativo com a
menor taxa de perda de clorola e o menor índice de sensibilidade
ao glifosato. Além disso, a linha avançada G4 registrou o maior
vazamento de eletrólitos (80,16%), enquanto G6 apresentou a
estimativa mais baixa (50,77 %). Portanto, as linhas avançadas G5 e
G6 parecem ser as mais adequadas para as condições de crescimento.
Palabras-chave: vazamento de eletrólitos, perda de clorola,
tolerante, sensibilidade.
Introduction
During the last 50 years, increased global population and varied
consumption preference have led to the elevated demand for wheat
commodities worldwide, also considering that wheat is a staple food
for more than 35 % of the world population (FAO, 2020). Durum
wheat often experiences drought stress conditions during crop cycle.
Thus, improvement of durum wheat tolerant to drought is a major
objective in plant breeding programs for arid and semi-arid regions
(Oulmi and Aissaoui, 2022; Singh et al., 2022; Thakur et al., 2022).
Glyphosate (N-[phosphonomethyl]-glycine) is the most commonly
used non-selective herbicide worldwide (Soares et al., 2019) since
its commercialisation by Monsanto in the 1970. Glyphosate has
been shown to aect plant physiological mechanisms such as
photosynthesis, mineral nutrition and oxidative events (Rivas-Garcia
et al., 2022; Singh et al., 2020; Gomes et al., 2014). Along with the
inhibition of specic target sites, glyphosate action also leads to
oxidative stress in plants, which is most probably a secondary eect
of the blocked shikimate pathway (Freitas-Silva et al., 2017; Gomes
et al., 2014). Oxidative stress in wheat and maize was observed in
plants exposed to glyphosate as a consequence of reactive oxygen
species (ROS) accumulation. Plants are able to avoid ROS adverse
eects by detoxify them through the action of both enzymatic and
non-enzymatic antioxidants. Additionally, increasing ROS production
may adversely aect photosynthetic processes, i.e. by decreasing
the amount of chlorophyll and the photochemical eciency, which
reduces plant growth. Indeed, previous studies have shown that plants
exposed to glyphosate application have lower chlorophyll content.
These ndings have been attributed to either increased chlorophyll
degradation or decreased chlorophyll synthesis (Ibrahim et al., 2022;
Gomes et al., 2017). Photosynthesis plays a vital role in the synthesis
and accumulation of organic matter, plant growth, nutrient absorption
and response to abiotic or biotic stress. The aim of this research is to
evaluate the behaviour of some advanced lines of durum wheat under
the eects of oxidative stress induced by glyphosate, based on the
estimation of chlorophyll degradation and electrolyte leakage from
injured cells in order to select the adapted advanced lines.
Materials and methods
Plant material
This study was conducted during the 2021/2022 cropping seasons
at National Institute of Agronomic Research of Algeria – INRAA -
Setif. The genetic material used in this study consisted of 6 advanced
lines and 4 genotypes, 3 out of them were local varieties used as
control to evaluate their performance under oxidative stress (table 1).
Table 1. The pedigrees of the genotypes lines tested.
Genotype/Lines
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
Bousselem Heider/Martes/Huevos de Oro. ICD-414
Boutaleb GTA dur /Ofanto
Oued el bared Hedba3/Ofanto
Experimental details
The genotypes tested were sown on December 14th, 2021 with
sowing density adjusted to 300 grains.m
-2
in a random block design
with three replications, each plot consisted of 6 lines of 10 m long
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Benkadja et al. Rev. Fac. Agron. (LUZ). 2023 40(1): e234007
3-5 |
spaced of 0.2 m which make 12 m
2
as plot area. At heading stage,
three ag leaves of each genotype were cut and dipped in 10 mL
of 5 mM glyphosate solution (dissolved in distilled water). Daily,
the chlorophyll contents (CC) of each ag leaf were measured using
digital chlorophyll meter (CCM) with (cci) units; this device allows
to measure the absorbance of light in the leaf. Electrolyte leakage of
leaf tissues were measured using the method developed by Baji et al.
(2001) with minor modications: two leaves were randomly collected
for each genotypes, washed with tap water then with distilled water
and cut into 1 cm length segments. The segments were placed in
tubes with 10 mL of distilled water and incubated for 24 h at the
ambient temperature of the laboratory. Subsequently, the rst reading
(EC1) was carried out. The nal conductivity (EC2) was measured
after adding 0.02 mL of pure glyphosate to each tube. The relative
electrolyte leakage (REL %) was calculated as follows: REL (%) =
(EC1/EC2) × 100. Glyphosate sensitivity index (GSI) was calculated
to determine the genotypes sensitivity to oxidative stress induced
by glyphosate herbicide, GSI = chlorophyll loss for each genotype
/ Mean.
Results and discussion
Degradation of Chlorophyll content
Chlorophyll content of leaf before and after 6 days of treatment
with glyphosate is presented in table 2. Chlorophyll content values
before treatment ranged from 31.85 cci for the advanced line G5 to
53.7 cci for the introduced genotype Jupare C 2001 with an average
of 45.76 cci over all genotypes, while after glyphosate application
during six days the chlorophyll content decreased and the values
varied between 4.35 to 14.32 cci, the highest value was obtained
from the advanced line (G1) while the variety Boutaleb registered the
lowest value. The decrease in total chlorophyll amount correlates with the
increase in the number of days after glyphosate application (gure 1). Ahsan
et al. (2008) found that using glyphosate herbicide causes plants to
experience oxidative stress. Our nding agree with Malalgoda et
al. (2020) who reported that glyphosate herbicide could reduce the
synthesis of chlorophyll content, which might lead to less starch
accumulating. Furthermore, Bali and Sidhu (2019) reported that
a signicant reduction in yield might be due to the reduced rates
of net photosynthesis, stomatal closure, and oxidative damage to
chloroplast. Chlorophyll losses due to oxidative stress induced by
glyphosate application and its velocity are shown in Table 2. ANOVA
showed that genotypes eect was highly signicant (P<0.05) with all
parameters calculated. Chlorophyll loss ratio has been used to detect
the genotypic dierences in response to glyphosate application. The
local variety Boutaleb showed the highest loss ratio (48.75 %), and the
highest value of Velocity of degradation of chlorophyll (9.23). On the
contrary, the lowest chlorophyll loss ratio (26.42 %) was registered
by the line G5, with the lowest Velocity of chlorophyll degradation
(4.64). Gomez et al. (2017) studied the response of willow to oxidative
stress induced by various glyphosate concentrations and found that
the decrease in chlorophyll concentration may also be due to its
Table 2. Chlorophyll content of leaf before and after glyphosate application, chlorophyll loss (%), index of sensitivity to glyphosate, and
velocity of chlorophyll degradation for genotypes tested.
Genotypes
CC before Gly
application
(cci)
CC after Gly
application
(6 Days after) (cci)
Chlorophyll loss
ratio(%)
Velocity of
chlorophyll
degradation
Gly sensitivity index
(GSI)
Score
G1
51.67
bc
14.32
a
37.35
de
6.16
e
0.93
de
4
G2
40.8
e
4.35
fg
36.45
de
6.44
de
0.9
de
3
G3
43.27
d
6.02
de
37.25
de
6.41
de
0.96 5
G4
44.97
d
6.82
bcd
38.15
d
6.79
d
0.95
d
7
G5
31.85
f
5.42
ef
26.42
f
4.64
g
0.65
f
1
G6
50.02
c
7.47
bc
42.55
c
7.35
c
1.06
C
8
Jupare C 2001
53.7
a
7.2
bcd
46.5
b
8.65
b
1.15
b
9
Bousselem
44.62
d
6.6
cde
38.02
d
6.64
d
0.94
d
6
Boutaleb
52.87ab 4.12
g
48.75
a
9.23
a
1.21
a
10
Oued el Bared
43.87
d
7.9
b
35.97
e
5.59
f
0.89
e
2
Mean
45.76 7.02 40.11 6.79 0.96
Min
31.85 4.12 26.42 4.64 0.65
Max
53.7 14.32 48.75 9.23 1.21
LSD (5%)
1.95 1.25 1.85 0.48 0.04
Eect genotype *** *** *** *** ***
***: highly signicant eect at 5%, CC: Chlorophyll content, Gly: glyphosate, GSI: Glyphosate sensitivity index.
Figure 1. Degradation of chlorophyll content for durum wheat
genotypes after glyphosate application.
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(1): e234007. Enero-Marzo. ISSN 2477-9407.
4-5 |
degradation by increased ROS content. Chlorophyll loss was shown
to be accompanied by the damage of the mesophyll chloroplasts,
which led to a lower photosynthetic rate (Khalilzadeh et al., 2016).
The study reported by Zobiole et al. (2011) demonstrated that
Glyphosate signicantly
decreased chlorophyll content in soybean
compared with the non-glyphosate control. This decrease could be
due to direct damage of the chloroplast in the presence of glyphosate,
as plants from all maturity groups exposed to a single or sequential
application of glyphosate frequently had chlorophyll concentrations
lower than plants that were not exposed to this herbicide. It’s also
well known that a decrease in the chlorophyll content could be
due to a decrease in the stomata aperture, aimed at limiting water
losses by evaporation and by increased resistance to the entry of
atmospheric CO
2
necessary for photosynthesis (Zhu et al., 2016;
Enneb et al., 2020). Karabulut and Çanakcı (2021) showed that the
oxidative stress created by glyphosate treatment caused decrease in
chlorophyll (a+b). As well, Caglar et al. (2011) analyzed the eects
of the herbicide paraquat on chlorophyll content, observing that
bread wheat varieties after paraquat herbicide treatment decreased
chlorophyll content. Glyphosate sensitivity index (GSI) for the
examined durum wheat varied between 0.65-1.21, the dierences
among all genotypes tested were highly signicant (table 2). The
variety Boutaleb was observed as the most sensitive to oxidative
stress followed by Jupare C 2001. However, advanced line G5
recorded the lowest GSI thus appeared as the most tolerant to
oxidative stress. Based on the ranking for traits illustrated in table
2, genotypes G5 and Oued el bared were the best performing under
oxidative stress.
Electrolyte leakage
Plant membranes are subject to changes often associated with
increases in permeability and loss of integrity under environmental
stresses (Masoumi et al., 2010). Evaluation of cell damage degree
was accomplished for the ten genotypes using membrane stability
index: Electrolyte leakage has been recommended as a useful
criterion for the selection of stress-tolerant cultivars in several crop
species (Slama et al., 2018). Moreover, ion leakage has been used
as an ecient measure for the evaluation of the damage induced by
herbicide that aects the integrity of the membranes (Silva et al.,
2016). There was a signicant dierence in the amount of electrolyte
leakage (REL %) from leaf tissues for the genotypes tested, with
a mean of 64.8 % (table 3). Line G6 exhibited the lowest value
implying that this genotype was the most resistant under oxidative
stress and line G4 the most susceptible ones. The ability of cell
membranes to control the rate of ion movement in and out of cells is
used as a test of damage to a great range of tissues (Masoumi et al.,
2010). Glyphosate caused oxidative damage in plants and disturbed
cellular homeostasis of plants. Under oxidative stress production of
ROS increased, thus oxidizing lipids of membranes, and increasing
their permeability that leads to ion leakage (Sakya et al., 2018).
Conclusion
Oxidative damage induced by glyphosate herbicide aects the
physiological parameters of the examined durum wheat. Hence, these
parameters can be used as a criterion to select adapted genotypes to
oxidative stress. Our study revealed signicant variations among
the genotypes (P<0.05). The genotypes with the lowest velocity of
chlorophyll degradation and the lowest chlorophyll ratio yielded
the lowest sensitivity to oxidative stress. The advanced line G5
was recorded as the most tolerant to oxidative stress. Based on our
ndings, the highest value of injured cells was observed in advanced
line G4, while line G6 recorded the lowest, indicating that it could
maintain high membrane integrity during oxidative stress. We can
conclude that both advanced lines G5 and G6 are very suitable to
the growing conditions.
Table 3. Changes in relative electrolyte Leakage (%) of ten
durum wheat genotypes under Oxidative stress.
Genotypes
REL%
G1
61.86
bcd
G2
64.29
bc
G3
66.67
bc
G4
80.16
a
G5
72.57
ab
G6
50.77
d
Jupare C 2001
61.73
bcd
Bousselem
58.2
cd
Boutaleb
69.42
abc
Oued el bared
62.35
bcd
Mean
64.8
Max
80.16
Min
50.77
CV
13
LSD
11,64
Eect genotype **
**: signicant eect at 5 %, REL%: Electrolyte leakage.
Literature cited
Ahsan, N., Lee, D.G., Lee, K.W., Alam, I., Lee, S.H., Bahk, J.D., Lee, B.H.
(2008). Glyphosate induced oxidative stress in rice leaves revealed by
proteomic approach. Plant Physiology and Biochemistry 46, 1062–
1070. https://doi.org/10.1016/j.plaphy.2008.07.002.
Bajji, M., Lutts, S and Kinet, J.M. (2001). Water decit eects on solute
contribution to osmotic adjustment as a function of leaf ageing in three
durum wheat (Triticum durum Desf.) cultivars performing dierently in
arid conditions. Plant Science 160(4), 669–681. https://doi.org/10.1016/
S0168-9452(00)00443-X.
Bali, A.S. and Sidhu, G.P.S. (2019). Abiotic Stress-Induced Oxidative Stress
in Wheat. M. Hasanuzzaman et al. (eds.), Wheat Production in
Changing Environments, Springer Nature Singapore Pte Ltd. https://
doi.org/10.1079/9781789248098.0019.
Caglar, O., Ozturk, A., Aydin, M., Bayram, S. (2011). Paraquat tolerance of
bread wheat (Triticum aestivum L.) Genotypes. Journal of animal
and veterinary advances 10, 3363-3367. https://doi.org/10.3923/
javaa.2011.3363.3367.
Enneb, H., Ben Yahya, L., Ilyas, M., Asaram Dhale, D., Bagues, M. and
Nagaz, K. (2020). Inuence of Water Stress on Growth, Chlorophyll
Contents and Solute Accumulation in Three Accessions of Vicia faba
L. from Tunisian Arid Region. Abiotic stress in plants. http://dx.doi.
org/10.5772/intechopen.94563.
FAO. Food and Agriculture Organization. Crop Prospects and Food Situation
- Quarterly Global Report n°. 4, December (2020). Rome. http://www.
fao.org/faostat/en/#data/QC.
Freitas-Silva, L., Rodríguez-Ruiz, M., Houmani, H., da Silva, L.C., Palma,
J.M., and Corpas F.J. (2017). Glyphosate-induced oxidative stress in
Arabidopsis thaliana aecting peroxisomal metabolism and triggers
activity in the oxidative phase of the pentose phosphate pathway
(OxPPP) involved in NADPH generation. Journal Plant Physiology,
218, 196–205. https://doi.org/10.1016/j.jplph.2017.08.007.
Gomes, M. P., Le Manac’h, S. G., Hénault-Ethier, L., Labrecque, M., Lucotte,
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
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Benkadja et al. Rev. Fac. Agron. (LUZ). 2023 40(1): e234007
5-5 |
acid: an overview. Journal of Experimental Botany, 65(17), 4691–4703.
https://doi.org/10.1093/jxb/eru269.
Ibrahim, R.I.H., Alkhudairi, U.A., and Alhusayni, S.A.S. (2022). Alleviation
of Herbicide Toxicity in Solanum lycopersicum L.-An Antioxidant
Stimulation Approach. Plants, 11(17), 2261. https://doi.org/10.3390/
plants11172261.
Karabulut, F., and Çanakcı, S. (2021). Eects of Glyphosate Herbicide on
Photosynthetic Pigments and Antioxidant Enzyme Activities in Corn
(Zea mays L.) and Wheat (Triticum aestivum L.) Varieties. Journal of
Physical Chemistry and Functional Materials, 4(2), 61-66. https://doi.
org/10.54565/jphcfum.1004433
Khalilzadeh, R., Shari, R., and Jalilian, J. (2016). Antioxidant status and
physiological responses of wheat (Triticum aestivum L.) to cycocel
application and bio fertilizers under water limitation condition. Journal
of Plant Interactions, 11(1), 130-137. https://doi.org/10.1080/17429145
.2016.1221150.
Malalgoda, M., Ohm, J.B, Howatt, K.A., and Simsek, S. (2020). Pre-harvest
glyphosate application and eects on wheat starch chemistry: Analysis
from application to harvest. Journal of Food Biochemistry, 44(8), e13330.
https://doi.org/10.1111/jfbc.13330.
Masoumi, A., Ka, M., Khazaei, H., and Davari, K. (2010). Eect of drought
stress on water status, electrolyte leakage and enzymatic antioxidants of
kochia (Kochia scoparia) under saline condition. Pakistan Journal of
Botany, 42(5), 3517-3524.
Oulmi, A., and Aissaoui, M.R. (2022). Canopy temperature and chlorophyll content
as plant traits indicators for durum wheat (Triticum durum Desf.) superior
lines selection under semi-arid conditions. Agricultural Science and
Technology, 14(2), 114-122. https://doi.org/10.15547/ast.2022.02.027.
Rivas-Garcia, T., Espinosa-Calderón, A., Hernández-Vázquez, B., and
Schwentesius-Rindermann, R. (2022). Overview of Environmental and
Health Eects Related to Glyphosate Usage. Sustainability, 14(11), 6868.
https://doi.org/10.3390/su14116868.
Sakya, A.T., Sulistyaningsih, E., Indradewa, D., and Purwanto, B.H. (2018).
Physiological characters and tomato yield under drought stress. IOP
Conference Series: Earth and Environmental Science 200, 012043.
https://doi.org/10.1088/1755-1315/200/1/012043.
Silva, K.S., Urban, L.J. K., Balbinota, A., Gnocato, F.S., KRUSE, N.D.,
Marchesan, E., and Machado, S.L.O. (2016). Electrolyte Leakage and
the Protective Eect of Nitric Oxide On Leaves Of Flooded Rice Exposed
To Herbicides. Planta Daninha, 29(4), 837-847. https://doi.org/10.1590/
S0100-83582016340400018.
Singh, S.K, Kumar, J. P., Kaur G.S., Datta, S., Singh, V., Dhaka, D., Kapoor, A.B.,
Wani, D. S., Dhanjal, M., Kumar, L., Harikumar, and J. Singh. (2020).
Herbicide Glyphosate: Toxicity and Microbial Degradation. International
Journal of Environmental Research and Public Health, 17(20): 7519.
https://doi.org/10.3390/ijerph17207519.
Singh, S.K., Barman, M., Prasad J.P., and Bahuguna. R.N. (2022). Phenotyping
diverse wheat genotypes under terminal heat stress reveal canopy
temperature as critical determinant of grain yield. Plant Physiology
Reports 27, 335-344. https://doi.org/10.1007/s40502-022-00647-y
Slama, A., Mallek-Maalej, E., Ben Mohamed, H., Rhim, T., and Radhouane, L.
(2018). A return to the genetic heritage of durum wheat to cope with
drought heightened by climate change. PLoS ONE 13(5), e0196873..
https://doi.org/10.1371/journal.pone.0196873.
Soares, C., Pereira, R., Spormann, S., and 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. Environmental pollution, 247, 256-265. https://doi.org/10.1016/j.
envpol.2019.01.063.
Thakur, V., Rane, J., and Nankar, A.N. (2022). Comparative Analysis of Canopy
Cooling in wheat under High Temperature and Drought Stress. Agronomy,
12(4), 978. https://doi.org/10.3390/agronomy12040978.
Zhu, M., Li F.H., and Shi, Z.S. (2016). Morphological and photosynthetic
response of waxy corn inbred line to waterlogging. Photosynthetica 54,
636–640. https://doi.org/10.1007/s11099-016-0203-0.
Zobiole, L.H.S., Kremer, R.J., Oliveira, J.R.S., Constantin, J., and Oliveira
RS. (2011). Glyphosate aects chlorophyll, nodulation and nutrient
accumulation of “second generation” glyphosate-resistant soybean
(Glycine max L.). Pesticide Biochemistry and Physiology 99, 53–60.
https://doi.org/10.1016/j.pestbp.2010.10.005.