Delineating drought-induced antioxidative traits as potential mechanisms for climate resilience in Argania spinosa

Authors

  • Abdelghani CHAKHCHAR Université Cadi Ayyad, Ecole Normale Supérieure de Marrakech, Laboratoire Interdisciplinaire de Recherche en Bioressources, Environnement et Matériaux, Marrakech 40000; Université Cadi Ayyad, Faculté des Sciences et Techniques, Centre Agrobiotechnologie et Bioingénierie, Unité de Recherche Labellisée CNRST (AgroBiotech-URL-CNRST 05), Marrakech 40000 (MA)
  • Merieme SOUFIANI Université Cadi Ayyad, Faculté des Sciences et Techniques, Centre Agrobiotechnologie et Bioingénierie, Unité de Recherche Labellisée CNRST (AgroBiotech-URL-CNRST 05), Marrakech 40000 (MA)
  • Mouna LAMAOUI Université Sultan Moulay Slimane, Faculté Polydisciplinaire, Laboratoire Polyvalent en Recherche et Développement, Beni Mellal (MA)
  • Abderrahim FERRADOUS Centre Régional de la Recherche Forestière, Marrakech (MA)
  • Said WAHBI Université Cadi Ayyad, Faculté des Sciences, Laboratoire Agro-Alimentaire, Biotechnologies et Valorisation des Bioressources Végétales, Marrakech 40000 (MA)
  • Abdelhamid EL MOUSADIK Université Ibn Zohr, Faculté des Sciences, Laboratoire de Biotechnologie et Valorisation des Ressources Naturelles (MA)
  • Saad IBNSOUDA-KORAICHI Université Sidi Mohamed Ben Abdellah, Faculté des Sciences et Techniques, Laboratoire de Biotechnologie Microbienne et de Molécules Bioactives (MA)
  • Abdelkarim FILALI-MALTOUF Université Mohammed V, Faculté des Sciences, Laboratoire de Microbiologie et Biologie Moléculaire, Centre de Biotechnologie Végétale et Microbienne Biodiversité et Environnement, Rabat 10000 (MA)
  • Cherkaoui EL MODAFAR Université Cadi Ayyad, Faculté des Sciences et Techniques, Centre Agrobiotechnologie et Bioingénierie, Unité de Recherche Labellisée CNRST (AgroBiotech-URL-CNRST 05), Marrakech 40000 (MA)

DOI:

https://doi.org/10.55779/nsb16312000

Keywords:

antioxidants, Argania spinosa, ascorbate-glutathione cycle, drought tolerance, oxidative stress, reactive oxygen species

Abstract

Drought stress ranks among the most critical environmental challenges facing agriculture today, causing significant impairments to plant growth and development. In Morocco, these negative impacts are projected to intensify further under the combined pressures of climate change and the worsening water shortage crisis. The imperative need for sustainable arganiculture (cultivation of Argane trees) in dry lands necessitates the expeditious identification of drought-tolerant elite Argania spinosa trees. In this context, we investigated the drought tolerance of 2-year-old A. spinosa seedlings from two contrasting provenances Lakhssas (LKS) and Aoulouz (ALZ) under severe stress by evaluating their antioxidative defense mechanisms. A total of 24 parameters related to reactive oxygen species (ROS), oxidative damage, and enzymatic and non-enzymatic antioxidant defense were measured and compared between both provenances. The results showed that the drought-stressed conditions significantly increased the activity of enzymatic antioxidants, including superoxide dismutase, catalase, peroxidase, polyphenoloxidase, glutathione peroxidase, glutathione S-transferase, and ascorbate-glutathione cycle enzymes, as well as the content of non-enzymatic antioxidants, including reduced glutathione (GSH), ascorbic acid (AsA), α-Tocopherols (α-toc), polyphenols, anthocyanins, and group thiols. The ability of A. spinosa trees to greatly enhance their antioxidant system to limit cellular damage caused by ROS production might be an important attribute linked to drought tolerance. Regarding the inter-provenance variation under drought stress conditions, LKS provenance exhibited superior antioxidative capacity through enhanced AsA-GSH cycle activity and elevated levels of AsA-GSH, α-toc, and polyphenols. However, ALZ demonstrated elevated anthocyanin levels and reduced peroxidative stress markers (hydrogen peroxide and malonyldialdehyde). Significant and positive correlations were recorded between studied ROS and antioxidants. Investigating the multifaceted antioxidative defense system underpinning drought tolerance in A. spinosa can facilitate the identification of drought-tolerant argane trees for the development of a future breeding program allowing sustainable arganiculture in dry lands.

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References

Aebi H (1984). Catalase in vitro. Methods in Enzymology 105:121-126. https://doi.org/10.1016/S0076-6879(84)05016-3

Axelrod B, Cheesbrough TM, Laakso S (1981). Lipoxygenase from soybeans: EC 1.13.11.12 linoleate: oxygenoxidoreductase. Methods in Enzymology 71:441-451. https://doi.org/10.1016/0076-6879(81)71055-3

Baccari S, Elloumi O, Chaari-Rkhis A, Fenollosa E, Morales M, Drira N, Ben Abdallah F, Fki L, Munné-Bosch S (2020). Linking leaf water potential, photosynthesis and chlorophyll loss with mechanisms of photo- and antioxidant protection in juvenile olive trees subjected to severe drought. Frontiers in Plant Science 11:614144. https://doi.org/10.3389/fpls.2020.614144

Beauchamp C, Fridovich I (1971). Superoxide dismutase: improved assays and applicable to acrylamide gels. Analytical Biochemistry 44:276-287. https://doi.org/10.1016/0003-2697(71)90370-8

Biswas MS, Mano J (2021). Lipid peroxide-derived reactive carbonyl species as mediators of oxidative stress and signaling. Frontiers in Plant Science 12:720867. https://doi.org/10.3389/fpls.2021.720867

Bowler CL, Slooten S, Vandenbranden R, De Rycke J, Botterman C, Sybesma M, Van Montagu M, Inzé D (1991). Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. The EMBO Journal 10:1723-1732. https://doi.org/10.1002/j.1460-2075.1991.tb07696.x

Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254. https://doi.org/10.1006/abio.1976.9999

Chae HB, Bae SB, Paeng SK., Wi SD, Phan KAT, Kim MG, Kim WY, Yun DJ, Lee SY (2023). The physiological role of thiol-based redox sensors in plant defense signaling. New Phytologist 239:1203-1211. https://doi.org/10.1111/nph.19018

Chaitanya KSK, Naithani SC (1994). Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertnf. New Phytologist 126:623-627. https://doi.org/10.1111/j.1469-8137.1994.tb02957.x

Chakhchar A, Ben Salah I, El Kharrassi Y, Filali-Maltouf A, El Modafar C, Lamaoui M (2022). Agro-fruit-forest systems based on argan tree in Morocco: A review of recent results. Frontiers in Plant Science 12:783615. https://doi.org/10.3389%2Ffpls.2021.783615

Chakhchar A, Aissam S, El Modafar C (2016a). Quantitative and qualitative study of phenolic compounds involved in germination inhibition of wheat under water deficit. Technology and Investment 7:86-95. https://doi.org/10.4236/ti.2016.73011

Chakhchar A, Lamaoui M, Aissam S, Ferradous A, Wahbi S, El Mousadik A, Ibnsouda Koraichi S, Filali-Maltouf A El Modafar C (2018). Physiological and biochemical mechanisms of drought stress tolerance in the argan tree. In: Ahmad P, Ahanger MA, Singh VP, Tripathi DK, Alam P, Alyemeni MN (Eds). Plant metabolites and regulation under environmental stress. 2018 Elsevier, Academic Press.

Chakhchar A, Haworth M, El Modafar C, Lauteri M, Mattioni C, Wahbi S, Centritto M (2017). An assessment of genetic diversity and drought tolerance in argan tree (Argania spinosa) populations: Potential for the development of improved drought tolerance. Frontiers in Plant Science 8:276. https://doi.org/10.3389/fpls.2017.00276

Cirillo V, D’Amelia V, Esposito M, Amitrano C, Carillo P, Caputo D, Maggio A (2021). Anthocyanins are key regulators of drought stress tolerance in tobacco. Biology 10:139. https://doi.org/10.3390/biology10020139

Corpas FJ, González-Gordo S, Rodríguez-Ruiz M, Muñoz-Vargas, MA, Palma, JM (2022). Thiol-based oxidative posttranslational modifications (OxiPTMs) of plant proteins. Plant and Cell Physiology 63:889-900. https://doi.org/10.1093/pcp/pcac036

Dvořák P, Krasylenko Y, Zeiner A, Šamaj J, Takáč T (2021). Signaling toward reactive oxygen species-scavenging enzymes in plants. Frontiers in Plant Science 11:618835. https://doi.org/10.3389/fpls.2020.618835

Edwards EA, Rawsthone S, Mullineaux PM (1990). Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278-284. https://doi.org/10.1007/bf00194008

Farooq MA, Niazi AK, Akhtar J, Saifullah, Farooq M, Souri Z, Karimi N, Rengel Z (2019). Acquiring control: The evolution of ROS-Induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiology and Biochemistry 141:353-369. https://doi.org/10.1016/j.plaphy.2019.04.039

Farouk S, AL-Huqail AA (2022). Sustainable biochar and/or melatonin improve salinity tolerance in borage plants by modulating osmotic adjustment, antioxidants, and ion homeostasis. Plants 11:765. https://doi.org/10.3390/plants11060765

Gailing O, Vornam B, Leinemann L, Finkeldey R (2009). Genetic and genomic approaches to assess adaptive genetic variation in plants: forest trees as a model. Physiologia Plantarum 137:509-519. https://doi.org/10.1111/j.1399-3054.2009.01263.x

García-Caparrós P, De Filippis L, Gul A, Hasanuzzaman M, Ozturk M, Altay V, Lao MT (2021). Oxidative stress and antioxidant metabolism under adverse environmental conditions: a Review. The Botanical Review 87:421-466. https://doi.org/10.1007/s12229-020-09231-1

Gill SS, Tuteja N (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48:909-930. https://doi.org/10.1016/j.plaphy.2010.08.016

Gohari S, Imani A, Talaei AR, Abdossi V, Asghari MR (2023). Physiological responses of almond genotypes to drought stress. Russian Journal of Plant Physiology 70:141. https://doi.org/10.1134/S1021443723601751

Guerfel M, Ouni Y, Boujnah D, Zarrouk (2009). Photosynthesis parameters and activities of enzymes of oxidative stress in two young ‘Chemlali’ and ‘Chetoui’ olive trees under water deficit. Photosynthetica 47: 340-346. https://doi.org/10.1007/s11099-009-0054-z

Habig WH, Jacoby WB (1981). Assays for differentiation of glutathione S-transferases. Methods in Enzymology 77:398-405. https://doi.org/10.1016/s0076-6879(81)77053-8

Habig WH, Pabst MJ, Jakoby WB (1974). Glutathione-S-transferases: The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249:7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8

Haider MS, Kurjogi MM, Khalil-ur-Rehman M, Pervez T, Songtao J, Fiaz M, Jogaiah S, Wang C, Fang J (2018). Drought stress revealed physiological, biochemical and gene-expressional variations in ‘Yoshihime’ peach (Prunus Persica L) cultivar. Journal of Plant Interactions 13:83-90. https://doi.org/10.1080/17429145.2018.1432772

Hasanuzzaman M, Nahar K, Gill SS, Fujita M (2014). Drought stress responses in plants, oxidative stress, and antioxidant defense. In: Tuteja N, Gill SS (Eds). Climate change and plant abiotic stress tolerance, 1st Edition, Wiley-VCH Verlag GmbH & Co. KGaA.

Hernandez JA, Almansa MS (2002). Short-term effects of salt stress on antioxidant systems and leaf water relations of pea leaves. Physiologia Plantarum 115:251-257. https://doi.org/10.1034/j.1399-3054.2002.1150211.x

Hossain MA, Nakano Y, Asada K (1984). Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant and Cell Physiology 25:385-395. https://doi.org/10.1093/oxfordjournals.pcp.a076726

Jaleel CA, Gopi R, Manivannan P, Gomathinayagam M, Sridharan R, Panneerselvam R (2008). Antioxidant potential and indole alkaloid profile variations with water deficits along different parts of two varieties of Catharanthus roseus. Colloids and Surfaces B: Biointerfaces 62:312-318. https://doi.org/10.1016/j.colsurfb.2007.10.013

Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ (2019). The role of the plant antioxidant system in drought tolerance. Antioxidants 8:94. https://doi.org/10.3390/antiox8040094

Levine RL, Willians JA, Stadtman ER, Shacter E (1994). Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology 233:346-363. https://doi.org/10.1016/s0076-6879(94)33040-9

Mobin M, Khan NA (2007). Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. Journal of Plant Physiology 164:601-610. https://doi.org/10.1016/j.jplph.2006.03.003

Moore BM, FIurkey WH (1990). Sodium dodecyl sulfate activation of a plant polyphenol oxidase. Effect of sodium dodecyl sulfate on enzymatic and physical characteristics of purified broad bean polyphenoloxidase. Journal of Biological Chemistry 265:4982-4988. https://doi.org/10.1016/S0021-9258(19)34072-4

Mouafik M, Chakhchar A, Ouajdi M, El Antry S, Ettaleb I, Aoujdad J, El Aboudi A (2022). Drought Stress Responses of four contrasting provenances of Argania spinosa. Environmental Sciences Proceedings 16:25. https://doi.org/10.3390/environsciproc2022016025

Muñoz P, Munné-Bosch S (2019). Vitamin E in plants: biosynthesis, transport, and function. Trends in Plant Science 24:1040-1051. https://doi.org/10.1016/j.tplants.2019.08.006

Nag S, Saha K, Choudhuri A (2000). A rapid and sensitive assay method for measuring amine oxidase based on hydrogen peroxide-titanium complex formation. Plant Science 157:157-163. https://doi.org/10.1016/s0168-9452(00)00281-8

Nagalakshmi N, Prasad MNV (2001). Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Science 160:291-299. https://doi.org/10.1016/s0168-9452(00)00392-7

Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 11:867-880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Peng B, Guan K, Tang J, Ainsworth EA, Asseng S, Bernacchi CJ, … Zhou W (2020) (2020). Towards a multiscale crop modelling framework for climate change adaptation assessment. Nature Plants 6:338-348. https://doi.org/10.1038/s41477-020-0625-3

Pinheiro HA, Damatta FM, Chaves ARM, Fontes EPB, Loureiro ME (2004). Drought tolerance in relation to protection against oxidative stress in clones of Coffea canephora subjected to long-term drought. Plant Science 167:1307-1314. https://doi.org/10.1016/j.plantsci.2004.06.027

Rajput V.D, Harish, Singh RK, Verma KK, Sharma L, Quiroz-Figueroa FR, Meena M, Gour VS, Minkina T, Sushkova S, Mandzhieva S (2021). Recent developments in enzymatic antioxidant defence mechanism in plants with special reference to abiotic stress. Biology 10:267. https://doi.org/10.3390/biology10040267

Rico-Chávez AK, Franco JA, Fernandez-Jaramillo AA, Contreras-Medina LM, Guevara-González RG, Hernandez-Escobedo Q (2022). Machine learning for plant stress modeling: a perspective towards hormesis management. Plants 11:970. https://doi.org/10.3390/plants11070970

Safronov O, Kreuzwieser J, Haberer G, Alyousif MS, Schulze W, Al-Harbi N, … Kangasjärvi J (2017). Detecting early signs of heat and drought stress in Phoenix dactylifera (date palm). PLoS One 12:e0177883. https://doi.org/10.1371/journal.pone.0177883

Šamec D, Karalija E, Šola I, Vujčić Bok V, Salopek-Sondi B (2021). The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants 10:118. https://doi.org/10.3390/plants10010118

Sofo A, Dichio B, Xiloyannis C, Masia A (2005). Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Functional Plant Biology 32:45-53. https://doi.org/10.1071/FP04003

Srivastav AL, Dhyani R, Ranjan M, Madhav S, Sillanpää M (2021). Climate-resilient strategies for sustainable management of water resources and agriculture. Environmental Science and Pollution Research 28:41576-41595. https://doi.org/10.1007/s11356-021-14332-4

Verma A, Deepti S (2016) Abiotic stress and crop improvement: current scenario. Advances in Plants & Agriculture Research 4:345-346. https://doi.org/10.15406/apar.2016.04.00149

Wang Z, Li G, Sun H, Ma L, Guo Y, Zhao Z, Gao H, Mei L (2018). Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves. Biology Open 7:bio035279. https://doi.org/10.1242/bio.035279

WHO (2020). A report about Drought. Retrieved from: https://www.who.int/health-topics/drought#tab=tab_1

Yadav B, Jogawat A, Rahman MS, Narayan OP (2021). Secondary metabolites in the drought stress tolerance of crop plants: A review. Gene Reports 23:101040. https://doi.org/10.1016/j.genrep.2021.101040

Yang X, Lu M, Wang Y, Wang Y, Liu Z, Chen S (2021). Response mechanism of plants to drought stress. Horticulturae 7:50. https://doi.org/10.3390/horticulturae7030050

Zafar MM, Chattha WS, Khan AI, Zafar S, Subhan M, Saleem H, … Xuefei J (2023). Drought and heat stress on cotton genotypes suggested agro-physiological and biochemical features for climate resilience. Frontiers in Plant Science 14:1265700. https://doi.org/10.3389/fpls.2023.1265700

Zhang B, Du H, Yang S, Wu X, Liu W, Guo J, Xiao Y, Peng F (2023). Physiological and transcriptomic analyses of the effects of exogenous lauric acid on drought resistance in peach (Prunus persica (L.) Batsch). Plants 12(7):1492. https://doi.org/10.3390/plants12071492

Zhang S, Lu S, Xu X, Korpelainen H, Li C (2009). Changes in antioxidant enzyme activities and isozyme profiles in leaves of male and female Populus cathayana infected with Melampsora larici-populina. Tree Physiology 30:116-128. https://doi.org/10.1093/treephys/tpp094

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2024-09-24

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CHAKHCHAR, A., SOUFIANI, M., LAMAOUI, M., FERRADOUS, A., WAHBI, S., EL MOUSADIK, A., IBNSOUDA-KORAICHI, S., FILALI-MALTOUF, A., & EL MODAFAR, C. (2024). Delineating drought-induced antioxidative traits as potential mechanisms for climate resilience in Argania spinosa. Notulae Scientia Biologicae, 16(3), 12000. https://doi.org/10.55779/nsb16312000

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DOI: 10.55779/nsb16312000

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