Molybdenum improves Sorghum bicolor tolerance to salt stress by regulating the antioxidant system and the heat shock protein 70 expression

Authors

  • Thembeka Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Kaylin Hendricks Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Mulisa Nkuna Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Andrew Faro Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Ibrahim Zan Doumbia Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Rachel Fanelwa Ajayi Sensor Lab, Department of Chemical Sciences, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Emmanuel Iwuoha Sensor Lab, Department of Chemical Sciences, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Bongani Kaiser Ndimba Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa
  • Takalani Mulaudzi Life Sciences Building, Department of Biotechnology, University of the Western Cape, Private Bag X17, Bellville 7535, South Africa

Keywords:

antioxidant, molybdenum, oxidative, reactive oxygen species, sorghum, salt stress, heat shock protein

Abstract

Salinity is the most severe abiotic stress affecting crop growth and yield worldwide. Molybdenum (Mo), a micronutrient required in small quantities by plants, has the potential to alleviate effects of stress in plants. This study aimed to determine the mechanism of Molybdenum-induce salt tolerance in Sorghum bicolor using the lowest Mo concentration. Sorghum plants grown on potting soil stressed with NaCl (0 mM - 200 mM NaCl) were treated with 0.5 and 1 µM Molybdenum [(NH4)6Mo7O24.4H2O]. NaCl reduced shoot growth and caused severe deformation in the epidermis and xylem layers of sorghum shoots, and these growth attributes were restored by Mo. While chlorophyll content was also reduced by NaCl, proline content increased by 11-fold, and these effects were also reversed by Mo. NaCl-induced oxidative damage was also reversed by Mo, resulting in significantly low levels of reactive oxygen species (ROS) in 0.5 µM Mo treated plants. NaCl also increased superoxide dismutase (SOD) and ascorbate peroxidase (APX) activities, suggesting a high antioxidant scavenging capacity in sorghum. Mo further increased SOD activity in the roots of control and NaCl-treated plants. APX activity increased in control plants, while a decrease occurred in NaCl-treated plants upon Mo application. The HSP70 expression, which was highly induced by NaCl, was slightly reduced by 0.5 µM Mo and completely reduced by 1 µM Mo. The study concludes that low (0.5 µM) Mo concentrations effectively reduced NaCl-induced oxidative damage by regulating ROS detoxification and the expression of HSP70 thereby restoring membrane structure and improving growth

Downloads

Download data is not yet available.

References

Proietti I, Frazzoli C, Mantovani A. Exploiting nutritional value of staple foods in the world’s semi-arid areas: risks, benefits, challenges and opportunities of Sorghum. Healthcare. 2015;3(2):172-193.

FAO. The future of food and agriculture- Trends and challenges. Rome, 2017. Available: http://www.fao.org/3/a-i6583e.pdf.

Rosenow DT, Quisenberry JE, Wendt CW, Clark LE. Drought tolerant sorghum and cotton germplasm. Agric. Water Manag. 1983;7(1-3):207-222.

Krishnamurthy L, Serraj R, Hash CT, Dakheel AJ, Reddy BVS. Screening sorghum genotypes for salinity tolerant biomass production. Euphytica. 2007;156:15-24.

Igartua E, Gracia MP, Lasa JM. Field responses of grain sorghum to a salinity gradient. Field Crops Res. 1995;42(1):407-421.

Nemati I, Moradi F, Gholizadeh S, Esmaeili MA, Bihamta MR. The effects of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths and roots of rice (Oryza sativa L.) seedlings. Plant Soil Environ. 2011;57(1):26-33.

Flowers TJ, Yeo AR. Breeding for salinity resistance in crop plants: where next? Aust. J. Plant Physiol. 1995;22(6):875-884.

Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi W, et al. Osmotic stress in barley regulates expression of a different set of genes than salt stress does. J. Exp. Bot. 2004;55(6):2213-2218.

Munns R, Tester M. Mechanisms of salt tolerance. Annu. Rev. Plant Biol. 2008;59:651-681.

Cheng Y, Qi Y, Zhu Q, Chen X, Wang N, Zhao X, et al. New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics. 2009;9(11):3100-3114.

Cherifi K, Haddioui A, Hansali ME, Boufous EH. Growth and proline content in NaCl stressed plants of annual medic species. Int. J. Adv. Res. Biol. Sci. 2016;9:82-90.

Csiszár J, Lantos E, Tari I, Madoşă E, Wodala B, Vashegyi Á, et al. Antioxidant enzyme activities in Allium species and their cultivars under water stress. Plant Soil Environ. 2018;53(12):517-523.

Taïbi K, Taïbi F, Abderrahim LA, Ennajah A, Belkhodja M, Mulet JM. Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South African J. Bot. 2016;105:306-312.

Ul Haq S, Khan A, Ali M, Khattak AM, Gai WX, Zhang HX, et al. Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int. J. Mol. Sci. 2019;20(21):5321.

Gutteridge JMC, Halliwell B. Free radicals and antioxidants in the year. A hystorical look to the future. Ann. N. Y. Acad. Sci. 2000;899(1):136-147.

Yu M, Hu C, Wang Y. Influences of seed molybdenum and molybdenum application on nitrate reductase activity, shoot dry matter, and grain yields of winter wheat cultivars. J. of Plant Nutr. 1999;22(9):1433-1441.

Kaiser B, Gridley KL, Ngaire-Brady J, Phillips T, Tyerman SD. The role of molybdenum in agricultural plant production. Ann. Bot. 2005;96(6):745-754.

Babenko ON, Brychkova G, Sagi M, Alikulov ZA. Molybdenum application enhances adaptation of crested wheatgrass to salinity stress. Acta Physiol. Plant. 2015;37:1-13.

Liu P, Yang YS, Xu GD, Fang YH, Yang YA, Kalin R. The effects of molybdenum and boron in soil on the growth and photosynthesis of three soybean varieties. Plant Soil and Environ. 2005;51(5):197-205.

Bagheri A, Jafari A. Effect of salinity and molybdenum application on photosynthesis, nitrogenase activity and yield of barley inoculated with Azosprillium brasilense. Cereal Res. Commun. 2012;40(2):235-245.

Zhang M, Hu C, Sun X, Zhao X, Tan Q, Zhang Y, et al. Molybdenum affects photosynthesis and Ionic homeostasis of Chinese Cabbage under salinity stress. Commun. Soil Sci. Plant Anal. 2014:45(20):2660-2672.

Salha B, Chaabane R. Expression of some molybdenzymes genes under salt stress conditions in Chickpea, Bean and Lentil plant. Int. J. Environ. Agric. Biotech. 2016;4:748-759.

Farhangi-Abriz S, Faegi-Analou R, Nikpour-Rashidabad N. Foliar application of sodium molybdate enhanced nitrogen uptake and translocation in soybean plants by improving nodulation process under salt stress. Cercet. Agron. Mold. 2017;50:71-82.

Mulaudzi-Masuku T, Mutepe RD, Mukhoro OC, Faro A, Ndimba B. Identification and characterization of a heat-inducible Hsp70 gene from Sorghum bicolor which confers tolerance to thermal stress. Cell Stress Chaperones. 2015;20:793-804.

Rakgotho T, Ndou N, Mulaudzi T, Iwuoha E, Mayedwa N, Ayayi RF. Green–synthesized zinc oxide nanoparticles mitigate salt stress in Sorghum bicolor. Agriculture. 2022;12:597.

Arnon IA. Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris. Plant Physiol. 1949;24:1-15.

Khare T, Desai D, Kumar V. Effect of MgCl2 stress on germination, plant growth, chlorophyll content, proline content and lipid peroxidation in sorghum cultivars. J. stress Physiol. Biochem. 2012;8(4):169-178.

Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB. Modulation of antioxidant machinery in alpha-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma. 2013;250:1079-1089.

Junglee S, Urban L, Sallanon H, Lopez-Laurie F. Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. Am. J. Anal. Chem. 2014;5(11):730-736.

Niu L, Zhang H, Wu Z, Wang Y, Liu H, Wu X, et al. Modified TCA/acetone precipitation of plant proteins for proteomic analysis. PLoS One. 2018;13(12):e0202238.

Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248-254.

Giannopolitis CN, Resi SK. Superoxide dismutase. Plant Physiol. 1977;59(2):309-314.

Ngara R, Ndimba R, Borch-Jensen J, Jensen ON, Ndimba B. Identification and profiling of salinity stress-responsive proteins in Sorghum bicolor seedlings. J. Proteom. 2012;75(13):13, 4139-4150.

Punia H, Tokas J, Bhadu S, Mohanty AK, Rawat P, Malik A Satpal. Proteome dynamics and transcriptome profiling in sorghum [Sorghum bicolor (L.) Moench] under salt stress. Biotechnol J. 2020;10:412.

Mulaudzi T, Hendricks K, Mabiya T, Muthevhuli M, Ajayi RF, Mayedwa N, et al. Calcium improves germination and growth of Sorghum bicolor seedlings under salt stress. Plants. 2020;9(6):730.

Zhuo Y, Zhang Y, Xie G, Xiong S. Effects of salt stress on biomass and ash composition of switchgrass (Panicum virgatum). Acta Agric. Scand.- B - Soil Plant Sci. 2015;65(4):300-309.

De Oliveira AB, Mendes Alencar NL, Gomes-Filho E. Comparison between the water and salt stress effects on plant growth and development. In: Akinci S, eds. Responses of Organisms to Water Stress. Intech: United States, 2013, 67-94.

Batyrshina Z, Yergaliyev TM, Nurbekova Z, Moldakimova NA, Masalimov ZK, Sagi M, et al. Differential influence of molybdenum and tungsten on the growth of barley seedlings and the activity of aldehyde oxidase under salinity. J. Plant Physiol. 2018;228:189-196.

Al-Issawi M, Rihan HZ, Al-Shmgani H, Fuller MP. Molybdenum application enhances antioxidant enzyme activity and COR15a protein expression under cold stress in wheat. J. Plant Interact. 2016;11(1):5-10.

Wu S, Sun X, Tan Q, Hu C. Molybdenum improves water uptake via extensive root morphology, aquaporin expressions and increased ionic concentrations in wheat under drought stress. Environ. Exp. Bot. 2016;157:241-249.

Han Z, Wei X, Wan D, He W, Wang X, Xiong Y. Effect of molybdenum on plant physiology and cadmium uptake and translocation in rape (Brassica napus L.) under different levels of cadmium stress. Int. J. Environ. Res. Pub. He. 2020;7(17):2355.

Imran M, Hussain S, El-Esawi MA, Rana MS, Saleem MH, Riaz M, et al. Molybdenum supply alleviates the cadmium toxicity in fragrant rice by modulating oxidative stress and antioxidant gene expression. Biomolecules. 2020;10(11):1582.

Hameed M, Ashraf M, Naz N. Anatomical adaptions to salinity in cogon grass [Imperata cylindrica (L.) Raeuschel] from the salt range, Pakistan. Plant Soil Environ. 2009;322:229-238.

Kutschera U. The growing outer epidermal wall: design and physiological role of a composite structure. Ann. Bot. 2008;101(5):615-621.

Savaldi-Goldstein S, Chory J. Growth coordination and the shoot epidermis. Curr. Opin. Plant Biol. 2008;11(11):42-48.

Hajibagheri MA, Hall JL, Flowers TJ. Stereological analysis of leaf cells of the halophyte Suaeda maritima (L.) dum. J. Exp. Bot. 1984;35(10):1547-1557.

Bray S, Reid DM. The effect of salinity and CO2 enrichment on the growth and anatomy of the second trifoliate leaf of Phaseolus vulgaris. Can. JB. 2002;80(4):349-359.

Mostafa H. Effects of salinity stress on growth, chlorophyll content and osmotic components of two basil (Ocimum basilicum L.) genotypes. Afr. J. Biotechnol. 2011;11(2):379-384.

Siddiqui H, Hayat S, Bajguz A. Regulation of photosynthesis by brassinosteriods in plants. Acta Physiol. Plant, 2018, 40-59.

Ashraf MA, Ashraf M. Salt induced variation in some potential physiochemical attributes of two genetically diverse spring wheat (Tricum aestivum L.) cultivars: Photosynthesis and photosystem Π efficiency. Pak. J. Bot. 2012;44(1):53-64.

Foyer CH, Lelandais M, Kunert KJ. Photooxidative stress in plants. Physiol. Plant. 1994;92:696-717.

Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7(9):405-410.

Hasanuzzaman M, Nahar K, Gill SS, Fujita M. Drought stress responses in plants, oxidative stress and antioxidant defense. In: Tuteja N, Gill SS, eds. Climate change and plant abiotic stress tolerance, 2014, 209-249.

Bambara S, Ndakidemi A. Effects of Rhizobium inocultion, lime and molybdenum on photosynthesis and chlorophyll content of Phaseolus vulgaris L. Afr. J. Microbiol. Res. 2019;3:791-798.

Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25(2):239-250.

Chun SC, Paramasivan M, Chandrasekaran M. Proline accumulation influenced by osmotic stress in arbuscular mycorrhizal symbiotic plants. Front. Microbiol. 2018;9:2525.

Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant Signal. Behav. 2012;7(11):1456-1466.

Sairam RK, Tyagi A. Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci. 2004;86:407-421.

Rahneshan Z, Nasibi F, Moghadam AA. Effects of salinity stress on some growth, physiology, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks. J. Plant Interact. 2018;13(1):73-82.

Kumar D, Al Hassan M, Naranjo MA, Agrawal V, Boscaiu M, Vicente O. Effects of salinity and drought on growth, ionic relations, compatible solutes and activation of antioxidant systems in oleander (Nerium oleander L.). PLoS One. 2017;12(9):e0185017.

Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive Oxygen Species, Oxidative Damage, and Antioxidative Defense Mechanism in Plants under Stressful Conditions. J. Bot, 2012, 1-26.

Asada K. The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Biol. 1999;50(1):601-639.

Wu S, Hu C, Tan Q, Nie Z, Sun X. Effects of molybdenum on water utilization, antioxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum) under drought stress. Plant Physiol. Biochem. 2014;83:365-374.

Al-Whaibi MH. Plant heat-shock proteins: A mini review. J. King Saud Univ. Sci. 2011;23(2):139-150.

Mayer MP, Bukau B. Hsp70 chaperon: Cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005;62:670-84.

Downloads

Published

2023-03-17

How to Cite

[1]
T. . Confidence Mabiya, “Molybdenum improves Sorghum bicolor tolerance to salt stress by regulating the antioxidant system and the heat shock protein 70 expression”, Int. J. Phytol. Res., vol. 3, no. 1, pp. 30–40, Mar. 2023.

Issue

Section

Articles