Regulatory Mechanism Through Which Old Soybean Leaves Respond to Mn Toxicity Stress

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 May 25

PMID 38791379

Authors

Yuhu Pan

Jianning Shi

Jianyu Li

Rui Zhang

Yingbin Xue

Ying Liu

Affiliations

Soon will be listed here.

Abstract

Manganese (Mn) is a heavy metal that can cause excessive Mn poisoning in plants, disrupting microstructural homeostasis and impairing growth and development. However, the specific response mechanisms of leaves to Mn poisoning have not been fully elucidated. This study revealed that Mn poisoning of soybean plants resulted in yellowing of old leaves. Physiological assessments of these old leaves revealed significant increases in the antioxidant enzymes activities (peroxidase (POD), superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT)) and elevated levels of malondialdehyde (MDA), proline, indoleacetic acid (IAA), and salicylic acid (SA), under 100 μM Mn toxicity. Conversely, the levels of abscisic acid (ABA), gibberellin 3 (GA), and jasmonic acid (JA) significantly decreased. The Mn content in the affected leaves significantly increased, while the levels of Ca, Na, K, and Cu decreased. Transcriptome analysis revealed 2258 differentially expressed genes in the Mn-stressed leaves, 744 of which were upregulated and 1514 were downregulated; these genes included genes associated with ion transporters, hormone synthesis, and various enzymes. Quantitative RT-PCR (qRT-PCR) verification of fifteen genes confirmed altered gene expression in the Mn-stressed leaves. These findings suggest a complex gene regulatory mechanism under Mn toxicity and stress, providing a foundation for further exploration of Mn tolerance-related gene regulatory mechanisms in soybean leaves. Using the methods described above, this study will investigate the molecular mechanism of old soybean leaves' response to Mn poisoning, identify key genes that play regulatory roles in Mn toxicity stress, and lay the groundwork for cultivating high-quality soybean varieties with Mn toxicity tolerance traits.

References

Caverzan A, Passaia G, Rosa S, Werner Ribeiro C, Lazzarotto F, Margis-Pinheiro M . Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol. 2013; 35(4 (suppl)):1011-9. PMC: 3571416. DOI: 10.1590/s1415-47572012000600016. View

Mandal C, Ghosh N, Maiti S, Das K, Gupta S, Dey N . Antioxidative responses of Salvinia (Salvinia natans Linn.) to aluminium stress and it's modulation by polyamine. Physiol Mol Biol Plants. 2014; 19(1):91-103. PMC: 3550683. DOI: 10.1007/s12298-012-0144-4. View

Pan G, Liu W, Zhang H, Liu P . Morphophysiological responses and tolerance mechanisms of Xanthium strumarium to manganese stress. Ecotoxicol Environ Saf. 2018; 165:654-661. DOI: 10.1016/j.ecoenv.2018.08.107. View

Yin R, Liu X, Yu J, Ji Y, Liu J, Cheng L . Up-regulation of autophagy by low concentration of salicylic acid delays methyl jasmonate-induced leaf senescence. Sci Rep. 2020; 10(1):11472. PMC: 7351724. DOI: 10.1038/s41598-020-68484-3. View

Fernando D, Lynch J . Manganese phytotoxicity: new light on an old problem. Ann Bot. 2015; 116(3):313-9. PMC: 4549964. DOI: 10.1093/aob/mcv111. View

Racz A, Hideg E, Czegeny G . Selective responses of class III plant peroxidase isoforms to environmentally relevant UV-B doses. J Plant Physiol. 2017; 221:101-106. DOI: 10.1016/j.jplph.2017.12.010. View

Shao J, Yamaji N, Shen R, Ma J . The Key to Mn Homeostasis in Plants: Regulation of Mn Transporters. Trends Plant Sci. 2017; 22(3):215-224. DOI: 10.1016/j.tplants.2016.12.005. View

Noor I, Sohail H, Zhang D, Zhu K, Shen W, Pan J . Silencing of PpNRAMP5 improves manganese toxicity tolerance in peach (Prunus persica) seedlings. J Hazard Mater. 2023; 454:131442. DOI: 10.1016/j.jhazmat.2023.131442. View

Khew C, Mori I, Matsuura T, Hirayama T, Harikrishna J, Lau E . Hormonal and transcriptional analyses of fruit development and ripening in different varieties of black pepper (Piper nigrum). J Plant Res. 2019; 133(1):73-94. DOI: 10.1007/s10265-019-01156-0. View

10.

Liu P, Huang R, Hu X, Jia Y, Li J, Luo J . Physiological responses and proteomic changes reveal insights into Stylosanthes response to manganese toxicity. BMC Plant Biol. 2019; 19(1):212. PMC: 6530018. DOI: 10.1186/s12870-019-1822-y. View

11.

Hafeez A, Rasheed R, Ashraf M, Rizwan M, Ali S . Effects of exogenous taurine on growth, photosynthesis, oxidative stress, antioxidant enzymes and nutrient accumulation by Trifolium alexandrinum plants under manganese stress. Chemosphere. 2022; 308(Pt 3):136523. DOI: 10.1016/j.chemosphere.2022.136523. View

12.

Miao Y, Zentgraf U . The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell. 2007; 19(3):819-30. PMC: 1867371. DOI: 10.1105/tpc.106.042705. View

13.

Chen Z, Fujii Y, Yamaji N, Masuda S, Takemoto Y, Kamiya T . Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J Exp Bot. 2013; 64(14):4375-87. PMC: 3808320. DOI: 10.1093/jxb/ert243. View

14.

Huang D, Sherman B, Lempicki R . Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4(1):44-57. DOI: 10.1038/nprot.2008.211. View

15.

Fecht-Christoffers M, Braun H, Lemaitre-Guillier C, VanDorsselaer A, Horst W . Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiol. 2003; 133(4):1935-46. PMC: 300745. DOI: 10.1104/pp.103.029215. View

16.

Zhang Y, Zhao L, Zhao J, Li Y, Wang J, Guo R . Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis. Plant Physiol. 2017; 175(3):1082-1093. PMC: 5664462. DOI: 10.1104/pp.17.00695. View

17.

Alonso-Ramirez A, Rodriguez D, Reyes D, Jimenez J, Nicolas G, Lopez-Climent M . Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol. 2009; 150(3):1335-44. PMC: 2705047. DOI: 10.1104/pp.109.139352. View

18.

Abreu M, Munne-Bosch S . Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J Exp Bot. 2009; 60(4):1261-71. PMC: 2657544. DOI: 10.1093/jxb/ern363. View

19.

Sasaki A, Yamaji N, Yokosho K, Ma J . Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell. 2012; 24(5):2155-67. PMC: 3442593. DOI: 10.1105/tpc.112.096925. View

20.

Xiao Z, Pan G, Li X, Kuang X, Wang W, Liu W . Effects of exogenous manganese on its plant growth, subcellular distribution, chemical forms, physiological and biochemical traits in Cleome viscosa L. Ecotoxicol Environ Saf. 2020; 198:110696. DOI: 10.1016/j.ecoenv.2020.110696. View