Response Mechanisms of Leaves to Varying Levels of Calcium Stress

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2024 Sep 14

PMID 39273242

Authors

Fengxia Yan

Ronghui Jiang

Chao Yang

Yanbing Yang

Zaiqi Luo

Yunli Jiang

Affiliations

Soon will be listed here.

Abstract

Calcium stress can negatively impact plant growth, prompting plants to respond by mitigating this effect. However, the specific mechanisms underlying this response remain unclear. In this study, we used non-targeted metabolomics and transcriptomics to investigate the response mechanisms of leaves under varying degrees of calcium stress. Results revealed that calcium stress led to wilt in young leaves. When calcium stress exceeds the tolerance threshold of the leaf, it results in wilting of mature leaves, rupture of chloroplasts in palisade tissue, and extensive wrinkling and breakage of leaf cells. Transcriptomic analysis indicated that calcium stress inhibited photosynthesis by suppressing the expression of genes related to photosynthetic system II and electron transport. Leaf cells activate phenylpropanoid biosynthesis, flavonoid biosynthesis, and Vitamin B6 metabolism to resist calcium stress. When calcium accumulation gradually surpassed the tolerance threshold of the cells, this results in failure of conventional anti-calcium stress mechanisms, leading to cell death. Furthermore, excessive calcium stress inhibits the expression of CNGC and anti-pathogen genes. The results of the metabolomics study showed that five key metabolites increased in response to calcium stress, which may play an important role in countering calcium stress. This study provides insights into the response of leaves to different levels of calcium stress, which could provide a theoretical basis for cultivating in karst areas and enhance our understanding of plant responses to calcium stress.

References

An J, Yao J, Xu R, You C, Wang X, Hao Y . An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol Plant. 2018; 164(3):279-289. DOI: 10.1111/ppl.12724. View

Li J, Shen L, Han X, He G, Fan W, Li Y . Phosphatidic acid-regulated SOS2 controls sodium and potassium homeostasis in Arabidopsis under salt stress. EMBO J. 2023; 42(8):e112401. PMC: 10106984. DOI: 10.15252/embj.2022112401. View

Yang Z, Yang X, Dong S, Ge Y, Zhang X, Zhao X . Overexpression of β-Ketoacyl-CoA Synthase From L. Improves Salt Tolerance in . Front Plant Sci. 2020; 11:564385. PMC: 7688582. DOI: 10.3389/fpls.2020.564385. View

Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K . AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta. 2011; 1819(2):86-96. DOI: 10.1016/j.bbagrm.2011.08.004. View

Rodrigues Neto J, Salgado F, Braga I, Carvalho da Silva T, Belo Silva V, Leao A . Osmoprotectants play a major role in the resistance to high levels of salinity stress-insights from a metabolomics and proteomics integrated approach. Front Plant Sci. 2023; 14:1187803. PMC: 10296175. DOI: 10.3389/fpls.2023.1187803. View

Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J . The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 2000; 23(4):441-50. DOI: 10.1046/j.1365-313x.2000.00804.x. View

Gupta K, Shah J, Brotman Y, Jahnke K, Willmitzer L, Kaiser W . Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J Exp Bot. 2012; 63(4):1773-84. DOI: 10.1093/jxb/ers053. View

Li B, Dewey C . RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12:323. PMC: 3163565. DOI: 10.1186/1471-2105-12-323. View

Cai X, Sun H, Yan B, Bai H, Zhou X, Shen P . Salt stress perception and metabolic regulation network analysis of a marine probiotic GXDK6. Front Microbiol. 2023; 14:1193352. PMC: 10387536. DOI: 10.3389/fmicb.2023.1193352. View

10.

Bricker T, Frankel L . Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant Photosystem II: a critical analysis. J Photochem Photobiol B. 2011; 104(1-2):165-78. DOI: 10.1016/j.jphotobiol.2011.01.025. View

11.

Sun Z, Zhou M, Xiao X, Tang Y, Wu Y . Genome-wide analysis of AP2/ERF family genes from Lotus corniculatus shows LcERF054 enhances salt tolerance. Funct Integr Genomics. 2014; 14(3):453-66. DOI: 10.1007/s10142-014-0372-5. View

12.

Ran X, Wang X, Gao X, Liang H, Liu B, Huang X . Effects of salt stress on the photosynthetic physiology and mineral ion absorption and distribution in white willow (Salix alba L.). PLoS One. 2021; 16(11):e0260086. PMC: 8601552. DOI: 10.1371/journal.pone.0260086. View

13.

Wang Y, Kang Y, Ma C, Miao R, Wu C, Long Y . CNGC2 Is a Ca2+ Influx Channel That Prevents Accumulation of Apoplastic Ca2+ in the Leaf. Plant Physiol. 2016; 173(2):1342-1354. PMC: 5291024. DOI: 10.1104/pp.16.01222. View

14.

White P, Broadley M . Calcium in plants. Ann Bot. 2003; 92(4):487-511. PMC: 4243668. DOI: 10.1093/aob/mcg164. View

15.

Clough S, Fengler K, Yu I, Lippok B, Smith Jr R, Bent A . The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A. 2000; 97(16):9323-8. PMC: 16866. DOI: 10.1073/pnas.150005697. View

16.

Hasanuzzaman M, Bhuyan M, Zulfiqar F, Raza A, Mohsin S, Mahmud J . Reactive Oxygen Species and Antioxidant Defense in Plants under Abiotic Stress: Revisiting the Crucial Role of a Universal Defense Regulator. Antioxidants (Basel). 2020; 9(8). PMC: 7465626. DOI: 10.3390/antiox9080681. View

17.

Langmead B, Trapnell C, Pop M, Salzberg S . Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25. PMC: 2690996. DOI: 10.1186/gb-2009-10-3-r25. View

18.

Dayod M, Tyerman S, Leigh R, Gilliham M . Calcium storage in plants and the implications for calcium biofortification. Protoplasma. 2010; 247(3-4):215-31. DOI: 10.1007/s00709-010-0182-0. View

19.

Gan T, Lin Z, Bao L, Hui T, Cui X, Huang Y . Comparative Proteomic Analysis of Tolerant and Sensitive Varieties Reveals That Phenylpropanoid Biosynthesis Contributes to Salt Tolerance in Mulberry. Int J Mol Sci. 2021; 22(17). PMC: 8431035. DOI: 10.3390/ijms22179402. View

20.

Xu Z, Gongbuzhaxi , Wang C, Xue F, Zhang H, Ji W . Wheat NAC transcription factor TaNAC29 is involved in response to salt stress. Plant Physiol Biochem. 2015; 96:356-63. DOI: 10.1016/j.plaphy.2015.08.013. View