Hydrogen Peroxide and Nitric Oxide Crosstalk Mediates Brassinosteroids Induced Cold Stress Tolerance in

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2019 Jan 6

PMID 30609774

Citations 11

Authors

Muhammad Arfan

Da-Wei Zhang

Li-Juan Zou

Shi-Shuai Luo

Wen-Rong Tan

Tong Zhu

Hong-Hui Lin

Affiliations

Soon will be listed here.

Abstract

Brassinosteroids (BRs) play pivotal roles in modulating plant growth, development, and stress responses. In this study, a plant pretreated with brassinolide (BL, the most active BR), enhanced cold stress tolerance by regulating the expression of several cold-related genes and antioxidant enzymes activities. Previous studies reported that hydrogen peroxide (H₂O₂) and nitric oxide (NO) are involved during environmental stress conditions. However, how these two signaling molecules interact with each other in BRs-induced abiotic stress tolerance remain largely unclear. BL-pretreatment induced, while brassinazole (BRZ, a specific inhibitor of BRs biosynthesis) reduced H₂O₂ and NO production. Further, application of dimethylthiourea (DMTU, a H₂O₂ and OH scavenger) blocked BRs-induced NO production, but BRs-induced H₂O₂ generation was not sensitive to 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (PTIO, a scavenger of NO). Moreover, pretreatment with DMTU and PTIO decreased BL-induced mitochondrial alternative oxidase (AOX) and the photosystem capacity. However, pretreatment with PTIO was found to be more effective than DMTU in reducing BRs-induced increases in , , and gene expression. Similarly, BRs-induced photosystem II efficiency was found in NO dependent manner than H₂O₂. Finally, we conclude that H₂O₂ was involved in NO generation, whereas NO was found to be crucial in BRs-induced AOX capacity, which further contributed to the protection of the photosystem under cold stress conditions in .

Citing Articles

Plant Coping with Cold Stress: Molecular and Physiological Adaptive Mechanisms with Future Perspectives.

Feng Y, Li Z, Kong X, Khan A, Ullah N, Zhang X Cells. 2025; 14(2).

PMID: 39851537 PMC: 11764090. DOI: 10.3390/cells14020110.

Analysis of the Mechanisms Underlying the Specificity of the Variation Potential Induced by Different Stimuli.

Mudrilov M, Ladeynova M, Vetrova Y, Vodeneev V Plants (Basel). 2024; 13(20).

PMID: 39458843 PMC: 11511009. DOI: 10.3390/plants13202896.

Functional and Transcriptome Analysis Reveal Specific Roles of and in Root Hair Development, Reproductive Growth, and Stress Tolerance.

Tian Q, Xie X, Lai R, Cheng C, Zhang Z, Chen Y Plants (Basel). 2024; 13(4).

PMID: 38498444 PMC: 10891736. DOI: 10.3390/plants13040480.

Effect of Reactive Oxygen Scavenger N,N'-Dimethylthiourea (DMTU) on Seed Germination and Radicle Elongation of Maize.

Li W, Li J, Zhang Y, Luo W, Dou Y, Yu S Int J Mol Sci. 2023; 24(21).

PMID: 37958543 PMC: 10649595. DOI: 10.3390/ijms242115557.

Transcriptome Analysis Reveals Brassinolide Signaling Pathway Control of Foxtail Millet Seedling Starch and Sucrose Metabolism under Freezing Stress, with Implications for Growth and Development.

Zhao X, Ma K, Li Z, Li W, Zhang X, Liu S Int J Mol Sci. 2023; 24(14).

PMID: 37511348 PMC: 10380969. DOI: 10.3390/ijms241411590.

References

Neill S, Desikan R, Hancock J . Hydrogen peroxide signalling. Curr Opin Plant Biol. 2002; 5(5):388-95. DOI: 10.1016/s1369-5266(02)00282-0. View

Szekely G, Abraham E, Cseplo A, Rigo G, Zsigmond L, Csiszar J . Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 2007; 53(1):11-28. DOI: 10.1111/j.1365-313X.2007.03318.x. View

Hansen M, Chae H, Kieber J . Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J. 2008; 57(4):606-14. PMC: 2807401. DOI: 10.1111/j.1365-313X.2008.03711.x. View

Xing W, Li D, Liu G . Antioxidative responses of Elodea nuttallii (Planch.) H. St. John to short-term iron exposure. Plant Physiol Biochem. 2010; 48(10-11):873-8. DOI: 10.1016/j.plaphy.2010.08.006. View

Bilger W, Bjorkman O . Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res. 2014; 25(3):173-85. DOI: 10.1007/BF00033159. View

Mizuno N, Sugie A, Kobayashi F, Takumi S . Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat. J Plant Physiol. 2007; 165(4):462-7. DOI: 10.1016/j.jplph.2007.04.004. View

Deng X, Zhu T, Zhang D, Lin H . The alternative respiratory pathway is involved in brassinosteroid-induced environmental stress tolerance in Nicotiana benthamiana. J Exp Bot. 2015; 66(20):6219-32. PMC: 4588879. DOI: 10.1093/jxb/erv328. View

Bright J, Desikan R, Hancock J, Weir I, Neill S . ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J. 2005; 45(1):113-22. DOI: 10.1111/j.1365-313X.2005.02615.x. View

Deng X, Zhu T, Zou L, Han X, Zhou X, Xi D . Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid-mediated systemic virus resistance in Nicotiana benthamiana. Plant J. 2016; 85(4):478-93. DOI: 10.1111/tpj.13120. View

10.

Graham P, Vance C . Legumes: importance and constraints to greater use. Plant Physiol. 2003; 131(3):872-7. PMC: 1540286. DOI: 10.1104/pp.017004. View

11.

Neill S, Desikan R, Hancock J . Nitric oxide signalling in plants. New Phytol. 2021; 159(1):11-35. DOI: 10.1046/j.1469-8137.2003.00804.x. View

12.

Wang H, Liang X, Huang J, Zhang D, Lu H, Liu Z . Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol. 2010; 51(10):1754-65. DOI: 10.1093/pcp/pcq134. View

13.

Giraud E, Van Aken O, Ho L, Whelan J . The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 2009; 150(3):1286-96. PMC: 2705018. DOI: 10.1104/pp.109.139782. View

14.

Xu F, Zhang D, Zhu F, Tang H, Lv X, Cheng J . A novel role for cyanide in the control of cucumber (Cucumis sativus L.) seedlings response to environmental stress. Plant Cell Environ. 2012; 35(11):1983-97. DOI: 10.1111/j.1365-3040.2012.02531.x. View

15.

Yoshioka H, Mase K, Yoshioka M, Kobayashi M, Asai S . Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity. Nitric Oxide. 2011; 25(2):216-21. DOI: 10.1016/j.niox.2010.12.008. View

16.

Zhou J, Wang J, Li X, Xia X, Zhou Y, Shi K . H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses. J Exp Bot. 2014; 65(15):4371-83. PMC: 4112640. DOI: 10.1093/jxb/eru217. View

17.

Moore A, Albury M, Crichton P, Affourtit C . Function of the alternative oxidase: is it still a scavenger?. Trends Plant Sci. 2002; 7(11):478-81. DOI: 10.1016/s1360-1385(02)02366-x. View

18.

Zhang L, Zhang Z, Gao H, Xue Z, Yang C, Meng X . Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant. 2011; 143(4):396-407. DOI: 10.1111/j.1399-3054.2011.01514.x. View

19.

Kagale S, Divi U, Krochko J, Keller W, Krishna P . Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta. 2006; 225(2):353-64. DOI: 10.1007/s00425-006-0361-6. View

20.

Ning J, Li X, Hicks L, Xiong L . A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 2009; 152(2):876-90. PMC: 2815886. DOI: 10.1104/pp.109.149856. View