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Arabidopsis CaM3 inhibits nitric oxide accumulation and improves thermotolerance by promoting S-nitrosoglutathione reductase via direct binding

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Abstract

Calmodulin 3 (CaM3) is a key component of heat shock (HS) signal transduction in Arabidopsis (Arabidopsis thaliana). We previously reported that nitric oxide (NO) acts as an upstream signal of AtCaM3 in plant thermotolerance. In this study, we demonstrated the effect of AtCaM3 on NO accumulation in the tolerance of Arabidopsis plants to HS. In vivo and in vitro protein–protein interaction assays displayed a direct binding between AtCaM3 and S-nitrosoglutathione reductase (GSNOR), inducing an increased GSNOR activity and an inhibited NO level. The cam3 mutant seedlings exhibited a high internal NO accumulation under HS. A gsnor deficiency decreased the survival ratio of cam3 plants accompanied by an increased internal NO level. However, treatment with 2-phenyl-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide (cPTIO, a special NO scavenger) elevated the survival ratio of cam3 mutant seedlings under HS conditions. Collectively, these data suggest an interesting finding that AtCaM3 serves as a signal in plant thermotolerance by reducing excessive NO accumulation through the binding and promoting of GSNOR, suggesting a feedback inhibition between AtCaM3 and NO in thermotolerance.

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References

  • Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11:545–555

    Article  CAS  Google Scholar 

  • Chen C, Li Q, Wang Q, Lu D, Zhang H, Wang J, Fu R (2017) Transcriptional profiling provides new insights into the role of nitric oxide in enhancing Ganoderma oregonense resistance to heat stress. Sci Rep 7:15694

    Article  Google Scholar 

  • Chu M, Li J, Zhang J, Shen S, Li C, Gao Y, Zhang S (2018) AtCaM4 interacts with a Sec14-like protein, PATL1, to regulate freezing tolerance in Arabidopsis in a CBF-independent manner. J Exp Bot 69:5241–5253

    Article  CAS  Google Scholar 

  • Dai C, Lee Y, Lee IC, Nam HG, Kwak JM (2018) Calmodulin 1 regulates senescence and ABA response in Arabidopsis. Front Plant Sci 9:803

    Article  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059

    Article  CAS  Google Scholar 

  • Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398

    Article  Google Scholar 

  • Gao F, Han X, Wu J, Zheng S, Shang Z, Sun D, Zhou RG, Li B (2012) A heat-activated calcium-permeable channel-Arabidopsis cyclic nucleotide-gated ion channel 6-is involved in heat shock responses. Plant J 70:1056–1069

    Article  CAS  Google Scholar 

  • Hsu SF, Lai HC, Jinn TL (2010) Cytosol-localized heat shock factor-binding protein, AtHSBP, functions as a negative regulator of heat shock response by translocation to the nucleus and is required for seed development in Arabidopsis. Plant Physiol 153:773–784

    Article  CAS  Google Scholar 

  • Jensen DE, Belka GK, du Bois GC (1998) S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem J 331:659–668

    Article  CAS  Google Scholar 

  • Khan M, Sakakima H, Dhammu TS, Shunmugavel A, Im YB, Gilg AG, Singh AK, Singh I (2011) S-Nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in rats. J Neuroinflamm 8:78

    Article  CAS  Google Scholar 

  • Krzysztof B, Simone A, Isabel B (2019) BRUSHY1/TONSOKU/MGOUN3 is required for heat stress memory. Plant Cell Environ 42:771–781

    Article  Google Scholar 

  • Lewis AM, Matzdorf SS, Rice KC (2016) Fluorescent detection of intracellular nitric oxide in Staphylococcus aureus. Bio-Protocol 6:e1878

    Article  Google Scholar 

  • Li CH, Wang G, Zhao JL, Zhang LQ, Ai LF, Han YF, Sun DY, Zhang SW, Sun Y (2014) The receptor-like kinase SIT1 mediates salt sensitivity by activating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell 26:2538–2553

    Article  CAS  Google Scholar 

  • Li J, Zhang Y, Zhang YY, Lü SL, Miao YT, Yang J, Huang SM, Ma XL, Han LL, Deng JC, Fan FF, Liu B, Huo Y, Xu QB, Chen C, Wang X, Feng J (2018) GSNOR modulates hyperhomocysteinemia-induced T cell activation and atherosclerosis by switching Akt S-nitrosylation to phosphorylation. Redox Biol 17:386–399

    Article  CAS  Google Scholar 

  • McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389

    Article  CAS  Google Scholar 

  • Park HJ, Ding L, Dai M, Lin R, Wang H (2008) Multisite phosphorylation of Arabidopsis FR1 by casein kinase II and a plausible role in regulating its degradation rate. J Biol Chem 283:23264–23273

    Article  CAS  Google Scholar 

  • Petersen A, Gerges NZ (2015) Neurogranin regulates CaM dynamics at dendritic spines. Sci Rep 5:11135

    Article  CAS  Google Scholar 

  • Rai KK, Rai N, Rai SP (2018) Salicylic acid and nitric oxide alleviate high temperature induced oxidative damage in Lablab purpureus L. plants by regulating bio-physical processes and DNA methylation. Plant Physiol Biochem 128:72–88

    Article  CAS  Google Scholar 

  • Sakamoto A, Ueda M, Morikawa H (2002) Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett 515:20–24

    Article  CAS  Google Scholar 

  • Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868

    Article  CAS  Google Scholar 

  • Shi YF, Wang DL, Wang C, Culler AH, Kreiser MA, Suresh J, Cohen JD, Pan J, Baker B, Liu JZ (2015) Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol Plant 8:1350–1365

    Article  CAS  Google Scholar 

  • Stigler J, Ziegler F, Gieseke A, Gebhardt JCM, Rief M (2011) The complex folding network of single calmodulin molecule. Science 334:512–516

    Article  CAS  Google Scholar 

  • Tian M, Zhu L, Lin H, Lin Q, Huang P, Yu X, Jing Y (2017) Hsp-27 levels and thrombus burden relate to clinical outcomes in patients with ST-segment elevation myocardial infarction. Oncotarget 8:73733–73744

    PubMed  PubMed Central  Google Scholar 

  • Waadt R, Kudla J (2008) In planta visualization of protein interactions using bimolecular fluorescence complementation (BiFC). CSH Protoc. https://doi.org/10.1101/pdb.prot3944

    Article  PubMed  Google Scholar 

  • Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438

    Article  CAS  Google Scholar 

  • Wang Y, Ries A, Wu K, Yang A, Crawford NM (2010) The Arabidopsis prohibition genes PHB3 functions in nitric oxide-mediated responses and in hydrogen peroxide-induced nitric oxide accumulation. Plant Cell 22:249–259

    Article  CAS  Google Scholar 

  • Wang L, Guo Y, Jia L, Chu H, Zhou S, Chen K, Wu D, Zhao L (2014) Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol 164:2184–2196

    Article  CAS  Google Scholar 

  • Westerlund AM, Delemotte L (2018) Effect of Ca2+ on the promiscuous targetprotein binding of calmodulin. PLoS Comput Biol 14:e1006072

    Article  Google Scholar 

  • Wu D, Chu H, Jia L, Chen K, Zhao L (2015) A feedback inhibition between nitric oxide and hydrogen peroxide in the heat shock pathway in Arabidopsis seedlings. Plant Growth Regul 75:503–509

    Article  CAS  Google Scholar 

  • Xuan Y, Zhou S, Wang L, Cheng Y, Zhao L (2010) Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiol 153:1895–1906

    Article  CAS  Google Scholar 

  • Yang Z, Wang Z, Doulias P, Wei W, Ischiropoulos H, Locksley RM, Liu L (2010) Lymphocyte development requires S-nitrosoglutathione reductase. J Immunol 185:6664–6669

    Article  CAS  Google Scholar 

  • Zhang W, Zhou RG, Gao YJ, Zheng SZ, Xu P, Zhang SQ, Sun DY (2009) Molecular and genetic evidence for the key role of AtCaM3 in heat-Shock signal transduction in Arabidopsis. Plant Physiol 149:1773–1784

    Article  CAS  Google Scholar 

  • Zhang L, Li G, Wang M, Di D, Sun L, Kronzucker H, Shi W (2018) Excess iron stress reduces root tip zone growth through nitric oxide-mediated repression of potassium homeostasis in Arabidopsis. New Phytol 219:259–274

    Article  CAS  Google Scholar 

  • Zhou S, Jia L, Chu H, Wu D, Peng X, Liu X, Zhang J, Zhao J, Chen K, Zhao L (2016) Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S-nitrosoglutathione reductase via direct binding. PLoS Genet 12:e1006255

    Article  Google Scholar 

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Acknowledgements

We thanks Dr. Daye Sun (Hebei Normal University) for providing the seeds used in this research. This work was supported by the Natural Science Foundation of China (Grant No. 31770297).

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LZ conceived the project. XZ, WW and XK carried out experiments and analyzed the data. LZ revised and proofread the manuscript. All authors read and approved the final manuscript.

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Correspondence to Liqun Zhao.

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Zhang, X., Wang, W., Kang, X. et al. Arabidopsis CaM3 inhibits nitric oxide accumulation and improves thermotolerance by promoting S-nitrosoglutathione reductase via direct binding. Plant Growth Regul 90, 41–50 (2020). https://doi.org/10.1007/s10725-019-00552-9

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