Recent Progress in Oxidative Stress Signaling and Response in Plants

doi:10.13560/j.cnki.biotech.bull.1985.2023-0519

Abstract

Abstract:

Abiotic stress such as drought, salt, and extreme temperature are important factors affecting plant growth and development. The rapid accumulation of reactive oxygen species can lead to the disruption of intracellular redox homeostasis, further inducing secondary oxidative stress damage, when plants are subjected to stress. In addition to primary stress signals, plant cells also need secondary oxidative stress signals to respond abiotic stress. The perception and transmission of redox signals play an important role in plant oxidative stress response, which relies on reversible oxidative post-translational modifications of proteins mediated by a variety of small molecules with redox activity. This article reviews the research progress in plant redox signals, and discusses the future direction in this field, aiming to provide reference for further research on plant oxidative stress response and redox signal transduction.

Key words: oxidative stress, reactive oxygen species, redox signaling, post-translational modification

ZHOU Heng, XIE Yan-jie. Recent Progress in Oxidative Stress Signaling and Response in Plants[J]. Biotechnology Bulletin, 2023, 39(11): 36-43.

Figures/Tables 1

References 59

[1]	Zhu JK. Abiotic stress signaling and responses in plants[J]. Cell, 2016, 167(2): 313-324. doi: 10.1016/j.cell.2016.08.029 URL
[2]	Hancock JT, Veal D. Nitric oxide, other reactive signalling compounds, redox, and reductive stress[J]. J Exp Bot, 2021, 72(3): 819-829. doi: 10.1093/jxb/eraa331 pmid: 32687173
[3]	Mittler R, Zandalinas SI, Fichman Y, et al. Reactive oxygen species signalling in plant stress responses[J]. Nat Rev Mol Cell Biol, 2022, 23(10): 663-679. doi: 10.1038/s41580-022-00499-2
[4]	Del Río LA. ROS and RNS in plant physiology: an overview[J]. J Exp Bot, 2015, 66(10): 2827-2837. doi: 10.1093/jxb/erv099 pmid: 25873662
[5]	Zhou H, Huang JJ, Willems P, et al. Cysteine thiol-based post-translational modification: what do we know about transcription factors?[J]. Trends Plant Sci, 2023, 28(4): 415-428. doi: 10.1016/j.tplants.2022.11.007 URL
[6]	Kolbert Z, Lindermayr C, Loake GJ. The role of nitric oxide in plant biology: current insights and future perspectives[J]. J Exp Bot, 2021, 72(3): 777-780. doi: 10.1093/jxb/erab013 pmid: 33570126
[7]	Zhang J, Zhou MJ, Zhou H, et al. Hydrogen sulfide, a signaling molecule in plant stress responses[J]. J Integr Plant Biol, 2021, 63(1): 146-160. doi: 10.1111/jipb.13022
[8]	Noctor G, Foyer CH. Intracellular redox compartmentation and ROS-related communication in regulation and signaling[J]. Plant Physiol, 2016, 171(3): 1581-1592. doi: 10.1104/pp.16.00346 pmid: 27208308
[9]	Dietz KJ, Turkan I, Krieger-Liszkay A. Redox- and reactive oxygen species-dependent signaling into and out of the photosynthesizing chloroplast[J]. Plant Physiol, 2016, 171(3): 1541-1550.
[10]	Correa-Aragunde N, Foresi N, Lamattina L. Structure diversity of nitric oxide synthases(NOS): the emergence of new forms in photosynthetic organisms[J]. Front Plant Sci, 2013, 4: 232. doi: 10.3389/fpls.2013.00232 pmid: 23847637
[11]	Astier J, Gross I, Durner J. Nitric oxide production in plants: an update[J]. J Exp Bot, 2018, 69(14): 3401-3411. doi: 10.1093/jxb/erx420 pmid: 29240949
[12]	Chamizo-Ampudia A, Sanz-Luque E, Llamas A, et al. Nitrate reductase regulates plant nitric oxide homeostasis[J]. Trends Plant Sci, 2017, 22(2): 163-174. doi: S1360-1385(16)30201-1 pmid: 28065651
[13]	Gotor C, García I, Aroca Á, et al. Signaling by hydrogen sulfide and cyanide through post-translational modification[J]. J Exp Bot, 2019, 70(16): 4251-4265. doi: 10.1093/jxb/erz225 pmid: 31087094
[14]	Knuesting J, Scheibe R. Small molecules govern thiol redox switches[J]. Trends Plant Sci, 2018, 23(9): 769-782. doi: S1360-1385(18)30137-7 pmid: 30149854
[15]	Corpas FJ, González-Gordo S, Rodríguez-Ruiz M, et al. Thiol-based oxidative posttranslational modifications(OxiPTMs)of plant proteins[J]. Plant Cell Physiol, 2022, 63(7): 889-900. doi: 10.1093/pcp/pcac036 URL
[16]	Poole LB, Schöneich C. Introduction: what we do and do not know regarding redox processes of thiols in signaling pathways[J]. Free Radic Biol Med, 2015, 80: 145-147. doi: 10.1016/j.freeradbiomed.2015.02.005 URL
[17]	Sevilla F, Camejo D, Ortiz-Espín A, et al. The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species[J]. J Exp Bot, 2015, 66(10): 2945-2955. doi: 10.1093/jxb/erv146 pmid: 25873657
[18]	Chen LC, Wu R, Feng J, et al. Transnitrosylation mediated by the non-canonical catalase ROG1 regulates nitric oxide signaling in plants[J]. Dev Cell, 2020, 53(4): 444-457.e5. doi: S1534-5807(20)30232-X pmid: 32330424
[19]	Kneeshaw S, Gelineau S, Tada Y, et al. Selective protein denitrosylation activity of Thioredoxin-h5 modulates plant Immunity[J]. Mol Cell, 2014, 56(1): 153-162. doi: 10.1016/j.molcel.2014.08.003 pmid: 25201412
[20]	Zhang TR, Ma MY, Chen T, et al. Glutathione-dependent denitrosation of GSNOR1 promotes oxidative signalling downstream of H₂ O₂[J]. Plant Cell Environ, 2020, 43(5): 1175-1191. doi: 10.1111/pce.v43.5 URL
[21]	Tian YC, Fan M, Qin ZX, et al. Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor[J]. Nat Commun, 2018, 9(1): 1063. doi: 10.1038/s41467-018-03463-x pmid: 29540799
[22]	Shen J, Zhang J, Zhou MJ, et al. Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling[J]. Plant Cell, 2020, 32(4): 1000-1017. doi: 10.1105/tpc.19.00826 URL
[23]	Wu FH, Chi Y, Jiang ZH, et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis[J]. Nature, 2020, 578(7796): 577-581. doi: 10.1038/s41586-020-2032-3
[24]	Drerup MM, Schlücking K, Hashimoto K, et al. The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF[J]. Mol Plant, 2013, 6(2): 559-569. doi: 10.1093/mp/sst009 URL
[25]	Han JP, Köster P, Drerup MM, et al. Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca²⁺ binding[J]. New Phytol, 2019, 221(4): 1935-1949. doi: 10.1111/nph.2019.221.issue-4 URL
[26]	Vogelsang L, Dietz KJ. Plant thiol peroxidases as redox sensors and signal transducers in abiotic stress acclimation[J]. Free Radic Biol Med, 2022, 193(Pt 2): 764-778. doi: 10.1016/j.freeradbiomed.2022.11.019 URL
[27]	Bi GZ, Hu M, Fu L, et al. The cytosolic thiol peroxidase PRXIIB is an intracellular sensor for H₂O₂ that regulates plant immunity through a redox relay[J]. Nat Plants, 2022, 8(10): 1160-1175. doi: 10.1038/s41477-022-01252-5
[28]	Zhou H, Zhang F, Zhai FC, et al. Rice GLUTATHIONE PEROXIDASE1-mediated oxidation of bZIP68 positively regulates ABA-independent osmotic stress signaling[J]. Mol Plant, 2022, 15(4): 651-670. doi: 10.1016/j.molp.2021.11.006 URL
[29]	Chae HB, Kim MG, Kang CH, et al. Redox sensor QSOX1 regulates plant immunity by targeting GSNOR to modulate ROS generation[J]. Mol Plant, 2021, 14(8): 1312-1327. doi: 10.1016/j.molp.2021.05.004 pmid: 33962063
[30]	Ji T, Zheng LH, Wu JL, et al. The thioesterase APT1 is a bidirectional-adjustment redox sensor[J]. Nat Commun, 2023, 14(1): 2807. doi: 10.1038/s41467-023-38464-y pmid: 37198152
[31]	Duan M, Zhang RX, Zhu FG, et al. A lipid-anchored NAC transcription factor is translocated into the nucleus and activates Glyoxalase I expression during drought stress[J]. Plant Cell, 2017, 29(7): 1748-1772. doi: 10.1105/tpc.17.00044 URL
[32]	Liu WC, Song RF, Qiu YM, et al. Sulfenylation of ENOLASE2 facilitates H₂O₂-conferred freezing tolerance in Arabidopsis[J]. Dev Cell, 2022, 57(15): 1883-1898.e5. doi: 10.1016/j.devcel.2022.06.012 URL
[33]	Liu WC, Song RF, Zheng SQ, et al. Coordination of plant growth and abiotic stress responses by tryptophan synthase β subunit 1 through modulation of tryptophan and ABA homeostasis in Arabidopsis[J]. Mol Plant, 2022, 15(6): 973-990. doi: 10.1016/j.molp.2022.04.009 URL
[34]	Yuan HM, Liu WC, Lu YT. CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses[J]. Cell Host Microbe, 2017, 21(2): 143-155. doi: 10.1016/j.chom.2017.01.007 URL
[35]	Fu ZW, Feng YR, Gao X, et al. Salt stress-induced chloroplastic hydrogen peroxide stimulates pdTPI sulfenylation and methylglyoxal accumulation[J]. Plant Cell, 2023, 35(5): 1593-1616. doi: 10.1093/plcell/koad019 URL
[36]	Li JG, Fan M, Hua WB, et al. Brassinosteroid and hydrogen peroxide interdependently induce stomatal opening by promoting guard cell starch degradation[J]. Plant Cell, 2020, 32(4): 984-999. doi: 10.1105/tpc.19.00587 URL
[37]	Tian YC, Zhao N, Wang MM, et al. Integrated regulation of periclinal cell division by transcriptional module of BZR1-SHR in Arabidopsis roots[J]. New Phytol, 2022, 233(2): 795-808. doi: 10.1111/nph.v233.2 URL
[38]	Lee ES, Park JH, Wi SD, et al. Redox-dependent structural switch and CBF activation confer freezing tolerance in plants[J]. Nat Plants, 2021, 7(7): 914-922. doi: 10.1038/s41477-021-00944-8 pmid: 34155371
[39]	Camejo D, Ortiz-Espín A, Lázaro JJ, et al. Functional and structural changes in plant mitochondrial PrxII F caused by NO[J]. J Proteomics, 2015, 119: 112-125. doi: 10.1016/j.jprot.2015.01.022 pmid: 25682994
[40]	Klupczyńska EA, Dietz KJ, Małecka A, et al. Mitochondrial peroxiredoxin-IIF(PRXIIF)activity and function during seed aging[J]. Antioxidants, 2022, 11(7): 1226. doi: 10.3390/antiox11071226 URL
[41]	He NY, Chen LS, Sun AZ, et al. A nitric oxide burst at the shoot apex triggers a heat-responsive pathway in Arabidopsis[J]. Nat Plants, 2022, 8(4): 434-450. doi: 10.1038/s41477-022-01135-9
[42]	Ying SB, Yang WJ, Li P, et al. Phytochrome B enhances seed germination tolerance to high temperature by reducing S-nitrosylation of HFR1[J]. EMBO Rep, 2022, 23(10): e54371. doi: 10.15252/embr.202154371 URL
[43]	Liu H, Wang JC, Liu JH, et al. Hydrogen sulfide(H₂S)signaling in plant development and stress responses[J]. aBIOTECH, 2021, 2(1): 32-63. doi: 10.1007/s42994-021-00035-4
[44]	Huang JJ, Xie YJ. Hydrogen sulfide signaling in plants[J]. Antioxid Redox Signal, 2023, 10.1089/ars.2023.0267.
[45]	Chen SS, Jia HL, Wang XF, et al. Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells[J]. Mol Plant, 2020, 13(5): 732-744. doi: S1674-2052(20)30004-6 pmid: 31958520
[46]	Zhou MJ, Zhang J, Shen J, et al. Hydrogen sulfide-linked persulfidation of ABI4 controls ABA responses through the transactivation of MAPKKK18 in Arabidopsis[J]. Mol Plant, 2021, 14(6): 921-936. doi: 10.1016/j.molp.2021.03.007 URL
[47]	Zhou H, Zhou Y, Zhang F, et al. Persulfidation of nitrate reductase 2 is involved in l-cysteine desulfhydrase-regulated rice drought tolerance[J]. Int J Mol Sci, 2021, 22(22): 12119. doi: 10.3390/ijms222212119 URL
[48]	Laureano-Marín AM, Aroca Á, Esther Pérez-Pérez M, et al. Abscisic acid-triggered persulfidation of the cys protease ATG4 mediates regulation of autophagy by sulfide[J]. Plant Cell, 2020, 32(12): 3902-3920. doi: 10.1105/tpc.20.00766 URL
[49]	Aroca A, Yruela I, Gotor C, et al. Persulfidation of ATG18a regulates autophagy under ER stress in Arabidopsis[J]. Proc Natl Acad Sci USA, 2021, 118(20): e2023604118. doi: 10.1073/pnas.2023604118 URL
[50]	Li JS, Chen SS, Wang XF, et al. Hydrogen sulfide disturbs actin polymerization via S-sulfhydration resulting in stunted root hair growth[J]. Plant Physiol, 2018, 178(2): 936-949. doi: 10.1104/pp.18.00838 URL
[51]	Sun C, Yao GF, Li LX, et al. E3 ligase BRG3 persulfidation delays tomato ripening by reducing ubiquitination of the repressor WRKY71[J]. Plant Physiol, 2023, 192(1): 616-632. doi: 10.1093/plphys/kiad070 pmid: 36732924
[52]	Yun BW, Feechan A, Yin MH, et al. S-nitrosylation of NADPH oxidase regulates cell death in plant immunity[J]. Nature, 2011, 478(7368): 264-268. doi: 10.1038/nature10427
[53]	Kovacs I, Holzmeister C, Wirtz M, et al. ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of anti-oxidative mechanisms[J]. Front Plant Sci, 2016, 7: 1669.
[54]	Hu JL, Huang XH, Chen LC, et al. Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis[J]. Plant Physiol, 2015, 167(4): 1731-1746. doi: 10.1104/pp.15.00026 URL
[55]	Aroca A, Benito JM, Gotor C, et al. Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis[J]. J Exp Bot, 2017, 68(17): 4915-4927. doi: 10.1093/jxb/erx294 URL
[56]	Huang JJ, Willems P, Wei B, et al. Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites[J]. Proc Natl Acad Sci USA, 2019, 116(42): 21256-21261. doi: 10.1073/pnas.1906768116 URL
[57]	Wei B, Willems P, Huang JJ, et al. Identification of sulfenylated cysteines in Arabidopsis thaliana proteins using a disulfide-linked peptide reporter[J]. Front Plant Sci, 2020, 11: 777. doi: 10.3389/fpls.2020.00777 pmid: 32714340
[58]	Jurado-Flores A, Romero LC, Gotor C. Label-free quantitative proteomic analysis of nitrogen starvation in Arabidopsis root reveals new aspects of H₂S signaling by protein persulfidation[J]. Antioxidants, 2021, 10(4): 508. doi: 10.3390/antiox10040508 URL
[59]	Jurado-Flores A, Aroca A, Romero LC, et al. Sulfide promotes tolerance to drought through protein persulfidation in Arabidopsis[J]. J Exp Bot, 2023, erad165. doi:10.1093/jxb/erad165.