Hydrogen peroxide-induced stress acclimation in plants
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
35141765
PubMed Central
PMC11073338
DOI
10.1007/s00018-022-04156-x
PII: 10.1007/s00018-022-04156-x
Knihovny.cz E-zdroje
- Klíčová slova
- Chromatin remodeling, Oxidative posttranslational modifications, Redox signalling, Stress priming,
- MeSH
- peroxid vodíku farmakologie MeSH
- reaktivní formy kyslíku metabolismus MeSH
- rostlinné proteiny metabolismus MeSH
- rostliny * účinky léků metabolismus MeSH
- vývoj rostlin účinky léků MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- peroxid vodíku MeSH
- reaktivní formy kyslíku MeSH
- rostlinné proteiny MeSH
Among all reactive oxygen species (ROS), hydrogen peroxide (H2O2) takes a central role in regulating plant development and responses to the environment. The diverse role of H2O2 is achieved through its compartmentalized synthesis, temporal control exerted by the antioxidant machinery, and ability to oxidize specific residues of target proteins. Here, we examine the role of H2O2 in stress acclimation beyond the well-studied transcriptional reprogramming, modulation of plant hormonal networks and long-distance signalling waves by highlighting its global impact on the transcriptional regulation and translational machinery.
Zobrazit více v PubMed
Mills G, Sharps K, Simpson D, Pleijel H, Frei M, Burkey K, Emberson L, Uddling J, Broberg M, Feng Z, Kobayashi K, Agrawal M. Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance. Glob Chang Biol. 2018;24:4869–4893. doi: 10.1111/gcb.14381. PubMed DOI
Bailey-Serres J, Parker JE, Ainsworth EA, Oldroyd GED, Schroeder JI. Genetic strategies for improving crop yields. Nature. 2019;575:109–118. doi: 10.1038/s41586-019-1679-0. PubMed DOI PMC
Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006;11:15–19. doi: 10.1016/j.tplants.2005.11.002. PubMed DOI
Sinha R, Fritschi FB, Zandalinas SI, Mittler R. The impact of stress combination on reproductive processes in crops. Plant Sci. 2021;311:111007. doi: 10.1016/j.plantsci.2021.111007. PubMed DOI
Rivero RM, Mittler R, Blumwald E, Zandalinas SI. Developing climate-resilient crops: improving plant tolerance to stress combination. Plant J. 2021 doi: 10.1111/tpj.15483. PubMed DOI
Walter J, Jentsch A, Beierkuhnlein C, Kreyling J. Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. Environ Exp Bot. 2013;94:3–8. doi: 10.1016/J.ENVEXPBOT.2012.02.009. DOI
Godwin J, Farrona S. Plant Epigenetic Stress Memory Induced by Drought: A Physiological and Molecular Perspective. Methods Mol Biol. 2020;2093:243–259. doi: 10.1007/978-1-0716-0179-2_17. PubMed DOI
Serrano N, Ling Y, Bahieldin A, Mahfouz MM (2019) Thermopriming reprograms metabolic homeostasis to confer heat tolerance. Sci Rep 2019 9:1 9:1–14. 10.1038/s41598-018-36484-z PubMed PMC
Crisp PA, Ganguly D, Eichten SR, et al. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv. 2016 doi: 10.1126/SCIADV.1501340. PubMed DOI PMC
Leuendorf JE, Frank M. Schmülling T (2020) Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress. Sci Rep. 2020;10:1–11. doi: 10.1038/s41598-019-56797-x. PubMed DOI PMC
Wiszniewska A, Muszyńska E, Kołton A, Kamińska I, Hanus-Fajerska E. In vitro acclimation to prolonged metallic stress is associated with modulation of antioxidant responses in a woody shrub Daphne jasminea. Plant Cell Tiss Organ Cult. 2019;139:339–357. doi: 10.1007/s11240-019-01688-2. DOI
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490–498. doi: 10.1016/j.tplants.2004.08.009. PubMed DOI
Mittler R. ROS are good. Trends Plant Sci. 2017;22:11–19. doi: 10.1016/j.tplants.2016.08.002. PubMed DOI
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55:373–399. doi: 10.1146/annurev.arplant.55.031903.141701. PubMed DOI
Gómez R, Vicino P, Carrillo N, Lodeyro AF. Manipulation of oxidative stress responses as a strategy to generate stress-tolerant crops. From damage to signaling to tolerance. Crit Rev Biotechnol. 2019;39:693–708. doi: 10.1080/07388551.2019.1597829. PubMed DOI
Kerchev PI, Van Breusegem F. Improving oxidative stress resilience in plants. Plant J. 2021 doi: 10.1111/tpj.15493. PubMed DOI
Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell. 2005;17:1866–1875. doi: 10.1105/tpc.105.033589. PubMed DOI PMC
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010;33:453–467. doi: 10.1111/j.1365-3040.2009.02041.x. PubMed DOI
Mhamdi A, Van Breusegem F. Reactive oxygen species in plant development. Development. 2018;145:164376. doi: 10.1242/dev.164376. PubMed DOI
Foyer CH, Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal. 2009;11:861–905. doi: 10.1089/ars.2008.2177. PubMed DOI
Dikalov SI, Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal. 2014;20:372–382. doi: 10.1089/ars.2012.4886. PubMed DOI PMC
Noctor G, Mhamdi A, Foyer CH. Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ. 2016;39:1140–1160. doi: 10.1111/pce.12726. PubMed DOI
Petrov VD, Van Breusegem F. Hydrogen peroxide-a central hub for information flow in plant cells. AoB Plants. 2012 doi: 10.1093/aobpla/pls014. PubMed DOI PMC
Foyer CH. Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ Exp Bot. 2018;154:134–142. doi: 10.1016/j.envexpbot.2018.05.003. PubMed DOI PMC
Levine A, Tenhaken R, Dixon R, Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994;79:583–593. doi: 10.1016/0092-8674(94)90544-4. PubMed DOI
Wang Y, Zhang J, Li JL, Ma XR. Exogenous hydrogen peroxide enhanced the thermo tolerance of Festuca arundinacea and Lolium perenne by increasing the antioxidative capacity. Acta Physiol Plant. 2014;36:2915–2924. doi: 10.1007/s11738-014-1661-2. DOI
Ashfaque F, Iqbal M, Khan R, Khan NA. Exogenously Applied H2O2 promotes proline accumulation, water relations, photosynthetic efficiency and growth of wheat (Triticum aestivum L.) under salt stress. Annu Res Rev Biol. 2014;4:105–120. doi: 10.9734/ARRB/2014/5629. DOI
Phua SY, De Smet B, Remacle C, Chan KX, Van Breusegem F. Reactive oxygen species and organellar signaling. J Exp Bot. 2021;72:5807–5824. doi: 10.1093/jxb/erab218. PubMed DOI
Foyer CH. How plant cells sense the outside world through hydrogen peroxide. Nature. 2020;578:518–519. doi: 10.1038/d41586-020-00403-y. PubMed DOI
Aranega-Bou P, de la O Leyva M, Finiti I, García-Agustín P, González-Bosch C (2014) Priming of plant resistance by natural compounds Hexanoic acid as a model. Front Plant Sci 5:488. 10.3389/fpls.2014.00488 PubMed PMC
Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B. The ‘prime-ome’: Towards a holistic approach to priming. Trends Plant Sci. 2015;20:443–452. doi: 10.1016/j.tplants.2015.04.002. PubMed DOI
Vincent C, Rowland D, Schaffer B, Bassil E, Racette K, Zurweller B. Primed acclimation: A physiological process offers a strategy for more resilient and irrigation-efficient crop production. Plant Sci. 2020;295:110240. doi: 10.1016/j.plantsci.2019.110240. PubMed DOI
Zhang J, Zhou M, Zhou H, et al. Hydrogen sulfide, a signaling molecule in plant stress responses. J Integr Plant Biol. 2021;63:146–160. doi: 10.1111/JIPB.13022. PubMed DOI
Wang H, Ji F, Zhang Y, et al. Interactions between hydrogen sulphide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminium toxicity. Plant Cell Environ. 2019;42:2340–2356. doi: 10.1111/PCE.13555. PubMed DOI
Ishibashi Y, Yamaguchi H, Yuasa T, Iwaya-Inoue M, Arima S, Zheng SH. Hydrogen peroxide spraying alleviates drought stress in soyabean plants. J Plant Physiol. 2011;168:1562–1567. doi: 10.1016/j.jplph.2011.02.003. PubMed DOI
Conrath U, Beckers GJ, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B. Priming: getting ready for battle. Mol Plant Microbe Interact. 2006;19:1062–1071. doi: 10.1094/MPMI-19-1062. PubMed DOI
Vaidya AS, Peterson FC, Eckhardt J, Xing Z, Park SY, Dejonghe W, Takeuchi J, Pri-Tal O, Faria J, Elzinga D, Volkman BF, Todoroki Y, Mosquna A, Okamoto M, Cutler SR. Click-to-lead design of a picomolar ABA receptor antagonist with potent activity in vivo. Proc Natl Acad Sci USA. 2021;118:e2108281118. doi: 10.1073/pnas.2108281118. PubMed DOI PMC
Kerchev P, van der Meer T, Sujeeth N, Verlee A, Stevens CV, Van Breusegem F, Gechev T. Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol Adv. 2020;40:107503. doi: 10.1146/10.1016/j.biotechadv.2019.107503. PubMed DOI
Gondim FA, Gomes-Filho E, Costa JH, Alencar NLM, Priso JT. CAT plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. J Plant Physiol Biochem. 2012;56:62–71. doi: 10.1016/j.plaphy.2012.04.012. PubMed DOI
Habib N, Ali Q, Ali S, Javed MT, Zulqurnain Haider M, Perveen R, Shahid MR, Rizwan M, Abdel-Daim MM, Elkelish A, Bin-Jumah M. Use of nitric oxide and hydrogen peroxide for better yield of wheat (Triticum aestivum L.) under water deficit conditions: growth, osmoregulation, and antioxidative defense mechanism. Plants. 2020;9:285. doi: 10.3390/plants9020285. PubMed DOI PMC
Silva PCC, Azevedo Neto ADD, Gheyi HJ, Ribas RF, Silva CRDR, Cova AMD. Salt tolerance induced by hydrogen peroxide priming on seed is related to improvement of ion homeostasis and antioxidative defense in sunflower plants. J Plant Nutr. 2021;44:1207–2121. doi: 10.1080/01904167.2020.1862202. DOI
de Azevedo Neto AD, Prisco JT, Enéas-Filho J, Medeiros JV, Gomes-Filho E. Hydrogen peroxide pre-treatment induces salt-stress acclimation in maize plants. J Plant Physiol. 2005;162:1114–1122. doi: 10.1016/j.jplph.2005.01.007. PubMed DOI
Wahid A, Perveen M, Gelani S, Basra SM. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol. 2007;164:283–294. doi: 10.1016/j.jplph.2006.01.005. PubMed DOI
Xu FJ, Jin CW, Liu WJ, Zhang YS, Lin XY. Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings. J Integr Plant Biol. 2010;53:44–53. doi: 10.1111/j.1744-7909.2010.01008.x. PubMed DOI
Dos Santos AG, de Oliveira P-M, de Paiva Pinheiro SK, de Castro ME, de Sousa LL, Camelo Marques E, de Carvalho HH, Gomes-Filho E. H2O2 priming promotes salt tolerance in maize by protecting chloroplasts ultrastructure and primary metabolites modulation. Plant Sci. 2021;303:110774. doi: 10.1016/j.plantsci.2020.110774. PubMed DOI
Claeys H, Van Landeghem S, Dubois M, Maleux K, Inzé D. What Is Stress? Dose-Response Effects in Commonly Used in Vitro Stress Assays. Plant Physiol. 2014;165:519–527. doi: 10.1104/pp.113.234641. PubMed DOI PMC
Gechev T, Gadjev I, Van Breusegem F, Inzé D, Dukiandjiev S, Toneva V, Minkov I. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell Mol Life Sci. 2002;59:708–714. doi: 10.1007/s00018-002-8459-x. PubMed DOI PMC
Yu CW, Murphy TM, Lin CH. Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol. 2003;30:955–963. doi: 10.1071/FP03091. PubMed DOI
İşeri ÖD, Körpe DA, Sahin FI, Haberal M. Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress. Acta Physiol Plant. 2013;35:1905–1913. doi: 10.1007/s11738-013-1228-7. DOI
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 2002;163:515–523. doi: 10.1016/S0168-9452(02)00159-0. DOI
Mubarakshina Borisova MM, Kozuleva MA, Rudenko NN, Naydov IA, Klenina IB, Ivanov BN. Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins. Biochim Biophys Acta. 2012;1817:1314–1321. doi: 10.1016/j.bbabio.2012.02.036. PubMed DOI
Del Río LA, López-Huertas E. ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol. 2016;57:1364–1376. doi: 10.1093/pcp/pcw076. PubMed DOI
Segal AW. NADPH oxidases as electrochemical generators to produce ion fluxes and turgor in fungi, plants and humans. Open Biol. 2016;6:160028. doi: 10.1098/rsob.160028. PubMed DOI PMC
Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. 2009 doi: 10.1126/scisignal.2000448. PubMed DOI
Marino D, Dunand C, Puppo A, Pauly N. A burst of plant NADPH oxidases. Trends Plant Sci. 2012;17:9–15. doi: 10.1016/j.tplants.2011.10.001. PubMed DOI
Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou JM. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe. 2014;15:329–338. doi: 10.1016/j.chom.2014.02.009. PubMed DOI
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol. 2011;14:691–699. doi: 10.1016/j.pbi.2011.07.014. PubMed DOI
Gong M, Chen B, Li ZG, Guo LH. Heat-shock-induced cross adaptation to heat, chilling, drought and salt stress in maize seedlings and involvement of H2O2. J Plant Physiol. 2001;158:112–1130. doi: 10.1078/0176-1617-00327. DOI
Wu F, Chi Y, Jiang Z, et al. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature. 2020;578:577–581. doi: 10.1038/s41586-020-2032-3. PubMed DOI
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy Amith R, Karpinski S, Mittler R. ROS, calcium and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 2016;171:1606–1615. doi: 10.1104/pp.16.00434. PubMed DOI PMC
Winterbourn CC. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochem Biophys Acta. 2014;1840:730–738. doi: 10.1016/j.bbagen.2013.05.004. PubMed DOI
Wang Y, Li J, Wang J, Li Z. Exogenous H2O2 improves the chilling tolerance of manilagrass and mascarenegrass by activating the antioxidative system. Plant Growth Regul. 2010;61:195–204. doi: 10.1007/s10725-010-9470-0. DOI
Marthandan V, Geetha R, Kumutha K, Renganathan VG, Karthikeyan A, Ramalingam J. Seed Priming: A feasible strategy to enhance drought tolerance in crop plants. Int J Mol Sci. 2020;21:8258. doi: 10.3390/ijms21218258. PubMed DOI PMC
Hu T, Chen K, Hu L, Amombo E, Fu J. H2O2 and Ca2+-based signaling and associated ion accumulation, antioxidant systems and secondary metabolism orchestrate the response to NaCl stress in perennial ryegrass. Sci Rep. 2016;6:36396. doi: 10.1038/srep36396. PubMed DOI PMC
Hu Y, Ge Y, Zhang C, Ju T, Cheng W. Cadmium toxicity and translocation in rice seedlings are reduced by hydrogen peroxide pretreatment. Plant Growth Regul. 2009;59:51–61. doi: 10.1007/s10725-009-9387-7. DOI
Couturier J, Chibani K, Jacquot JP, Rouhier N. Cysteine-based redox regulation and signaling in plants. Front Plant Sci. 2013;4:105. doi: 10.3389/fpls.2013.00105. PubMed DOI PMC
Jacques S, Ghesquière B, De Bock PJ, Demol H, Wahni K, Willems P, Messens J, Van Breusegem F, Gevaert K. Protein methionine sulfoxide dynamics in Arabidopsis thaliana under oxidative stress. Mol Cell Proteomics. 2015;14:1217–1229. doi: 10.1074/mcp.M114.043729. PubMed DOI PMC
Huang J, Willems P, Van Breusegem F, Messens J. Pathways crossing mammalian and plant sulfenomic landscapes. Free Radic Biol Med. 2018;122:193–201. doi: 10.1016/j.freeradbiomed.2018.02.012. PubMed DOI
Roos G, Foloppe N, Messens J. Understanding the pK(a) of redox cysteines: the key role of hydrogen bonding. Antioxid Redox Signal. 2013;18:94–127. doi: 10.1089/ars.2012.4521. PubMed DOI
Roos G, Messens J. Protein sulfenic acid formation: from cellular damage to redox regulation. Free Radic Biol Med. 2011;51:314–326. doi: 10.1016/j.freeradbiomed.2011.04.031. PubMed DOI
Waszczak C, Akter S, Eeckhout D, Persiau G, Wahni K, Bodra N, Van Molle I, De Smet B, Vertommen D, Gevaert K, De Jaeger G, Van Montagu M, Messens J, Van Breusegem F. Sulfenome mining in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2014;111:11545–11550. doi: 10.1073/pnas.1411607111. PubMed DOI PMC
Akter S, Fu L, Jung Y, Conte ML, Lawson JR, Lowther WT, Sun R, Liu K, Yang J, Carroll KS. Chemical proteomics reveals new targets of cysteine sulfinic acid reductase. Nat Chem Biol. 2018;14:995–1004. doi: 10.1038/s41589-018-0116-2. PubMed DOI PMC
De Smet B, Willems P, Fernandez-Fernandez AD, Alseekh S, Fernie AR, Messens J, Van Breusegem F. In vivo detection of protein cysteine sulfenylation in plastids. Plant J. 2019;97:765–778. doi: 10.1111/tpj.14146. PubMed DOI
Gadjev I, Vanderauwera S, Gechev TS, et al. Transcriptomic Footprints Disclose Specificity of Reactive Oxygen Species Signaling in Arabidopsis. Plant Physiol. 2006;141:436–445. doi: 10.1104/PP.106.078717. PubMed DOI PMC
Willems P, Mhamdi A, Stael S, Storme V, Kerchev P, Noctor G, Gevaert K, Van Breusegem F. The ROS wheel: Refining ROS transcriptional footprints. Plant Physiol. 2016;171:1720–1733. doi: 10.1104/pp.16.00420. PubMed DOI PMC
Beauclair L, Yu A, Bouché N. microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J. 2010;62:454–462. doi: 10.1111/J.1365-313X.2010.04162.X. PubMed DOI
Sunkar R, Kapoor A, Zhu JK. Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance. Plant Cell. 2006;18:2051. doi: 10.1105/TPC.106.041673. PubMed DOI PMC
Vivarelli S, Lenzken SC, Ruepp MD, et al. Paraquat Modulates Alternative Pre-mRNA Splicing by Modifying the Intracellular Distribution of SRPK2. PLoS ONE. 2013;8:e61980. doi: 10.1371/JOURNAL.PONE.0061980. PubMed DOI PMC
Ding F, Cui P, Wang Z, et al. Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genom. 2014;15:1–14. doi: 10.1186/1471-2164-15-431. PubMed DOI PMC
John S, Olas JJ, Mueller-Roeber B. Regulation of alternative splicing in response to temperature variation in plants. J Exp Bot. 2021;72:6150–6163. doi: 10.1093/JXB/ERAB232. PubMed DOI PMC
Zhou Y, Li XH, Guo QH, et al. Salt responsive alternative splicing of a RING finger E3 ligase modulates the salt stress tolerance by fine-tuning the balance of COP9 signalosome subunit 5A. PLoS Genet. 2021 doi: 10.1371/JOURNAL.PGEN.1009898. PubMed DOI PMC
Gu J, Xia Z, Luo Y, et al. Spliceosomal protein U1A is involved in alternative splicing and salt stress tolerance in Arabidopsis thaliana. Nucleic Acids Res. 2018;46:1777. doi: 10.1093/NAR/GKX1229. PubMed DOI PMC
Moeder W, del Pozo O, Navarre DA, et al. Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Mol Biol. 2007;63:273–287. doi: 10.1007/S11103-006-9087-X. PubMed DOI
Ling Y, Serrano N, Gao G, et al. Thermopriming triggers splicing memory in Arabidopsis. J Exp Bot. 2018;69:2659–2675. doi: 10.1093/JXB/ERY062. PubMed DOI PMC
Urquidi Camacho RA, Lokdarshi A, von Arnim AG. Translational gene regulation in plants: A green new deal. Wiley Interdiscip Rev RNA. 2020 doi: 10.1002/WRNA.1597. PubMed DOI PMC
Martinez-Seidel F, Beine-Golovchuk O, Hsieh YC, Kopka J. Systematic review of plant ribosome heterogeneity and specialization. Front Plant Sci. 2020;11:948. doi: 10.3389/fpls.2020.00948. PubMed DOI PMC
Xue S, Barna M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol. 2012;13:355–369. doi: 10.1038/nrm3359. PubMed DOI PMC
Genuth NR, Barna M. Heterogeneity and specialized functions of translation machinery: from genes to organisms. Nat Rev Genet. 2018;19:431–452. doi: 10.1038/s41576-018-0008-z. PubMed DOI PMC
Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W. Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics. 2013;14:783. doi: 10.1186/1471-2164-14-783. PubMed DOI PMC
Salih KJ, Duncan O, Li L, O'Leary B, Fenske R, Trösch J, Millar AH. Impact of oxidative stress on the function, abundance, and turnover of the Arabidopsis 80S cytosolic ribosome. Plant J. 2020;103:128–139. doi: 10.1111/tpj.14713. PubMed DOI
Chen GH, Liu MJ, Xiong Y, Sheen J, Wu SH. TOR and RPS6 transmit light signals to enhance protein translation in deetiolating Arabidopsis seedlings. Proc Natl Acad Sci USA. 2018;115:12823–12828. doi: 10.1073/pnas.1809526115. PubMed DOI PMC
Bakshi A, Moin M, Madhav MS, Kirti PB. Target of rapamycin, a master regulator of multiple signalling pathways and a potential candidate gene for crop improvement. Plant Biol (Stuttg) 2019;21:190–205. doi: 10.1111/plb.12935. PubMed DOI
Pereyra CM, Aznar NR, Rodriguez MS, Salerno GL, Martínez-Noël GMA. Target of rapamycin signaling is tightly and differently regulated in the plant response under distinct abiotic stresses. Planta. 2019;251:21. doi: 10.1007/s00425-019-03305-0. PubMed DOI
Gerashchenko MV, Lobanov AV, Gladyshev VN. Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proc Natl Acad Sci USA. 2012;109:17394–17399. doi: 10.1073/pnas.1120799109. PubMed DOI PMC
Moore M, Smith A, Wesemann C, Schmidtpott S, Wegener M, Farooq MA, Seidel T, Pogson B, Dietz K-J. Retrograde control of cytosolic translation targets synthesis of plastid localized proteins and nuclear responses for efficient light acclimation. bioRxiv. 2021 doi: 10.1101/2021.02.18.431817. PubMed DOI
Ahn CS, Lee DH, Pai HS. Characterization of Maf1 in Arabidopsis: function under stress conditions and regulation by the TOR signaling pathway. Planta. 2019;249:527–542. doi: 10.1007/s00425-018-3024-5. PubMed DOI
Torrent M, Chalancon G, de Groot NS, Wuster A, Madan Babu M. Cells alter their tRNA abundance to selectively regulate protein synthesis during stress conditions. Sci Signal. 2018 doi: 10.1126/scisignal.aat6409. PubMed DOI PMC
Lalande S, Merret R, Salinas-Giegé T, Drouard L. Arabidopsis tRNA-derived fragments as potential modulators of translation. RNA Biol. 2020;17:1137–1148. doi: 10.1080/15476286.2020.1722514. PubMed DOI PMC
Thompson DM, Lu C, Green PJ, Parker R. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA. 2008;14:2095–2103. doi: 10.1261/rna.1232808. PubMed DOI PMC
Cognat V, Morelle G, Megel C, Lalande S, Molinier J, Vincent T, Small I, Duchêne AM, Maréchal-Drouard L. The nuclear and organellar tRNA-derived RNA fragment population in Arabidopsis thaliana is highly dynamic. Nucleic Acids Res. 2020;48:8812–8813. doi: 10.1093/nar/gkaa651. PubMed DOI PMC
Lokdarshi A, Guan J, Urquidi Camacho RA, Cho SK, Morgan PW, Leonard M, Shimono M, Day B, von Arnim AG. Light activates the translational regulatory kinase GCN2 via reactive oxygen species emanating from the chloroplast. Plant Cell. 2020;32:1161–1178. doi: 10.1105/tpc.19.00751. PubMed DOI PMC
Liu X, Afrin T, Pajerowska-Mukhtar KM. Arabidopsis GCN2 kinase contributes to ABA homeostasis and stomatal immunity. Commun Biol. 2019;2:302. doi: 10.1038/s42003-019-0544-x. PubMed DOI PMC
David R, Burgess A, Parker B, Li J, Pulsford K, Sibbritt T, Preiss T, Searle IR. Transcriptome-Wide Mapping of RNA 5-Methylcytosine in Arabidopsis mRNAs and Noncoding RNAs. Plant Cell. 2017;29:445–460. doi: 10.1105/tpc.16.00751. PubMed DOI PMC
Giorgio M, Dellino GI, Gambino V, Roda N, Pelicci PG. On the epigenetic role of guanosine oxidation. Redox Biol. 2020;29:101398. doi: 10.1016/j.redox.2019.101398. PubMed DOI PMC
Hofer T, Badouard C, Bajak E, Ravanat JL, Mattsson A, Cotgreave IA. Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA. Biol Chem. 2005;386:333–337. doi: 10.1515/BC.2005.040. PubMed DOI
Bazin J, Langlade N, Vincourt P, Arribat S, Balzergue S, El-Maarouf-Bouteau H, Bailly C. Targeted mRNA oxidation regulates sunflower seed dormancy alleviation during dry after-ripening. Plant Cell. 2011;23:2196–2208. doi: 10.1105/tpc.111.086694. PubMed DOI PMC
Zhan Y, Dhaliwal JS, Adjibade P, Uniacke J, Mazroui R, Zerges W. Localized control of oxidized RNA. J Cell Sci. 2015;128:4210–4219. doi: 10.1242/jcs.175232. PubMed DOI
Chantarachot T, Bailey-Serres J. Polysomes, stress granules, and processing bodies: a dynamic triumvirate controlling cytoplasmic mRNA fate and function. Plant Physiol. 2018;176:254–269. doi: 10.1104/pp.17.01468. PubMed DOI PMC
Maruri-López I, Figueroa NE, Hernández-Sánchez IE, Chodasiewicz M. Plant Stress Granules: Trends and Beyond. Front Plant Sci. 2021;12:722643. doi: 10.3389/fpls.2021.722643. PubMed DOI PMC
Emara MM, Fujimura K, Sciaranghella D, Ivanova V, Ivanov P, Anderson P. Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation. Biochem Biophys Res Commun. 2012;423:763–769. doi: 10.1016/j.bbrc.2012.06.033. PubMed DOI PMC
Lokdarshi A, Conner WC, McClintock C, Li T, Roberts DM. Arabidopsis CML38, a calcium sensor that localizes to ribonucleoprotein complexes under hypoxia stress. Plant Physiol. 2016;170:1046–1059. doi: 10.1104/pp.15.01407. PubMed DOI PMC
Nguyen CC, Nakaminami K, Matsui A, Kobayashi S, Kurihara Y, Toyooka K, Tanaka M, Seki M. Oligouridylate binding protein 1b plays an integral role in plant heat stress tolerance. Front Plant Sci. 2016;7:853. doi: 10.3389/fpls.2016.00853. PubMed DOI PMC
Chodasiewicz M, Sokolowska EM, Nelson-Dittrich AC, Masiuk A, Beltran JCM, Nelson ADL, Skirycz A. Identification and characterization of the heat-induced plastidial stress granules reveal new insight into Arabidopsis stress response. Front Plant Sci. 2020;11:595792. doi: 10.3389/fpls.2020.595792. PubMed DOI PMC
Uniacke J, Zerges W. Stress induces the assembly of RNA granules in the chloroplast of Chlamydomonas reinhardtii. J Cell Biol. 2008;182:641–646. doi: 10.1083/jcb.200805125. PubMed DOI PMC
Møller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Annu Rev Plant Biol. 2007;58:459–481. doi: 10.1146/annurev.arplant.58.032806.103946. PubMed DOI
Rodrigues O, Reshetnyak G, Grondin A, Saijo Y, Leonhardt N, Maurel C, Verdoucq L. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc Natl Acad Sci USA. 2017;114:9200–9205. doi: 10.1073/pnas.1704754114. PubMed DOI PMC
Exposito-Rodriguez M, Laissue PP, Yvon-Durocher G, Smirnoff N, Mullineaux PM. Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat Commun. 2017;8:49. doi: 10.1038/s41467-017-00074-w. PubMed DOI PMC
Caplan JL, Kumar AS, Park E, Padmanabhan MS, Hoban K, Modla S, Czymmek K, Dinesh-Kumar SP. Chloroplast stromules function during innate immunity. Dev Cell. 2015;34:45–57. doi: 10.1016/j.devcel.2015.05.011. PubMed DOI PMC
Ashtamker C, Kiss V, Sagi M, Davydov O, Fluhr R. Diverse subcellular locations of cryptogein-induced reactive oxygen species production in tobacco bright yellow-2 cells. Plant Physiol. 2007;143:1817–1826. doi: 10.1104/pp.106.090902. PubMed DOI PMC
Roschzttardtz H, Séguéla-Arnaud M, Briat JF, Vert G, Curie C. The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell. 2011;23:2725–2737. doi: 10.1105/tpc.111.088088. PubMed DOI PMC
El-Esawi M, Arthaut LD, Jourdan N, d’Harlingue A, Link J, Martino CF, Ahmad M. Blue-light induced biosynthesis of ROS contributes to the signaling mechanism of Arabidopsis cryptochrome. Sci Rep. 2017;7:13875. doi: 10.1038/s41598-017-13832-z. PubMed DOI PMC
Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardó FV, Pellny TK, Verrier PJ, Foyer CH. Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J. 2010;64:825–838. doi: 10.1111/j.1365-313X.2010.04371.x. PubMed DOI
Zechmann B, Stumpe M, Mauch F. Immunocytochemical determination of the subcellular distribution of ascorbate in plants. Planta. 2011;233:1–12. doi: 10.1007/s00425-010-1275-x. PubMed DOI PMC
Go YM, Jones DP. Redox control systems in the nucleus: mechanisms and functions. Antioxid Redox Signal. 2010;13:489–509. doi: 10.1089/ars.2009.3021. PubMed DOI PMC
Gaber A, Ogata T, Maruta T, Yoshimura K, Tamoi M, Shigeoka S. The Involvement of Arabidopsis glutathione peroxidase 8 in the suppression of oxidative damage in the nucleus and cytosol. Plant Cell Physiol. 2012;53:1596–1606. doi: 10.1093/pcp/pcs100. PubMed DOI
Delorme-Hinoux V, Bangash SA, Meyer AJ, Reichheld JP. Nuclear thiol redox systems in plants. Plant Sci. 2016;243:84–95. doi: 10.1016/j.plantsci.2015.12.002. PubMed DOI
Serrato AJ, Crespo JL, Florencio FJ, Cejudo FJ. Characterization of two thioredoxin h with predominant localization in the nucleus of aleurone and scutellum cells of germinating wheat seeds. Plant Mol Biol. 2001;46:361–371. doi: 10.1023/a:1010697331184. PubMed DOI
Ying Y, Yue W, Wang S, Li S, Wang M, Zhao Y, Wang C, Mao C, Whelan J, Shou H. Two h-Type Thioredoxins Interact with the E2 Ubiquitin conjugase PHO2 to fine-tune phosphate homeostasis in Rice. Plant Physiol. 2017;173:812–824. doi: 10.1104/pp.16.01639. PubMed DOI PMC
Serrato AJ, Cejudo FJ. Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta. 2003;217:392–399. doi: 10.1007/s00425-003-1009-4. PubMed DOI
Kim J-H. Multifaceted chromatin structure and transcription changes in plant stress response. Int J Mol Sci. 2021;22:2013. doi: 10.3390/ijms22042013. PubMed DOI PMC
Kinoshita T, Seki M. Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 2014;55:1859–1863. doi: 10.1093/pcp/pcu125. PubMed DOI
Bilichak A, Kovalchuk I. Transgenerational response to stress in plants and its application for breeding. J Exp Bot. 2016;67:2081–2092. doi: 10.1093/jxb/erw066. PubMed DOI
Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv. 2016;2:e1501340. doi: 10.1126/sciadv.1501340. PubMed DOI PMC
Sani E, Herzyk P, Perrella G, Colot V, Amtmann A. Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 2013;14:r59. doi: 10.1186/gb-2013-14-6-r59. PubMed DOI PMC
Singh D, Chaudhary P, Taunk J, Singh CK, Sharma S, Singh VJ, Singh D, Chinnusamy V, Yadav R, Pal M. Plant epigenomics for extenuation of abiotic stresses: Challenges and future perspectives. J Exp Bot. 2021 doi: 10.1093/jxb/erab337. PubMed DOI
Sudan J, Raina M, Singh R. Plant epigenetic mechanisms: role in abiotic stress and their generational heritability. 3 Biotech. 2018;8:172. doi: 10.1007/s13205-018-1202-6. PubMed DOI PMC
Matsuda M, Shimomura I. Increased oxidative stress in obesity: implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obes Res Clin Pract. 2013;7:330–341. doi: 10.1016/j.orcp.2013.05.004. PubMed DOI
Dimauro I, Paronetto MP, Caporossi D. Exercise, redox homeostasis and the epigenetic landscape. Redox Biol. 2020;35:101477. doi: 10.1016/j.redox.2020.10147. PubMed DOI PMC
Rm SK, Wang Y, Zhang X, et al. Redox Components: Key Regulators of Epigenetic Modifications in Plants. Int J Mol Sci. 2020 doi: 10.3390/IJMS21041419. PubMed DOI PMC
O'Hagan HM, Wang W, Sen S, Destefano Shields C, Lee SS, Zhang YW, Clements EG, Cai Y, Van Neste L, Easwaran H, Casero RA, Sears CL, Baylin SB. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell. 2011;20:606–619. doi: 10.1016/j.ccr.2011.09.012. PubMed DOI PMC
Bazopoulou D, Knoefler D, Zheng Y, et al. Developmental ROS individualizes organismal stress resistance and lifespan. Nature. 2019;576:301–305. doi: 10.1038/s41586-019-1814-y. PubMed DOI PMC
Buzas DM. Emerging links between iron-sulfur clusters and 5-methylcytosine base excision repair in plants. Genes Genet Syst. 2016;91:51–62. doi: 10.1266/ggs.16-00015. PubMed DOI
Lamadema N, Burr S, Brewer AC. Dynamic regulation of epigenetic demethylation by oxygen availability and cellular redox. Free Radic Biol Med. 2019;131:282–298. doi: 10.1016/j.freeradbiomed.2018.12.009. PubMed DOI
Lindermayr C, Rudolf EE, Durner J, Groth M. Interactions between metabolism and chromatin in plant models. Mol Metab. 2020;38:100951. doi: 10.1016/j.molmet.2020.01.015. PubMed DOI PMC
Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell. 2008;133:978–993. doi: 10.1016/j.cell.2008.04.041. PubMed DOI
Schader T, Löwe O, Reschke C, Malacarne P, Hahner F, Müller N, Gajos-Draus A, Backs J, Schröder K. Oxidation of HDAC4 by Nox4-derived H2O2 maintains tube formation by endothelial cells. Redox Biol. 2020;36:101669. doi: 10.1016/j.redox.2020.101669. PubMed DOI PMC
Mengel A, Ageeva A, Georgii E, Bernhardt J, Wu K, Durner J, Lindermayr C. Nitric Oxide modulates histone acetylation at stress genes by inhibition of histone deacetylases. Plant Physiol. 2017;173:1434–1452. doi: 10.1104/pp.16.01734. PubMed DOI PMC
Ageeva-Kieferle A, Georgii E, Winkler B, Ghirardo A, Albert A, Hüther P, Mengel A, Becker C, Schnitzler JP, Durner J, Lindermayr C. Nitric oxide coordinates growth, development, and stress response via histone modification and gene expression. Plant Physiol. 2021;187:336–360. doi: 10.1093/plphys/kiab222. PubMed DOI PMC
Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A. S-nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature. 2008;455:411–415. doi: 10.1038/nature07238. PubMed DOI
Nott A, Nitarska J, Veenvliet JV, Schacke S, Derijck AA, Sirko P, Muchardt C, Pasterkamp RJ, Smidt MP, Riccio A. S-nitrosylation of HDAC2 regulates the expression of the chromatin-remodeling factor Brm during radial neuron migration. Proc Natl Acad Sci USA. 2013;110:3113–3118. doi: 10.1073/pnas.1218126110. PubMed DOI PMC
Kreuz S, Fischle W. Oxidative stress signaling to chromatin in health and disease. Epigenomics. 2016;8:843–862. doi: 10.2217/epi-2016-0002. PubMed DOI PMC
Galligan JJ, Marnett LJ. Histone Adduction and Its Functional Impact on Epigenetics. Chem Res Toxicol. 2017;30:376–387. doi: 10.1021/acs.chemrestox.6b00379. PubMed DOI PMC
Galligan JJ, Rose KL, Beavers WN, Hill S, Tallman KA, Tansey WP, Marnett LJ. Stable histone adduction by 4-oxo-2-nonenal: a potential link between oxidative stress and epigenetics. J Am Chem Soc. 2014;136:11864–11866. doi: 10.1021/ja503604t. PubMed DOI PMC
Borg M, Berger F. Chromatin remodelling during male gametophyte development. Plant J. 2015;83:177–188. doi: 10.1111/tpj.12856. PubMed DOI
Zheng M, Lin J, Liu X, Chu W, Li J, Gao Y, An K, Song W, Xin M, Yao Y, Peng H, Ni Z, Sun Q, Hu Z. Histone acetyltransferase TaHAG1 acts as a crucial regulator to strengthen salt tolerance of hexaploid wheat. Plant Physiol. 2021;186:1951–1969. doi: 10.1093/plphys/kiab187. PubMed DOI PMC
Sanders YY, Liu H, Liu G, Thannickal VJ. Epigenetic mechanisms regulate NADPH oxidase-4 expression in cellular senescence. Free Radic Biol Med. 2015;79:197–205. doi: 10.1016/j.freeradbiomed.2014.12.008. PubMed DOI
Brewer AC. Physiological interrelationships between NADPH oxidases and chromatin remodelling. Free Radic Biol Med. 2021;170:109–115. doi: 10.1016/j.freeradbiomed.2021.01.052. PubMed DOI
Zelko IN, Folz RJ. Regulation of Oxidative Stress in Pulmonary Artery Endothelium. Modulation of Extracellular Superoxide Dismutase and NOX4 Expression Using Histone Deacetylase Class I Inhibitors. Am J Respir Cell Mol Biol. 2015;53:513–524. doi: 10.1165/rcmb.2014-0260OC. PubMed DOI PMC
Manea SA, Constantin A, Manda G, Sasson S, Manea A. Regulation of Nox enzymes expression in vascular pathophysiology: Focusing on transcription factors and epigenetic mechanisms. Redox Biol. 2015;5:358–366. doi: 10.1016/j.redox.2015.06.012. PubMed DOI PMC
He H, Van Breusegem F, Mhamdi A. Redox-dependent control of nuclear transcription in plants. J Exp Bot. 2018;69:3359–3372. doi: 10.1093/jxb/ery130. PubMed DOI
Dietz KJ. Redox regulation of transcription factors in plant stress acclimation and development. Antioxid Redox Signal. 2014;21:1356–1372. doi: 10.1089/ars.2013.5672. PubMed DOI
Mou Z, Fan W, Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell. 2003;113:935–944. doi: 10.1016/s0092-8674(03)00429-x. PubMed DOI
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science. 2008;321:952–956. doi: 10.1126/science.1156970. PubMed DOI PMC
Hieno A, Naznin HA, Inaba-Hasegawa K, Yokogawa T, et al. Transcriptome analysis and identification of a transcriptional regulatory network in the response to H2O2. Plant Physiol. 2019;180:1629–1646. doi: 10.1104/pp.18.01426. PubMed DOI PMC
Babbar R, Karpinska B, Grover A, Foyer CH. Heat-Induced Oxidation of the Nuclei and Cytosol. Front Plant Sci. 2021;11:617779. doi: 10.3389/fpls.2020.617779. PubMed DOI PMC
Giesguth M, Sahm A, Simon S, Dietz KJ. Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett. 2015;589:718–725. doi: 10.1016/j.febslet.2015.01.039. PubMed DOI
Liu Y, Zhang C, Chen J, Guo L, Li X, Li W, Yu Z, Deng J, Zhang P, Zhang K, Zhang L. Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol Biochem. 2013;64:92–98. doi: 10.1016/j.plaphy.2012.12.013. PubMed DOI
Petrov V, Vermeirssen V, De Clercq I, Van Breusegem F, Minkov I, Vandepoele K, Gechev TS. Identification of cis-regulatory elements specific for different types of reactive oxygen species in Arabidopsis thaliana. Gene. 2012;499:52–60. doi: 10.1016/j.gene.2012.02.035. PubMed DOI
De Clercq I, Van de Velde J, Luo X, Liu L, Storme V, Van Bel M, Pottie R, Vaneechoutte D, Van Breusegem F, Vandepoele K. Integrative inference of transcriptional networks in Arabidopsis yields novel ROS signalling regulators. Nat Plants. 2021;7:500–513. doi: 10.1038/s41477-021-00894-1. PubMed DOI
Moffat CS, Ingle RA, Wathugala DL, Saunders NJ, Knight H, Knight MR. ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLoS ONE. 2012;7:e35995. doi: 10.1371/journal.pone.0035995. PubMed DOI PMC
Babitha KC, Ramu SV, Pruthvi V, Mahesh P, Nataraja KN, Udayakumar M. Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in Arabidopsis. Transgenic Res. 2013;22:327–341. doi: 10.1007/s11248-012-9645-8. PubMed DOI
Sewelam N, Kazan K, Thomas-Hall SR, Kidd BN, Manners JM, Schenk PM. Ethylene response factor 6 is a regulator of reactive oxygen species signaling in Arabidopsis. PLoS ONE. 2013;8:e70289. doi: 10.1371/journal.pone.0070289. PubMed DOI PMC
Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, De Bodt S, Vanden Bossche R, De Milde L, Yoshizumi T, Matsui M, Inzé D. Ethylene Response Factor6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiol. 2013;162:319–332. doi: 10.1104/pp.113.216341. PubMed DOI PMC
Shahnejat-Bushehri S, Nobmann B, Devi Allu A, Balazadeh S. JUB1 suppresses Pseudomonas syringae-induced defense responses through accumulation of DELLA proteins. Plant Signal Behav. 2016;11:e1181245. doi: 10.1080/15592324.2016.1181245. PubMed DOI PMC
Chen X, Liu J, Lin G, Wang A, Wang Z, Lu G. Overexpression of AtWRKY28 and AtWRKY75 in Arabidopsis enhances resistance to oxalic acid and Sclerotinia sclerotiorum. Plant Cell Rep. 2013;32:1589–1599. doi: 10.1007/s00299-013-1469-3. PubMed DOI
Ebrahimian-Motlagh S, Ribone PA, Thirumalaikumar VP, Allu AD, Chan RL, Mueller-Roeber B, Balazadeh S. JUNGBRUNNEN1 Confers Drought Tolerance Downstream of the HD-Zip I Transcription Factor AtHB13. Front Plant Sci. 2017;8:2118. doi: 10.3389/fpls.2017.02118. PubMed DOI PMC
Vanderauwera S, Vandenbroucke K, Inzé A, van de Cotte B, Mühlenbock P, De Rycke R, Naouar N, Van Gaever T, Van Montagu MC, Van Breusegem F. AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis. Proc Natl Acad Sci USA. 2012;109:20113–20118. doi: 10.1073/pnas.1217516109. PubMed DOI PMC