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Functions of heat shock transcription factors involved in response to photooxidative stresses in Arabidopsis

Pages 1254-1263 | Received 30 Oct 2015, Accepted 03 Apr 2016, Published online: 20 Apr 2016

References

  • Kreps JA, Wu Y, Chang HS, et al. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 2002;130:2129–2141.10.1104/pp.008532
  • Rossel JB, Wilson IW, Pogson BJ. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 2002;130:1109–1120.10.1104/pp.005595
  • Seki M, Narusaka M, Ishida J, et al. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA micro array. Plant J. 2002;31:279–292.10.1046/j.1365-313X.2002.01359.x
  • Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006;57:781–803.10.1146/annurev.arplant.57.032905.105444
  • Nakashima K, Takasaki H, Mizoi J, et al. NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta. 2012;1819:97–103.10.1016/j.bbagrm.2011.10.005
  • Hua J. From freezing to scorching, transcriptional responses to temperature variations in plants. Curr. Opin. Plant Biol. 2009;12:568–573.10.1016/j.pbi.2009.07.012
  • Riechmann JL, Heard J, Martin G, et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000;290:2105–2110.10.1126/science.290.5499.2105
  • Jin J, Zhang H, Kong L, et al. PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 2014;42:D1182–D1187.10.1093/nar/gkt1016
  • Foyer CH, Lelandais M, Kunert kJ. Photooxidative stress in plants. Physiol. Plant. 1994;92:696–717.10.1111/ppl.1994.92.issue-4
  • Alscher RG, Donahue JL, Cramer CL. Reactive oxygen species and antioxidants: relationships in green cells. Physiol. Plant. 1997;100:224–233.10.1111/ppl.1997.100.issue-2
  • Shigeoka S, Ishikawa T, Tamoi M, et al. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 2002;53:1305–1319.10.1093/jexbot/53.372.1305
  • Nishizawa A, Yabuta Y, Yoshida E, et al. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 2006;48:535–547.10.1111/tpj.2006.48.issue-4
  • Morishita T, Kojima Y, Maruta T, et al. Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol. 2009;50:2210–2222.10.1093/pcp/pcp159
  • Yabuta Y, Morishita T, Kojima Y, et al. Identification of recognition sequence of ANAC078 protein by the cyclic amplification and selection of targets technique. Plant Signal. Behav. 2010;5:695–697.10.4161/psb.5.6.11577
  • Yabuta Y, Osada R, Morishita T, et al. Involvement of Arabidopsis NAC transcription factor in the regulation of 20S and 26S proteasomes. Plant Sci. 2011;181:421–427.10.1016/j.plantsci.2011.07.001
  • Mishra SK, Tripp J, Winkelhaus S, et al. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 2002;16:1555–1567.10.1101/gad.228802
  • Kotak S, Port M, Ganguli A, et al. Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J. 2004;39:98–112.10.1111/tpj.2004.39.issue-1
  • Nover L, Bharti K, Döring P, et al. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones. 2001;6:177–189.10.1379/1466-1268(2001)006<0177:AATHST>2.0.CO;2
  • Scharf KD, Berberich T, Ebersberger I, et al. The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta. 2012;1819:104–119.10.1016/j.bbagrm.2011.10.002
  • Wiederrecht G, Seto D, Parker CS. Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell. 1988;54:841–853.10.1016/S0092-8674(88)91197-X
  • Sorger PK, Pelham HR. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988;54:855–864.10.1016/S0092-8674(88)91219-6
  • Jedlicka P, Mortin MA, Wu C. Multiple functions of Drosophila heat shock transcription factor in vivo. EMBO J. 1997;16:2452–2462.10.1093/emboj/16.9.2452
  • Bu L, Jin Y, Shi Y, et al. Mutant DNA-binding domain of HSF4 is associated with autosomal dominant lamellar and Marner cataract. Nat. Genet. 2002;31:276–278.10.1038/ng921
  • Xiao X, Zuo X, Davis AA, et al. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 1999;18:5943–5952.10.1093/emboj/18.21.5943
  • Nakai A. New aspects in the vertebrate heat shock factor system: Hsf3 and Hsf4. Cell Stress Chaperones. 1999;4:86–93.10.1379/1466-1268(1999)004<0086:NAITVH>2.3.CO;2
  • Nover L, Scharf KD, Gagliardi D, et al. The Hsf world: classification and properties of plant heat stress transcription factors. Cell Stress Chaperones. 1996;1:215–223.10.1379/1466-1268(1996)001<0215:THWCAP>2.3.CO;2
  • Fujimoto M, Nakai A. The heat shock factor family and adaptation to proteotoxic stress. FEBS J. 2010;277:4112–4125.10.1111/j.1742-4658.2010.07827.x
  • Ikeda M, Ohme-Takagi M. A novel group of transcriptional repressors in Arabidopsis. Plant Cell Physiol. 2009;50:970–975.10.1093/pcp/pcp048
  • Ikeda M, Mitsuda N, Ohme-Takagi M. Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol. 2011;157:1243–1254.10.1104/pp.111.179036
  • Wunderlich M, Werr W, Schöffl F. Generation of dominant-negative effects on the heat shock response in Arabidopsis thaliana by transgenic expression of a chimaeric HSF1 protein fusion construct. Plant J. 2003;35:442–451.10.1046/j.1365-313X.2003.01815.x
  • Lohmann C, Eggers-Schumacher G, Wunderlich M, et al. Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol. Genet. Genomics. 2004;271:11–21.10.1007/s00438-003-0954-8
  • Panchuk II, Volkov RA, Schöffl F. Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 2002;129:838–853.10.1104/pp.001362
  • Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, et al. Galactinol synthase1. a novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol. 2004;136:3148–3158.10.1104/pp.104.042606
  • Busch W, Wunderlich M, Schöffl F. Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 2005;41:1–14.
  • Liu HC, Liao HT, Charng YY. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ. 2011;34:738–751.10.1111/pce.2011.34.issue-5
  • Sakuma Y, Maruyama K, Qin F, et al. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. USA. 2006;103:18822–18827.10.1073/pnas.0605639103
  • Schramm F, Larkindale J, Kiehlmann E, et al. A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 2008;53:264–274.
  • Yoshida T, Sakuma Y, Todaka D, et al. Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem. Biophys. Res. Commun. 2008;368:515–521.10.1016/j.bbrc.2008.01.134
  • Yoshida T, Ohama N, Nakajima J, et al. Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol. Genet. Genomics. 2011;286:321–332.10.1007/s00438-011-0647-7
  • Schramm F, Ganguli A, Kiehlmann E, et al. The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 2006;60:759–772.10.1007/s11103-005-5750-x
  • Miller G, Mittler R. Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 2006;98:279–288.10.1093/aob/mcl107
  • Charng YY, Liu HC, Liu NY, et al. A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 2007;143:251–262.
  • Ogawa D, Yamaguchi K, Nishiuchi T. High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J. Exp. Bot. 2007;58:3373–3383.10.1093/jxb/erm184
  • Nishizawa-Yokoi A, Nosaka R, Hayashi H, et al. HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol. 2011;52:933–945.10.1093/pcp/pcr045
  • Yokotani N, Ichikawa T, Kondou Y, et al. Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta. 2008;227:957–967.10.1007/s00425-007-0670-4
  • Chauhan H, Khurana N, Agarwal P, et al. Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress. Mol. Genet. Genomics. 2011;286:171–187.10.1007/s00438-011-0638-8
  • Lin YX, Jiang HY, Chu ZX, et al. Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics. 2011;12:76.10.1186/1471-2164-12-76
  • Chauhan H, Khurana N, Agarwal P, et al. A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment. PLoS ONE. 2013;8:e79577.10.1371/journal.pone.0079577
  • Guo M, Lu JP, Zhai YF, et al. Genome-wide analysis, expression profile of heat shock factor gene family (CaHsfs) and characterisation of CaHsfA2 in pepper (Capsicum annuum L.). BMC Plant Biol. 2015;15:151.10.1186/s12870-015-0512-7
  • Gong B, Yi J, Wu J, et al. LlHSFA1, a novel heat stress transcription factor in lily (Lilium longiflorum), can interact with LlHSFA2 and enhance the thermotolerance of transgenic Arabidopsis thaliana. Plant Cell Rep. 2014;33:1519–1533.10.1007/s00299-014-1635-2
  • Amano M, Iida S, Kosuge K. Comparative studies of thermotolerance: different modes of heat acclimation between tolerant and intolerant aquatic plants of the genus Potamogeton. Ann. Bot. 2012;109:443–452.10.1093/aob/mcr300
  • Banti V, Mafessoni F, Loreti E, et al. The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol. 2010;152:1471–1483.10.1104/pp.109.149815
  • Nishizawa A, Yabuta Y, Shigeoka S. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008;147:1251–1263.10.1104/pp.108.122465
  • Nishizawa-YOKOI A, Yoshida E, Yabuta Y, et al. Analysis of the regulation of target genes by an Arabidopsis heat shock transcription factor, HsfA2. Biosci. Biotechnol. Biochem. 2009;73:890–895.10.1271/bbb.80809
  • Scharf KD, Heider H, Höhfeld I, et al. The tomato Hsf System: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol. Cell Biol. 1998;18:2240–2251.10.1128/MCB.18.4.2240
  • Heerklotz D, Döring P, Bonzelius F, et al. The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. Mol. Cell Biol. 2001;21:1759–1768.10.1128/MCB.21.5.1759-1768.2001
  • Chan-Schaminet KY, Baniwal SK, Bublak D, et al. Specific interaction between tomato HsfA1 and HsfA2 creates hetero-oligomeric superactivator complexes for synergistic activation of heat stress gene expression. J Biol. Chem. 2009;284:20848–20857.10.1074/jbc.M109.007336
  • Liu HC, Charng YY. Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol. 2013;163:276–290.10.1104/pp.113.221168
  • Bharti K, Schmidt E, Lyck R, et al. Isolation and characterization of HsfA3, a new heat stress transcription factor of Lycopersicon peruvianum. Plant J. 2000;22:355–365.10.1046/j.1365-313x.2000.00746.x
  • Chen H, Hwang JE, Lim CJ, et al. Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem. Biophys. Res. Commun. 2010;401:238–244.10.1016/j.bbrc.2010.09.038
  • Yamanouchi U, Yano M, Lin H, et al. A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc. Natl. Acad. Sci. USA. 2002;99:7530–7535.10.1073/pnas.112209199
  • Shim D, Hwang JU, Lee J, et al. Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell. 2009;21:4031–4043.10.1105/tpc.109.066902
  • Pnueli L, Liang H, Rozenberg M, et al. Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J. 2003;34:187–203.10.1046/j.1365-313X.2003.01715.x
  • Davletova S, Rizhsky L, Liang H, et al. Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell. 2005;17:268–281.10.1105/tpc.104.026971
  • Rizhsky L, Davletova S, Liang H, et al. The zinc finger protein Zat12 Is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 2004;279:11736–11743.10.1074/jbc.M313350200
  • Fortunati A, Piconese S, Tassone P, et al. A new mutant of Arabidopsis disturbed in its roots, right-handed slanting, and gravitropism defines a gene that encodes a heat-shock factor. J. Exp. Bot. 2008;59:1363–1374.10.1093/jxb/ern047
  • Baniwal SK, Chan KY, Scharf KD, et al. Role of heat stress factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 2007;282:3605–3613.
  • Hwang SM, Kim DW, Woo MS, et al. Functional characterization of Arabidopsis HsfA6a as a heat-shock transcription factor under high salinity and dehydration conditions. Plant Cell Environ. 2014;37:1202–1222.10.1111/pce.12228
  • Kotak S, Vierling E, Bäumlein H, et al. A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell. 2007;19:182–195.10.1105/tpc.106.048165
  • Almoguera C, Rojas A, Díaz-Martín J, et al. A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. J. Biol. Chem. 2002;277:43866–43872.10.1074/jbc.M207330200
  • Prieto-Dapena P, Castaño R, Almoguera C, et al. Improved resistance to controlled deterioration in transgenic seeds. Plant Physiol. 2006;142:1102–1112.10.1104/pp.106.087817
  • Li Z, Tian Y, Zhao W, et al. Functional characterization of a grape heat stress transcription factor VvHsfA9 in transgenic Arabidopsis. Acta Physiol. Plant. 2015;37:133.10.1007/s11738-015-1884-x
  • Tejedor-Cano J, Prieto-Dapena P, Almoguera C, et al. Loss of function of the HSFA9 seed longevity program. Plant Cell Environ. 2010;33:1408–1417.
  • Carranco R, Espinosa JM, Prieto-Dapena P, et al. Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proc. Natl. Acad. Sci. USA. 2010;107:21908–21913.10.1073/pnas.1014856107
  • Tejedor-Cano J, Carranco R, Personat JM, et al. A passive repression mechanism that hinders synergic transcriptional activation by heat shock factors involved in sunflower seed longevity. Mol. Plant. 2014;7:256–259.10.1093/mp/sst117
  • Personat JM, Tejedor-Cano J, Prieto-Dapena P, et al. Co-overexpression of two heat shock factors results in enhanced seed longevity and in synergistic effects on seedling tolerance to severe dehydration and oxidative stress. BMC Plant Biol. 2014;14:56.10.1186/1471-2229-14-56
  • Almoguera C, Prieto-Dapena P, Díaz-Martín J, et al. The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biol. 2009;9:75.10.1186/1471-2229-9-75
  • Giesguth M, Sahm A, Simon S, et al. Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett. 2015;589:718–725.10.1016/j.febslet.2015.01.039
  • von Koskull-Döring P, Scharf KD, Nover L. The diversity of plant heat stress transcription factors. Trends Plant Sci. 2007;12:452–457.10.1016/j.tplants.2007.08.014
  • Czarnecka-Verner E, Yuan CX, Scharf KD, et al. Plants contain a novel multi-member class of heat shock factors without transcriptional activator potential. Plant Mol. Biol. 2000;43:459–471.10.1023/A:1006448607740
  • Kumar M, Busch W, Birke H, et al. Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol. Plant. 2009;2:152–165.10.1093/mp/ssn095
  • Bharti K, Von Koskull-Döring P, Bharti S, et al. Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB binding protein ortholog HAC1. Plant Cell. 2004;16:1521–1535.10.1105/tpc.019927
  • Begum T, Reuter R, Schöffl F. Overexpression of AtHsfB4 induces specific effects on root development of Arabidopsis. Mech. Dev. 2013;130:54–60.10.1016/j.mod.2012.05.008
  • Kolmos E, Chow BY, Pruneda-Paz JL, et al. HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock. Proc. Natl. Acad. Sci. USA. 2014;111:16172–16177.10.1073/pnas.1418483111
  • Schmidt R, Schippers JH, Welker A, et al. Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. japonica. AoB Plants. 2012;2012:pls0110.
  • Malik MK, Slovin JP, Hwang CH, et al. Modified expression of a carrot small heat shock protein gene, hsp17. 7, results in increased or decreased thermotolerancedouble dagger. Plant J. 1999;20:89–99.10.1046/j.1365-313X.1999.00581.x
  • Sun W, Bernard C, van de Cotte B, et al. At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J. 2001;27:407–415.10.1046/j.1365-313X.2001.01107.x
  • Mu C, Zhang S, Yu G, et al. Overexpression of small heat shock protein LimHSP16.45 in Arabidopsis enhances tolerance to abiotic stresses. PLoS ONE. 2013;8:e82264.10.1371/journal.pone.0082264
  • Ham DJ, Moon JC, Hwang SG, et al. Molecular characterization of two small heat shock protein genes in rice: their expression patterns, localizations, networks, and heterogeneous overexpressions. Mol. Biol. Rep. 2013;40:6709–6720.10.1007/s11033-013-2786-x
  • Yamada K, Fukao Y, Hayashi M, et al. Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J. Biol. Chem. 2007;282:37794–37804.10.1074/jbc.M707168200
  • Nishizawa-Yokoi A, Tainaka H, Yoshida E, et al. The 26S proteasome function and Hsp90 activity involved in the regulation of HsfA2 expression in response to oxidative stress. Plant Cell Physiol. 2010;51:486–496.10.1093/pcp/pcq015
  • Yabuta Y, Maruta T, Yoshimura K, et al. Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol. 2004;45:1586–1594.10.1093/pcp/pch181
  • Shigeoka S, Maruta T. Cellular redox regulation, signaling, and stress response in plants. Biosci. Biotechnol. Biochem. 2014;78:1457–1470.10.1080/09168451.2014.942254
  • Volkov RA, Panchuk II, Mullineaux PM, et al. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol. Biol. 2006;61:733–746.10.1007/s11103-006-0045-4
  • Fu S, Rogowsky P, Nover L, et al. The maize heat shock factor-binding protein paralogs EMP2 and HSBP2 interact non-redundantly with specific heat shock factors. Planta. 2006;224:42–52.10.1007/s00425-005-0191-y
  • Hsu SF, Lai HC, Jinn TL. 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. 2010;153:773–784.10.1104/pp.109.151225
  • Liu HT, Gao F, Li GL, et al. The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J. 2008;55:760–773.10.1111/tpj.2008.55.issue-5
  • Cohen-Peer R, Schuster S, Meiri D, et al. Sumoylation of Arabidopsis heat shock factor A2 (HsfA2) modifies its activity during acquired thermotholerance. Plant Mol. Biol. 2010;74:33–45.10.1007/s11103-010-9652-1
  • Jung HS, Crisp PA, Estavillo GM, et al. Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light. Proc. Natl. Acad. Sci. USA. 2013;110:14474–14479.10.1073/pnas.1311632110
  • Liu Y, Zhang C, Chen J, et al. Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiol. Biochem. 2013;64:92–98.10.1016/j.plaphy.2012.12.013

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