植物亚硝基谷胱甘肽还原酶在胁迫反应中的作用研究
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摘要
信号分子一氧化氮(Nitric oxide,NO)参与植物的许多生理反应过程,例如:萌发、气孔的关闭、侧根的发育以及生物与非生物的胁迫反应过程等,主要的调控形式是与半胱氨酸上的硫基发生可逆的S-亚硝基化作用。NO的半衰期很短,这限制了它在细胞中的生理功能,与胞内含硫基的分子形成的S-亚硝基硫醇(S-nitrosothiols,SNOs)的化学性质稳定,在植物的生长发育及抗逆过程中SNOs参与NO的运输、扩散、储存以及蛋白的翻译后修饰过程。谷胱甘肽(Glutathione,GSH)与NO发生S-亚硝基化作用形成S-亚硝基谷胱甘肽(S-nitrosoglutathione,GSNO),GSNO作为NO的储存与转运形式,可以把NO转到靶蛋白上,使靶蛋白发生亚硝基化。亚硝基谷胱甘肽还原酶(S-Nitrosoglutathione reductase,GSNOR)是生物体中的一类保守蛋白,通过还原亚硝基谷胱甘肽从而调节细胞内NO及亚硝基硫醇(S-nitrosothiols,SNOs)水平,保护机体免受亚硝化的胁迫,间接的调控的细胞的氧化状态。GSNO是一个天然的NO储存库,GSNOR是调节机体亚硝基化水平的关键基因。主要对GSNOR参与的植物生长发育、生物与非生物胁迫等过程进行了概述,探讨GSNOR在植物生长发育及胁迫反应中的作用机制,将有助于我们对NO生理功能的了解,旨在为将来GSNOR的研究提供理论参考和思路。
Nitric oxide(NO)as a signaling molecule is involved in diverse physiological processes such as germination,stomataclosing,lateral root development and biotic and abiotic stress response. The predominant regulating way of NO action is S-nitrosylation,thereversible covalent attachment of NO to cysteine thiols. As a free radical,NO's half-life is very short,which restricts their physiologicalfunction in cells;while the S-nitrosothiols(SNOs)from the interaction of NO with intracellular sulfhydryl-containing molecules are generallymore stable in solution,and it participates in the transport,diffusion,and storage of NO,as well as the post-translational modifications ofproteins. S-nitrosoglutathione(GSNO)from s-nitrosation with NO is the storage and transport form of NO,which can transfer its NO moietyto proteins and enable target protein to be in nitrosylation. As a type of conserved protein,S-nitrosoglutathione reductase(GSNOR)regulatesthe level of intracellular NO and nitroso mercaptan(SNOs)by reducing GSNO,thus which may protect the body from nitrosation stress andindirectly regulate the oxidative state cell. GSNO is a natural NO repository and GSNOR is the key gene that regulates the level of nitrosylation.This paper mainly summarizes the processes of plant growth and development,biological and abiotic stress involved in GSNOR. Exploring themechanism of GSNOR in plant growth and stress response will help us to understand the physiological function of NO,aiming at providing atheoretical reference and thought for future GSNOR research.
Nitric oxide(NO)as a signaling molecule is involved in diverse physiological processes such as germination,stomataclosing,lateral root development and biotic and abiotic stress response. The predominant regulating way of NO action is S-nitrosylation,thereversible covalent attachment of NO to cysteine thiols. As a free radical,NO's half-life is very short,which restricts their physiologicalfunction in cells;while the S-nitrosothiols(SNOs)from the interaction of NO with intracellular sulfhydryl-containing molecules are generallymore stable in solution,and it participates in the transport,diffusion,and storage of NO,as well as the post-translational modifications ofproteins. S-nitrosoglutathione(GSNO)from s-nitrosation with NO is the storage and transport form of NO,which can transfer its NO moietyto proteins and enable target protein to be in nitrosylation. As a type of conserved protein,S-nitrosoglutathione reductase(GSNOR)regulatesthe level of intracellular NO and nitroso mercaptan(SNOs)by reducing GSNO,thus which may protect the body from nitrosation stress andindirectly regulate the oxidative state cell. GSNO is a natural NO repository and GSNOR is the key gene that regulates the level of nitrosylation.This paper mainly summarizes the processes of plant growth and development,biological and abiotic stress involved in GSNOR. Exploring themechanism of GSNOR in plant growth and stress response will help us to understand the physiological function of NO,aiming at providing atheoretical reference and thought for future GSNOR research.
引文
[1]Benhar M, Forrester MT, Stamler JS. Nitrosative stress in the ER:A new role for S-nitrosylation in neurodegenerative diseases[J].ACS Chem Biol, 2006, 1(6):355-358.
[2]Stamler JS, Lamas S, Fang FC. Nitrosylation the prototypicredoxbased signaling mechanism[J]. Cell, 2001, 6:675-683.
[3]Jensen DE, Belka GK, Du Bois GC. S-Nitrosoglutathione is asubstrate for rat alcohol dehydrogenase class III isoenzyme[J].Biochem J, 1998, 331(2):659-568.
[4]Liu L, Hausladen A, Zeng M, et al. A metabolic enzyme forS-nitrosothiol conserved from bacteria to humans[J]. Nature,2001, 410(6827):490-494.
[5]Corpas FJ, Barroso JB, Palma JM, et al. Plant peroxisomes:a nitrooxidative cocktail[J]. Redox Biol, 2017, 11:535-542.
[6]Sakamoto A, Ueda M, Morikawa H. Arabidopsis glutathionedependent formaldehyde dehydrogenase is an S-nitrosoglutathionereductase[J]. FEBS Letters, 2002, 515(1-3):20-24.
[7]Winter D, Vinegar B, Nahal H, et al. An“Electronic FluorescentPictograph”browser for exploring and analyzing large-scalebiological data sets[J]. PLoS One, 2007, 2(8):718.
[8]Chen R, Sun S, Wang C, et al. The Arabidopsis PARAQUATRESISTANT2 gene encodes an S-nitrosoglutathione reductase that isa key regulator of cell death[J]. Cell Res, 2009, 12:1377-1387.
[9]Cheng T, Chen J, Ef AA, et al. Quantitative proteomics analysisreveals that S-nitrosoglutathione reductase(GSNOR)and nitricoxide signaling enhance poplar defense against chilling stress[J].Planta, 2015, 242(6):1361-1390.
[10]Gong B, Wen D, Wang X, et al. S-nitrosoglutathione reductasemodulated redox signaling controls sodic alkaline stress responsesin Solanum lycopersicum L.[J]. Plant Cell Physiol, 2015, 56(4):790-802.
[11]Xu S, Guerra D, Lee U, et al. S-nitrosoglutathione reductases arelow-copy number, cysteine-rich proteins in plants that controlmultiple developmental and defense responses in Arabidopsis[J].Front Plant Sci, 2013, 5(4):430.
[12]Reumann S, Babujee L, Ma C, et al. Proteome analysis ofArabidopsis leaf peroxisomes reveals novel targeting peptides,metabolic pathways and defense mechanisms[J]. Plant Cell,2007, 19(10):3170-3193.
[13]TicháT,?in?alováL, Kope?nyD, et al. Characterization ofS-nitrosoglutathione reductase from Brassica and Lactuca spp. andits modulation during plant development[J]. Nitric Oxide, 2017,68(1):68-76.
[14]Chaki M, Valderrama R, et al. Mechanical wounding induces anitrosative stress by down-regulation of GSNO reductase and anincrease in S-nitrosothiols in sunflower(Helianthus annuus)seedlings[J]. J Exp Bot, 2011, 62(6):1803-1813.
[15]Barroso JB, Valderrama R, Corpas FJ. Immunolocalization ofS-nitrosoglutathione, S-nitrosoglutathione reductase and tyrosinenitration in pea leaf organelles[J]. Acta Physiol Plant, 2013, 35(8):2635-2640.
[16]Feechan A, Kwon E, Yun BW, et al. A central role for S-nitrosothiolsin plant disease resistance[J]. Proc Natl Acad Sci USA, 2005,102(22):8054-8059.
[17]Rustérucci C, Espunya MC, et al. S-nitrosoglutathione reductaseaffords protection against pathogens in Arabidopsis, both locally andsystemically[J]. Plant Physiol, 2007, 3:1282-1292.
[18]Chaki M, Fernández-Oca?a AM, et al. Involvement of reactivenitrogen and oxygen species(RNS and ROS)in sunflowermildewinteraction[J]. Plant Cell Physiol, 2009, 50(2):265-279.
[19]TicháT, Sedlá?ováM,?in?alováL, et al. Involvement ofS-nitrosothiols modulation by S-nitrosoglutathione reductase indefence responses of lettuce and wild Lactuca spp. to biotrophicmildews[J]. Planta, 2018, 247(5):1203-1215.
[20]Barroso JB, et al. Localization of S-nitrosoglutathione andexpression of S-nitrosoglutathione reductase in pea plants undercadmium stress[J]. J Exp Bot, 2006, 8:1785-1793.
[21]Liu S, Yang R, et al. Signalling cross-talk between nitric oxide andactive oxygen in Trifolium repens L. plants responses to cadmiumstress[J]. Environ Pollut, 2018, 239:53-68.
[22]Leterrier M, Airaki M, Palma JM, et al. Arsenic triggers the nitricoxide(NO)and S-nitrosoglutathione(GSNO)metabolism inArabidopsis[J]. Environ Pollut, 2012, 166:136-143.
[23]Lee U, Wie C, Fernandez BO, et al. Modulation of nitrosative stressby S-nitrosoglutathione reductase is critical for thermotolerance andplant growth in Arabidopsis[J]. Plant Cell, 2008, 3:786-802.
[24]Chaki M, Valderrama R, Fernández-Oca?a AM, et al. Hightemperature triggers the metabolism of S-nitrosothiols in sunflowermediating a process of nitrosative stress which provokes theinhibition of ferredoxin-NADP reductase by tyrosine nitration[J].Plant Cell Environ, 2011, 34(11):1803-1818.
[25]CorpasFJ,AlcheJD,BarrosoJB.CurrentoverviewofS-nitrosoglutathione(GSNO)in higher plants[J]. Front PlantSci, 2013, 5(4):126.
[26]Airaki M, Leterrier M, Mateos RM, et al. Metabolism of reactiveoxygen species and reactive nitrogen species in pepper(Capsicum annuum L.)plants under low temperature stress[J]. Plant CellEnviron, 2011, 35(2):281-295.
[27]Díaz M, Achkor H, Titarenko E, et al. The gene encodingglutathione-dependent formaldehyde dehydrogenase/GSNOreductase is responsive to wounding, jasmonic acid and salicylicacid[J]. FEBS Lett, 2003, 543(1-3):136-139.
[28]Zhou S, Jia L, Chu H, et al. Arabidopsis CaM1 and CaM4promote nitric oxide production and salt resistance by inhibitingS-nitrosoglutathione reductase via direct binding[J]. PLoSGenet, 2016, 29;12(9):e1006255.
[29]Jain P, von Toerne C, Lindermayr C, et al. S-nitrosylation/denitrosylation as a regulatory mechanism of salt stress sensing insunflower seedlings[J]. Physiol Plant, 2018, 162(1):49-72.
[30]Wang PC, Du YY, Hou YJ, et al. Nitric oxide negatively regulatesabscisic acid signaling in guard cells by S-nitrosylation ofOST1[J]. Proc Natl Acad Sci USA, 2015, 112(2):613-618.
[31]Kovacs I, Holzmeister C, Wirtz M, et al. ROS-mediated inhibition ofS-nitrosoglutathione reductase contributes to the activation of antioxidative mechanisms[J]. Front Plant Sci, 2016, 7:1669.
[32]Hung KT, Chang CH, et al. Paraquat toxicity is reduced by nitricoxide in rice leaves[J]. J Plant Physiol, 2002, 2159-166.
[33]Corpas FJ, Barroso JB. Peroxynitrit(ONOO-)is endogenouslyproduced in Arabidopsis peroxisomes and is overproduced undercadmium stress[J]. Ann Bot, 2014, 113(1):87-96.
[34]Sun C, Liu L, Zhou W, et al. Aluminum induces distinct changes inthe metabolism of reactive oxygen and nitrogen species in the rootsof two wheat genotypes with different aluminum resistance[J]. JAgric Food Chem, 2017, 65(43):9419-9427.
[35]Yun BW, Feechan A, Yin M, et al. S-nitrosylation of NADPHoxidase regulates cell death in plant immunity[J]. Nature, 2011,478(7368):264-268.
[36]Yang H, Mu J, Chen L, et al. S-nitrosylation positively regulatesascorbate peroxidase activity during plant stress responses[J].Plant Physiol, 2015, 167(4):1604-1615.
[37]Begara-Morales JC, Sánchez-Calvo B, Chaki M, et al. Dualregulation of cytosolic ascorbate peroxidase(APX)by tyrosinenitration and S-nitrosylation[J]. J Exp Bot, 2014, 2:527-538.
[38]Begara-Morales JC. GSNOR regulates VND7-mediated xylemvessel cell differentiation[J]. Plant Cell Physiol, 2018, 59(1):5-7.
[39]Ohtani M, Kawabe H, Demura T. Evidence that thiol-based redoxstate is critical for xylem vessel cell differentiation[J]. PlantSignal Behav, 2018, 13(4):e1428512.
[2]Stamler JS, Lamas S, Fang FC. Nitrosylation the prototypicredoxbased signaling mechanism[J]. Cell, 2001, 6:675-683.
[3]Jensen DE, Belka GK, Du Bois GC. S-Nitrosoglutathione is asubstrate for rat alcohol dehydrogenase class III isoenzyme[J].Biochem J, 1998, 331(2):659-568.
[4]Liu L, Hausladen A, Zeng M, et al. A metabolic enzyme forS-nitrosothiol conserved from bacteria to humans[J]. Nature,2001, 410(6827):490-494.
[5]Corpas FJ, Barroso JB, Palma JM, et al. Plant peroxisomes:a nitrooxidative cocktail[J]. Redox Biol, 2017, 11:535-542.
[6]Sakamoto A, Ueda M, Morikawa H. Arabidopsis glutathionedependent formaldehyde dehydrogenase is an S-nitrosoglutathionereductase[J]. FEBS Letters, 2002, 515(1-3):20-24.
[7]Winter D, Vinegar B, Nahal H, et al. An“Electronic FluorescentPictograph”browser for exploring and analyzing large-scalebiological data sets[J]. PLoS One, 2007, 2(8):718.
[8]Chen R, Sun S, Wang C, et al. The Arabidopsis PARAQUATRESISTANT2 gene encodes an S-nitrosoglutathione reductase that isa key regulator of cell death[J]. Cell Res, 2009, 12:1377-1387.
[9]Cheng T, Chen J, Ef AA, et al. Quantitative proteomics analysisreveals that S-nitrosoglutathione reductase(GSNOR)and nitricoxide signaling enhance poplar defense against chilling stress[J].Planta, 2015, 242(6):1361-1390.
[10]Gong B, Wen D, Wang X, et al. S-nitrosoglutathione reductasemodulated redox signaling controls sodic alkaline stress responsesin Solanum lycopersicum L.[J]. Plant Cell Physiol, 2015, 56(4):790-802.
[11]Xu S, Guerra D, Lee U, et al. S-nitrosoglutathione reductases arelow-copy number, cysteine-rich proteins in plants that controlmultiple developmental and defense responses in Arabidopsis[J].Front Plant Sci, 2013, 5(4):430.
[12]Reumann S, Babujee L, Ma C, et al. Proteome analysis ofArabidopsis leaf peroxisomes reveals novel targeting peptides,metabolic pathways and defense mechanisms[J]. Plant Cell,2007, 19(10):3170-3193.
[13]TicháT,?in?alováL, Kope?nyD, et al. Characterization ofS-nitrosoglutathione reductase from Brassica and Lactuca spp. andits modulation during plant development[J]. Nitric Oxide, 2017,68(1):68-76.
[14]Chaki M, Valderrama R, et al. Mechanical wounding induces anitrosative stress by down-regulation of GSNO reductase and anincrease in S-nitrosothiols in sunflower(Helianthus annuus)seedlings[J]. J Exp Bot, 2011, 62(6):1803-1813.
[15]Barroso JB, Valderrama R, Corpas FJ. Immunolocalization ofS-nitrosoglutathione, S-nitrosoglutathione reductase and tyrosinenitration in pea leaf organelles[J]. Acta Physiol Plant, 2013, 35(8):2635-2640.
[16]Feechan A, Kwon E, Yun BW, et al. A central role for S-nitrosothiolsin plant disease resistance[J]. Proc Natl Acad Sci USA, 2005,102(22):8054-8059.
[17]Rustérucci C, Espunya MC, et al. S-nitrosoglutathione reductaseaffords protection against pathogens in Arabidopsis, both locally andsystemically[J]. Plant Physiol, 2007, 3:1282-1292.
[18]Chaki M, Fernández-Oca?a AM, et al. Involvement of reactivenitrogen and oxygen species(RNS and ROS)in sunflowermildewinteraction[J]. Plant Cell Physiol, 2009, 50(2):265-279.
[19]TicháT, Sedlá?ováM,?in?alováL, et al. Involvement ofS-nitrosothiols modulation by S-nitrosoglutathione reductase indefence responses of lettuce and wild Lactuca spp. to biotrophicmildews[J]. Planta, 2018, 247(5):1203-1215.
[20]Barroso JB, et al. Localization of S-nitrosoglutathione andexpression of S-nitrosoglutathione reductase in pea plants undercadmium stress[J]. J Exp Bot, 2006, 8:1785-1793.
[21]Liu S, Yang R, et al. Signalling cross-talk between nitric oxide andactive oxygen in Trifolium repens L. plants responses to cadmiumstress[J]. Environ Pollut, 2018, 239:53-68.
[22]Leterrier M, Airaki M, Palma JM, et al. Arsenic triggers the nitricoxide(NO)and S-nitrosoglutathione(GSNO)metabolism inArabidopsis[J]. Environ Pollut, 2012, 166:136-143.
[23]Lee U, Wie C, Fernandez BO, et al. Modulation of nitrosative stressby S-nitrosoglutathione reductase is critical for thermotolerance andplant growth in Arabidopsis[J]. Plant Cell, 2008, 3:786-802.
[24]Chaki M, Valderrama R, Fernández-Oca?a AM, et al. Hightemperature triggers the metabolism of S-nitrosothiols in sunflowermediating a process of nitrosative stress which provokes theinhibition of ferredoxin-NADP reductase by tyrosine nitration[J].Plant Cell Environ, 2011, 34(11):1803-1818.
[25]CorpasFJ,AlcheJD,BarrosoJB.CurrentoverviewofS-nitrosoglutathione(GSNO)in higher plants[J]. Front PlantSci, 2013, 5(4):126.
[26]Airaki M, Leterrier M, Mateos RM, et al. Metabolism of reactiveoxygen species and reactive nitrogen species in pepper(Capsicum annuum L.)plants under low temperature stress[J]. Plant CellEnviron, 2011, 35(2):281-295.
[27]Díaz M, Achkor H, Titarenko E, et al. The gene encodingglutathione-dependent formaldehyde dehydrogenase/GSNOreductase is responsive to wounding, jasmonic acid and salicylicacid[J]. FEBS Lett, 2003, 543(1-3):136-139.
[28]Zhou S, Jia L, Chu H, et al. Arabidopsis CaM1 and CaM4promote nitric oxide production and salt resistance by inhibitingS-nitrosoglutathione reductase via direct binding[J]. PLoSGenet, 2016, 29;12(9):e1006255.
[29]Jain P, von Toerne C, Lindermayr C, et al. S-nitrosylation/denitrosylation as a regulatory mechanism of salt stress sensing insunflower seedlings[J]. Physiol Plant, 2018, 162(1):49-72.
[30]Wang PC, Du YY, Hou YJ, et al. Nitric oxide negatively regulatesabscisic acid signaling in guard cells by S-nitrosylation ofOST1[J]. Proc Natl Acad Sci USA, 2015, 112(2):613-618.
[31]Kovacs I, Holzmeister C, Wirtz M, et al. ROS-mediated inhibition ofS-nitrosoglutathione reductase contributes to the activation of antioxidative mechanisms[J]. Front Plant Sci, 2016, 7:1669.
[32]Hung KT, Chang CH, et al. Paraquat toxicity is reduced by nitricoxide in rice leaves[J]. J Plant Physiol, 2002, 2159-166.
[33]Corpas FJ, Barroso JB. Peroxynitrit(ONOO-)is endogenouslyproduced in Arabidopsis peroxisomes and is overproduced undercadmium stress[J]. Ann Bot, 2014, 113(1):87-96.
[34]Sun C, Liu L, Zhou W, et al. Aluminum induces distinct changes inthe metabolism of reactive oxygen and nitrogen species in the rootsof two wheat genotypes with different aluminum resistance[J]. JAgric Food Chem, 2017, 65(43):9419-9427.
[35]Yun BW, Feechan A, Yin M, et al. S-nitrosylation of NADPHoxidase regulates cell death in plant immunity[J]. Nature, 2011,478(7368):264-268.
[36]Yang H, Mu J, Chen L, et al. S-nitrosylation positively regulatesascorbate peroxidase activity during plant stress responses[J].Plant Physiol, 2015, 167(4):1604-1615.
[37]Begara-Morales JC, Sánchez-Calvo B, Chaki M, et al. Dualregulation of cytosolic ascorbate peroxidase(APX)by tyrosinenitration and S-nitrosylation[J]. J Exp Bot, 2014, 2:527-538.
[38]Begara-Morales JC. GSNOR regulates VND7-mediated xylemvessel cell differentiation[J]. Plant Cell Physiol, 2018, 59(1):5-7.
[39]Ohtani M, Kawabe H, Demura T. Evidence that thiol-based redoxstate is critical for xylem vessel cell differentiation[J]. PlantSignal Behav, 2018, 13(4):e1428512.