Basic-leucine zipper 17 and Hmg-CoA reductase degradation 3A are involved in salt acclimation memory in Arabidopsis
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摘要
Salt acclimation, which is induced by previous salt exposure, increases the resistance of plants to future exposure to salt stress. However, little is known about the underlying mechanism, particularly how plants store the"memory" of salt exposure. In this study, we established a system to study salt acclimation in Arabidopsis thaliana.Following treatment with a low concentration of salt,seedlings were allowed to recover to allow transitory salt responses to subside while maintaining the sustainable effects of salt acclimation. We performed transcriptome profiling analysis of these seedlings to identify genes related to salt acclimation memory. Notably, the expression of Basic-leucine zipper 17(b ZIP17) and Hmg-Co A reductase degradation 3 A(HRD3 A), which are important in the unfolded protein response(UPR) and endoplasmic High-Imreticulum-associated degradation(ERAD), respectively,increased following treatment with a low concentration of salt and remained at stably high levels after the stimulus was removed, a treatment which improved plant tolerance to future high-salinity challenge. Our findings suggest that the upregulated expression of important genes involved in the UPR and ERAD represents a "memory" of the history of salt exposure and enables more potent responses to future exposure to salt stress, providing new insights into the mechanisms underlying salt acclimation in plants.
Salt acclimation, which is induced by previous salt exposure, increases the resistance of plants to future exposure to salt stress. However, little is known about the underlying mechanism, particularly how plants store the"memory" of salt exposure. In this study, we established a system to study salt acclimation in Arabidopsis thaliana.Following treatment with a low concentration of salt,seedlings were allowed to recover to allow transitory salt responses to subside while maintaining the sustainable effects of salt acclimation. We performed transcriptome profiling analysis of these seedlings to identify genes related to salt acclimation memory. Notably, the expression of Basic-leucine zipper 17(b ZIP17) and Hmg-Co A reductase degradation 3 A(HRD3 A), which are important in the unfolded protein response(UPR) and endoplasmic High-Imreticulum-associated degradation(ERAD), respectively,increased following treatment with a low concentration of salt and remained at stably high levels after the stimulus was removed, a treatment which improved plant tolerance to future high-salinity challenge. Our findings suggest that the upregulated expression of important genes involved in the UPR and ERAD represents a "memory" of the history of salt exposure and enables more potent responses to future exposure to salt stress, providing new insights into the mechanisms underlying salt acclimation in plants.
Salt acclimation, which is induced by previous salt exposure, increases the resistance of plants to future exposure to salt stress. However, little is known about the underlying mechanism, particularly how plants store the"memory" of salt exposure. In this study, we established a system to study salt acclimation in Arabidopsis thaliana.Following treatment with a low concentration of salt,seedlings were allowed to recover to allow transitory salt responses to subside while maintaining the sustainable effects of salt acclimation. We performed transcriptome profiling analysis of these seedlings to identify genes related to salt acclimation memory. Notably, the expression of Basic-leucine zipper 17(b ZIP17) and Hmg-Co A reductase degradation 3 A(HRD3 A), which are important in the unfolded protein response(UPR) and endoplasmic High-Imreticulum-associated degradation(ERAD), respectively,increased following treatment with a low concentration of salt and remained at stably high levels after the stimulus was removed, a treatment which improved plant tolerance to future high-salinity challenge. Our findings suggest that the upregulated expression of important genes involved in the UPR and ERAD represents a "memory" of the history of salt exposure and enables more potent responses to future exposure to salt stress, providing new insights into the mechanisms underlying salt acclimation in plants.
引文
Avramova Z(2015)Transcriptional‘memory’of a stress:Transient chromatin and memory(epigenetic)marks at stress-response genes.Plant J 83:149-159
Bardwell JC,Mc Govern K,Beckwith J(1991)Identification of a protein required for disulfide bond formation in vivo.Cell67:581-589
Baxter A,Mittler R,Suzuki N(2014)ROS as key players in plant stress signalling.J Exp Bot 65:1229-1240
Bruce TJA,Matthes MC,Napier JA,Pickett JA(2007)Stressful“memories”of plants:Evidence and possible mechanisms.Plant Sci 173:603-608
Cayuela E,Estan MT,Parra M,Caro M,Bolarin MC(2001)Na Cl pre-treatment at the seedling stage enhances fruit yield of tomato plants irrigated with salt water.Plant Soil 230:231-238
Charng YY,Liu HC,Liu NY,Hsu FC,Ko SS(2006)Arabidopsis Hsa32,a novel heat shock protein,is essential for acquired thermotolerance during long recovery after acclimation.Plant Physiol 140:1297-1305
Che P,Bussell JD,Zhou W,Estavillo GM,Pogson BJ,Smith SM(2010)Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis.Sci Signal 3:ra69
Christianson JC,Ye Y(2014)Cleaning up in the endoplasmic reticulum:ubiquitin in charge.Nat Struct Mol Biol 21:325-335
Conrath U(2011)Molecular aspects of defence priming.Trends Plant Sci 16:524-531
Crisp PA,Ganguly D,Eichten SR,Borevitz JO,Pogson BJ(2016)Reconsidering plant memory:Intersections between stress recovery,RNA turnover,and epigenetics.Sci Adv2:e1501340
Dang ZH,Zheng LL,Jia W,Zhe G,Wu SB,Zhi Q,Wang YC(2013)Transcriptomic profiling of the salt-stress response in the wild recretohalophyte Reaumuria trigyna.BMC Genomics14:29-46
Deinlein U,Stephan AB,Horie T,Luo W,Xu G,Schroeder JI(2014)Plant salt-tolerance mechanisms.Trends Plant Sci19:371-379
Eichten SR,Schmitz RJ,Springer NM(2014)Epigenetics:Beyond chromatin modifications and complex genetic regulation.Plant Physiol 165:933-947
Fedoroff N(2006)Redox regulatory mechanisms in cellular stress responses.Ann Bot 98:289-300
Feng XJ,Li JR,Qi SL,Lin QF,Jin JB,Hua XJ(2016)Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis.Proc Natl Acad Sci USA 113:E8335-E8343
Foreman J,Demidchik V,Bothwell JH,Mylona P,Miedema H,Torres MA,Linstead P,Costa S,Brownlee C,Jones JD,Davies JM,Dolan L(2003)Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature 422:442-446
Fujita M,Mizukado S,Fujita Y,Ichikawa T,Nakazawa M,Seki M,Matsui M,Yamaguchi-Shinozaki K,Shinozaki K(2007)Identification of stress-tolerance-related transcriptionfactor genes via mini-scale Full-length c DNA Over-e Xpressor(FOX)gene hunting system.Biochem Biophys Res Commun 364:250-257
Galvan-Ampudia CS,Testerink C(2011)Salt stress signals shape the plant root.Curr Opin Plant Biol 14:296-302
Gao H,Brandizzi F,Benning C,Larkin RM(2008)A membranetethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana.Proc Natl Acad Sci USA 105:16398-16403
Garcia de la Garma J,Fernandez-Garcia N,Bardisi E,Pallol B,Asensio-Rubio JS,Bru R,Olmos E(2015)New insights into plant salt acclimation:The roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system.New Phytol 205:216-239
Gauss R,Sommer T,Jarosch E(2006)The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment.EMBO J 25:1827-1835
Geng Y,Wu R,Wee CW,Xie F,Wei X,Chan PM,Tham C,Duan L,Dinneny JR(2013)A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis.Plant Cell 25:2132-2154
Guerra DD,Callis J(2012)Ubiquitin on the move:The ubiquitin modification system plays diverse roles in the regulation of endoplasmic reticulum-and plasma membrane-localized proteins.Plant Physiol 160:56-64
Hegde RS,Ploegh HL(2010)Quality and quantity control at the endoplasmic reticulum.Cur Opin Cell Biol 22:437-446
Helenius A,Aebi M(2004)Roles of N-linked glycans in the endoplasmic reticulum.Annu Rev Biochem 73:1019-1049
Henriquez-Valencia C,Moreno AA,Sandoval-Ibanez O,Mitina I,Blanco-Herrera F,Cifuentes-Esquivel N,Orellana A(2015)b ZIP17 and b ZIP60 regulate the expression of Bi P3 and other salt stress responsive genes in an UPR-independent manner in Arabidopsis thaliana.J Cell Biochem 116:1638-1645
Holst B,Tachibana C,Winther JR(1997)Active site mutations in yeast protein disulfide isomerase cause dithiothreitol sensitivity and a reduced rate of protein folding in the endoplasmic reticulum.J Cell Biol 138:1229-1238
Howell SH(2013)Endoplasmic reticulum stress responses in plants.Annu Rev Plant Biol 64:477-499
Huang D,Wu W,Abrams SR,Cutler AJ(2008)The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors.J Exp Bot 59:2991-3007
Irsigler AS,Costa MD,Zhang P,Reis PA,Dewey RE,Boston RS,Fontes EP(2007)Expression profiling on soybean leaves reveals integration of ER-and osmotic-stress pathways.BMC Genomics 8:431
Janda T,Darko E,Shehata S,Kovacs V,Pal M,Szalai G(2016)Salt acclimation processes in wheat.Plant Physiol Biochem 101:68-75
Jiang C,Belfield EJ,Cao Y,Smith JA,Harberd NP(2013)An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis.Plant Cell 25:3535-3552
Jossier M,Kroniewicz L,Dalmas F,Le Thiec D,Ephritikhine G,Thomine S,Barbier-Brygoo H,Vavasseur A,Filleur S,Leonhardt N(2010)The Arabidopsis vacuolar anion transporter,At CLCc,is involved in the regulation of stomatal movements and contributes to salt tolerance.Plant J 64:563-576
Kamauchi S,Nakatani H,Nakano C,Urade R(2005)Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana.FEBS J 272:3461-3476
Kinoshita T,Seki M(2014)Epigenetic memory for stress response and adaptation in plants.Plant Cell Physiol 55:1859-1863
Kronzucker HJ,Britto DT(2011)Sodium transport in plants:Acritical review.New Phytol 189:54-81
Li B,Byrt CS,Qiu J,Baumann U,Hrmova M,Evrard A,Johnson AA,Birnbaum KD,Mayo GM,Jha D,Henderson SW,Tester M,Gilliham M,Roy SJ(2015)Identification of a stelar-localised transport protein that facilitates root-toshoot transfer of chloride in Arabidopsis.Plant Physiol 170:1024-1029
Liu DY,Smith PM,Barton DA,Day DA,Overall RL(2015)Characterisation of Arabidopsis calnexin 1 and calnexin 2 in the endoplasmic reticulum and at plasmodesmata.Protoplasma 254:1-12
Liu JX,Howell SH(2010)Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants.Plant Cell 22:2930-2942
Liu JX,Srivastava R,Che P,Howell SH(2007a)An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor,b ZIP28.Plant Cell 19:4111-4119
Liu JX,Srivastava R,Che P,Howell SH(2007b)Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling.Plant J 51:897-909
Liu L,Cui F,Li Q,Yin B,Zhang H,Lin B,Wu Y,Xia R,Tang S,Xie Q(2011)The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance.Cell Res 21:957-969
Liu X,Zhu Y,Zhai H,Cai H,Ji W,Luo X,Li J,Bai X(2012)At PP2CG1,a protein phosphatase 2C,positively regulates salt tolerance of Arabidopsis in abscisic acid-dependent manner.Biochem Biophys Res Commun 422:710-715
Mirouze M,Paszkowski J(2011)Epigenetic contribution to stress adaptation in plants.Curr Opin Plant Biol 14:267-274
Munns R,Tester M(2008)Mechanisms of salinity tolerance.Annu Rev Plant Biol 59:651-681
Oh DH,Leidi E,Zhang Q,Hwang SM,Li Y,Quintero FJ,Jiang X,D’Urzo MP,Lee SY,Zhao Y,Bahk JD,Bressan RA,Yun DJ,Pardo JM,Bohnert HJ(2009)Loss of halophytism by interference with SOS1 expression.Plant Physiol 151:210-222
Ozgur R,Uzilday B,Sekmen AH,Turkan I(2015)The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in Arabidopsis.Ann Bot 116:541-553
Pandolfi C,Azzarello E,Mancuso S,Shabala S(2016)Acclimation improves salt stress tolerance in Zea mays plants.J Plant Physiol 201:1-8
Pandolfi C,Mancuso S,Shabala S(2012)Physiology of acclimation to salinity stress in pea(Pisum sativum).Environ Exp Bot 84:44-51
Prime APG,Conrath U,Beckers GJ,Flors V,Garcia-Agustin 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(2006)Priming:Getting ready for battle.Mol Plant Microbe Interact 19:1062-1071
Pruthvi V,Narasimhan R,Nataraja KN(2014)Simultaneous expression of abiotic stress responsive transcription factors,At DREB2A,At HB7 and At ABF3 improves salinity and drought tolerance in peanut(Arachis hypogaea L.).PLo S ONE 9:e111152
Rengasamy P(2010)Soil processes affecting crop production in salt-affected soils.Funct Plant Biol 37:613-620
Rodriguez HG,Roberts J,Jordan WR,Drew MC(1997)Growth,water relations,and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress.Plant Physiol 113:881-893
Roy SJ,Huang W,Wang XJ,Evrard A,Schmockel SM,Zafar ZU,Tester M(2013)A novel protein kinase involved in Natexclusion revealed from positional cloning.Plant Cell Environ 36:553-568
Sani E,Herzyk P,Perrella G,Colot V,Amtmann A(2013)Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome.Genome Biol 14:R59
Santos AP,Serra T,Figueiredo DD,Barros P,Lourenco T,Chander S,Oliveira MM,Saibo NJ(2011)Transcription regulation of abiotic stress responses in rice:A combined action of transcription factors and epigenetic mechanisms.Omics 15:839-857
Shen X,Wang Z,Song X,Xu J,Jiang C,Zhao Y,Ma C,Zhang H(2014)Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis.Plant Mol Biol 86:303-317
Su W,Liu Y,Xia Y,Hong Z,Li J(2011)Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis.Proc Natl Acad Sci USA 108:870-875
Sunarpi,Horie T,Motoda J,Kubo M,Yang H,Yoda K,Horie R,Chan WY,Leung HY,Hattori K,Konomi M,Osumi M,Yamagami M,Schroeder JI,Uozumi N(2005)Enhanced salt tolerance mediated by At HKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells.Plant J 44:928-938
Szekely G,Abraham E,Cseplo A,Rigo G,Zsigmond L,Csiszar J,Ayaydin F,Strizhov N,Jasik J,Schmelzer E,Koncz C,Szabados L(2008)Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis.Plant J53:11-28
Takahashi S,Katagiri T,Yamaguchi-Shinozaki K,Shinozaki K(2000)An Arabidopsis gene encoding a Ca2t-binding protein is induced by abscisic acid during dehydration.Plant Cell Physiol 41:898-903
Torres MA,Dangl JL,Jones JD(2002)Arabidopsis gp91phox homologues Atrboh D and Atrboh F are required for accumulation of reactive oxygen intermediates in the plant defense response.Proc Natl Acad Sci USA 99:517-522
Umezawa T,Shimizu K,Morio Kato K,Takao Ueda T(2000)Enhancement of salt tolerance in soybean with Na Cl pretreatment.Physiol Plant 110:59-63
Webster TMU,Santos EM(2015)Global transcriptomic profiling demonstrates induction of oxidative stress and of compensatory cellular stress responses in brown trout exposed to glyphosate and Roundup.BMC Genomics 16:32-46
Wu TY,Juan YT,Hsu YH,Wu SH,Liao HT,Fung RW,Charng YY(2013)Interplay between heat shock proteins HSP101 and HSA32 prolongs heat acclimation memory posttranscriptionally in Arabidopsis.Plant Physiol 161:2075-2084
Xie YJ,Xu S,Han B,Wu MZ,Yuan XX,Han Y,Gu Q,Xu DK,Yang Q,Shen WB(2011)Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of Rboh D-derived reactive oxygen species synthesis.Plant J66:280-292
Young MD,Wakefield MJ,Smyth GK,Oshlack A(2010)Gene ontology analysis for RNA-seq:accounting for selection bias.Genome Biol 11:R14
Zhang K,Gan SS(2012)An abscisic acid-At NAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves.Plant Physiol 158:961-969
Zhu JK(2002)Salt and drought stress signal transduction in plants.Annu Rev Plant Biol 53:247-273
Bardwell JC,Mc Govern K,Beckwith J(1991)Identification of a protein required for disulfide bond formation in vivo.Cell67:581-589
Baxter A,Mittler R,Suzuki N(2014)ROS as key players in plant stress signalling.J Exp Bot 65:1229-1240
Bruce TJA,Matthes MC,Napier JA,Pickett JA(2007)Stressful“memories”of plants:Evidence and possible mechanisms.Plant Sci 173:603-608
Cayuela E,Estan MT,Parra M,Caro M,Bolarin MC(2001)Na Cl pre-treatment at the seedling stage enhances fruit yield of tomato plants irrigated with salt water.Plant Soil 230:231-238
Charng YY,Liu HC,Liu NY,Hsu FC,Ko SS(2006)Arabidopsis Hsa32,a novel heat shock protein,is essential for acquired thermotolerance during long recovery after acclimation.Plant Physiol 140:1297-1305
Che P,Bussell JD,Zhou W,Estavillo GM,Pogson BJ,Smith SM(2010)Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis.Sci Signal 3:ra69
Christianson JC,Ye Y(2014)Cleaning up in the endoplasmic reticulum:ubiquitin in charge.Nat Struct Mol Biol 21:325-335
Conrath U(2011)Molecular aspects of defence priming.Trends Plant Sci 16:524-531
Crisp PA,Ganguly D,Eichten SR,Borevitz JO,Pogson BJ(2016)Reconsidering plant memory:Intersections between stress recovery,RNA turnover,and epigenetics.Sci Adv2:e1501340
Dang ZH,Zheng LL,Jia W,Zhe G,Wu SB,Zhi Q,Wang YC(2013)Transcriptomic profiling of the salt-stress response in the wild recretohalophyte Reaumuria trigyna.BMC Genomics14:29-46
Deinlein U,Stephan AB,Horie T,Luo W,Xu G,Schroeder JI(2014)Plant salt-tolerance mechanisms.Trends Plant Sci19:371-379
Eichten SR,Schmitz RJ,Springer NM(2014)Epigenetics:Beyond chromatin modifications and complex genetic regulation.Plant Physiol 165:933-947
Fedoroff N(2006)Redox regulatory mechanisms in cellular stress responses.Ann Bot 98:289-300
Feng XJ,Li JR,Qi SL,Lin QF,Jin JB,Hua XJ(2016)Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis.Proc Natl Acad Sci USA 113:E8335-E8343
Foreman J,Demidchik V,Bothwell JH,Mylona P,Miedema H,Torres MA,Linstead P,Costa S,Brownlee C,Jones JD,Davies JM,Dolan L(2003)Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.Nature 422:442-446
Fujita M,Mizukado S,Fujita Y,Ichikawa T,Nakazawa M,Seki M,Matsui M,Yamaguchi-Shinozaki K,Shinozaki K(2007)Identification of stress-tolerance-related transcriptionfactor genes via mini-scale Full-length c DNA Over-e Xpressor(FOX)gene hunting system.Biochem Biophys Res Commun 364:250-257
Galvan-Ampudia CS,Testerink C(2011)Salt stress signals shape the plant root.Curr Opin Plant Biol 14:296-302
Gao H,Brandizzi F,Benning C,Larkin RM(2008)A membranetethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana.Proc Natl Acad Sci USA 105:16398-16403
Garcia de la Garma J,Fernandez-Garcia N,Bardisi E,Pallol B,Asensio-Rubio JS,Bru R,Olmos E(2015)New insights into plant salt acclimation:The roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system.New Phytol 205:216-239
Gauss R,Sommer T,Jarosch E(2006)The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment.EMBO J 25:1827-1835
Geng Y,Wu R,Wee CW,Xie F,Wei X,Chan PM,Tham C,Duan L,Dinneny JR(2013)A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis.Plant Cell 25:2132-2154
Guerra DD,Callis J(2012)Ubiquitin on the move:The ubiquitin modification system plays diverse roles in the regulation of endoplasmic reticulum-and plasma membrane-localized proteins.Plant Physiol 160:56-64
Hegde RS,Ploegh HL(2010)Quality and quantity control at the endoplasmic reticulum.Cur Opin Cell Biol 22:437-446
Helenius A,Aebi M(2004)Roles of N-linked glycans in the endoplasmic reticulum.Annu Rev Biochem 73:1019-1049
Henriquez-Valencia C,Moreno AA,Sandoval-Ibanez O,Mitina I,Blanco-Herrera F,Cifuentes-Esquivel N,Orellana A(2015)b ZIP17 and b ZIP60 regulate the expression of Bi P3 and other salt stress responsive genes in an UPR-independent manner in Arabidopsis thaliana.J Cell Biochem 116:1638-1645
Holst B,Tachibana C,Winther JR(1997)Active site mutations in yeast protein disulfide isomerase cause dithiothreitol sensitivity and a reduced rate of protein folding in the endoplasmic reticulum.J Cell Biol 138:1229-1238
Howell SH(2013)Endoplasmic reticulum stress responses in plants.Annu Rev Plant Biol 64:477-499
Huang D,Wu W,Abrams SR,Cutler AJ(2008)The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors.J Exp Bot 59:2991-3007
Irsigler AS,Costa MD,Zhang P,Reis PA,Dewey RE,Boston RS,Fontes EP(2007)Expression profiling on soybean leaves reveals integration of ER-and osmotic-stress pathways.BMC Genomics 8:431
Janda T,Darko E,Shehata S,Kovacs V,Pal M,Szalai G(2016)Salt acclimation processes in wheat.Plant Physiol Biochem 101:68-75
Jiang C,Belfield EJ,Cao Y,Smith JA,Harberd NP(2013)An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis.Plant Cell 25:3535-3552
Jossier M,Kroniewicz L,Dalmas F,Le Thiec D,Ephritikhine G,Thomine S,Barbier-Brygoo H,Vavasseur A,Filleur S,Leonhardt N(2010)The Arabidopsis vacuolar anion transporter,At CLCc,is involved in the regulation of stomatal movements and contributes to salt tolerance.Plant J 64:563-576
Kamauchi S,Nakatani H,Nakano C,Urade R(2005)Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana.FEBS J 272:3461-3476
Kinoshita T,Seki M(2014)Epigenetic memory for stress response and adaptation in plants.Plant Cell Physiol 55:1859-1863
Kronzucker HJ,Britto DT(2011)Sodium transport in plants:Acritical review.New Phytol 189:54-81
Li B,Byrt CS,Qiu J,Baumann U,Hrmova M,Evrard A,Johnson AA,Birnbaum KD,Mayo GM,Jha D,Henderson SW,Tester M,Gilliham M,Roy SJ(2015)Identification of a stelar-localised transport protein that facilitates root-toshoot transfer of chloride in Arabidopsis.Plant Physiol 170:1024-1029
Liu DY,Smith PM,Barton DA,Day DA,Overall RL(2015)Characterisation of Arabidopsis calnexin 1 and calnexin 2 in the endoplasmic reticulum and at plasmodesmata.Protoplasma 254:1-12
Liu JX,Howell SH(2010)Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants.Plant Cell 22:2930-2942
Liu JX,Srivastava R,Che P,Howell SH(2007a)An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor,b ZIP28.Plant Cell 19:4111-4119
Liu JX,Srivastava R,Che P,Howell SH(2007b)Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling.Plant J 51:897-909
Liu L,Cui F,Li Q,Yin B,Zhang H,Lin B,Wu Y,Xia R,Tang S,Xie Q(2011)The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance.Cell Res 21:957-969
Liu X,Zhu Y,Zhai H,Cai H,Ji W,Luo X,Li J,Bai X(2012)At PP2CG1,a protein phosphatase 2C,positively regulates salt tolerance of Arabidopsis in abscisic acid-dependent manner.Biochem Biophys Res Commun 422:710-715
Mirouze M,Paszkowski J(2011)Epigenetic contribution to stress adaptation in plants.Curr Opin Plant Biol 14:267-274
Munns R,Tester M(2008)Mechanisms of salinity tolerance.Annu Rev Plant Biol 59:651-681
Oh DH,Leidi E,Zhang Q,Hwang SM,Li Y,Quintero FJ,Jiang X,D’Urzo MP,Lee SY,Zhao Y,Bahk JD,Bressan RA,Yun DJ,Pardo JM,Bohnert HJ(2009)Loss of halophytism by interference with SOS1 expression.Plant Physiol 151:210-222
Ozgur R,Uzilday B,Sekmen AH,Turkan I(2015)The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in Arabidopsis.Ann Bot 116:541-553
Pandolfi C,Azzarello E,Mancuso S,Shabala S(2016)Acclimation improves salt stress tolerance in Zea mays plants.J Plant Physiol 201:1-8
Pandolfi C,Mancuso S,Shabala S(2012)Physiology of acclimation to salinity stress in pea(Pisum sativum).Environ Exp Bot 84:44-51
Prime APG,Conrath U,Beckers GJ,Flors V,Garcia-Agustin 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(2006)Priming:Getting ready for battle.Mol Plant Microbe Interact 19:1062-1071
Pruthvi V,Narasimhan R,Nataraja KN(2014)Simultaneous expression of abiotic stress responsive transcription factors,At DREB2A,At HB7 and At ABF3 improves salinity and drought tolerance in peanut(Arachis hypogaea L.).PLo S ONE 9:e111152
Rengasamy P(2010)Soil processes affecting crop production in salt-affected soils.Funct Plant Biol 37:613-620
Rodriguez HG,Roberts J,Jordan WR,Drew MC(1997)Growth,water relations,and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress.Plant Physiol 113:881-893
Roy SJ,Huang W,Wang XJ,Evrard A,Schmockel SM,Zafar ZU,Tester M(2013)A novel protein kinase involved in Natexclusion revealed from positional cloning.Plant Cell Environ 36:553-568
Sani E,Herzyk P,Perrella G,Colot V,Amtmann A(2013)Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome.Genome Biol 14:R59
Santos AP,Serra T,Figueiredo DD,Barros P,Lourenco T,Chander S,Oliveira MM,Saibo NJ(2011)Transcription regulation of abiotic stress responses in rice:A combined action of transcription factors and epigenetic mechanisms.Omics 15:839-857
Shen X,Wang Z,Song X,Xu J,Jiang C,Zhao Y,Ma C,Zhang H(2014)Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis.Plant Mol Biol 86:303-317
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