Abstract
Plants can successfully improve their resistance to previously lethal salinity stress by a short exposure to low levels of salt stress, a process known as salt acclimation (SA). In spite of its fundamental significance in theoretical study and agricultural practice, the molecular mechanisms underlying plant SA remain elusive. In this study, we found that salt acclimated Arabidopsis young seedlings can survive subsequent 200 mM NaCl stress. RNA-seq was performed to analyze the genome-wide transcriptional response under SA conditions. Among 518 differentially expressed genes (DEGs) under SA, 366 up-regulated genes were enriched for cell wall biosynthesis, osmoregulation, oxidative stress, or transcription factors. Seven DEGs participate in the synthesis of lignin and 24 DEGs encode plant cell wall proteins, suggesting the importance of cell wall remodeling under SA. Furthermore, in comparison to non-acclimated salt stress, 228 of 245 DEGs were repressed by acclimated salt stress, including many genes related to ethylene biosynthesis and signaling pathway. In addition, MAPK6, a major component of the ethylene signaling pathway, was found to play a crucial role in SA. Our transcriptomic analysis has provided important insight on the roles of transcription factors, cell wall remodeling, and the ethylene biosynthesis and signaling pathways during SA in Arabidopsis.
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Abbreviations
- ACC:
-
1-Aminocyclopropane-1-carboxylic acid
- ACS:
-
1-Aminocyclopropane-1-carboxylic acid synthase
- DEG:
-
Differentially expressed gene
- FDR:
-
False discovery rate
- GO:
-
Gene ontology
- KEGG:
-
Kyoto encyclopedia of genes and genomes
- NASS:
-
Non-acclimated salt stress
- P5CS1:
-
Pyrroline-5-carboxylate synthase 1
- ROS:
-
Reactive oxygen species
- RPKM:
-
Reads per KB per million reads
- SA:
-
Salt acclimation
- SASS:
-
Salt acclimated salt stress
References
Amzallag G, Lerner H, Poljakoff-Mayber A (1990) Induction of increased salt tolerance in Sorghum bicolor by NaCl pretreatment. J Exp Bot 41(222):29–34. doi:10.1093/jxb/41.1.29
Argueso G, Hansen M, Kieber J (2007) Regulation of ethylene biosynthesis. J Plant Growth Regul 26:92–105. doi:10.1007/s00344-007-0013-5
Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta Vulgaris. Plant Physiol 24(1):1–15. doi:10.1104/pp.24.1.1
Atreya A, Vartak V, Bhargava S (2009) Salt priming improves tolerance to dessication stress and to extreme salt stress in Bruguiera cylindrica. Int J Integr Biol 6(2):68–73
Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21(3):944–953. doi:10.1105/tpc.108.062158
Bruce T, Matthes M, Napier J, Pickett J (2007) Stressful “memories” of plants evidence and possible mechanisms. Plant Sci 173(6):603–608. doi:10.1016/j.plantsci.2007.09.002
Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143(2):707–719. doi:10.1104/pp.106.094292
Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95(6):901–915. doi:10.1093/aob/mci100
Chen Y, Yang X, He K, Liu M, Li J, Gao Z, Lin Z, Zhang Y, Wang X, Qiu X, Shen Y, Zhang L, Deng X, Luo J, Deng X, Chen Z, Gu H, Qu L (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60(1):107–124. doi:10.1007/s11103-005-2910-y
Cheng MC, Hsieh EJ, Chen JH, Chen HY, Lin TP (2012) Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol 158(1):363–375. doi:10.1104/pp.111.189738
Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic-stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162(3):1566–1582. doi:10.1104/pp.113.221911
Chinnusamy V, Zhu J, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. Genet Eng (NY) 27:141–177
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(10):1062–1071. doi:10.1094/MPMI-19-1062
Denekamp M, Smeekens SC (2003) Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene. Plant Physiol 132(3):1415–1423. doi:10.1104/pp.102.019273
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7(7):1085–1097. doi:10.1105/tpc.7.7.1085
Ferrante A, Francini A (2006) Ethylene and leaf senescence. In: Khan NA (ed) Ethylene action in plants. Springer, Heidelberg, pp 51–67
Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247(1):1–11
Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99(25):15898–15903. doi:10.1073/pnas.252637799
Guo H, Ecker J (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49
Hagemann M (2011) Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol Rev 35(1):87–123. doi:10.1111/j.1574-6976.2010.00234.x
Hahn A, Harter K (2009) Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both? Plant Physiol 149(3):1207–1210. doi:10.1104/pp.108.132241
Hernández J, Olmos E, Corpas F, Sevilla F, Del Río L (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167
Hsieh E, Cheng M, Lin T (2013) Functional characterization of an abiotic stress-inducible transcription factor AtERF53 in Arabidopsis thaliana. Plant Mol Biol 82:223–237. doi:10.1007/s11103-013-0054-z
Hu Y, Li WC, Xu YQ, Li GJ, Liao Y, Fu FL (2009) Differential expression of candidate genes for lignin biosynthesis under drought stress in maize leaves. J Appl Genet 50(3):213–223. doi:10.1007/BF03195675
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24(5):655–665. doi:10.1046/j.1365-313x.2000.00913.x
Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240(4857):1302–1309
Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6(1):25. doi:10.1186/1471-2229-6-25
Joo S, Liu Y, Lueth A, Zhang S (2008) MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J 54(1):129–140. doi:10.1111/j.1365-313X.2008.03404.x
Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 160(2):846–867. doi:10.1104/pp.112.200444
Kieber J, Rothenberg M, Roman G, Feldmann K, Ecker J (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72(3):427–441
Kim SY, Lim JH, Park MR, Kim YJ, Park TI, Seo YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. J Biochem Mol Biol 38(2):218–224
Koyama T, Nii H, Mitsuda N, Ohta M, Kitajima S, Ohme-Takagi M, Sato F (2013) A regulatory cascade involving class II ETHYLENE RESPONSE FACTOR transcriptional repressors operates in the progression of leaf senescence. Plant Physiol 162(2):991–1005. doi:10.1104/pp.113.218115
Lee D, Kim Y, Lee C (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158(6):737–745. doi:10.1078/0176-1617-00174
Li X, Chapple C (2010) Understanding lignification: challenges beyond monolignol biosynthesis. Plant Physiol 154(2):449–452. doi:10.1104/pp.110.162842
Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8(6):e1002767. doi:10.1371/journal.pgen.1002767
Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16(12):3386–3399. doi:10.1105/tpc.104.026609
Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21(16):3448–3449. doi:10.1093/bioinformatics/bti551
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158. doi:10.1016/j.abb.2005.10.018
McCue K, Hanson A (1990) Drought and salt tolerance towards understanding and application. Trends Biotechnol 8:358–362
Meng X, Xu J, He Y, Yang KY, Mordorski B, Liu Y, Zhang S (2013) Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25(3):1126–1142. doi:10.1105/tpc.112.109074
Morgan P, Drew M (1997) Ethylene and plant responses to stress. Physiol Plant 100:620–630. doi:10.1111/j.1399-3054.1997.tb03068.x
Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27(1):29–34
O’Rourke JA, Yang SS, Miller SS, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu ZJ, Allan D, Gronwald JW, Vance CP (2013) An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161(2):705–724. doi:10.1104/pp.112.209254
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349. doi:10.1016/j.ecoenv.2004.06.010
Qiu Q, Ma T, Hu Q, Liu B, Wu Y, Zhou H, Wang Q, Wang J, Liu J (2011) Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiol 31(4):452–461. doi:10.1093/treephys/tpr015
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(6):R59. doi:10.1186/gb-2013-14-6-r59
Sasidharan R, Voesenek L, Pierik R (2011) Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic stresses. Crit Rev Plant Sci 30(6):548–562. doi:10.1080/07352689.2011.615706
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31(3):279–292. doi:10.1046/j.1365-313X.2002.01359.x
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. doi:10.1101/gr.1239303
Shavrukov Y (2013) Salt stress or salt shock: which genes are we studying? J Exp Bot 64(1):119–127. doi:10.1093/jxb/ers316
Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21(1):81–85. doi:10.1038/nbt766
Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5(1):9–23. doi:10.1105/tpc.5.1.9
Sottosanto JB, Saranga Y, Blumwald E (2007) Impact of AtNHX1, a vacuolar Na+/H+ antiporter, upon gene expression during short- and long-term salt stress in Arabidopsis thaliana. BMC Plant Biol 7(1):18. doi:10.1186/1471-2229-7-18
Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89. doi:10.1016/j.plaphy.2013.04.009
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29(4):417–426. doi:10.1046/j.0960-7412.2001.01227.x
Tanou G, Fotopoulos V, Molassiotis A (2012) Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front Plant Sci 3:216. doi:10.3389/fpls.2012.00216
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller L, Rhee S, Stitt M (2004) MAPMAN:a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939. doi:10.1111/j.1365-313X.2004.02016.x
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50(1):571–599. doi:10.1146/annurev.arplant.50.1.571
Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136(2):2982–3000. doi:10.1104/pp.104.049999
Tsugama D, Liu S, Takano T (2012) Drought-induced activation and rehydration-induced inactivation of MPK6 in Arabidopsis. Biochem Biophys Res Commun 426(4):626–629. doi:10.1016/j.bbrc.2012.08.141
Umezawa T, Shimizu K, Kato M, Ueda T (2000) Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiol Plant 110:59–63. doi:10.1034/j.1399-3054.2000.110108.x
Van Loon LC, Geraats BP, Linthorst HJ (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11(4):184–191. doi:10.1016/j.tplants.2006.02.005
Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18(1):259–288. doi:10.1146/annurev.py.18.090180.001355
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20. doi:10.1093/mp/ssp106
Wang NN, Shih MC, Li N (2005) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J Exp Bot 56(413):909–920. doi:10.1093/jxb/eri083
Wang Y, Liu C, Li K, Sun F, Hu H, Li X, Zhao Y, Han C, Zhang W, Duan Y, Liu M, Li X (2007) Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. Plant Mol Biol 64(6):633–644. doi:10.1007/s11103-007-9182-7
Wang P, Du Y, Zhao X, Miao Y, Song CP (2013) The MPK6-ERF6-ROS-responsive cis-acting Element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiol 161(3):1392–1408. doi:10.1104/pp.112.210724
Wi SJ, Jang SJ, Park KY (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30(1):37–49. doi:10.1007/s10059-010-0086-z
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 RbohD-derived reactive oxygen species synthesis. Plant J 66(2):280–292. doi:10.1111/j.1365-313X.2011.04488.x
Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H, Liu G, Ren D (2008) Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem 283(40):26996–27006. doi:10.1074/jbc.M801392200
Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451(7180):789–795. doi:10.1038/nature06543
Zhao XC, Schaller GE (2004) Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett 562(1):189–192. doi:10.1016/S0014-5793(04)00238-8
Zhou C, Cai Z, Guo Y, Gan S (2009) An Arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol 150(1):167–177. doi:10.1104/pp.108.133439
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This study was funded by the National Basic Research Program of China (Grant No. 2012CB114204) and the Foundation for “Taishan Scholar” from the People’s Government of Shandong Province.
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Xiaoyan Shen and Zenglan Wang have contributed equally to this work.
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Shen, X., Wang, Z., Song, X. et al. 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 (2014). https://doi.org/10.1007/s11103-014-0230-9
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DOI: https://doi.org/10.1007/s11103-014-0230-9