Abstract
Ethylene responsive factors (ERFs) are important transcriptional regulators involved in plant responses to abiotic stress. LeERF1 and LeERF2, two members of the ERF family in tomato (Solanum lycopersicum), have previously been cloned. In this study, we investigated the salt-stress tolerance of transgenic tomato overexpressing LeERF1 and LeERF2. The transgenic lines had longer roots than wild-type (WT) plants under salt stress conditions. Furthermore, we examined physiological and biochemical indexes in the plants and found that overexpression of LeERF1 and LeERF2 enhanced the release of chlorophyll and free proline, but decreased the malondialdehyde contents of the plants. Transgenic tomato displayed higher superoxide dismutase and guaiacol peroxidase activity than WT tomato under high salinity conditions. Moreover, quantitative RT-PCR analysis revealed that the expression levels of salt stress-related genes, including TAS14, HVA22, LHA1, PR5, and RBOHC, which were upregulated in the transgenic plants. Therefore, overexpression of LeERF1 and LeERF2 positively modulates the ethylene-mediated response to salt stress in tomato.
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References
Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a [beta]-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17:5484–5496. doi:10.1093/emboj/17.18.5484
Basu S, Gangopadhyay G, Mukherjee BB (2002) Salt tolerance in rice in vitro: implication of accumulation of Na+, K+ and proline. Plant Cell Tissue Organ Cult 69(1):55–64. doi:10.1023/a:1015028919620
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207. doi:10.1007/BF00018060
Beyer WF Jr, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566. doi:10.1016/0003-2697(87)90489-1
Beyer M, Menzel C, Quack R, Scheper T, Schügerl K, Treichel W, Voigt H, Ullrich M, Ferretti R (1994) Development and application of a new enzyme sensor type based on the EIS-capacitance structure for bioprocess control. Biosen Bioelectr 9(1):17–21. doi:10.1016/0956-5663(94)80010-3
Cao Y, Song F, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol 163(11):1167–1178. doi:10.1016/j.jplph.2005.11.004
Cramer GR, Jones RL (1996) Osmotic stress and abscisic acid reduce cytosolic calcium activities in roots of Arabidopsis thaliana*. Plant Cell Environ 19(11):1291–1298. doi:10.1111/j.1365-3040.1996.tb00007.x
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163. doi:10.1186/1471-2229-11-163
Ehsanpour AA, Fatahian N (2003) Effects of salt and proline on Medicago sativa callus. Plant Cell Tissue Organ Cult 73(1):53–56. doi:10.1023/a:1022619523726
Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia––is survival a balancing act? Trends Plant Sci 9(9):449–456. doi:10.1016/j.tplants.2004.07.005
Godoy J, Lunar R, Torres-Schumann S, Moreno J, Rodrigo R, Pintor-Toro J (1994) Expression, tissue distribution and subcellular localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol Biol 26(6):1921–1934. doi:10.1007/BF00019503
Grichko VP, Glick BR (2001) Ethylene and flooding stress in plants. Plant Physiol Biochem 39(1):1–9. doi:10.1016/s0981-9428(00)01213-4
Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217(2):290–298. doi:10.1007/s00425-003-0986-7
Jaleel CA, Riadh K, Gopi R, Manivannan P, Inès J, Al-Juburi HJ, Chang-Xing Z, Hong-Bo S, Panneerselvam R (2009) Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiologiae Plantarum 31(3):427–436. doi:10.1007/s11738-009-0275-6
Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D (2004) The water- and salt-stress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein. Biochem J 381:373–378
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5(4):325–331. doi:10.1016/s1369-5266(02)00275-3
Larré CF, Fernando JA, Marini P, Bacarin MA, Peters JA (2013) Growth and chlorophyll a fluorescence in Erythrina crista-galli L. plants under flooding conditions. Acta Physiologiae Plantarum 35(5):1463–1471. doi:10.1007/s11738-012-1187-4
Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30(2):151–155. doi:10.1023/a:1006345126589
Liu JP, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of arabidopsis. Plant Physiol 114(2):591–596. doi:10.1104/pp.114.2.591
Lutts S, Kinet JM, Bouharmont J (1996) Effects of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L) cultivars differing in salinity resistance. Plant Growth Regul 19(3):207–218. doi:10.1007/bf00037793
Marti E, Gisbert C, Bishop GJ, Dixon MS, Garcia-Martinez JL (2006) Genetic and physiological characterization of tomato cv Micro-Tom. J Exp Bot 57(9):2037–2047. doi:10.1093/jxb/erj154
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophy Acta 1819(2):86–96. doi:10.1016/j.bbagrm.2011.08.004
Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99(6):1161–1173. doi:10.1093/aob/mcm052
Potters G, Pasternak TP, Guisez Y, Jansen MA (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 32(2):158–169. doi:10.1111/j.1365-3040.2008.01908.x
Prescott J, Laing D, Bell G, Yoshida M, Gillmore R, Allen S, Yamazaki K, Ishii R (1992) Hedonic responses to taste solutions: a cross-cultural study of Japanese and Australians. Chem Senses 17(6):801–809. doi:10.1093/chemse/17.6.801
Sairam RK, Srivastava GC, Agarwal S, Meena RC (2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biol Plant 49(1):85–91. doi:10.1007/s10535-005-5091-2
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophy Res Commun 290(3):998–1009. doi:10.1006/bbrc.2001.6299
Schmittgen TD, Lee EJ, Jiang J, Sarkar A, Yang L, Elton TS, Chen C (2008) Real-time PCR quantification of precursor and mature microRNA. Methods 44(1):31–38. doi:10.1016/j.ymeth.2007.09.006
Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genomics 284(6):455–475. doi:10.1007/s00438-010-0580-1
Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52(2):344–360. doi:10.1093/pcp/pcq196
Shen Q, Chen C-N, Brands A, Pan S-M, Tuan-Hua D (2001) The stress- and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms. Plant Mol Biol 45(3):327–340. doi:10.1023/A:1006460231978
Singh K (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5(5):430–436. doi:10.1016/s1369-5266(02)00289-3
Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilisation. Plant Growth Regul 49(1):77–83. doi:10.1007/s10725-006-0019-1
Tang M, Sun J, Liu Y, Chen F, Shen S (2007) Isolation and functional characterization of the JcERF gene, a putative AP2/EREBP domain-containing transcription factor, in the woody oil plant Jatropha curcas. Plant Mol Biol 63(3):419–428. doi:10.1007/s11103-006-9098-7
Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32(5):465–475. doi:10.1111/j.1365-3040.2009.01938.x
Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latché A, Pech J-C, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550(1–3):149–154. doi:10.1016/s0014-5793(03)00757-9
Véry AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97(17):9801–9806. doi:10.1073/pnas.160250397
Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahlgoy P, Metraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired-resistance. Plant Cell 3(10):1085–1094. doi:10.2307/3869297
Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220(2):262–270. doi:10.1007/s00425-004-1347-x
Zhuang J, Peng R-H, Cheng Z-M, Zhang J, Cai B, Zhang Z, Gao F, Zhu B, Fu X-Y, Jin X-F, Chen J-M, Qiao Y-S, Xiong A-S, Yao Q-H (2009) Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. Sci Hortic 123(1):73–81. doi:10.1016/j.scienta.2009.08.002
Acknowledgments
This study was partly funded by the Universitéde Toulouse, INP-ENSA Toulouse, Génomiqueet Biotechnologie des Fruits of France. The authors thank the China Scholarship Council (CSC) for supporting N.H.
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Hu, N., Tang, N., Yan, F. et al. Effect of LeERF1 and LeERF2 overexpression in the response to salinity of young tomato (Solanumlycopersicum cv. Micro-Tom) seedlings. Acta Physiol Plant 36, 1703–1712 (2014). https://doi.org/10.1007/s11738-014-1545-5
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DOI: https://doi.org/10.1007/s11738-014-1545-5