Identification of the ERF gene family in Aeluropus littoralis halophyte plant and analysis of their expression pattern in response to salt stress

Document Type : Research Paper

Authors

1 Assistant Preofessor, Department of Genetic Engineering and Biology, Genetics and Agricultural Biotechnology Institute of Tabarestan (GABIT), Sari Agricultural Sciences and Natural Resources University (SANRU), Sari, Iran.

2 Ph.D. Candidate in Plant Breeding, Sari Agricultural Sciences and Natural Resources University (SANRU), Sari, Iran.

Abstract

Salt stress is one of the abiotic stresses limiting plant growth and development. The ethylene response factor (ERF) is one of the transcription factor family that involved in plant development and responses to biotic and abiotic stresses. Regarding to importance role of genes belonging to ERF gene family in plant responses to salt stress, identification of these genes in the Aeluropus littoralis, halophyte plant, was considered in this study. In total, 36 non-redundant ERF genes were identified in A. littoralis genome. The phylogenetic tree classified the AlERF gene family into six distinct groups (B1 to B6) based on hemology with the Araboidopsis thaliana. Gene structure analysis revealed that AlERF genes contained zero to two introns. Domain search and conserved motif analyses in AlERF protein sequences determined that 2 motifs (1 and 2) out of the identified 10 motifs participate in the AP2/ERF domain structure. Based on transcriptome data and heatmap diagram, AlERF6.3 gene was expressed more in root tissue under salinity stress, and the least expression level was observed in AlERF6.7 gene in leaf tissue under recovery conditions. The different expression patterns of genes in leaf and root tissues under salt stress suggested different regulatory mechanisms in the gene expression. The results of this study, as the first report on the ERF gene family in A. littoralis, provides basic information for further studies of the functional characteristics of AlERF genes.

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Allen MD, Yamasaki K, Ohme‐Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a β‐sheet revealed by the solution structure of the GCC‐box binding domain in complex with DNA. EMBO J. 17(18): 5484-5496.
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37: 202-208.
Broun P, Poindexter P, Osborne E, Jiang C-Z, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci U S A. 101(13): 4706-4711.
Chen L, Han J, Deng X, Tan S, Li L, Li L, Zhou J, Peng H, Yang G, He G (2016) Expansion and stress responses of AP2/EREBP superfamily in Brachypodium distachyon. Sci. Rep. 6: 21623.
Cui L, Feng K, Wang M, Wang M, Deng P, Song W, Nie X (2016) Genome-wide identification, phylogeny and expression analysis of AP2/ERF transcription factors family in Brachypodium distachyon. BMC Genomics. 17(1): 636.
Dong W, Ai X, Xu F, Quan T, Liu S, Xia G (2012) Isolation and characterization of a bread wheat salinity responsive ERF transcription factor. Gene. 511(1): 38-45.
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 39(4): 783-791.
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A (2015) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44: 279-285.
Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM. (ed) The proteomics protocols handbook, Humana Press, New York City, New York, United States, pp571-607.
Guo B, Wei Y, Xu R, Lin S, Luan H, Lv C, Zhang X, Song X, Xu R (2016) Genome-wide analysis of APETALA2/ethylene-responsive factor (AP2/ERF) gene family in barley (Hordeum vulgare L.). PLoS One. 11(9): e0161322.
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symposium series. 41: 95-98.
Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35: 585-587.
Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 31(8): 1296-1297.
Huang W, Xian Z, Kang X, Tang N, Li Z (2015) Genome-wide identification, phylogeny and expression analysis of GRAS gene family in tomato. BMC Plant Biol. 15(1): 209.
Jones P, Binns D, Chang H-Y, Fraser M, Li W, Mcanulla C, Mcwilliam H, Maslen J, Mitchell A, Nuka G (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics. 30(9): 1236-1240.
Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, Mouille G, Höfte H, Pauly M, Riechmann JL, Broun P (2007) The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell. 19(4): 1278-1294.
Kawahara Y, De La Bastide M, Hamilton JP, Kanamori H, Mccombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice. 6(1): 4.
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40(D1): D1202-D1210.
Letunic I, Doerks T, Bork P (2014) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res.43(D1):D257-D260.
Liu M, Sun W, Ma Z, Zheng T, Huang L, Wu Q, Zhao G, Tang Z, Bu T, Li C (2019) Genome-wide investigation of the AP2/ERF gene family in tartary buckwheat (Fagopyum Tataricum). BMC Plant Biol. 19(1): 84.
Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran L-SP, Shinozaki K, Yamaguchi-Shinozaki K (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet. 9(9): e1003790.
Magnani E, Sjölander K, Hake S (2004) From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell. 16(9): 2265-2277.
Mao D, Chen C (2012) Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. PLoS One. 7(10): e47275.
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140(2): 411-432.
Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell. 7(2): 173-182.
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe O, Samaha R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Sci. 290(5499): 2105-2110.
Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor Ta ERF 3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol. J. 12(4): 468-479.
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the AP2/ERF domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem. Biophys. Res. Commun. 290(3): 998-1009.
Scherf U, Ross DT, Waltham M, Smith LH, Lee JK, Tanabe L, Kohn KW, Reinhold WC, Myers TG, Andrews DT (2000) A gene expression database for the molecular pharmacology of cancer. Nat. Genet. 24(3): 236.
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.
Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2010) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol. 52(2): 344-360.
Sigrist CJ, De Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I (2012) New and continuing developments at PROSITE. Nucleic Acids Res. 41(D1): D344-D347.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30(12): 2725-2729.
Thompson JD, Gibson TJ, Higgins DG (2003) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. 1: 2-3.
Wang S, Zhou B, Yao W, Jiang T (2018) PsnERF75 Transcription Factor from Populus simonii× P. nigra Confers Salt Tolerance in Transgenic Arabidopsis. J Plant Biol. 61(2): 61-71.
Wang X, Hou C, Zheng K, Li Q, Chen S, Wang S (2017) Overexpression of ERF96, a small ethylene response factor gene, enhances salt tolerance in Arabidopsis. Biologia Plantarum. 61(4): 693-701.
Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol. Biol. 65(6): 719-732.
Yan HW, Hong L, Zhou YQ, Jiang HY, Zhu SW, Fan J, Cheng BJ (2013) A genome-wide analysis of the ERF gene family in sorghum. Gen. Mol. Res. 12(2): 2038-2055.
Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol. Biol. 58(4): 585-596.
Yao W, Wang L, Zhou B, Wang S, Li R, Jiang T (2016a) Over-expression of poplar transcription factor ERF76 gene confers salt tolerance in transgenic tobacco. J. Plant Physiol. 198: 23-31.
Yao W, Wang S, Zhou B, Jiang T (2016b) Transgenic poplar overexpressing the endogenous transcription factor ERF76 gene improves salinity tolerance. Tree physiology. 36(7): 896-908.
Zhang G, Chen M, Chen X, Xu Z, Guan S, Li LC, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J. Exp. Bot. 59(15): 4095-4107.
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 60(13): 3781-3796.
Zhang H, Li W, Chen J, Yang Y, Zhang Z, Zhang H, Wang XC, Huang R (2007) Transcriptional activator TSRF1 reversely regulates pathogen resistance and osmotic stress tolerance in tobacco. Plant Mol. Biol. 63(1): 63-71.
Zhang L, Li Z, Quan R, Li G, Wang R, Huang R (2011) An AP2 domain-containing gene, ESE1, targeted by the ethylene signaling component EIN3 is important for the salt response in Arabidopsis. Plant Physiol. 157(2): 854-865.
Zhou ML, Tang YX, Wu YM (2012) Genome-wide analysis of AP2/ERF transcription factor family in Zea Mays. Curr. Bioinform. 7(3): 324-332.
Zhuang J, Chen JM, Yao QH, Xiong F, Sun CC, Zhou XR, Zhang J, Xiong AS (2011) Discovery and expression profile analysis of AP2/ERF family genes from Triticum aestivum. Mol. Biol. Rep. 38(2): 745-753.
Zouari N, Saad RB, Legavre T, Azaza J, Sabau X, Jaoua M, Masmoudi K, Hassairi A (2007) Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Gene. 404(1): 61-69.