Abstract
The EF1α is a multifunctional protein with additional unrelated activities to its primary function in translation. This protein is encoded by a multigene family and few studies are still available in plants. Expression of six EF1α genes in Glycine max was performed using RT-qPCR and RNA-seq data to advance in the function of each gene during plant development, stress conditions and phytohormone treatments. A phylogenetic classification in Phaseoleae tribe was used to identify the G. max EF1α genes (EF1α 1a1, 1a2, 1b, 2a, 2b and 3). Three EF1α types (1–3) were found in Phaseoleae revealing duplications in G. max types 1 and 2. EF1α genes were expressed in all studied tissues, however, specific amount of each transcript was detected. In plant development, all EF1α transcripts were generally more expressed in younger tissues, however, in unifoliolate leaves and cotyledons a higher expression occurred in older tissues. Five EF1α genes (except 2a) were up-regulated under stress in a response tissue/stress/cultivar-dependent. EF1α 3 was the most stress-induced gene linked to cultivar stress tolerance mainly in aerial tissues. Auxin, salicylate and ethylene induced differentially the EF1α expression. Overall, this study provides a consistent EF1α classification in Phaseoleae tribe to better understand their functional evolution. The RT-qPCR and RNA-seq EF1α expression profiles were consistent, both exhibiting expression diversification of each gene (spatio-temporal, stress and phytohormone stimuli). Our results point out the EF1α genes, especially EF1α 3, as candidate for developing a useful tool for future G. max breeding.
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References
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) MYCCONSENSUSAT Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
Aguilar F, Montadon P, Stutz E (1991) Two genes encoding the soybean translation elongation factor EF-1A are transcribed in seedling leaves. Plant Mol Biol 17:351–360
Altschul SF, Madden TL, Schäffer AA, Zhange J, Zhange Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Axelos M, Bardet C, Liboz T, Le VTA, Curie C, Lescure B (1989) Gene family encoding the Arabidopsis thaliana translation elongation factor EF-1 alpha: molecular cloning, characterization and expression. Mol Gen Genet 219:106–112
Baumann K, De Paolis A, Costantino P, Gualberti G (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11:323–333
Belamkar V, Weeks NT, Bharti AK, Farmer AD, Graham MA, Cannon SB (2014) Comprehensive characterization and RNA-Seq profiling of the HD-Zip transcription factor Family in soybean (Glycine max) during dehydration and salt stress. BMC Genom 15:950
Berberich T, Sugawara K, Harada M, Kusano T (1995) Molecular cloning, characterization and expression of an elongation factor 1 alpha gene in maize. Plant Mol Biol 29:611–615
Brown AV, Hudson KA (2015) Developmental profiling of gene expression in soybean trifoliate leaves and cotyledons. BMC Plant Biol 15:169
Browning KS (1996) The plant translational apparatus. Plant Mol Biol 32:107–144
Buchel AS, Brederode FT, Bol JF, Linthorst HJ (1999) Mutation of GT-1 binding sites in the Pr-1A promoter influences the level of inducible gene expression in vivo. Plant Mol Biol 40:387–396
Busk PK, Jensen AB, Pages M (1997) Regulatory elements in vivo in the promoter of the abscisic acid responsive gene rab17 from maize. Plant J 11:1285–1295
Carneiro NP, Hughes PA, Larkins BA (1999) The eEFlA gene family is differentially expressed in maize endosperm. Plant Mol Biol 41:801–814
Cavalcanti JH, Oliveira GM, Saraiva KD, Torquato JP, Maia IG, de Melo DF, Costa JH (2013) Identification of duplicated and stress-inducible Aox2b gene co-expressed with Aox1 in species of the Medicago genus reveals a regulation linked to gene rearrangement in leguminous genomes. J Plant Physiol 170:1609–1619
Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: plant Promoter Analysis Navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene group. BMC Genom 9:561
Chen YA, Wen YC, Chang WC (2012) AtPAN: an integrated system for reconstructing transcriptional regulatory networks in Arabidopsis thaliana. BMC Genom 13:85
Costa JH, Mota EF, Cambursano MV, Lauxmann MA, Oliveira LMN, Silva MGL et al (2010) Stress-induced co-expression of two alternative oxidase (VuAox1 and 2b) genes in Vigna unguiculata. J Plant Physiol 167:561–570
Costa JH, McDonald AE, Arnholdt-Schmitt B, de Melo DF (2014) A classification scheme for alternative oxidases reveals the taxonomic distribution and evolutionary history of the enzyme in angiosperms. Mitochondrion 19 Pt B:172–183
Duttaroy A, Bourbeau D, Wang XL, Wang E (1998) Apoptosis rate can be accelerated or decelerated by overexpression or reduction of the level of elongation factor-1a. Exp Cell Res 238:168–176
Ejiri S (2002) Moonlighting functions of polypeptide elongation factor1: from actin bundling to zinc Winger protein r1-associated nuclear localization. Biosci Biotechnol Biochem 66:1–21
Fei CK, Ismail I, Ismail SI, Natorajan D, Zainal Z (2009) Identification of a short putative 5′ regulatory sequence from transgenic hairy root of tomato-regulating specific expression pattern. Plant Omics 2:206–213
Goetze E (2006) Elongation factor 1α in marine copepods (Calanoida: Eucalanidae): Phylogenetic utility and unique intron structure. Mol Phylogenet Evol 40:880–886
Gonen H, Smith CE, Siegel NR, Kahana C, Merrick WC, Chakraburtty K, Schwartz AL, Ciechanover A (1994) Protein synthesis elongation factor EF-1 alpha is essential for ubiquitin-dependent degradation of certain n alpha-acetylated proteins and may be substituted for by the bacterial elongation factor EF-tu. Proc Natl Acad Sci USA 91:7648–7652
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE). Nucleic Acids Res 27:297–300
Hu R, Fan C, Li H, Zhang QF, Fu YF (2009) Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR. BMC Mol Biol 10:93
Infante C, Asensio E, Cañavate JP, Manchado M (2008) Molecular characterization and expression analysis of five different elongation factor 1 alpha genes in the flatfish Senegalese sole (Soleasene galensis Kaup): differential gene expression and thyroid hormones dependence during metamorphosis. BMC Mol Biol 9:19
Jasid S, Galatro A, Villordo JJ, Puntarulo S, Simontacchi M (2009) Role of nitric oxide in soybean cotyledon senescence. Plant Sci 176:662–668
Job C, Rajjou L, Lovigny Y, Belghazi M, Job D (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138:790–802
Kawahara R, Sunabori S, Fukuda H, Komamlne A (1992) A gene expressed preferentially in the globular stage of somatic embryogenesis encodes elongation-factor la in carrot. Eur J Biochem 209:157–162
Kidou S, Ejiri S (1998) Isolation, characterization and mRNA expression of four cDNAs encoding translation elongation factor 1A from rice (Oryza sativa L.). Plant Mol Biol 36:137–148
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0. Mol Biol Evol. (submitted)
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lee WS, Fu SF, Li Z, Murphy AM, Dobson EA, Garland L, Chaluvadi SR, Lewsey MG, Nelson RS, Carr JP (2016) Salicylic acid treatment and expression of an RNA-dependent RNA polymerase 1 transgene inhibit lethal symptoms and meristem invasion during tobacco mosaic virus infection in Nicotiana benthamiana. BMC Plant Biol 16:15
Leisner CP, Ming R, Ainsworth EA (2014) Distinct transcriptional profiles of ozone stress in soybean (Glycine max) flowers and pods. BMC Plant Biol 14:335
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Lin F, Zhao M, Baumann DD, Ping J, Sun L, Liu Y, Zhang B, Tang Z, Hughes E, Doerge WR, Hughes TJ, Ma J (2014) Molecular response to the pathogen Phytophthora sojae among ten soybean near isogenic lines revealed by comparative transcriptomics. BMC Genom 15:18
Luscher B, Eiseman RN (1990) New light on Myc and Myb. Part II. Myb. Genes Dev 4:2235–2241
Morelli JK, Shewmaker CK, Vayda ME (1994) Biphasic stimulation of translational activity correlates with induction of translation elongation factor 1 subunit alpha upon wounding in potato tubers. Plant Physiol 106:897–903
Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628
Park HC, Kim ML, Kang YH, Jeon JM, Yoo JH, Kim MC, Park CY, Jeong JC, Moon BC, Lee JH, Yoon HW, Lee SH, Chung WS, Lim CO, Lee SY, Hong JC, Cho MJ (2004) GT1GMSCAM4 Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol 135:2150–2161
Pokalsky AR, Hiatt WR, Ridge N, Rasmussen R, Houckand CM, Shewmaker CK (1989) Structure and expression of elongation factor 1 alpha in tomato. Nucleic Acids Res 17:4661–4673
Prince SJ, Joshi T, Mutava RN, Syed N, Vitor MSJ, Patil G, Song L, Wang J, Lin L, Chen W, Shannon JG, Valliyodan B, Xu D, Nguyen HT (2015) Comparative analysis of the drought-responsive transcriptome in soybean lines contrasting for canopy wilting. Plant Sci 240:65–78
Ransom-Hodgkins WD (2009) The application of expression analysis in elucidating the eukaryotic elongation factor one alpha gene family in Arabidopsis thaliana. Mol Genet Genomics 281:391–405
Ransom-Hodgkins WD, Brglez I, Wang XM, Boss WF (2000) Calcium regulated proteolysis of eEF1A. Plant Physiol 122:957–965
Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738
Roy A, Kucukural A, Zhang Y (2012) COFACTOR: an accurate comparative algorithm for structure-based protein function annotation. Nucleic Acids Res 40:471–477
Rutledge RG, Stewart D (2008) Critical evaluation of methods used to determine amplification efficiency refutes the exponential character of real-time PCR. BMC Mol Biol 9:96
Saitou N, Nei M (1987) The Neighbor-Joining method-a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Saraiva KDC, Fernandes de Melo D, Morais VD, Vasconcelos IM, Costa JH (2014) Selection of suitable soybean EF1a genes as internal controls for real-time PCR analyses of tissues during plant development and under stress conditions. Plant Cell Rep 33:1453–1465
Sasikumar AN, Perez WB, Kinzy TG (2012) The many roles of the eukaryotic elongation factor 1 complex. Wiley Interdiscip Rev RNA 3:543–555
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
Schrödinger LLC (2015) The PyMOL Molecular Graphics System, Version 1.6. http://www.pymol.org/. Accessed 25 Jan 2015
Shin R, Park CJ, Paek KH (2001) A translation elongation factor 1A (CaEFIA) gene from hot pepper (Capsicum annuum L.) is induced by the tobacco mosaic virus and by wounding. J Plant Bio 44:199–204
Shin JH, Vaughn JN, Abdel-Haleem H, Chavarro C, Abernathy B, Kim KD, Jackson AS, Li Z (2015) Transcriptomic changes due to water deficit define a general soybean response and accession-specific pathways for drought avoidance. BMC Plant Biol 15:26
Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) ABRE—Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270
Suhandono S, Hughes J, Brown K, Hughes MA (2001) Expression and structure of an elongation factor-1αgene (MeEF1) from cassava (Manihot esculenta Crantz). Euphytica 120:49–58
Toueille M, Saint-Jean B, Castroviejo M, Benedetto JP (2007) The elongation factor 1a: a novel regulator in the DNA replication/repair protein network in wheat cells? Plant Physiol Biochem 45:113–118
Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016
Vijaykumar D (2002) Molecular cloning, characterization and tissue specific expression of an elongation factor 1A gene in Saccharum officinarum L. Plant Sci 162:315–321
Wang L, Liu Y, Wang WN, Mai WJ, Xin Y, Zhou J, He WY, Wang AL, Sun R-Y (2011) Molecular characterization and expression analysis of elongation factors 1A and 2 from the Pacific white shrimp, Litopenaeus vannamei. Mol Biol Rep 38:2167–2178
Xu WL, Wang XL, Wang H, Li XB (2007) Molecular characterization and expression analysis of nine cotton GhEF1A genes encoding translation elongation factor 1A. Gene 389:27–35
Yang W, Burkhart W, Cavallius J, Merrick WC, Boss WF (1993) Purification and characterization of a phosphatidylinositol 4-kinaseactivator in carrot cells. J Biol Chem 268:392–398
Yendrek CR, Koester RP, Ainsworth EA (2015) A comparative analysis of transcriptomic, biochemical, and physiological responses to elevated ozone identifies species-specific mechanisms of resilience in legume crops. J Exp Bot 66:7101–7112
Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40
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This research was supported by CAPES (Coordination for the Improvement of Higher Education Personnel), CNPq (National Council of Technological and Scientific Development) and FUNCAP (Ceara Research Support Foundation).
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Saraiva, K.D.d., Oliveira, A.E.R., dos Santos, C.P. et al. Phylogenetic analysis and differential expression of EF1α genes in soybean during development, stress and phytohormone treatments. Mol Genet Genomics 291, 1505–1522 (2016). https://doi.org/10.1007/s00438-016-1198-8
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DOI: https://doi.org/10.1007/s00438-016-1198-8