Abstract
The calmodulin-binding transcriptional activator (CAMTA) family was first observed in tobacco (NtER1) during a screening for the CaM-binding proteins, which are known to be one of the fast response stress proteins. Due to the increased importance of plant transcription factors in recent years; genome-wide identification of CAMTA genes has been performed in several plant species, except for Phaseolus vulgaris. Therefore, our aim was to identify and characterize CAMTA genes in P. vulgaris via in silico genome-wide analysis approach. Our results showed a total of eight CAMTA genes that were identified and observed on five out of 11 chromosomes of P. vulgaris. Four gene couples were found to be segmentally-duplicated and these segmental duplication events were shown to occur from 29.97 to 92.06 MYA. The phylogenetic tree of CAMTA homologs from P. vulgaris, A. thaliana, and G. max. revealed three groups based on their homology and the intron numbers of Pvul-CAMTA genes, ranged from 11 to 12. According to the syteny analysis; CAMTA genes of P. vulgaris and G. max revealed higher similarity, because they have highly similar genomes compared to A. thaliana. All Pvul-CAMTA genes were targeted by miRNAs, which play a role in response mechanism of salt stress. To detect expression levels in different plant tissues, mRNA analysis of Pvul-CAMTA genes were performed using publicly available expression data in Phytozome v12.1. In addition, responses of Pvul-CAMTA genes to salt stress, were also examined via both RNAseq and qRT-PCR analysis. To identify and to obtain insight into biological functions of CAMTA genes in the genome of P. vulgaris, several analyses were conducted using many online and offline bioinformatic tools, genome databases and qRT-PCR analyses. Due to this study being the first in the identification of CAMTA genes in P. vulgaris, this study could be considered as an useful source for future CAMTA genes studies in either P. vulgaris or comparative different plant species.
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References
Buyuk I, Inal B, Ilhan E, Tanriseven M, Aras S, Erayman M (2016) Genome-wide identification of salinity responsive HSP70s in common bean. Mol Biol Rep 43:1251–1266. https://doi.org/10.1007/s11033-016-4057-0
Ilhan E, Buyuk I, Inal B (2018) Transcriptome—scale characterization of salt responsive bean TCP transcription factors. Gene 642:64–73. https://doi.org/10.1016/j.gene.2017.11.021
Inal B, Buyuk I, Ilhan E, Aras S (2017) Genome-wide analysis of Phaseolus vulgaris C2C2-YABBY transcription factors under salt stress conditions. 3 Biotech 7(5):302. https://doi.org/10.1007/S13205-017-0933-0
Pant P, Iqbal Z, Pandey BK, Sawant SV (2018) Genome-wide comparative and evolutionary analysis of calmodulin-binding transcription activator (CAMTA) family in Gossypium species. Sci Rep 8:5573. https://doi.org/10.1038/S41598-018-23846-W
Wei M, Xu XM, Li CH (2017) Identification and expression of CAMTA genes in Populus trichocarpa under biotic and abiotic stress. Sci Rep 7:17910. https://doi.org/10.1038/S41598-017-18219-8
Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21. https://doi.org/10.1093/mp/ssn091
Yamniuk AP, Vogel HJ (2004) Calmodulin’s flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 27:33–57, https://doi.org/10.1385/Mb:27:1:33
Bouche N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861. https://doi.org/10.1074/jbc.M200268200
Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032. https://doi.org/10.1105/tpc.111.084988
Finkler A, Ashery-Padan R, Fromm H, CAMTAs (2007) Calmodulin-binding transcription activators from plants to human. FEBS Lett 581:3893–3898. https://doi.org/10.1016/j.febslet.2007.07.051
Yang TB, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058. https://doi.org/10.1074/jbc.M207941200
Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell 18:2733–2748. https://doi.org/10.1105/tpc.106.042713
Yue RQ, Lu CX, Sun T, Peng TT, Han XH, Qi JS, Yan SF, Tie SG (2015) Identification and expression profiling analysis of calmodulin-binding transcription activator genes in maize (Zea mays L.) under abiotic and biotic stresses. Front Plant Sci 6:576. https://doi.org/10.3389/Fpls.2015.00576
Wang GP, Zeng HQ, Hu XY, Zhu YY, Chen Y, Shen CJ, Wang HZ, Poovaiah BW, Du LQ (2015) Identification and expression analyses of calmodulin-binding transcription activator genes in soybean. Plant Soil 386:205–221. https://doi.org/10.1007/s11104-014-2267-6
Yang YJ, Sun T, Xu LQ, Pi EX, Wang S, Wang HZ, Shen CJ (2015) Genome-wide identification of CAMTA gene family members in Medicago truncatula and their expression during root nodule symbiosis and hormone treatments. Front Plant Sci 6:459. https://doi.org/10.3389/Fpls.2015.00459
Du LQ, Ali GS, Simons KA, Hou JG, Yang TB, Reddy ASN, Poovaiah BW (2009) Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154. https://doi.org/10.1038/nature07612
Kim MH, Kim Y, Kim JW, Lee HS, Lee WS, Kim SK, Wang ZY, Kim SH (2013) Identification of Arabidopsis BAK1-associating receptor-like kinase 1 (BARK1) and characterization of its gene expression and brassinosteroid-regulated root phenotypes. Plant Cell Physiol 54:1620–1634. https://doi.org/10.1093/pcp/pct106
Rahman H, Yang J, Xu YP, Munyampundu JP, Cai XZ (2016) Phylogeny of plant CAMTAs and role of AtCAMTAs in nonhost resistance to Xanthomonas oryzae pv. oryzae. Front Plant Sci 7:177. https://doi.org/10.3389/Fpls.2016.00177
Hou J, Jiang P, Qi S, Zhang K, He Q, Xu C, Ding Z, Zhang K, Li K (2016) Isolation and functional validation of salinity and osmotic stress inducible promoter from the maize type-II H+-Pyrophosphatase gene by deletion analysis in transgenic tobacco plants. Plos ONE 11:e0154041. https://doi.org/10.1371/journal.pone.0154041
Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu SQ, Song QJ, Chavarro C et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713. https://doi.org/10.1038/ng.3008
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. Rna 14:836–843. https://doi.org/10.1261/rna.895308
Lu SF, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in populus. Plant J 55:131–151. https://doi.org/10.1111/j.1365-313X.2008.03497.x
Arenas-Huertero C, Perez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401. https://doi.org/10.1007/s11103-009-9480-3
Feng KW, Nie XJ, Cui LC, Deng PC, Wang MX, Song WN (2017) Genome-wide identification and characterization of salinity stress-responsive miRNAs in wild emmer wheat (Triticum turgidum ssp dicoccoides). Genes 8:156. https://doi.org/10.3390/genes8060156
Eren H, Pekmezci MY, Okay S, Turktas M, Inal B, Ilhan E, Atak M, Erayman M, Unver T (2015) Hexaploid wheat (Triticum aestivum) root miRNome analysis in response to salt stress. Ann Appl Biol 167:208–216. https://doi.org/10.1111/aab.12219
Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N et al. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. https://doi.org/10.1093/nar/gkr944
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373. https://doi.org/10.1093/nar/gkl198
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478. https://doi.org/10.1093/nar/gkr201
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971. https://doi.org/10.1038/nprot.2007.131
Zhang YJ (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:W701–W704. https://doi.org/10.1093/nar/gki383
Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612. https://doi.org/10.1093/nar/gkl315
Lynch M, Conery JS (2003) The evolutionary demography of duplicate genes. J Struct Funct Genomics 3:35–44
Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43. https://doi.org/10.1093/oxfordjournals.molbev.a026236
Lee TH, Tang HB, Wang XY, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152–D1158
Zheng Y, Jiao C, Sun HH, Rosli HG, Pombo MA, Zhang PF, Banf M, Dai XB, Martin GB, Giovannoni JJ et al (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9:1667–1670. https://doi.org/10.1016/j.molp.2016.09.014
Hiz MC, Canher B, Niron H, Turet M (2014) Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PLoS ONE 9:e92598. https://doi.org/10.1371/journal.pone.0092598
Caraux G, Pinloche S (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21:1280–1281. https://doi.org/10.1093/bioinformatics/bti141
Guler NS, Saglam A, Demiralay M, Kadioglu A (2012) Apoplastic and symplastic solute concentrations contribute to osmotic adjustment in bean genotypes during drought stress. Turk J Biol 36:151–160. https://doi.org/10.3906/biy-1101-177
Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld, J; van der (2004) Lelie, D. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol 22:583–588
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
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This research has been partly supported by Ankara University Scientific Research Projects Coordination Unit. Project Number: 16H0430010, 2016
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Büyük, İ., İlhan, E., Şener, D. et al. Genome-wide identification of CAMTA gene family members in Phaseolus vulgaris L. and their expression profiling during salt stress. Mol Biol Rep 46, 2721–2732 (2019). https://doi.org/10.1007/s11033-019-04716-8
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DOI: https://doi.org/10.1007/s11033-019-04716-8