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Identification and Characterization of SRS Genes in Phaseolus vulgaris Genome and Their Responses Under Salt Stress

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Abstract

SHI-Related Sequence (SRS) transcription factors comprise a protein family with important roles in growth and development. However, the genome-wide study of the SRS protein family has not yet been carried out in the common bean. For this reason, the SRS family has been characterized in depth at both gene and protein levels and several bioinformatics methods have been used. As a result, 10 SRS genes have been identified and their proteins have been phylogenetically categorized into three major groups within the common bean. By investigating duplications that play a major role in the development of gene families, 19 duplication events have been identified in the SRS family (18 segmental and 1 tandem). In addition, using available RNAseq data, comparative expression analysis of Pvul-SRS genes was performed and expression changes in Pvul-SRS-1, 2, 4, 6, 7, and 10 genes were observed under both salt and drought stress. Five Pvul-SRS genes were selected based on RNAseq data (Pvul-SRS-1, 2, 4, 6, and 10) and screened with RT-qPCR in two common bean cultivars (Yakutiye ‘salt-resistant’ and Zulbiye ‘salt-susceptible’ cv.). These genes also showed different levels of expression between two common bean cultivars under salt stress conditions and this may explain the responses of Pvul-SRS genes against abiotic stress. In summary, this work is the first study in which in silico identification and characterization of Pvul-SRS genes have been examined at gene expression level. The results could therefore provide the basis for future studies of functional characterization of Pvul-SRS genes.

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References

  • Atchley WR (2011) Walter M. Fitch (1929–2011). Science 332:804–904

    CAS  PubMed  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Büyük İ, 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

    PubMed  Google Scholar 

  • Büyük İ, İlhan E, Şener D, Özsoy AU, Aras S (2019) 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

    PubMed  Google Scholar 

  • Büyük İlker OKAY, Aybüke AT, Sümer A (2021) The NIN-LIKE PROTEIN (NLP) family in common bean: genome-wide identification, evolution and expression analysis. Commun Fac Sci Univ Ankara Ser C Biol 30(1):58–84

    Google Scholar 

  • Çakır Ö, Arıkan B, Karpuz B, Turgut-Kara N (2021) Expression analysis of miRNAs and their targets related to salt stress in Solanum lycopersicum H-2274. Biotechnol Biotechnol Equip 35:283–290

    Google Scholar 

  • Chen S, Ren H, Luo Y, Feng C, Li H (2021) Genome-wide identification of wheat (Triticum aestivum L.) expansin genes and functional characterization of TaEXPB1A. Environ Exp Bot 182:104307

    CAS  Google Scholar 

  • Elenbaas B, Dobbelstein M, Roth J, Shenk T, Levine AJ (1996) The MDM2 oncoprotein binds specifically to RNA through its RING finger domain. Mol Med 2:439–451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feyissa BA, Amyot L, Nasrollahi V, Papadopoulos Y, Kohalmi SE, Hannoufa A (2021) Involvement of the miR156/SPL module in flooding response in Medicago sativa. Sci Rep 11:1–16

    Google Scholar 

  • Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99–113

    CAS  PubMed  Google Scholar 

  • Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    PubMed  Google Scholar 

  • Fridborg I, Kuusk S, Moritz T, Sundberg E (1999) The Arabidopsis dwarf mutant shi exhibits reduced gibberellin responses conferred by overexpression of a new putative zinc finger protein. Plant Cell 11:1019–1031

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fridborg I, Kuusk S, Robertson M, Sundberg E (2001) The Arabidopsis protein SHI represses gibberellin responses in Arabidopsis and barley. Plant Physiol 127:937–948

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. The proteomics protocols handbook. Springer, Berlin

    Google Scholar 

  • Gomariz-Fernández A, Sánchez-Gerschon V, Fourquin C, Ferrándiz C (2017) The role of SHI/STY/SRS genes in organ growth and carpel development is conserved in the distant eudicot species Arabidopsis thaliana and Nicotiana benthamiana. Front Plant Sci 8:814

    PubMed  PubMed Central  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    CAS  PubMed  Google Scholar 

  • Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan=hereditas 29:1023–1026

    CAS  PubMed  Google Scholar 

  • He B, Shi P, Lv Y, Gao Z, Chen G (2020) Gene coexpression network analysis reveals the role of SRS genes in senescence leaf of maize (Zea mays L.). J Genet 99:1–10

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Holland PWH, Garcia-Fernàndez J, Williams NA, Sidow A (1994) Gene duplications and the origins of vertebrate development. Development 1994:125–133

    Google Scholar 

  • Hooft RWW, Sander C, Vriend G (1996) Positioning hydrogen atoms by optimizing hydrogen-bond networks in protein structures. Proteins: Struct Funct Bioinform 26:363–376

    CAS  Google Scholar 

  • Horton P, Park KJ, Obayashi T, and Nakai K(2006) Protein subcellular localization prediction with WoLF PSORT. In Proceedings of the 4th Asia-Pacific Bioinformatics Conference, 39–48. World Scientific

  • İnal B, Büyük İ, İlhan E, Aras S (2017) Genome-wide analysis of Phaseolus vulgaris C2C2-YABBY transcription factors under salt stress conditions. 3 Biotech 7:302

    PubMed  PubMed Central  Google Scholar 

  • Jorge JG, Villalobos-López MA, Chavarría-Alvarado KL, Ríos-Meléndez S, López-Meyer M, Arroyo-Becerra A (2020) Genome-wide transcriptional changes triggered by water deficit on a drought-tolerant common bean cultivar. BMC Plant Biol 20:1–20

    Google Scholar 

  • Kaulen H, Pognonec P, Gregor PD, Roeder RG (1991) The Xenopus B1 factor is closely related to the mammalian activator USF and is implicated in the developmental regulation of TFIIIA gene expression. Mol Cell Biol 11:412–424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley LA, Sternberg MJE (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4:363

    CAS  PubMed  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, DePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    CAS  PubMed  Google Scholar 

  • Kuusk S, Sohlberg JJ, Magnus Eklund D, Sundberg E (2006) Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner. Plant J 47:99–111

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Wang T, Zhang Y, Li Y (2016) Overexpression of soybean miR172c confers tolerance to water deficit and salt stress, but increases ABA sensitivity in transgenic Arabidopsis thaliana. J Exp Bot 67:175–194

    CAS  PubMed  Google Scholar 

  • Liu H-H, Tian X, Li Y-J, Wu C-A, Zheng C-C (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Ma Y, Xue H, Zhang F, Jiang Q, Yang S, Yue P, Wang F, Zhang Y, Li L, He P (2021) The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol J 19:311

    CAS  PubMed  Google Scholar 

  • Macovei A, Tuteja N (2012) microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol 12:1–12

    Google Scholar 

  • McClean PE, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics 11:1–10

    Google Scholar 

  • Nekrutenko A, Makova KD, Li W-H (2002) The KA/KS ratio test for assessing the protein-coding potential of genomic regions: an empirical and simulation study. Genom Res 12:198–202

    CAS  Google Scholar 

  • Schommer C, Bresso EG, Spinelli SV, Palatnik JF (2012) Role of microRNA miR319 in plant development. MicroRNAs in plant development and stress responses. Springer, Berlin

    Google Scholar 

  • Shoemaker RC, Polzin K, Labate J, James Specht EC, Brummer TO, Nevin Young V, Concibido JW, Tamulonis JP (1996) Genome duplication in soybean (Glycine subgenus soja). Genetics 144:329–338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shoemaker RC, Schlueter J, Doyle JJ (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 9:104–109

    CAS  PubMed  Google Scholar 

  • Singh S, Yadav S, Singh A, Mahima M, Singh A, Gautam V, Sarkar AK (2020) Auxin signaling modulates LATERAL ROOT PRIMORDIUM 1 (LRP 1) expression during lateral root development in Arabidopsis. Plant J 101:87–100

    CAS  PubMed  Google Scholar 

  • Smith DL, Fedoroff NV (1995) LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7:735–745

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tran L-S, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    CAS  PubMed  Google Scholar 

  • Wang H, Wang H (2015) miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol Plant 8:677–688

    CAS  PubMed  Google Scholar 

  • Wang J, Ye Y, Meng Xu, Feng L, Li-an Xu (2019a) Roles of the SPL gene family and miR156 in the salt stress responses of tamarisk (Tamarix chinensis). BMC Plant Biol 19:1–11

    Google Scholar 

  • Wang W, Liu D, Chen D, Cheng Y, Zhang X, Song L, Mengjiao Hu, Dong J, Shen F (2019b) MicroRNA414c affects salt tolerance of cotton by regulating reactive oxygen species metabolism under salinity stress. RNA Biol 16:362–375

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Feng C, Zhai Z, Peng X, Wang Y, Sun Y, Li J, Shen X, Xiao Y, Zhu S (2020) The Apple microR171i-SCARECROW-LIKE PROTEINS26. 1 module enhances drought stress tolerance by integrating ascorbic acid metabolism. Plant Physiol 184:194–211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    CAS  PubMed  Google Scholar 

  • Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43

    CAS  PubMed  Google Scholar 

  • Yang C, Li D, Mao D, Liu X, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of micro RNA 319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L). Plant Cell Environ 36:2207–2218

    CAS  PubMed  Google Scholar 

  • Yang J, Peng Xu, Diqiu Yu (2020) Genome-wide identification and characterization of the shi-related sequence gene family in rice. Evol Bioinform 16:117693432094149

    Google Scholar 

  • Yuo T, Yamashita Y, Kanamori H, Matsumoto T, Lundqvist U, Sato K, Ichii M, Jobling SA, Taketa S (2012) A SHORT INTERNODES (SHI) family transcription factor gene regulates awn elongation and pistil morphology in barley. J Exp Bot 63:5223–5232

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zawaski C, Kadmiel M, Ma C, Gai Y, Jiang X, Strauss SH, Busov VB (2011) SHORT INTERNODES-like genes regulate shoot growth and xylem proliferation in Populus. New Phytol 191:678–691

    CAS  PubMed  Google Scholar 

  • Zhang Y (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:W701–W704

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Zhang H, Srivastava AK, Pan Y, Bai J, Fang J, Shi H, Zhu J-K (2018) Knockdown of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol 176:2082–2094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao S-P, Song X-Y, Guo L-L, Zhang X-Z, Zheng W-J (2020) Genome-wide analysis of the shi-related sequence family and functional identification of GmSRS18 involving in drought and salt stresses in soybean. Int J Mol Sci 21:1810

    CAS  PubMed Central  Google Scholar 

  • Zhou M, Li D, Li Z, Qian Hu, Yang C, Zhu L, Luo H (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 161:1375–1391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Leng X, Sun X, Mu Q, Wang B, Li X, Wang C, Fang J (2015) Discovery of conservation and diversification of miR171 genes by phylogenetic analysis based on global genomes. Plant Genom. https://doi.org/10.3835/plantgenome2014.10.0076

    Article  Google Scholar 

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Experiment design: IB, SA. Experiment performance and data analyses: AO, IB. Data interpretation: IB, AO. Manuscript drafting: IB, AO, SA.

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Correspondence to İlker Büyük.

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Büyük, İ., Okay, A. & Aras, S. Identification and Characterization of SRS Genes in Phaseolus vulgaris Genome and Their Responses Under Salt Stress. Biochem Genet 60, 482–503 (2022). https://doi.org/10.1007/s10528-021-10108-0

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