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A genome-wide approach to the comprehensive analysis of GASA gene family in Glycine max

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Abstract

A vital role of short amino acid gene family, gibberellic acid stimulated arabidopsis (GASA), has been reported in plant growth and development. Although, little information is available about these cysteine rich short proteins in different plant species and this is the first comprehensive approach to exploit available genomic data and to analyze the GASA family in G. max. The phylogenetic and sequence composition analysis distributed the 37 identified GmGASA genes into three groups. Further investigation of the tissue expression pattern, phylogenetic analysis, motif, gene structure, chromosome distributions, duplication patterns, positive-selection pressure and cis-element analysis of 37 GmGASA genes. A conserved GASA domain was found in all identified GmGASA genes and exhibited similar characteristics. The online gene expression profile based analysis of GmGASA genes reveled that these genes were highly expressed in almost all soybean parts and some have high expression in flower which indicates that GmGASA genes displayed special or distinct expression pattern among different tissues. The segmental duplication was found in five pairs from 37 GmGASA genes and was distributed on 15 different chromosomes. The Ka/Ks ratio of 5 pairs of segmentally duplicated gene indicated that after the occurrence of duplication events, the duplicated gene pairs were purified and selected after restrictive functional differentiation. This investigated study of GmGASA gene will useful to support the statement about GASA genes role during flower induction in flowering plants.

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Data Availability

The datasets generated during and/or analysed during the current study are not publicly available as they are going to be used for further analyses but are available from the corresponding author upon reasonable request.

References

  • Ahmad MZ, Li P, Wang J, Rehman NU, Zhao J (2017) Isoflavone malonyltransferases GmIMaT1 and GmIMaT3 differently modify isoflavone glucosides in soybean (Glycine max) under various stresses. Front Plant Sci 8:735

    Article  PubMed  PubMed Central  Google Scholar 

  • Aubert D, Chevillard M, Dorne AM, Arlaud G, Herzog M (1998) Expression patterns of GASA genes in Arabidopsis thaliana: the GASA4 gene is up-regulated by gibberellins in meristematic regions. Plant Mol Biol 36(6):871–883

    Article  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(Web Server issue):W369–W373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balaji V, Smart CD (2012) Over-expression of snakin-2 and extensin-like protein genes restricts pathogen invasiveness and enhances tolerance to Clavibacter michiganensis subsp michiganensis in transgenic tomato (Solanum lycopersicum). Transgenic Res 21(1):23–37

    Article  CAS  PubMed  Google Scholar 

  • Ben-Nissan G, Lee JY, Borohov A, Weiss DGIP (2004) a Petunia hybrida GA-induced cysteine-rich protein: a possible role in shoot elongation and transition to flowering. Plant J 37(2):229–238

    Article  CAS  PubMed  Google Scholar 

  • Berrocal-Lobo M, Segura A, Moreno M, Lopez G, Garcia-Olmedo F, Molina A (2002) Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol 128(3):951–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bindschedler LV, Whitelegge JP, Millar DJ, Bolwell GP (2006) A two component chitin-binding protein from French bean—association of a proline-rich protein with a cysteine-rich polypeptide. FEBS Lett 580(6):1541–1546

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, Kozik A, Chan B, Michelmore R, Young ND (2003) DiagHunter and GenoPix2D: programs for genomic comparisons, large-scale homology discovery and visualization. Genome Biol 4:R68

    Article  PubMed  PubMed Central  Google Scholar 

  • Dossa K, Diouf D, Cisse N (2016) Genome-Wide investigation of Hsf genes in sesame reveals their segmental duplication expansion and their active role in drought stress response. Front Plant Sci 7:1522

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan S, Zhang D, Xing L, Qi S, Du L, Wu H, Shao H, Li Y, Ma J, Han M (2017) Comprehensive analysis of GASA family members in the Malus domestica genome: identification, characterization, and their expressions in response to apple flower induction. BMC Genomics 18:827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453

    Article  CAS  PubMed  Google Scholar 

  • Fuente JIDL, Valpuesta V (2006) The strawberry gene FaGAST affects plant growth through inhibition of cell elongation. J Exp Bot 57:2401–2411

    Article  CAS  PubMed  Google Scholar 

  • Furukawa T, Sakaguchi N, Shimada H (2006) Two OsGASR genes, rice GAST homologue genes that are abundant in proliferating tissues, show different expression patterns in developing panicles. Genes Genet Syst 81(3):171–180

    Article  CAS  PubMed  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186

    Article  CAS  PubMed  Google Scholar 

  • Guo RR, Xu XZ, Carole B, Li XQ, Gao M, Zheng Y, Wang XP (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genom 14:554

    Article  CAS  Google Scholar 

  • Herzog M, Dorne AM, Grellet F (1995) GASA, a gibberellin-regulated gene family from Arabidopsis thaliana related to the tomato GAST1 gene. Plant Mol Biol 27(4):743–752

    Article  CAS  PubMed  Google Scholar 

  • Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, de Pamphilis 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

    Article  CAS  PubMed  Google Scholar 

  • Kotilainen M, Helariutta Y, Mehto M, Pollanen E, Albert VA, Elomaa P, Teeri TH (1999) GEG participates in the regulation of cell and organ shape during corolla and carpel development in Gerbera hybrida. Plant Cell 11(6):1093–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar G, Arya P, Gupta K, Randhawa V, Acharya V, Singh AK (2016a) Comparative phylogenetic analysis and transcriptional profiling of MADS-box gene family identified DAM and FLC-like genes in apple (Malus x domestica). Sci Rep-Uk 6:20695

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016b) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(1):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li WH, Gojobori T, Nei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292:237–239

    Article  CAS  PubMed  Google Scholar 

  • Li KL, Bai X, Li Y, Cai H, Ji W, Tang LL, Wen YD, Zhu YM (2011) GsGASA1 mediated root growth inhibition in response to chronic cold stress is marked by the accumulation of DELLAs. J Plant Physiol 168(18):2153–2160

    Article  CAS  PubMed  Google Scholar 

  • Li J, Hou H, Li X, Xiang J, Yin X, Gao H, Zheng Y, Bassett CL, Wang X (2013) Genome-wide identification and analysis of the SBP-box family genes in apple (Malus x domestica Borkh.). Plant Physiol Biochem 70:100–114

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  CAS  PubMed  Google Scholar 

  • Mao ZC, Zheng JY, Wang YS, Chen GH, Yang YH, Feng DX, Xie BY (2011) The new CaSn gene belonging to the snakin family induces resistance against root-knot nematode infection in pepper. Phytoparasitica 39(2):151–164

    Article  CAS  Google Scholar 

  • Meng XC, Wang XJ (2004) Regulation of flower development and anthocyanin accumulation in Gerbera hybrida. J Hortic Sci Biotechnol 79:131–137

    Article  CAS  Google Scholar 

  • Meslin C, Mugnier S, Callebaut I, Laurin M, Pascal G, Poupon A, Goudet G, Monget P (2012) Evolution of genes involved in gamete interaction: Evidence for positive selection, duplications and losses in vertebrates. PLoS ONE 7:e44548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moyano-Canete E, Bellido ML, Garcia-Caparros N, Medina-Puche L, Amil-Ruiz F, Gonzalez-Reyes JA, Caballero JL, Munoz-Blanco J, Blanco-Portales R (2013) FaGAST2, a strawberry ripening-related gene, acts together with FaGAST1 to determine cell size of the fruit receptacle. Plant Cell Physiol 54(2):218–236

    Article  CAS  PubMed  Google Scholar 

  • Nahirnak V, Rivarola M, de Urreta MG, Paniego N, Hopp HE, Almasia NI, Vazquez-Rovere C (2016) Genome-wide analysis of the Snakin/GASA gene family in Solanum tuberosum cv. Kennebec. Am J Potato Res 93(2):172–188

    Article  CAS  Google Scholar 

  • Peng JZ, Lai LJ, Wang XJ (2010) Temporal and spatial expression analysis of PRGL in Gerbera hybrida. Mol Biol Rep 37(7):3311–3317

    Article  CAS  PubMed  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J et al (2012) The Pfam protein families database. Nucleic Acids Res 40(Database issue):D290–301. https://doi.org/10.1093/nar/gkr1065

    Article  CAS  PubMed  Google Scholar 

  • Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Ann Rev Ecol Syst 29:467–501

    Article  Google Scholar 

  • Ratnakumar A, Mousset S, Glémin S, Berglund J, Galtier N, Duret L, Webster MT (2010) Detecting positive selection within genomes: the problem of biased gene conversion. Philosophical transactions of the Royal Society of London. Ser B Biol Sci 365:2571–2580

    Article  CAS  Google Scholar 

  • Roxrud I, Lid SE, Fletcher JC, Schmidt ED, Opsahl-Sorteberg HG (2007) GASA4, one of the 14-member Arabidopsis GASA family of small polypeptides, regulates flowering and seed development. Plant Cell Physiol 48(3):471–483

    Article  CAS  PubMed  Google Scholar 

  • Rubinovich L, Weiss D (2010) The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. Plant J 64(6):1018–1027

    Article  CAS  PubMed  Google Scholar 

  • Schlueter JA, Lin JY, Schlueter SD, Vasylenko-Sanders IF, Deshpande S et al (2007) Gene duplication and paleopolyploidy in soybean and the implications for whole genome sequencing. BMC Genomics 8:330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Segura A, Moreno M, Madueño F, Molina A, Garcíaolmedo F (1999) Snakin-1, a peptide from potato that is active against plant pathogens. Mol Plant Microbe Interact 12:16–23

    Article  CAS  PubMed  Google Scholar 

  • Shahzad Y, Tahir MHN, Khan AA, Sadaqat HA, Sadia B (2017) Genetic evaluation of Korean soybean (Glycine max L. Merril) genotypes for various morphological and phenological. J Innov Bio-Res 1(1):127–131

    Google Scholar 

  • Shengchun Z, Xiaojing W (2017 ) One new kind of phytohormonal signaling integrator: up-and-coming GASA family genes. Plant Signal Behav 12(2):e1226453

    Article  CAS  Google Scholar 

  • Shi LF, Gast RT, Gopalraj M, Olszewski NE (1992) Characterization of a shoot-specific, GA3-regulated and ABA-regulated gene from tomato. Plant J 2(2):153–159

    CAS  PubMed  Google Scholar 

  • Silverstein KA, Moskal WA Jr, Wu HC, Underwood BA, Graham MA, Town CD, Vanden Bosch KA (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51(2):262–280

    Article  CAS  PubMed  Google Scholar 

  • Taylor BH, Scheuring CF (1994) A molecular marker for lateral root initiation: the RSI-1 gene of tomato (Lycopersicon esculentum Mill) is activated in early lateral root primordia. Mol Gen Genet 243:148–157

    CAS  PubMed  Google Scholar 

  • Tian Y, Dong QL, Ji ZR, Chi FM, Cong PH, Zhou ZS (2015) Genome-wide identification and analysis of the MADS-box gene family in apple. Gene 555(2):277–290

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Wang Z, Xu YY, Joo SH, Kim SK, Xue Z, Xu ZH, Wang ZY, Chong K (2009) OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J 57(3):498–510

    Article  CAS  PubMed  Google Scholar 

  • Wigoda N, Ben-Nissan G, Granot D, Schwartz A, Weiss D (2006) The gibberellin-induced, cysteine-rich protein GIP2 from Petunia hybrida exhibits in planta antioxidant activity. Plant J 48(5):796–805

    Article  CAS  PubMed  Google Scholar 

  • Xu GX, Guo CC, Shan HY, Kong HZ (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci USA 109(4):1187–1192

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci CABIOS 13:555–556

    CAS  PubMed  Google Scholar 

  • Yin G, Xu H, Xiao S, Qin Y, Li Y, Yan Y, Hu Y (2013) The large soybean (Glycine max) WRKY TF family expanded by segmental duplication events and subsequent divergent selection among subgroups. BMC Plant Biol 13:148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SC, Wang XJ (2008) Expression pattern of GASA, downstream genes of DELLA, in Arabidopsis. Chin Sci Bull 53(24):3839–3846

    Article  CAS  Google Scholar 

  • Zhang SC, Wang XJ (2011) Overexpression of GASA5 increases the sensitivity of Arabidopsis to heat stress. J Plant Physiol 168(17):2093–2101

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Yang C, Peng J, Sun S, Wang X (2009) GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol Biol 69(6):745–759

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Li L, Wu J, Peng J, Zhang L, Wang X (2012) Cell expansion and microtubule behavior in ray floret petals of Gerbera hybrida: responses to light and gibberellic acid. Photochem Photobiol Sci 11:279–288

    Article  CAS  PubMed  Google Scholar 

  • Zhong C, Xu H, Ye S, Wang S, Li L, Zhang S, Wang X (2015) Gibberellic acid-stimulated Arabidopsis serves as an integrator of gibberellin, abscisic acid, and glucose signaling during seed germination in Arabidopsis. Plant Physiol 169:2288–2303

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

All the authors thankful to the chairperson of PBG department, Faculty of Agriculture, Gomal University, D. I. Khan, Pakistan, who showed great interest and support to this study.

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Authors and Affiliations

  1. Department of Plant Breeding and Genetics, Faculty of Agriculture, Gomal University, Dera Ismail Khan, KP, Pakistan

    Muhammad Zulfiqar Ahmad, Aiman Sana, Arshad Jamil, Jamal Abdul Nasir &  Abdullah

  2. International Crop Research Center for Stress Resistance, College of Life Sciences, Guangzhou University, Guangzhou, China

    Shakeel Ahmed

  3. Department of Horticulture, Faculty of Agriculture, Gomal University, Dera Ismail Khan, KP, Pakistan

    Muhammad Uzair Hameed

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  1. Muhammad Zulfiqar Ahmad
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  2. Aiman Sana
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  3. Arshad Jamil
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Contributions

MZA designed the research. MZA, AS, AJ, JAN extracted the data. SA done the qRT-PCR analysis. MZA and AS analysed and wrote the manuscript. MUH and A arranged and revised the manuscript. All the contributors read and approved for submission.

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Correspondence to Muhammad Zulfiqar Ahmad.

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Ahmad, M.Z., Sana, A., Jamil, A. et al. A genome-wide approach to the comprehensive analysis of GASA gene family in Glycine max. Plant Mol Biol 100, 607–620 (2019). https://doi.org/10.1007/s11103-019-00883-1

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