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Genome-wide characterization and expression pattern of auxin response factor (ARF) gene family in soybean and common bean

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Abstract

Auxin response factors (ARFs) encode one of the most abundant groups of auxin-mediated response transcription factors in higher plants and play a major role in various biological processes. The success of whole genome sequencing allows for comprehensive phylogenetic analysis of ARF genes in plants. Here, we identified 80 ARF genes belonging to five different groups in legume species, soybean (Glycine max, 55) and common bean (Phaseolus vulgaris, 25), based on phylogenetic analysis and supported by motif analysis. There is no member ARF of common bean in group V which contained two members from soybean, GmARF12 and GmARF55. The duplication events among two species were also observed by using Ks values. A majority of the ARF genes (96.1 %; 38 GmARFs and 56.0 %, 14 PvARFs) were segmentally duplicated while only two and one of ARF G. max and P. vulgaris genes were tandemly duplicated, respectively. In addition, expression profiling indicated that ARF genes in soybean and common bean perform various functions in plant growth and development, excluding flowering development. Furthermore, diversity of cis-elements in promoter regions also revealed differential expression of ARF proteins.

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References

  • Attia KA, Abdelkhalik AF, Ammar MH, Wei C, Yang J, Lightfoot DA, El-Sayed WM, El-Shemy HA (2009) Antisense phenotypes reveal a functional expression of OsARF1, an auxin response factor, in transgenic rice. Curr Issues Mol Biol 11:29–34

    Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  CAS  PubMed  Google Scholar 

  • Calderon Villalobos LI, Lee S, De Oliveira C, Ivetac A, Brandt W, Armitage L, Sheard LB, Tan X, Parry G, Mao H et al (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8:477–485

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    Article  CAS  PubMed  Google Scholar 

  • Donaldson JG, Jackson CL (2011) ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 12:362–375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574

    Article  CAS  PubMed  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219

    Article  PubMed  PubMed Central  Google Scholar 

  • Finet C, Fourquin C, Vinauger M, Berne-Dedieu A, Chambrier P, Paindavoine S, Scutt CP (2010) Parallel structural evolution of auxin response factors in the angiosperms. Plant J 63:952–959

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Taniguchi N, Tasaka M (2006) PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J 48:380–389

    Article  CAS  PubMed  Google Scholar 

  • Goodstein DM, Shu S, 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:D1178–1186

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, Estelle I (2000) Function of the ubiquitin-proteasome pathway in auxin response. Trends Biochem Sci 25:133–138

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  CAS  PubMed  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  CAS  PubMed  Google Scholar 

  • Ha CV, Le DT, Nishiyama R, Watanabe Y, Sulieman S, Tran UT, Mochida K, Dong NV, Yamaguchi-Shinozaki K, Shinozaki K et al (2013) The auxin response factor transcription factor family in soybean: genome-wide identification and expression analyses during development and water stress. DNA Res 20:511–524

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

  • Haiyang JIANG, Wei WEI, Yan LIU, SuWen Z, BeiJiu C (2010) Genome-wide analysis and evolution of the auxin response factor (ARF) gene family in Sorghum bicolor. J Anhui Agric Univ 37:395–400

    Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59

    Article  PubMed  PubMed Central  Google Scholar 

  • Khomtchouk BB, Van Booven DJ, Wahlestedt C (2014) HeatmapGenerator: high performance RNAseq and microarray visualization software suite to examine differential gene expression levels using an R and C++ hybrid computational pipeline. Source Code Biol Med 9:30

    Article  PubMed  PubMed Central  Google Scholar 

  • Krogan NT, Ckurshumova W, Marcos D, Caragea AE, Berleth T (2012) Deletion of MP/ARF5 domains III and IV reveals a requirement for Aux/IAA regulation in Arabidopsis leaf vascular patterning. New Phytol 194:391–401

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics 285:245–260

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Li SB, OuYang WZ, Hou XJ, **e LL, Hu CG, Zhang JZ (2015) Genome-wide identification, isolation and expression analysis of auxin response factor (ARF) gene family in sweet orange (Citrus sinensis). Front Plant Sci 6:119

    PubMed  PubMed Central  Google Scholar 

  • Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD et al (2010a) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 152:541–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Libault M, Farmer A, Joshi T, Takahashi K, Langley RJ, Franklin LD, He J, Xu D, May G, Stacey G (2010b) An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J 63:86–99

    CAS  PubMed  Google Scholar 

  • Liu Y, Sanoff HK, Cho H, Burd CE, Torrice C, Mohlke KL, Ibrahim JG, Thomas NE, Sharpless NE (2009) INK4/ARF transcript expression is associated with chromosome 9p21 variants linked to atherosclerosis. PLoS ONE 4:e5027

    Article  PubMed  PubMed Central  Google Scholar 

  • McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41:W597–W600

    Article  PubMed  PubMed Central  Google Scholar 

  • Mun JH, Yu HJ, Shin JY, Oh M, Hwang HJ, Chung H (2012) Auxin response factor gene family in Brassica rapa: genomic organization, divergence, expression, and evolution. Mol Genet Genomics 287:765–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narise T, Kobayashi K, Baba S, Shimojima M, Masuda S, Fukaki H, Ohta H (2010) Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol Biol 72:533–544

    Article  CAS  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D et al (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlap** functions of ARF7 and ARF19. Plant Cell 17:444–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA, McClean PE, Li J, Dai X, Zhao PX et al (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genom 15:866

    Article  Google Scholar 

  • Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proost S, Pattyn P, Gerats T, Van de Peer Y (2011) Journey through the past: 150 million years of plant genome evolution. Plant J 66:58–65

    Article  CAS  PubMed  Google Scholar 

  • Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, Liu Y, Wu Y, Jiang D (2012) OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytol 193:109–120

    Article  CAS  PubMed  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 

  • Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713

    Article  CAS  PubMed  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    Article  CAS  PubMed  Google Scholar 

  • Shen C, Wang S, Bai Y, Wu Y, Zhang S, Chen M, Guilfoyle TJ, Wu P, Qi Y (2010) Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.). J Exp Bot 61:3971–3981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen C, Wang S, Zhang S, Xu Y, Qian Q, Qi Y, Jiang DA (2013) OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant Cell Environ 36:607–620

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627–13632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song X, Liu G, Duan W, Liu T, Huang Z, Ren J, Li Y, Hou X (2014) Genome-wide identification, classification and expression analysis of the heat shock transcription factor family in Chinese cabbage. Mol Genet Genom 289:541–551

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24

    Article  CAS  PubMed  Google Scholar 

  • Ward SP, Estelle M (2001) Auxin signaling involves regulated protein degradation by the ubiquitin-proteasome pathway: recent advances in auxin biology. J Plant Growth Regul 20:265–273

    Article  CAS  Google Scholar 

  • Wu J, Wang F, Cheng L, Kong F, Peng Z, Liu S, Yu X, Lu G (2011) Identification, isolation and expression analysis of auxin response factor (ARF) genes in Solanum lycopersicum. Plant Cell Rep 30:2059–2073

    Article  CAS  PubMed  Google Scholar 

  • **ng H, Pudake RN, Guo G, **ng G, Hu Z, Zhang Y, Sun Q, Ni Z (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genom 12:178

    Article  CAS  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A1A09060925).

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Correspondence to Gyuhwa Chung.

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Bao Le, Muhammad Amjad Nawaz, Hafiz Mamoon Rehman, Thu Le, Seung Hwan Yang, Kirill S. Golokhvast, Eunho Son and Gyuhwa Chung declares that they have no conflict of interest.

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Le, B., Nawaz, M.A., Rehman, H.M. et al. Genome-wide characterization and expression pattern of auxin response factor (ARF) gene family in soybean and common bean. Genes Genom 38, 1165–1178 (2016). https://doi.org/10.1007/s13258-016-0462-y

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