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A novel mutation in TFL1 homolog affecting determinacy in cowpea (Vigna unguiculata)

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Abstract

Mutations in the widely conserved Arabidopsis Terminal Flower 1 (TFL1) gene and its homologs have been demonstrated to result in determinacy across genera, the knowledge of which is lacking in cowpea. Understanding the molecular events leading to determinacy of apical meristems could hasten development of cowpea varieties with suitable ideotypes. Isolation and characterization of a novel mutation in cowpea TFL1 homolog (VuTFL1) affecting determinacy is reported here for the first time. Cowpea TFL1 homolog was amplified using primers designed based on conserved sequences in related genera and sequence variation was analysed in three gamma ray-induced determinate mutants, their indeterminate parent “EC394763” and two indeterminate varieties. The analyses of sequence variation exposed a novel SNP distinguishing the determinate mutants from the indeterminate types. The non-synonymous point mutation in exon 4 at position 1,176 resulted from transversion of cytosine (C) to adenine (A) leading to an amino acid change (Pro-136 to His) in determinate mutants. The effect of the mutation on protein function and stability was predicted to be detrimental using different bioinformatics/computational tools. The functionally significant novel substitution mutation is hypothesized to affect determinacy in the cowpea mutants. Development of suitable regeneration protocols in this hitherto recalcitrant crop and subsequent complementation assay in mutants or over-expressing assay in parents could decisively conclude the role of the SNP in regulating determinacy in these cowpea mutants.

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References

  • Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Adzhube PIA, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248–249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alvarez J, Guli CL, Yu XH, Smyth DR (1992) Terminal flower: a gene affecting inflorescence development in Arabidopsis thaliana. Plant J 2:103–116

    Article  Google Scholar 

  • Banfield MJ, Brady RL (2000) The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297:1159–1170

    Article  CAS  PubMed  Google Scholar 

  • Bendl J, Stourac J, Salanda O, Pavelka A, Wieben ED, Zendulka J, Brezovsky J, Damborsky J (2014) PredictSNP: robust and accurate consensus classifier for prediction of disease-related mutations. PLoS Comput Biol 10:e1003440. doi:10.1371/journal.pcbi.1003440

    Article  PubMed Central  PubMed  Google Scholar 

  • Berezin C, Glaser F, Rosenberg J, Paz I, Pupko T, Fariselli P, Casadio R, Ben-Tal N (2004) ConSeq: the identification of functionally and structurally important residues in protein sequences. Bioinformatics 20:1322–1324

    Article  CAS  PubMed  Google Scholar 

  • Bernard RL (1972) Two genes affecting stem termination in soybeans. Crop Sci 12:235–239

    Article  Google Scholar 

  • Boote KJ, Jones JW, Batchelor WD, Nafziger ED, Myers O (2003) Genetic coefficients in the CROPGRO-soybean model: links to field performance and genomics. Agron J 95:32–51

    Article  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inflorescence architecture in Antirrhinum. Nature 379:791–797

    Article  CAS  PubMed  Google Scholar 

  • Capriotti E, Fariselli P, Casadio R (2004) A neural network-based method for predicting protein stability changes upon single point mutations. In: Proceedings of the 2004 conference on intelligent systems for molecular biology (ISMB04), Bioinformatics (Suppl. 1), vol 20. Oxford University Press, New York, pp 190–201

  • Capriotti E, Fariselli P, Casadio R (2005) I-Mutant2.0: predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Res 33:W306–W310. doi:10.1093/nar/gki375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng J, Randall A, Baldi P (2006) Prediction of protein stability changes for single site mutations using support vector machines. Proteins: structure, function. Bioinformatics 62:1125–1132

    CAS  Google Scholar 

  • Cober E, Tanner J (1995) Performance of related indeterminate and tall determinate soybean lines in short-season areas. Crop Sci 35:361–364

    Article  Google Scholar 

  • Coen ES (1991) The role of homeotic genes in flower development and evolution. Annu Rev Plant Phys 42:241–279

    Article  Google Scholar 

  • Dehouck Y, Grosfils A, Folch B, Gilis D, Bogaerts P, Rooman M (2009) Fast and accurate predictions of protein stability changes upon mutations using statistical potentials and neural networks: poPMuSiC-2.0. Bioinformatics 25:2537–2543. doi:10.1093/bioinformatics/btp445

    Article  CAS  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Dhanasekar P, Dhumal KN, Reddy KS (2010) Identification of RAPD marker linked to plant type gene in pigeonpea. Ind J Biotechnol 9:58–63

    CAS  Google Scholar 

  • Flanagan SE, Patch AM, Ellard S (2010) Using SIFT and PolyPhen to predict loss-of-function and gain-of-function mutations. Genet Test Mol Biomark 14:533–537

    Article  CAS  Google Scholar 

  • Foucher F, Morin J, Courtiade J, Cadioux S, Ellis NI, Banfield MJ, Rameau C (2003) Determinate and late flowering are two Terminal Flower 1/Centroradialis homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15:2742–2754

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanano S, Goto K (2011) Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time and inflorescence development through transcriptional repression. Plant Cell 23:3172–3184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. PNAS 102:7748–7753

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Henikoff S, Comai L (2003) Single nucleotide mutations for plant functional genomics. Annu Rev Plant Biol 54:375–401

    Article  CAS  PubMed  Google Scholar 

  • Julio E, Laporte F, Reis S, Rothan C, de Borne FD (2008) Reducing the content of nornicotine in tobacco via targeted mutation breeding. Mol Breed 21:369–381

    Article  CAS  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965

    Article  CAS  PubMed  Google Scholar 

  • Kelly JD (2001) Remaking bean plant architecture for efficient production. Adv Agron 71:109–143

    Article  Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962

    Article  CAS  PubMed  Google Scholar 

  • Koinange EMK, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common bean. Crop Sci 36:1037–1045

    Article  Google Scholar 

  • Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073–1081

    Article  CAS  PubMed  Google Scholar 

  • Kwak M, Toro O, Debouck DG, Gepts P (2012) Multiple origins of the determinate growth habit in deomesticated common bean (Phaseolus vulgaris). Ann Bot 110:1573–1580

    Article  PubMed Central  PubMed  Google Scholar 

  • Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P (2009) Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 25:2744–2750

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McCallum CM, Slade AJ, Colbert TG, Knauf VC, Hurst S (2008) Tomatoes having reduced polygalacturonase activity caused by non-transgenic mutations in the polygalacturonase gene. US Patent 7.393.996

  • McGarry RC, Ayre BG (2012) Manipulating plant architecture with members of the CETS gene family. Plant Sci 188–189:71–81

    Article  PubMed  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oshima S, Murata M, Sakamoto W, Ogura F, Motoyoshi F (1997) Cloning and molecular analysis of the Arabidopsis gene Terminal Flower 1. Mol Gen Genet 254:186–194

    Article  Google Scholar 

  • Pandey RN, Dhanasekar P (2003) Radiation-induced high yielding determinate mutant in cowpea. In: Henri A, Kumar D, Singh NB (eds) Advances in arid legumes research. Scientific Publishers, Jodhpur (India), pp 30–33

    Google Scholar 

  • Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566

    Article  CAS  PubMed  Google Scholar 

  • Pidkowich MS, Klenz JE, Haughn GW (1999) The making of a flower: control of floral meristem identity in Arabidopsis. Trends Plant Sci 4:64–70

    Article  PubMed  Google Scholar 

  • Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989

    CAS  PubMed  Google Scholar 

  • Pnueli L, Gutfinger T, Hareven D, Ben-Naim O, Ron N, Adir N, Lifschitz E (2001) Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13:2687–2702

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpeneter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615

    CAS  PubMed  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Shirasawa K, Takahashi Y, Nishimura M, Nishio T (2006) Mutant selection from progeny of gamma-ray-irradiated rice by DNA heteroduplex cleavage using Brassica petiole extract. Breed Sci 56:179–183

    Article  CAS  Google Scholar 

  • Schultz EA, Haughn GW (1993) Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development 119:745–765

    CAS  Google Scholar 

  • Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • So Yeon Y, Kardailsky I, JongSeob L, Weigel D, JiHoon A (2004) Acceleration of flowering by overexpression of MFT (Mother of FT and TFL1). Mol Cells 17:95–101

    Google Scholar 

  • Tahery Y, Abhul-Hamid H, Tahery E (2011) Terminal Flower 1 (TFL1) homolog genes in dicot plants. World Appl Sci J 12(545):551

    Google Scholar 

  • Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13:2129–2141

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas PD, Kejariwal A, Guo N, Mi H, Campbell MJ, Muguganujan A, Lazareva-Ulitsky B (2006) Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools. Nucleic Acids Res 34:W645–W650. doi:10.1093/nar/gkl229

    Article  PubMed Central  PubMed  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 Central  PubMed  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Dr. (Mrs.) Archana Joshi Saha, BARC, for her guidance in cloning and Mr. Pandarinath Thokal, BARC, for the technical help rendered during the course of the experiment.

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  1. Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, 400 085, India

    P. Dhanasekar & K. S. Reddy

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  1. P. Dhanasekar
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  2. K. S. Reddy
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Correspondence to P. Dhanasekar.

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Communicated by R.K. Varshney.

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Dhanasekar, P., Reddy, K.S. A novel mutation in TFL1 homolog affecting determinacy in cowpea (Vigna unguiculata). Mol Genet Genomics 290, 55–65 (2015). https://doi.org/10.1007/s00438-014-0899-0

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  • DOI: https://doi.org/10.1007/s00438-014-0899-0

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