Abstract
In a common bean plant exhibiting determinate growth, the terminal shoot meristem switches from a vegetative to reproductive state, resulting in a terminal inflorescence. Contrary to this, indeterminate growth habit results in a terminal meristem that remains vegetative where it further regulates the production of lateral vegetative and reproductive growth. In the last century, breeders have selected determinate growth habit, in combination with photoperiod insensitivity, to obtain varieties with a shorter flowering period, earlier maturation and ease of mechanized harvest. Previous work has identified TFL1 as a gene controlling determinate growth habit in Arabidopsis thaliana. In this work, we have validated that the Phaseolus vulgaris candidate gene, PvTFL1y, is the functional homolog of TFL1 using three independent lines of evidence. First, in a population of ~1,500 plants, PvTFL1y was found to co-segregate with the phenotypic locus for determinate growth habit (fin) on chromosome 01. Second, using quantitative PCR, we found that two unique haplotypes associated with determinacy at the PvTFL1y locus, a 4.1-kb retrotransposon and a splice-site mutation, cause mRNA abundance to decrease 20–133 fold, consistent with the recessive nature of fin. Finally, using a functional complementation approach, through Agrobacterium-mediated transformation of determinate Arabidopsis, we rescued tfl1-1 mutants with the wild-type PvTFL1y gene. Together, these three lines of evidence lead to the conclusion that PvTFL1y is the functional homolog of the Arabidopsis gene, TFL1, and is the gene responsible for naturally occurring variation for determinacy in common bean. Further work exploring the different haplotypes at the PvTFL1y locus may lead to improved plant architecture and phenology of common bean cultivars.
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References
Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y et al (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056
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 25:605–614
Alvarez J, Guli CL, Yu X-H, Smyth DR (1992) Terminal flower: a gene affecting inflorescence development in Arabidopsis thaliana. Plant J 2:103–116
Bonfim K, Faria JC, Nogueira E, Mendes EA, Aragao FJL (2007) RNAi-mediated resistance to bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol Plant–Micr Inter 20:717–726
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
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510
Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen R (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83
Chen DH, Ronald PC (1999) A rapid DNA minipreparation method suitable for AFLP and other PCR applications. Plant Mol Biol Rep 17:53–57
Cober ER, Tanner JW (1995) Performance of related indeterminate and tall determinate soybean lines in short-season areas. Crop Sci 35:361–364
Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N et al (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15:2742–2754
Freyre R et al (1998) Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theor Appl Genet 97:847–856
Gepts P (1987) Characterizing plant phenology. In: Wisiol K, Hesketh J (eds) Plant growth modeling for resource management. CRC Press, Boca Raton, pp 3–24
Gepts P et al (2008) Genomics of Phaseolus beans, a major source of dietary protein and micronutrients in the tropics. In: Moore P, Ming R (eds) Genomics of tropical crop plants. Springer, New York, pp 113–143
Guo XZ, Zhao Z, Chen JH, Hu XH, Lou D (2006) A putative CENTRORADIALIS/TERMINAL FLOWER 1-like gene, Ljcen1, plays a role in phase transition in Lotus japonicus. J Plant Physiol 163:436–444
Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. PNAS 102:7748–7753
Huyghe C (1998) Genetics and genetic modifications of plant architecture in grain legumes: a review. Agronomie 18:383–411
Kelly JD (2001) Remaking bean plant architecture for efficient production. Adv Agron 71:109–143
Koinange EMS, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common-bean. Crop Sci 36:1037–1045
Kolkman JM, Kelly JD (2003) QTL conferring resistance and avoidance to white mold in common bean. Crop Sci 43:539–548
Kwak M (2008) Population structure and evolution of the determinacy gene (fin) during domestication in common bean (Phaseolus vulgaris L.). Dissertation, University of California, Davis
Kwak M, Velasco DM, Gepts P (2008) Mapping homologous sequences for determinacy and photoperiod sensitivity in common bean (Phaseolus vulgaris). J Hered 99:283–291
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2_DDCT method. Methods 25:402–408
Ma H (1998) To be, or not to be, a flower: a control of floral meristem identity. Trends Genet 14:26–32
Nilsson O, Lee I, Blazquez MA, Weigel D (1998) Flowering-time genes modulate the response to LEAFY activity. Genetics 150:403–410
Nocarova E, Fischer L (2009) Cloning of transgenic tobacco BY-2 cells; an efficient method to analyse and reduce high natural heterogeneity of transgene expression. BMC Plant Biol 9:44
Norton JB (1915) Inheritance of habit in the common bean. Am Nat 49:547–561
Ohshima S, Murata M, Sakamoto W, Ogura Y, Motoyoshi F (1997) Cloning and molecular analysis of the Arabidopsis gene Terminal Flower 1. Mol Gen Genet 254:186–194
Ojehomon OO, Morgan DG (1969) A quantitative study of inflorescence development in Phaseolus vulgaris. Ann Bot 33:325–332
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
Poncet V, Robert T, Sarr A, Gepts P (2004) Quantitative trait loci analyses of the domestication syndrome and domestication process. In: Goodman R (ed) Encyclopedia of plant and crop science. Marcel Dekker, New York, pp 1069–1073
Pröls F, Meyer P (1992) The methylation patterns of chromosomal integration regions influence gene activity of transferred DNA in Petunia hybrid. Plant J 2:465–475
Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892
Smartt J (1976) Comparative evolution of pulse crops. Euphytica 25:139–143
Tian Z, Wang X, Lee R, Li Y, Specht JE, Nelson RL, McClean PE, Qiu L, Ma J (2010) Artificial selection for determinate growth habit in soybean. PNAS 19:8563–8568
van Rheenen HA, Pundir RPS, Miranda JH (1994) Induction and inheritance of determinate growth habit in chickpea (Cicer arietinum L.). Euphytica 78:137–141
van Schoonhoven A, Pastor-Corrales MA (1987) Standard system for the evaluation of bean germplasm. CIAT, Cali
Waldia RS, Singh VP (1987) Inheritance of stem termination in Pigeon Pea (Cajanus cajan (L.) Mill sp.). Euphytica 36:525–527
Weigel D (1995) The genetics of flower development: from floral induction to ovule morphogenesis. Annu Rev Plant Physiol Plant Mol Biol 29:19–39
Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU et al (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059
Yanofsky MF (1995) Floral meristems to floral organs: genes controlling early events in Arabidopsis flower development. Annu Rev Plant Physiol Plant Mol Biol 46:167–188
Zambre M, Goossens A, Cardona C, Van Montagu M, Terryn N, Angenon G (2005) A reproducible genetic transformation system for cultivated Phaseolus acutifolius (tepary bean) and its use to assess the role of arcelins in resistance to the Mexican bean weevil. Theor Appl Genet 110:914–924
Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1(2):641–646
Acknowledgments
We thank Ohio State University Arabidopsis Biological Resource Center for supplying Arabidopsis seed samples. We also thank Drs. Tama Fox, David Gilchrist, James Lincoln, Juan P. Sanchez, as well as Joseph Ramahi and Diana Burkart-Waco for all of their thoughtful suggestions and scientific expertise as well as Drs. Carlos Quiros and Judy Jernstedt for comments on an earlier version of this paper. This work was supported by the USDA CSREES NRI Plant Genome program to PG, a Jastro-Shields Graduate Research Scholarship to SR and a UC Davis Department of Plant Science fellowship to MK.
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Communicated by R. Varshney.
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Repinski, S.L., Kwak, M. & Gepts, P. The common bean growth habit gene PvTFL1y is a functional homolog of Arabidopsis TFL1 . Theor Appl Genet 124, 1539–1547 (2012). https://doi.org/10.1007/s00122-012-1808-8
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DOI: https://doi.org/10.1007/s00122-012-1808-8