Skip to main content
Log in

The Role of epistasis in controlling seed yield and other agronomic traits in an Andean × Mesoamerican cross of common bean (Phaseolus vulgaris L.)

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Epistasis is a pervasive phenomenon in biology. Nevertheless, attempts at identifying epistatic interactions with quantitative trait loci (QTL) analyses have yielded inconsistent results. In this study, we attempt to determine the genetic control of outbreeding depression and the possible role of epistasis following a wide cross in common bean (Phaseolus vulgaris L.). A recombinant inbred population, derived from a cross between Andean and Mesoamerican common bean cultivars, was evaluated in two markedly contrasting environments. A low-density linkage map based on AFLPs was used to locate QTLs for the number of days to maturity, average daily biomass and seed yield accumulation, and harvest index. Both independently acting and digenic epistatic QTLs of similar magnitude were identified. A majority of the loci involved in these epistatic interactions did not have an independent effect. Although we did find evidence for strong epistatic control of the traits investigated, we also found, in contrast to other recent studies, that there was no evidence for a bias toward coadapted gene complexes at the level of digenic epistasis. We discuss these results in relation to the role of epistasis in the evolutionary history of the species and methodological difficulties in detecting epistasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adam-Blondon, A., M. Sévignac, H. Bannerot & M. Dron, 1994. SCAR, RAPD and RFLP markers tightly linked to a dominant gene (Are) conferring resistance to anthracnose in common bean. Theor Appl Genet 88: 865–870.

    Article  CAS  Google Scholar 

  • Avery, L. & S. Wasserman, 1993. Ordering gene function: the interpretation of epistasis in regulatory hierarchies. Trends Genet 8: 312–316.

    Google Scholar 

  • Cheverud, J. & E. Routman, 1996. Epistasis as a source of increased additive genetic variance at population bottlenecks. Evolution 50: 1042–1051.

    Article  Google Scholar 

  • Dobzhansky, T., 1937. Genetics and the Origin of Species. Columbia Univ. Press, New York.

    Google Scholar 

  • Doerge, R. & A. Rebai, 1996. Significance thresholds for QTL interval mapping tests. Heredity 76: 459–464.

    Google Scholar 

  • Edwards, M., T. Helentjaris, S. Wright & C. Stuber, 1992. Molecular-marker facilitated investigations of quantitative trait loci in maize. 4. Analysis based on genome saturation with isozyme and restriction fragment length polymorphism markers. Theor Appl Genet 83: 765–774.

    Article  CAS  Google Scholar 

  • Eshed, Y. & D. Zamir, 1995. An introgression line population of Lycoperison pennellii in the cultivated tomato enables the identi-fication and fine mapping of yield-associated QTL. Genetics 141: 1147–1162.

    PubMed  CAS  Google Scholar 

  • Eshed, Y. & D. Zamir, 1996. Less-than-additive epistatic interactions of quantitative trait loci in tomato. Genetics 143: 1807–1817.

    PubMed  CAS  Google Scholar 

  • Feinberg, A.P. & B. Vogelstein, 1984. Addendum: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Analyt Biochem 137: 266–267.

    Article  PubMed  CAS  Google Scholar 

  • Fenster, C., L. Galloway & L. Chao, 1997. Epistasis and its consequences for the evolution of natural populations. Trends Ecol Evol 12: 282–286.

    Article  Google Scholar 

  • Frankel, W. & N. Schork, 1996. Who's afraid of epistasis? Nature Genetics 14: 371–373.

    Article  PubMed  CAS  Google Scholar 

  • Freyre, R., P. Skroch, V. Geffroy, A.-F. Adam-Blondon, A. Shirmohamadali, W. Johnson, V. Llaca, R. Nodari, P. Pereira, S.-M. Tsai, J. Tohme, M. Dron, J. Nienhuis, C. Vallejos, & P. Gepts, 1998. Towards an integrated linkage map of common bean. 4. Development of a core map and alignment of RFLP maps. Theor Appl Genet 97: 847–856.

    Article  CAS  Google Scholar 

  • Gepts, P., 1993. The use of molecular and biochemical markers in crop evolution studies. Evol Biol 27: 51–94.

    Google Scholar 

  • Gepts, P., 1998. Origin and evolution of common bean: past events and recent trends. HortScience 33: 1124–1130.

    Google Scholar 

  • Gepts, P. & F.A. Bliss, 1985. F1 hybrid weakness in the common bean: differential geographic origin suggests two gene pools in cultivated bean germplasm. J Hered 76: 447–450.

    Google Scholar 

  • Gepts, P., V. Llaca, R.O. Nodari & L. Panella, 1992. Analysis of seed proteins, isozymes, and RFLPs for genetic and evolutionary studies in Phaseolus. In: H.-F. Linskens & J.F. Jackson (Eds.), Modern Methods of Plant Analysis (New Series): Seed Analysis, pp. 63–93. Springer, Berlin.

    Google Scholar 

  • Gepts, P., T.C. Osborn, K. Rashka & F.A. Bliss, 1986. Phaseolinprotein variability in wild forms and landraces of the common bean (Phaseolus vulgaris): evidence for multiple centers of domestication. Econ Bot 40: 451–468.

    CAS  Google Scholar 

  • Greenfield, A. & P. Koopman, 1996. SRY and mammalian sex determination. Curr Topics Dev Biol 34: 1–23.

    CAS  Google Scholar 

  • Hanson, M., B. Gaut, A. Stec, S. Fuerstenberg, M. Goodman, E. Coe & J. Doebley, 1996. Evolution of anthocyanin biosynthesis in maize kernels: the role of regulatory and enzymatic loci. Genetics 143: 1395–1407.

    PubMed  CAS  Google Scholar 

  • Holland, J., H. Moser, L. O'Donoghue & M. Lee, 1997. QTLs and epistasis associated with vernalization responses in oat. Crop Sci 37: 1306–1316.

    Article  Google Scholar 

  • Howell, P., D. Marshall & D. Lydiate, 1996. Towards developing intervarietal substitution lines in Brassica napus using markerassisted selection. Genome 39: 348–358.

    CAS  PubMed  Google Scholar 

  • Hutter, P., 1997. Genetics of hybrid inviability in Drosophila. Adv Genet 36: 157–185.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, W., 1997. Improving the Efficiency of Common Bean (Phaseolus vulgaris L.) Breeding Programs Using Molecular Markers. PhD dissertation, University of California, Davis.

    Google Scholar 

  • Johnson, W. & P. Gepts, 1999. Segregation for performance in recombinant inbred populations resulting from inter-gene pool crosses of common bean (Phaseolus vulgaris L). Euphytica 106.

  • Johnson, W., P. Guzmán, D. Mandala, A. Mkandawire, S. Temple, R. Gilbertson & P. Gepts, 1997. Molecular tagging of the bc-3 gene for introgression into Andean common bean. Crop Sci 37: 248–254.

    Article  CAS  Google Scholar 

  • Koenig, R. & P. Gepts, 1989. Allozyme diversity in wild Phaseolus vulgaris: further evidence for two major centers of diversity. Theor Appl Genet 78: 809–817.

    Google Scholar 

  • Koinange, E.M.K. & P. Gepts, 1992. Hybrid weakness in wild Phaseolus vulgaris L. J Hered 83: 135–139.

    Google Scholar 

  • Koornneef, M., C. Alonso-Blanco, H. Blankestijn-de Vries, C.J. Hanhart & A.J.M. Peeters, 1998. Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148: 885–892.

    PubMed  CAS  Google Scholar 

  • Kornegay, J., J.W. White & O.O. De la Cruz, 1992. Growth habit and gene pool effects on inheritance of yield in common bean. Euphytica 62: 171–180.

    Article  Google Scholar 

  • Lander, E.S., P. Green, J. Abrahamson, A. Barlow, M. Daly, S.E. Lincoln & L. Newburg, 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174–181.

    Article  PubMed  CAS  Google Scholar 

  • Leakey, C.L.A., 1988. Genotypic and phenotypic variation in common bean. In: P. Gepts, (Ed.), Genetic Resources of Phaseolus Beans, pp. 245–327. Kluwer, Dordrecht, the Netherlands.

    Google Scholar 

  • Li, Z., S. Pinson, W. Park, A. Paterson & J. Stansel, 1997. Epistasis for three grain yield components in rice (Oryza sativa L.). Genetics 145: 453–465.

    PubMed  CAS  Google Scholar 

  • Li, Z., S. Pinson, J. Stansel & W. Park, 1995. Identification of QTL for heading date and plant height in rice using RFLP markers. Theor Appl Genet 91: 374–381.

    CAS  Google Scholar 

  • Li, Z., S. Pinson, J. Stansel & W. Park, 1995. Characterization of quantitative trait loci contributing to field resistance to sheath blight (Rhizoctonia solani) in rice. Theor Appl Genet 91: 382–388.

    CAS  Google Scholar 

  • Long, A., S. Mullaney, L. Reid, J. Fry, C. Langley & T. Mackay, 1995. High resolution mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics 139: 1273–1291.

    PubMed  CAS  Google Scholar 

  • Lynch, M., 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622–629.

    Article  Google Scholar 

  • Ma, Y. & F.A. Bliss, 1978. Seed proteins of common bean. Crop Sci 17: 431–437.

    Article  Google Scholar 

  • Mayr, E., 1963. Animal Species and Evolution. Columbia Univ. Press, New York.

    Google Scholar 

  • Menéndez, C., A. Hall & P. Gepts, 1997. A genetic linkage map of cowpea (Vigna unguiculata) developed from a cross between two inbred, domesticated lines. Theor Appl Genet 95: 1210–1217.

    Article  Google Scholar 

  • Merlot, S. & J. Giraudat, 1997. Genetic analysis of abscisic acid signal transduction. Plant Phys 114: 751–757.

    Article  CAS  Google Scholar 

  • Muller, H., 1940. Bearing of the Drosophila work on systematics. In: J. Huxley (Ed.), The New Systematics, pp. 185–268. Clarendon, Oxford.

    Google Scholar 

  • Nodari, R.O., 1992. Towards an integrated linkage map of common bean (Phaseolus vulgaris L.). PhD dissertation, University of California, Davis.

    Google Scholar 

  • Nodari, R.O., S.M. Tsai, R.L. Gilbertson & P. Gepts, 1993. Towards an integrated linkage map of common bean. II. Development of an RFLP-based linkage map. Theor Appl Genet 85: 513–520.

    Article  CAS  Google Scholar 

  • Nodari, R.O., S.M. Tsai, P. Guzmán, R.L. Gilbertson & P. Gepts, 1993. Towards an integrated linkage map of common bean. 3. Mapping genetic factors controlling host-bacteria interactions. Genetics 134: 341–350.

    PubMed  CAS  Google Scholar 

  • Orr, H., 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805–1813.

    PubMed  CAS  Google Scholar 

  • Paterson, A.H., S. Damon, J.D. Hewitt, D. Zamir, H.D. Rabinowitch, S.E. Lincoln, E.S. Lander & S.D. Tanksley, 1991. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. Genetics 127: 181–197.

    PubMed  CAS  Google Scholar 

  • Patiño, H. & S. Singh, 1989. Visual selection for seed yield in the F2 and F3 generations of nine common bean crosses. Annu Rept Bean Improv Coop 32: 79–89.

    Google Scholar 

  • Ramsay, L., D. Jennings, E. Bohuon, A. Arthur, D. Lydiate, M. Kearsey & D. Marshall, 1996. The construction of a substitution library of recombinant backcross lines in Brassica oleracea for the precision mapping of quantitative trait loci. Genome 39: 558–567.

    CAS  PubMed  Google Scholar 

  • SAS, 1988. SAS/STAT User's Guide, Release 6.03 Edition. SAS Institute, Cary, NC.

    Google Scholar 

  • Shii, C.T., M.C. Mok, S.R. Temple & D.W.S. Mok, 1980. Expression of developmental abnormalities in hybrids of Phaseolus vulgaris L. J Hered 71: 218–222.

    Google Scholar 

  • Singh, S. & A. Molina, 1996. Inheritance of crippled trifoliolate leaves occurring in interracial crosses of common bean and its relationship with hybrid dwarfism. J Hered 87: 464–469.

    Google Scholar 

  • Singh, S.P., C. Cajiao, J.A. Gutiérrez, J. García, M.A. Pastor-Corrales & F.J. Morales, 1989. Selection for seed yield in inter-gene pool crosses of common bean. Crop Sci 29: 1126–1131.

    Article  Google Scholar 

  • Singh, S.P., P. Gepts & D.G. Debouck, 1991. Races of common bean (Phaseolus vulgaris L., Fabaceae). Econ Bot 45: 379–396.

    Google Scholar 

  • Sprecher, S. & M. Khairallah, 1989. Association of male sterility with gene pool recombinants in bean. Annu Rept Bean Improv Coop 32: 56–67.

    Google Scholar 

  • Tanksley, S., 1993. Mapping polygenes. Annu Rev Genet 27: 205–233.

    Article  PubMed  CAS  Google Scholar 

  • Templeton, A.R., 1981. Mechansisms of speciation - a population genetic approach. Annu Rev Ecol Syst 12: 23–48.

    Article  Google Scholar 

  • Tinker, N., 1996. MQTL documentation, version 0.98, ftp://gnome.agrenv.mcgill.ca/pub/genetics/software/MQTL/ mqtl.beta098/mqtl.doc.

  • Tinker, N. & D. Mather, 1995. Methods for QTL with progeny replicated in multiple environments. J Quant Trait Loci 1: http://probe.nalusda.gov:8000/otherdocs/jqtl/jqtl199501/ jqtl199515.html.

  • Tinker, N. & D. Mather, 1995. MQTL: software for simplified composite interval mapping of QTL in multiple environments. J Quant Trait Loci 1: http://probe.nalusda.gov:8000/otherdocs/jqtl/jqtl1995- 8002/jqtl8016r8002.html.

  • Vallejos, E.C., N.S. Sakiyama & C.D. Chase, 1992. A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131: 733–740.

    PubMed  CAS  Google Scholar 

  • Vos, P., R. Hogers, M. Bleeker, M., Reijans, T. Van de Lee, M. Hornes, A. Frijters, J. Pot, J., Peleman, M. Kuiper & M. Zabeau, 1995. AFLP: a new technique for DNA fingerprinting. Nucl Ac Res 23: 4407–4414.

    CAS  Google Scholar 

  • Welsh, W., W. Bushuk, W. Roca & S.P. Singh, 1995. Characterization of agronomic traits and markers of recombinant inbred lines from intra-and interracial populations of Phaseolus vulgaris L. Theor Appl Genet 91: 169–177.

    Article  Google Scholar 

  • Whitlock, M., P. Phillips, F. Moore & S. Tonsor, 1995. Multiple fitness peaks and epistasis. Ann Rev Ecol Syst 26: 601–629.

    Article  Google Scholar 

  • Williams, J.G.K., A.R. Kubelik, K.J. Livak, J.A. Rafalski & S.V. Tingey, 1990. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucl Ac Res 18: 6531–6535.

    CAS  Google Scholar 

  • Wright, S., 1968. Evolution and the Genetics of Populations. University of Chicago Press, Chicago.

    Google Scholar 

  • Yu, S., J. Li, C. Xu, Y. Tan, Y., Gao, X. Li, Q. Zhang & M. Saghai Maroof, 1997. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94: 9226–9231.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, W.C., Gepts, P. The Role of epistasis in controlling seed yield and other agronomic traits in an Andean × Mesoamerican cross of common bean (Phaseolus vulgaris L.). Euphytica 125, 69–79 (2002). https://doi.org/10.1023/A:1015775822132

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1015775822132

Navigation