Overdominant quantitative trait loci for yield and fitness in tomato

Heterosis, or hybrid vigor, is a major genetic force that contributes to world food production. The genetic basis of heterosis is not clear, and the importance of loci with overdominant (ODO) effects is debated. One problem has been the use of whole-genome segregating populations, where interactions often mask the effects of individual loci. To assess the contribution of ODO to heterosis in the absence of epistasis, we carried out quantitative genetic and phenotypic analyses on a population of tomato (Solanum lycopersicum) introgression lines (ILs), which carry single marker-defined chromosome segments from the distantly related wild species Solanum pennellii. The ILs revealed 841 quantitative trait loci (QTL) for 35 diverse traits measured in the field on homozygous and heterozygous plants. ILs showing greater reproductive fitness were characterized by the prevalence of ODO QTL, which were virtually absent for the nonreproductive traits. ODO can result from true ODO due to allelic interactions of a single gene or from pseudoODO that involves linked loci with dominant alleles in repulsion. The fact that we detected dominant and recessive QTL for all phenotypic categories but ODO only for the reproductive traits indicates that pseudoODO due to random linkage is unlikely to explain heterosis in the ILs. Thus, we favor the true ODO model involving a single functional Mendelian locus. We propose that the alliance of ODO QTL with higher reproductive fitness was selected for in evolution and was domesticated by man to improve yields of crop plants.

[1]  J. Mallet Hybridization as an invasion of the genome. , 2005, Trends in ecology & evolution.

[2]  A. Isogai,et al.  Self-incompatibility in plants. , 2005, Annual review of plant biology.

[3]  J. Molofsky,et al.  Extinction dynamics in experimental metapopulations. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  L. Moyle,et al.  Genetics of Hybrid Incompatibility Between Lycopersicon esculentum and L. hirsutum , 2005, Genetics.

[5]  D. Pomp,et al.  A large-sample QTL study in mice: III. Reproduction , 2004, Mammalian Genome.

[6]  Gordon Luikart,et al.  The alluring simplicity and complex reality of genetic rescue. , 2004, Trends in ecology & evolution.

[7]  D. Zamir,et al.  Unused Natural Variation Can Lift Yield Barriers in Plant Breeding , 2004, PLoS biology.

[8]  P. Ranjekar,et al.  Use of DNA Markers in Prediction of Hybrid Performance and Heterosis for a Three-Line Hybrid System in Rice , 2001, Biochemical Genetics.

[9]  D. Pomp,et al.  A large-sample QTL study in mice: I. Growth , 2004, Mammalian Genome.

[10]  D. Pomp,et al.  A large-sample QTL study in mice: II. Body composition , 2004, Mammalian Genome.

[11]  James A. Birchler,et al.  In Search of the Molecular Basis of Heterosis , 2003, The Plant Cell Online.

[12]  R. Bernardo,et al.  Genetic basis of heterosis explored by simple sequence repeat markers in a random-mated maize population , 2003, Theoretical and Applied Genetics.

[13]  H. Fu,et al.  Intraspecific violation of genetic colinearity and its implications in maize , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Daniel R. Richards,et al.  Dissecting the architecture of a quantitative trait locus in yeast , 2002, Nature.

[15]  A. Paterson,et al.  Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. , 2001, Genetics.

[16]  A. Paterson,et al.  Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. , 2001, Genetics.

[17]  M. Arnold,et al.  Genetics and the fitness of hybrids. , 2001, Annual review of genetics.

[18]  D. Duvick Biotechnology in the 1930s: the development of hybrid maize , 2001, Nature Reviews Genetics.

[19]  Michele R. Dudash,et al.  Genetics underlying inbreeding depression in Mimulus with contrasting mating systems , 1998, Nature.

[20]  Cai-guo Xu,et al.  Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Zamir,et al.  An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. , 1995, Genetics.

[22]  J Li,et al.  Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. , 1995, Genetics.

[23]  M. Kearsey,et al.  The genetic architecture of body weight and egg hatchability in Drosophila melanogaster. , 1967, Genetics.

[24]  D. Sundland Inbreeding and outbreeding. , 1966, The American psychologist.

[25]  J. Crow Alternative Hypotheses of Hybrid Vigor. , 1948, Genetics.

[26]  A. Bruce THE MENDELIAN THEORY OF HEREDITY AND THE AUGMENTATION OF VIGOR. , 1910, Science.