Overdominant quantitative trait loci for yield and fitness in tomato

Abstract

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.heterosis ͉ hybrid vigor ͉ domestication ͉ reproductive barriers ͉ breeding

Biological consequences of dosage dependent gene regulatory systems

“…The genetic and molecular basis of heterosis has eluded a consensus (32). However, recently an exhaustive study of introgression lines of overlapping portions of a wild tomato genome into domesticated tomato has suggested that the heterotic response results from so-called overdominant QTL (33). In other words, heterozygosity for the introgressed segment of the genome produced a response that was superior to homozygous lines of the respective introgressed line or of domesticated tomato itself.…”

Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models

“…Heterosis has been traditionally attributed to new heterozygous combinations with dominant effects created by the hybridization of genetically divergent parents. As heterosis is conditioned by dominant effects, it is expected to be seen more often with fitness-related traits than with traits that respond well to selection (Semel et al, 2006). Despite the importance of this phenomenon for agriculture and research on the subject that dates back more than 100 years (Darwin, 1876;Bruce, 1910;Jones, 1917), our understanding of the genetic basis for the manifestation of heterosis is still incomplete (Lippman and Zamir, 2007;Charlesworth and Willis, 2009;Baranwal et al, 2012;Schnable and Springer, 2013).…”

“…There are a few models, all involving dominant effects, that explain how different genetic constellations of heterozygous loci can improve the performance of a hybrid as compared with its divergent homozygous parents (Xiao et al, 1995;Lippman and Zamir, 2007). Although many studies in plants have favored one model or another Luo et al, 2001;Semel et al, 2006), other studies have indicated that a combination of a few models is needed to explain the genetic basis underlying heterosis (Yao et al, 2012;Guo et al, 2013;Schnable and Springer, 2013).…”

Genetic composition of yield heterosis in an elite rice hybrid

“…Although there have been a large number of genetic analyses in plants with results favoring one hypothesis or another (18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31), genetic composition pertaining to heterotic performance of crop hybrids has not been fully characterized in an experimental population. There has been no assessment about the relative contributions of these genetic components to heterosis in a crop hybrid.…”