Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Abstract

The ubiquity of nonparental hybrid phenotypes, such as hybrid vigor and hybrid inferiority, has interested biologists for over a century and is of considerable agricultural importance. Although examples of both phenomena have been subject to intense investigation, no general model for the molecular basis of nonadditive genetic variance has emerged, and prediction of hybrid phenotypes from parental information continues to be a challenge. Here we explore the genetics of hybrid phenotype in 435 Arabidopsis thaliana individuals derived from intercrosses of 30 parents in a half diallel mating scheme. We find that nonadditive genetic effects are a major component of genetic variation in this population and that the genetic basis of hybrid phenotype can be mapped using genome-wide association (GWA) techniques. Significant loci together can explain as much as 20% of phenotypic variation in the surveyed population and include examples that have both classical dominant and overdominant effects. One candidate region inherited dominantly in the half diallel contains the gene for the MADS-box transcription factor AGAMOUS-LIKE 50 (AGL50), which we show directly to alter flowering time in the predicted manner. Our study not only illustrates the promise of GWA approaches to dissect the genetic architecture underpinning hybrid performance but also demonstrates the contribution of classical dominance to genetic variance.T he often observed phenotypic superiority of progeny relative to their parents, or heterosis, is a universal phenomenon and of great importance to plant agriculture. The earliest description of heterosis (also known as hybrid vigor or superiority) dates to Darwin's studies of cross-fertilization in plants. He noticed that intercrossing distantly related individuals gave rise to larger, more vigorous progeny (1). Four decades later, George Shull coined the term "heterosis" (2) for this phenomenon, which he and Edward East had independently described for hybrids of inbred maize in 1908 (3, 4). Heterosis has long been of interest to evolutionary biologists as a potential explanation for the ubiquity of cross-fertilization in plants and animals, but it is also a central component of agricultural breeding programs. The combination of hybrid seed technology and inbred line improvement has driven an unprecedented improvement in maize yield over the past century (5). Despite the economic importance of heterosis and its intensive investigation in a wide spectrum of species, prediction of hybrid performance from parental information remains a major challenge (6).In the terms of quantitative genetics, hybrid vigor (and its opposite, inferiority) describes a deviation of progeny from the phenotypic mean of the parents. This means that heterosis cannot be explained by the addition of the effects of contributing alleles (7). Nonadditive genetic variance can result from a nonlinear phenotypic effect of alleles at one locus, as in the case of dominant/recessive allele pairs in classical genetics, or from epistatic interactions ...

Genomic architecture of biomass heterosis in Arabidopsis

“…30 accessions, which reported multiple heterosis-associated loci and candidate genes for flowering time and rosette traits (31). It is likely that the Arabidopsis hybrid populations used for GWAS were derived from different experimental designs and were different in scale.…”

“…To date, few genetic loci associated with heterosis have been identified through QTL mapping in Arabidopsis (28)(29)(30). Remarkably, a recent GWAS performed in Arabidopsis hybrids, generated by intercrossing 30 accessions, discovered significant loci and candidate genes for hybrid performance in flowering time and rosette traits (31), which demonstrated the feasibility of GWAS to dissect the genetic architecture of heterosis in Arabidopsis. However, in this case, limited genetic loci can be detected because sequence divergence among 30 accessions represented only a small proportion of the natural genetic variation in Arabidopsis.…”

Genetic relatedness and the ratio of subpopulation‐common alleles are related in genomic prediction across structured subpopulations in maize

“…The number of markers incorporated into the GBLUP model ranged from 100 to 3,500, with an increasing of 100. For each set of markers, PVC was calculated using the following the formula (Seymour et al, ):where y validate was the BLUP data of the validation population, was the estimated phenotype of the validation population calculated using GBLUP model. For each marker set, the PVC values along with PA were also calculated with 100 five‐fold CVs.…”

easyGWAS: A Cloud-Based Platform for Comparing the Results of Genome-Wide Association Studies

“…For Arabidopsis, data sets from various studies have been integrated (Atwell et al, 2010;Cao et al, 2011;Horton et al, 2012;Long et al, 2013;Schmitz et al, 2013;1001Genomes Consortium, 2016Seymour et al, 2016). The first data set (AtPolyDB) includes 1307 worldwide Arabidopsis accessions with a total of 214,051 SNPs genotyped with a 250k SNP chip .…”

“…Third, we included 1135 samples and 6,973,565 nonsingleton SNPs (1001 Genomes Data) from the final phase of the 1001 Genomes Project (1001Genomes Consortium, 2016. Lastly, we included 372 in silico F1 hybrid genotypes generated from parental genome sequences (Cao et al, 2011) with a total of 204,753 SNPs (Seymour et al, 2016). We also integrated the TAIR9 and TAIR10 gene annotation sets.…”