Analysis of a Triple Testcross Design With Recombinant Inbred Lines Reveals a Significant Role of Epistasis in Heterosis for Biomass-Related Traits in Arabidopsis

Kusterer, Barbara; Muminovic, J.; Utz, H. Friedrich; Piepho, Hans‐Peter; Barth, Susanne; Heckenberger, Martin; Meyer, Rhonda C.; Altmann, Thomas; Melchinger, Albrecht E.

doi:10.1534/genetics.106.069005

Cited by 72 publications

(81 citation statements)

References 30 publications

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“…On the other hand, Yu et al (1997), applying twoway analyses of variance using all possible pairwise combinations of marker genotypes to test epistasis, and Luo et al (2001) and Li et al (2001), using a mixed linear model with background variation control to map simultaneously main and epistatic effects, reported that epistasis is a common feature of most loci associated with inbreeding depression and heterosis in rice. In Arabidopsis Kusterer et al (2007a) found a significant role of epistasis in the expression of heterosis while analyzing generation means and variance components for biomass-related traits in a triple-testcross design with a recombinant inbred line population. Furthermore, in a study on QTL mapping in Arabidopsis using NIL libraries Melchinger et al (2007b) found about three times more loci with significant additive 3 additive epistatic interactions with the genetic background than with dominance effects.…”

Section: Discussionmentioning

confidence: 99%

Genetic Analysis of Heterosis for Yield and Yield Components in Rapeseed (Brassica napus L.) by Quantitative Trait Locus Mapping

2008

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The main objective in this research was the genetic analysis of heterosis in rapeseed at the QTL level. A linkage map comprising 235 SSR and 144 AFLP markers covering 2045 cM was constructed in a doubledhaploid population from a cross between the cultivar ''Express'' and the resynthesized line ''R53.'' In field experiments at four locations in Germany 250 doubled-haploid (DH) lines and their corresponding testcrosses with Express were evaluated for grain yield and three yield components. The heterosis ranged from 30% for grain yield to 0.7% for kernel weight. QTL were mapped using three different data sets, allowing the estimation of additive and dominance effects as well as digenic epistatic interactions. In total, 33 QTL were detected, of which 10 showed significant dominance effects. For grain yield, mainly complete dominance or overdominance was observed, whereas the other traits showed mainly partial dominance. A large number of epistatic interactions were detected. It was concluded that epistasis together with all levels of dominance from partial to overdominance is responsible for the expression of heterosis in rapeseed.

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Section: Discussionmentioning

confidence: 99%

Genetic Analysis of Heterosis for Yield and Yield Components in Rapeseed (Brassica napus L.) by Quantitative Trait Locus Mapping

2008

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“…S15), with the caveat that any correlation based on a large number of small-effect loci may be obscured by the moderate-effect size loci that we detected in the GWA studies. Several previous studies of heterosis using controlled crosses in A. thaliana have identified loci that exhibit all possible modes of gene action, including additive, dominant, and epistatic interactions (26)(27)(28)(94)(95)(96). Lack of support for the major heterosis hypotheses comes also from studies in crop species, particularly in maize and rice.…”

Section: Arabidopsis Thaliana In the Context Of Traditional Heterosismentioning

confidence: 99%

“…Finally, the pseudooverdominance hypothesis also explains heterosis with the complementation of recessive alleles but proposes that when linked in repulsion, such alleles appear overdominant. Outside of these classical hypotheses, some cases of hybrid inferiority (19)(20)(21)(22) and hybrid superiority (23)(24)(25)(26)(27)(28)(29)(30) have been linked to epistatic interactions between parental alleles.…”

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confidence: 99%

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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 ...

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“…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.…”

Section: Epistasis | Recombinant Inbred Intercrossmentioning

confidence: 99%

Genetic composition of yield heterosis in an elite rice hybrid

Zhou

Chen

Yao

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

215

213

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Heterosis refers to the superior performance of hybrids relative to the parents. Utilization of heterosis has contributed tremendously to the increased productivity in many crops for decades. Although there have been a range of studies on various aspects of heterosis, the key to understanding the biological mechanisms of heterotic performance in crop hybrids is the genetic basis, much of which is still uncharacterized. In this study, we dissected the genetic composition of yield and yield component traits using data of replicated field trials of an "immortalized F 2 " population derived from an elite rice hybrid. On the basis of an ultrahigh-density SNP bin map constructed with population sequencing, we calculated single-locus and epistatic genetic effects in the whole genome and identified components pertaining to heterosis of the hybrid. The results showed that the relative contributions of the genetic components varied with traits. Overdominance/pseudo-overdominance is the most important contributor to heterosis of yield, number of grains per panicle, and grain weight. Dominance × dominance interaction is important for heterosis of tillers per plant and grain weight and has roles in yield and grain number. Single-locus dominance has relatively small contributions in all of the traits. The results suggest that cumulative effects of these components may adequately explain the genetic basis of heterosis in the hybrid. epistasis | recombinant inbred intercross H eterosis, or hybrid vigor, refers to the superior performance of the hybrids relative to the parents (1). Utilization of heterosis has tremendously increased productivity of many crops globally. However, the understanding of the underpinning biological mechanism is still fragmentary after a century of debate and quest. Although there have been a range of studies on various aspects of heterosis (2-5), the key to understanding the biological mechanisms of heterotic performance in crop hybrids is the genetic basis (6), much of which is still uncharacterized (7).Three classic genetic hypotheses-dominance (8-11), overdominance (12-15), and epistasis (16, 17)-were proposed as explanations for the genetic basis of heterosis. Although there have been a large number of genetic analyses in plants with results favoring one hypothesis or another (18-31), 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.The following conditions should be met for complete genetic characterization of heterosis relevant to crop production: (i) the genetic materials are based on elite hybrids that have shown timehonored superiority in crop production; (ii) the targets are key traits of agronomic performance; (iii) the experimental population allows identification of all of the genetic components concerned, including dominance (d/a ≤1, where d is the dominant effect and a is the additiv...

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Analysis of a Triple Testcross Design With Recombinant Inbred Lines Reveals a Significant Role of Epistasis in Heterosis for Biomass-Related Traits in Arabidopsis

Cited by 72 publications

References 30 publications

Genetic Analysis of Heterosis for Yield and Yield Components in Rapeseed (Brassica napus L.) by Quantitative Trait Locus Mapping

Genetic Analysis of Heterosis for Yield and Yield Components in Rapeseed (Brassica napus L.) by Quantitative Trait Locus Mapping

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Genetic composition of yield heterosis in an elite rice hybrid

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