Heterosis for Biomass-Related Traits in Arabidopsis Investigated by Quantitative Trait Loci Analysis of the Triple Testcross Design With Recombinant Inbred Lines

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

doi:10.1534/genetics.107.077628

Cited by 57 publications

(69 citation statements)

References 66 publications

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“…In crosses between laboratory accessions (Col-0 and C24), Barth et al (2003) reported considerably stronger heterosis (60-69%) for biomass and rosette diameter than what we found here for fitness. Similarly, in a cross between the same pair of lines, Kusterer et al (2007b) found 49% heterosis for biomass yield. Direct comparison of these results with ours is difficult because heterosis between laboratory accessions may reflect fixation of alleles during cultivation rather than the historical effects of genetic drift in natural populations.…”

Section: Discussionmentioning

confidence: 85%

“…Kusterer et al (2007b) investigated the genetic basis of heterosis for biomass-related traits and found strong positive effects of dominance. Despite the expected positive correlation between biomass and fitness, another study using the same laboratory accessions found heterosis for biomass, but outbreeding depression for seed production (Barth et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

2015

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Understanding the causes and architecture of genetic differentiation between natural populations is of central importance in evolutionary biology. Crosses between natural populations can result in heterosis if recessive or nearly recessive deleterious mutations have become fixed within populations because of genetic drift. Divergence between populations can also result in outbreeding depression because of genetic incompatibilities. The net fitness consequences of between-population crosses will be a balance between heterosis and outbreeding depression. We estimated the magnitude of heterosis and outbreeding depression in the highly selfing model plant Arabidopsis thaliana, by crossing replicate line pairs from two sets of natural populations (C ↔ R, B ↔ S) separated by similar geographic distances (Italy ↔ Sweden). We examined the contribution of different modes of gene action to overall differences in estimates of lifetime fitness and fitness components using joint scaling tests with parental, reciprocal F 1 and F 2 , and backcross lines. One of these population pairs (C ↔ R) was previously demonstrated to be locally adapted, but locally maladaptive quantitative trait loci were also found, suggesting a role for genetic drift in shaping adaptive variation. We found markedly different genetic architectures for fitness and fitness components in the two sets of populations. In one (C ↔ R), there were consistently positive effects of dominance, indicating the masking of recessive or nearly recessive deleterious mutations that had become fixed by genetic drift. The other set (B ↔ S) exhibited outbreeding depression because of negative dominance effects. Additional studies are needed to explore the molecular genetic basis of heterosis and outbreeding depression, and how their magnitudes vary across environments.

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Section: Discussionmentioning

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

2015

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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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Heterosis for Biomass-Related Traits in Arabidopsis Investigated by Quantitative Trait Loci Analysis of the Triple Testcross Design With Recombinant Inbred Lines

Cited by 57 publications

References 66 publications

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Genetic composition of yield heterosis in an elite rice hybrid

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