The Genetic Basis of Heterosis: Multiparental Quantitative Trait Loci Mapping Reveals Contrasted Levels of Apparent Overdominance Among Traits of Agronomical Interest in Maize (<i>Zea mays</i> L.)

Lariepe, Amandine; Mangin, Brigitte; Jasson, Sylvain; Combes, Valérie; Dumas, Fabrice; Jamin, Philippe; Lariagon, Christine; Jolivot, Daniel; Madur, Delphine; Fiévet, Julie; Galláis, A.; Dubreuil, Pierre; Charcosset, Alain; Moreau, Laurence

doi:10.1534/genetics.111.133447

Cited by 123 publications

(133 citation statements)

References 54 publications

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“…S30). QTLs with significant effect on seven of nine key domestication traits are located on chromosome 5 (7), and several QTLs for important agronomic traits (35), including plant height (36) and yield (37), map near CEN5.…”

Section: Low Genetic Diversity At Most Maize Centromeresmentioning

confidence: 99%

Inbreeding drives maize centromere evolution

Schneider

Xie

Wolfgruber

et al. 2016

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

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Functional centromeres, the chromosomal sites of spindle attachment during cell division, are marked epigenetically by the centromerespecific histone H3 variant cenH3 and typically contain long stretches of centromere-specific tandem DNA repeats (∼1.8 Mb in maize). In 23 inbreds of domesticated maize chosen to represent the genetic diversity of maize germplasm, partial or nearly complete loss of the tandem DNA repeat CentC precedes 57 independent cenH3 relocation events that result in neocentromere formation. Chromosomal regions with newly acquired cenH3 are colonized by the centromere-specific retrotransposon CR2 at a rate that would result in centromere-sized CR2 clusters in 20,000-95,000 y. Three lines of evidence indicate that CentC loss is linked to inbreeding, including (i) CEN10 of temperate lineages, presumed to have experienced a genetic bottleneck, contain less CentC than their tropical relatives; (ii) strong selection for centromere-linked genes in domesticated maize reduced diversity at seven of the ten maize centromeres to only one or two postdomestication haplotypes; and (iii) the centromere with the largest number of haplotypes in domesticated maize (CEN7) has the highest CentC levels in nearly all domesticated lines. Rare recombinations introduced one (CEN2) or more (CEN5) alternate CEN haplotypes while retaining a single haplotype at domestication loci linked to these centromeres. Taken together, this evidence strongly suggests that inbreeding, favored by postdomestication selection for centromere-linked genes affecting key domestication or agricultural traits, drives replacement of the tandem centromere repeats in maize and other crop plants. Similar forces may act during speciation in natural systems.centromere drive | centromere paradox | founder effect | hemicentric inversion | linkage disequilibrium C entromere-specific tandemly arranged DNA repeats vary in length and nucleotide sequence between species. The puzzling observation that centromeres can consist of highly variable sequences despite being involved in an essential cellular function (i.e., chromosome segregation) has been coined the "centromere paradox" (1). "Centromere drive" has been proposed to preferentially segregate the "favored" centromere into the female gamete and thereby provide the selective force that acts on centromere DNA sequences and interacting proteins (2).Maize (Zea mays ssp. mays) was domesticated between 7.5 and 10 thousand years ago (ka) from wind-pollinated outcrossing wild teosinte (Z. mays ssp. parviglumis) (3, 4) in a process that dramatically changed its morphology. Several quantitative trait loci (QTLs) responsible for these morphological changes were identified in pioneering work (5-8), and a large number of additional genetic loci involved in maize domestication and improvement were subsequently identified in genome-wide scans (9). Gene (and centromere) flow between the fully interfertile maize and teosinte subspecies has been documented (10, 11). Functional centromeres of maize consist of 1-2 Mb of DN...

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Section: Low Genetic Diversity At Most Maize Centromeresmentioning

confidence: 99%

Inbreeding drives maize centromere evolution

Schneider

Xie

Wolfgruber

et al. 2016

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

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“…Several dominantly acting loci have been shown to contribute to heterosis (29,77,78), and more recently, heterosis-associated loci in maize have been shown to be enriched for deleterious mutations (43). Although dominance remains the prevailing explanation, some assumptions of this hypothesis are not consistently supported; the correlation between the degree of heterosis and the genetic distance between parents is not always evident (37,(55)(56)(57)(79)(80)(81)(82), and there are loci with moderate effect sizes (29,77,78).…”

Section: Arabidopsis Thaliana In the Context Of Traditional Heterosismentioning

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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“…Initial QTL studies indicated many QTL with overdominant gene action in populations derived from heterotic maize hybrids for traits such as yield and plant height [37,38]. However, subsequent genetic dissection of an QTL with estimated overdominant gene action showed that the original QTL could be separated into two, linked QTLs in repulsion phase with dominant gene action [39,40] conducted a QTL mapping study using 3 recombinant inbred populations using a North Carolina Design III approach. The results of this study were consistent with previous studies in maize.…”

Section: A Case For the Dominance Hypothesis: Early 1900s To Presentmentioning

confidence: 99%

Heterosis: Many Genes, Many Mechanisms—End the Search for an Undiscovered Unifying Theory

Kaeppler

2012

ISRN Botany

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Heterosis is the increase in vigor that is observed in progenies of matings of diverse individuals from different species, isolated populations, or selected strains within species or populations. Heterosis has been of immense economic value in agriculture and has important implications regarding the fitness and fecundity of individuals in natural populations. Genetic models based on complementation of deleterious alleles, especially in the context of linkage and epistasis, are consistent with many observed manifestations of heterosis. The search for the genes and alleles that underlie heterosis, as well as for broader allele-independent, genomewide mechanisms, has encompassed many species and systems. Common themes across these studies indicate that sequence diversity is necessary but not sufficient to produce heterotic phenotypes, and that the molecular pathways that produce heterosis involve chromatin modification, transcriptional control, translation and protein processing, and interactions between and within developmental and biochemical pathways. Taken together, there are many and diverse molecular mechanisms that translate DNA into phenotype, and it is the combination of all these mechanisms across many genes that produce heterosis in complex traits.

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The Genetic Basis of Heterosis: Multiparental Quantitative Trait Loci Mapping Reveals Contrasted Levels of Apparent Overdominance Among Traits of Agronomical Interest in Maize (Zea mays L.)

Cited by 123 publications

References 54 publications

Inbreeding drives maize centromere evolution

Inbreeding drives maize centromere evolution

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Heterosis: Many Genes, Many Mechanisms—End the Search for an Undiscovered Unifying Theory

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