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Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize.

ABSTRACT: Deleterious alleles have long been proposed to play an important role in patterning phenotypic variation and are central to commonly held ideas explaining the hybrid vigor observed in the offspring of a cross between two inbred parents. We test these ideas using evolutionary measures of sequence conservation to ask whether incorporating information about putatively deleterious alleles can inform genomic selection (GS) models and improve phenotypic prediction. We measured a number of agronomic traits in both the inbred parents and hybrids of an elite maize partial diallel population and re-sequenced the parents of the population. Inbred elite maize lines vary for more than 350,000 putatively deleterious sites, but show a lower burden of such sites than a comparable set of traditional landraces. Our modeling reveals widespread evidence for incomplete dominance at these loci, and supports theoretical models that more damaging variants are usually more recessive. We identify haplotype blocks using an identity-by-decent (IBD) analysis and perform genomic prediction analyses in which we weigh blocks on the basis of complementation for segregating putatively deleterious variants. Cross-validation results show that incorporating sequence conservation in genomic selection improves prediction accuracy for grain yield and other fitness-related traits as well as heterosis for those traits. Our results provide empirical support for an important role for incomplete dominance of deleterious alleles in explaining heterosis and demonstrate the utility of incorporating functional annotation in phenotypic prediction and plant breeding.

SUBMITTER: Yang J

PROVIDER: S-EPMC5633198 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Correction: Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize.

Project description:[This corrects the article DOI: 10.1371/journal.pgen.1007019.].

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Epistasis Activation Contributes Substantially to Heterosis in Temperate by Tropical Maize Hybrids.

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Dominance of Deleterious Alleles Controls the Response to a Population Bottleneck.

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Project description:The dominance model of heterosis explains the superior performance of F1-hybrids via the complementation of deleterious alleles by beneficial alleles in many genes. Genes active in one parent but inactive in the second lead to single-parent expression (SPE) complementation in maize (Zea mays L.) hybrids. In this study, SPE complementation resulted in approximately 700 additionally active genes in different tissues of genetically diverse maize hybrids on average. We established that the number of SPE genes is significantly associated with mid-parent heterosis (MPH) for all surveyed phenotypic traits. In addition, we highlighted that maternally (SPE_B) and paternally (SPE_X) active SPE genes enriched in gene co-expression modules are highly correlated within each SPE type but separated between these two SPE types. While SPE_B-enriched co-expression modules are positively correlated with phenotypic traits, SPE_X-enriched modules displayed a negative correlation. Gene ontology term enrichment analyses indicated that SPE_B patterns are associated with growth and development, whereas SPE_X patterns are enriched in defense and stress response. In summary, these results link the degree of phenotypic MPH to the prevalence of gene expression complementation observed by SPE, supporting the notion that hybrids benefit from SPE complementation via its role in coordinating maize development in fluctuating environments.

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Genome-wide proteomic profiling reveals the role of dominance protein expression in heterosis in immature maize ears.

Project description:Heterosis refers to the phenomenon in which hybrid progeny show superior performance relative to their parents. Early maize ear development shows strong heterosis in ear architecture traits and greatly affects grain yield. To explore the underlying molecular mechanisms, genome-wide proteomics of immature ears of maize hybrid ZD909 and its parents were analyzed using tandem mass tag (TMT) technology. A total of 9,713 proteins were identified in all three genotypes. Among them, 3,752 (38.6%) proteins were differentially expressed between ZD909 and its parents. Multiple modes of protein action were discovered in the hybrid, while dominance expression patterns accounted for 63.6% of the total differentially expressed proteins (DEPs). Protein pathway enrichment analysis revealed that high parent dominance proteins mainly participated in carbon metabolism and nitrogen assimilation processes. Our results suggested that the dominant expression of favorable alleles related to C/N metabolism in the hybrid may be essential for ZD909 ear growth and heterosis formation. Integrated analysis of proteomic and quantitative trait locus (QTL) data further support our DEP identification and provide useful information for the discovery of genes associated with ear development. Our study provides comprehensive insight into the molecular mechanisms underlying heterosis in immature maize ears from a proteomic perspective.

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Project description:Hybrids account for nearly all commercially planted varieties of maize and many other crop plants because crosses between inbred lines of these species produce first-generation [F1] offspring that greatly outperform their parents. The mechanisms underlying this phenomenon, called heterosis or hybrid vigor, are not well understood despite over a century of intensive research. The leading hypotheses-which focus on quantitative genetic mechanisms (dominance, overdominance, and epistasis) and molecular mechanisms (gene dosage and transcriptional regulation)-have been able to explain some but not all of the observed patterns of heterosis. Abiotic stressors are known to impact the expression of heterosis; however, the potential role of microbes in heterosis has largely been ignored. Here, we show that heterosis of root biomass and other traits in maize is strongly dependent on the belowground microbial environment. We found that, in some cases, inbred lines perform as well by these criteria as their F1 offspring under sterile conditions but that heterosis can be restored by inoculation with a simple community of seven bacterial strains. We observed the same pattern for seedlings inoculated with autoclaved versus live soil slurries in a growth chamber and for plants grown in steamed or fumigated versus untreated soil in the field. In a different field site, however, soil steaming increased rather than decreased heterosis, indicating that the direction of the effect depends on community composition, environment, or both. Together, our results demonstrate an ecological phenomenon whereby soil microbes differentially impact the early growth of inbred and hybrid maize.

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Negative dominance and dominance-by-dominance epistatic effects reduce grain-yield heterosis in wide crosses in wheat.

Project description:The genetics underlying heterosis, the difference in performance of crosses compared with midparents, is hypothesized to vary with relatedness between parents. We established a unique germplasm comprising three hybrid wheat sets differing in the degree of divergence between parents and devised a genetic distance measure giving weight to heterotic loci. Heterosis increased steadily with heterotic genetic distance for all 1903 hybrids. Midparent heterosis, however, was significantly lower in the hybrids including crosses between elite and exotic lines than in crosses among elite lines. The analysis of the genetic architecture of heterosis revealed this to be caused by a higher portion of negative dominance and dominance-by-dominance epistatic effects. Collectively, these results expand our understanding of heterosis in crops, an important pillar toward global food security.

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Project description:Kernel shape related traits (KSRTs) have been shown to have important influences on grain yield. The previous studies that emphasize kernel length (KL) and kernel width (KW) lack a comprehensive evaluation of characters affecting kernel shape. In this study, materials of the basic generations (B73, Mo17, and B73 × Mo17), 82 intermated B73 × Mo17 (IBM) individuals, and the corresponding triple testcross (TTC) populations were used to evaluate heterosis, investigate correlations, and characterize the quantitative trait loci (QTL) for six KSRTs: KL, KW, length to width ratio (LWR), perimeter length (PL), kernel area (KA), and circularity (CS). The results showed that the mid-parent heterosis (MPH) for most of the KSRTs was moderate. The performance of KL, KW, PL, and KA exhibited significant positive correlation with heterozygosity but their Pearson's R values were low. Among KSRTs, the strongest significant correlation was found between PL and KA with R values was up to 0.964. In addition, KW, PL, KA, and CS were shown to be significant positive correlation with 100-kernel weight (HKW). 28 QTLs were detected for KSRTs in which nine were augmented additive, 13 were augmented dominant, and six were dominance × additive epistatic. The contribution of a single QTL to total phenotypic variation ranged from 2.1% to 32.9%. Furthermore, 19 additive × additive digenic epistatic interactions were detected for all KSRTs with the highest total R2 for KW (78.8%), and nine dominance × dominance digenic epistatic interactions detected for KL, LWR, and CS with the highest total R2 (55.3%). Among significant digenic interactions, most occurred between genomic regions not mapped with main-effect QTLs. These findings display the complexity of the genetic basis for KSRTs and enhance our understanding on heterosis of KSRTs from the quantitative genetic perspective.

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