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Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids.

ABSTRACT: 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.

SUBMITTER: Baldauf JA

PROVIDER: S-EPMC9237695 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:IntroductionNumerous crops have transitioned to hybrid seed production to increase yields and yield stability through heterosis. However, the molecular mechanisms underlying heterosis and its stability across environments are not yet fully understood.ObjectivesThis study aimed to (1) elucidate the genetic and molecular mechanisms underlying heterosis in sunflower, and (2) determine how heterosis is maintained under different environments.MethodsGenome-wide association (GWA) analyses were employed to assess the effects of presence/absence variants (PAVs) and stop codons on 16 traits phenotyped in the sunflower association mapping population at three locations. To link the GWA results to transcriptomic variation, we sequenced the transcriptomes of two sunflower cultivars and their F1 hybrid (INEDI) under both control and drought conditions and analyzed patterns of gene expression and alternative splicing.ResultsThousands of PAVs were found to affect phenotypic variation using a relaxed significance threshold, and at most such loci the "absence" allele reduced values of heterotic traits, but not those of non-heterotic traits. This pattern was strengthened for PAVs that showed expression complementation in INEDI. Stop codons were much rarer than PAVs and less likely to reduce heterotic trait values. Hybrid expression patterns were enriched for the GO category, sensitivity to stimulus, but all genotypes responded to drought similarily - by up-regulating water stress response pathways and down-regulating metabolic pathways. Changes in alternative splicing were strongly negatively correlated with expression variation, implying that alternative splicing in this system largely acts to reinforce expression responses.ConclusionOur results imply that complementation of expression of PAVs in hybrids is a major contributor to heterosis in sunflower, consistent with the dominance model of heterosis. This mechanism can account for yield stability across different environments. Moreover, given the much larger numbers of PAVs in plant vs. animal genomes, it also offers an explanation for the stronger heterotic responses seen in the former.

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Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids.

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