Dissecting repulsion linkage in the dwarfing gene Dw3 region for sorghum plant height provides insights into heterosis

Significance Heterosis, the better performance of hybrids over their parents, holds great economic and biological significance. Different theories have been proposed, but specific examples with detailed dissection are limited. If close linkage of alleles with opposite effects exists, the superiority of hybrids over inbreds is observed and may appear as overdominance at a single locus. We present a case of pseudo-overdominance generated by repulsion linkage between two quantitative trait loci in sorghum plant height. A combination of approaches were used: linkage mapping under a defined genetic background, genome-wide association study with a diversity panel, computer simulation, and designed crosses with selected genetic stocks. Our findings provide insights into heterosis and a tool box for plant breeders to develop ideal cultivars. Heterosis is a main contributor to yield increase in many crop species. Different mechanisms have been proposed for heterosis: dominance, overdominance, epistasis, epigenetics, and protein metabolite changes. However, only limited examples of molecular dissection and validation of these mechanisms are available. Here, we present an example of discovery and validation of heterosis generated by a combination of repulsion linkage and dominance. Using a recombinant inbred line population, a separate quantitative trait locus (QTL) for plant height (qHT7.1) was identified near the genomic region harboring the known auxin transporter Dw3 gene. With two loci having repulsion linkage between two inbreds, heterosis in the hybrid can appear as a single locus with an overdominance mode of inheritance (i.e., pseudo-overdominance). Individually, alleles conferring taller plant height exhibited complete dominance over alleles conferring shorter height. Detailed analyses of different height components demonstrated that qHT7.1 affects both the upper and lower parts of the plant, whereas Dw3 affects only the part below the flag leaf. Computer simulations show that repulsion linkage could influence QTL detection and estimation of effect in segregating populations. Guided by findings in linkage mapping, a genome-wide association study of plant height with a sorghum diversity panel pinpointed genomic regions underlying the trait variation, including Dw1, Dw2, Dw3, Dw4, and qHT7.1. Multilocus mixed model analysis confirmed the advantage of complex trait dissection using an integrated approach. Besides identifying a specific genetic example of heterosis, our research indicated that integrated molecular dissection of complex traits in different population types can enable plant breeders to fine tune the breeding process for crop production.

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