Low additive genetic variation in a trait under selection in domesticated rice

Authors: KARAVOLIAS, NICHOLAS - Cornell University; GREENBERG, ANTHONY - Cornell University; BARRERO, LUZ - Columbian Caribbean Observatory; MARON, LYZA - Cornell University; SHI, YUXIN - Cornell University; MONTEVERDE, ELIANA - Cornell University; Pineros, Miguel; MCCOUCH, SUSAN - Cornell University

Submitted to: Genes, Genomes, Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/17/2020
Publication Date: 7/1/2020
Citation: Karavolias, N.G., Greenberg, A.J., Barrero, L.S., Maron, L.G., Shi, Y., Monteverde, E., Pineros, M., Mccouch, S. 2020. Low additive genetic variation in a trait under selection in domesticated rice. Genes, Genomes, Genetics. 10(7):2435-2443. https://doi.org/10.1534/g3.120.401194.
DOI: https://doi.org/10.1534/g3.120.401194

Interpretive Summary: The efficiency of plant breeding depends on two basic requirements: 1) the accuracy with which we can measure the trait of interest, and 2) whether the variation in this trait can be linked to genetic variation in the genome. We took advantage of the inbred nature of rice, where the variation on a trait of genetically identical individuals can be measured in replicate, in conjunction with an existing detailed genetic map. With these tools, we investigated what proportion of variation observed in the tolerance to aluminum stress could be associated with genetic markers. The results showed that the association between the marker and the trait (e.g. tolerance) was very low, even in subpopulation known to be highly aluminum tolerant; we were unable to identify any genetic marker associated with the aluminum stress trait. Our study highlights the importance of performing detailed genomic investigations of measurable (quantitative) traits under selection, which will guide practical decisions in plant breeding for crop improvement.

Technical Abstract: Quantitative traits are important targets of both natural and artificial selection. The genetic architecture of these traits and its change during the adaptive process is thus of fundamental interest. The fate of the additive effects of variants underlying a trait receives particular attention because they constitute the genetic variation component that is transferred from parents to offspring and thus governs the response to selection. While estimation of this component of phenotypic variation is challenging, the increasing availability of dense molecular markers puts it within reach. Inbred plant species offer an additional advantage because phenotypes of genetically identical individuals can be measured in replicate. This makes it possible to estimate marker effects separately from the contribution of the genetic background. We focused on root growth in domesticated rice, Oryza sativa, under normal and aluminum (Al) stress conditions. This trait has been under long-term selection because root growth correlates with several fitness components. A dense single nucleotide polymorphism (SNP) map is available for all accessions studied. Taking advantage of this map and a set of Bayesian models, we assessed additive marker effects. While total genetic variation accounted for a large proportion of phenotypic variance, marker effects carried little information particularly in the Al tolerant tropical japonica population of rice. We were unable to identify any loci associated with root growth in this population. Models estimating the aggregate effects of all measured genotypes likewise produced low estimates of marker heritability and were unable to predict total genetic values accurately. Our results support the long-standing conjecture that additive genetic variation is depleted in traits under selection. We further provide evidence that this depletion is due to the prevalence of low-frequency alleles that underlie the trait.