Gene disruption by structural mutations drives selection in US rice breeding over the last century

Authors: Vaughn, Justin; KORANI, WALID - University Of Georgia; STEIN, JOSHUA - Cold Spring Harbor Laboratory; Edwards, Jeremy; PETERSON, DANIEL - Mississippi State University; Simpson, Sheron; YOUNGBLOOD, RAMSEY - Mississippi State University; GRIMWOOD, JANE - Hudsonalpha Institute For Biotechnology; Ware, Doreen; McClung, Anna; Scheffler, Brian

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/28/2021
Publication Date: 3/18/2021
Citation: Vaughn, J.N., Korani, W., Stein, J.C., Edwards, J., Peterson, D.G., Simpson, S.A., Youngblood, R.C., Grimwood, J., Ware, D., Mcclung, A.M., Scheffler, B.E. 2021. Gene disruption by structural mutations drives selection in US rice breeding over the last century. PLoS Genetics. 17(3): e1009389. https://doi.org/10.1371/journal.pgen.1009389.
DOI: https://doi.org/10.1371/journal.pgen.1009389

Interpretive Summary: Some crop varieties have superior performance across years and environments. This vigor is often observed in first generation hybrids and is thought to be related to the fact that many harmful mutations (or “deleterious alleles”) in one parent are being masked by functional, “wild-type” alleles in the other parent. Unfortunately, these alleles are very difficult to identify precisely because, individually, they only have a small effect; thus, the mutational mechanisms responsible for vigor remain unclear. In this study, we use long-read sequencing to characterize the entire mutational spectrum between two rice varieties. We then track these mutations through the last century of rice breeding. We show that large structural mutations in exons are selected against at a greater rate than any other mutational class. These findings illuminate the nature of deleterious alleles and will guide attempts to predict variety vigor based solely on genomic information.

Technical Abstract: The genetic basis of general plant vigor is of major interest to food producers, yet the trait is recalcitrant to genetic mapping because of the number of loci involved, their small effects, and linkage. Observations of heterosis in many crops suggests that recessive, malfunctioning versions of genes are a major cause of poor performance, yet we have little information on the mutational spectrum underlying these disruptions. To address this question, we generated a long-read assembly of a tropical japonica rice variety, Carolina Gold, which allowed us to identify structural mutations (>50 bp) and orient them with respect to their ancestral state using the outgroup, Oryza glaberrima. Supporting prior work, we find substantial genome expansion is the sativa branch. While transposable elements (TEs) account for the largest share of size variation, the majority of events are not directly TE-mediated. Tandem duplications are the most common source of insertions and are highly enriched among 50-200bp mutations. To explore the relative impact of various mutational classes on crop fitness, we then track these structural events over the last century of US rice improvement using 101 resequenced varieties. Within this material, a pattern of temporary hybridization between medium and long-grain varieties was followed by recent divergence. During this long-term selection, structural mutations that impact gene exons have been removed at a greater rate than intronic indels and single-nucleotide mutations. These results support the use of ab initio estimates of mutational burden, based on structural data, as an orthogonal predictor in genomic selection.