Gene disruption by structural mutations drives selection in U.S. rice breeding over the last century

Authors: Vaughn, Justin; STEIN, JOSHUA - COLD SPRING HARBOR LABORATORY; KORANI, WALID - UNIVERSITY OF GEORGIA; Edwards, Jeremy; PETERSON, DANIEL - MISSISSIPPI STATE UNIVERSITY; Simpson, Sheron; GRIMWOOD, JANE - HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY; Ware, Doreen; MCCLUNG, ANNA; Scheffler, Brian

Submitted to: Rice Technical Working Group Meeting Proceedings
Publication Type: Proceedings
Publication Acceptance Date: 12/4/2019
Publication Date: 1/6/2021
Citation: Vaughn, J.N., Stein, J.C., Korani, W., Edwards, J., Peterson, D.G., Simpson, S.A., Grimwood, J., Ware, D., McClung, A.M., Scheffler, B.E. 2021. Gene disruption by structural mutations drives selection in U.S. rice breeding over the last century. Proceedings of 38th Rice Technical Working Group Meeting, February 24-27, 2020, Orange Beach, Alabama. p 77. Electronic Publication.

Interpretive Summary:

Technical Abstract: The genetic basis of general plant vigor is of major interest to food producers, yet the trait is typically impossible to map to gene level resolution due to the number of loci involved, their small effects, and linkage. Observations of heterosis in all major crops suggests that recessive, malfunctioning versions of genes are a major source of poor performance. The source of these broken genes has yet to be extensively characterized in an agronomic context. We generated a long-read assembly of a tropical japonica rice variety, Carolina Gold, to identify gene scale structural events and orient them with respect to their ancestral state using the outgroup, Oryza glabberima. Supporting prior work, we find substantial genome expansion in the O. sativa lineage. 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 50-200 bp 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 developed across the Mississippi valley. Within this material, a pattern of temporary hybridization between medium and short-grain varieties was followed by recent divergence. During this long term selection, >50 bp structural events that impact gene exons have been removed at a greater rate than intronic indels and even single-nucleotide mutations that introduce stop codons. These results support the use of ab initio estimates of mutational burden as an additional predictor in genomic selection, and they illuminate research gaps that currently hinder such estimates.