Evidence for the Accumulation of Nonsynonymous Mutations and Favorable Pleiotropic Alleles During Wheat Breeding

Abstract

Plant breeding leads to the genetic improvement of target traits by selecting a small number of genotypes from among typically large numbers of candidate genotypes after careful evaluation. In this study, we first investigated how mutations at conserved nucleotide sites normally viewed as deleterious, such as nonsynonymous sites, accumulated in a wheat, Triticum aestivum, breeding lineage. By comparing a 150 year old ancestral and modern cultivar, we found recent nucleotide polymorphisms altered amino acids and occurred within conserved genes at frequencies expected in the absence of purifying selection. Mutations that are deleterious in other contexts likely had very small or no effects on target traits within the breeding lineage. Second, we investigated if breeders selected alleles with favorable effects on some traits and unfavorable effects on others and used different alleles to compensate for the latter. An analysis of a segregating population derived from the ancestral and modern parents provided one example of this phenomenon. The recent cultivar contains the Rht-B1b green revolution semi-dwarfing allele and compensatory alleles that reduce its negative effects. However, improvements in traits other than plant height were due to pleiotropic loci with favorable effects on traits and to favorable loci with no detectable pleiotropic effects. Wheat breeding appears to tolerate mutations at conserved nucleotide sites and to only select for alleles with both favorable and unfavorable effects on traits in exceptional situations.

Separation of the effects of two reduced height (Rht) genes and genomic background to select for less Fusarium head blight of short-strawed winter wheat (Triticum aestivum L.) varieties

“…This exhibits Rht-D1 as a major gene conveying a negatively pleiotropic effect on FHB resistance. As indicated by Raherison et al ( 2020 ), alleles of negatively pleiotropic loci exert favourable effects on one trait and unfavourable effects on the other trait depending on the breeding objectives. In commercial wheat breeding, the reduction effect of Rht-D1b on plant height represents a favourable effect, while its increase effect on FHB severity or susceptibility is perceived as an unfavourable effect.…”

The effects of crop attributes, selection, and recombination on Canadian bread wheat molecular variation

“…Current entries could harbor relatively beneficial allele combinations whose inheritance stably contributes to positive, progeny values (Fradgley et al., 2019), but these long haplotypes certainly make suboptimal trait contributions. Nonsynonymous mutations accumulate during wheat breeding (Raherison et al., 2020), and the mutations may preferentially accumulate in these pericentromeric regions. Recombination could generate phenotypic diversity and reduce genetic load by decoupling linked deleterious alleles and beneficial variants (Rodgers‐Melnick et al., 2015).…”

Multi-trait ensemble genomic prediction and simulations of recurrent selection highlight importance of complex trait genetic architecture in long-term genetic gains in wheat

“…Trade-offs between grain yield and both protein content and weed competitive ability seem not to have been generally addressed by commercial breeding due to yield being considered the highest economically important trait. Recent analysis by Raherison et al (2020) suggested that negative pleiotropic genetic effects in wheat have rarely been compensated for and optimised by breeding, and Yang et al (2022) showed that breeders’ selections have almost always been in favour of yield at the expense of protein. Changing economic, legislational, environmental and societal factors mean that breeding focus will increasingly need to consider how to deliver sustainable intensification of food supply, ensuring yield stability of our future crops in the face of such pressures.…”