The genetic architecture of disease resistance in plants and the maintenance of recombination by parasites

Abstract

Parasites represent strong selection on host populations because they are ubiquitous and can drastically reduce host fitness. It has been hypothesized that parasite selection could explain the widespread occurrence of recombination because it is a coevolving force that favours new genetic combinations in the host. A review of deterministic models for the maintenance of recombination reveals that for recombination to be favoured, multiple genes that interact with each other must be under selection. To evaluate whether parasite selection can explain the maintenance of recombination, we review 85 studies that investigated the genetic architecture of plant disease resistance and discuss whether they conform to the requirements that emerge from theoretical models. General characteristics of disease resistance in plants and problems in evaluating resistance experimentally are also discussed. We found strong evidence that disease resistance in plants is determined by multiple loci. Furthermore, in most cases where loci were tested for interactions, epistasis between loci that affect resistance was found. However, we found weak support for the idea that specific allelic combinations determine resistance to different host genotypes and there was little data on whether epistasis between resistance genes is negative or positive. Thus, the current data indicate that it is possible that parasite selection can favour recombination, but more studies in natural populations that specifically address the nature of the interactions between resistance genes are necessary. The data summarized here suggest that disease resistance is a complex trait and that environmental effects and fitness trade-offs should be considered in future models of the coevolutionary dynamics of host and parasites.

The role of epistasis on the evolution of recombination in host–parasite coevolution

“…Intuitively epistasis seems to play an important role for the RQH, because the hypothesis is based on the phase shift between the oscillations of epistasis and LD (Peters and Lively, 1999). Accordingly, several experimental studies have attempted to determine the amount of epistasis between the loci that govern the host parasite interaction (Kover and Caicedo, 2001;Wilfert et al, 2007a,b). Epistasis in host-parasite systems can come from two distinct sources.…”

Four QTLs determine crown rust (Puccinia coronata f. sp. lolii) resistance in a perennial ryegrass (Lolium perenne) population

“…The traits controlled by such QTLs can be considered almost Mendelian and are of extreme interest to breeders for use in selection programmes (Manly and Olson, 1999). QTL pairs were tested for epistatic interactions using GLM analysis (Kover and Caicedo, 2001) but no epistatic effects were identified. Dumsday et al (2003) detected a major QTL for crown rust resistance on LG2.…”

The conversion of variance and the evolutionary potential of restricted recombination

“…Empirical evidence for epistatic variance: Despite the notorious difficulty of detecting epistatic variance (eg Cheverud and Routman, 1995;Goodnight, 1995;Whitlock, 1995;Frankel and Schork, 1996;Wade and Goodnight, 1998;Cheverud, 2000;Wade, 2001), epistatic variance can and does contribute to fitness-related traits (eg Bryant and Meffert, 1996;Long et al, 1996;Routman and Cheverud, 1997;Cheverud et al, 1999;Meffert, 2000;Kover and Caicedo, 2001;Bonhoeffer et al, 2004;Sanjuán et al, 2004). Recent QTL studies provide additional, more direct evidence that genes important to fitness do interact epistatically (Brockmann et al, 2000;Rü ppell et al, 2004;reviewed in Cheverud, 2000).…”