Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation

Abstract

Plant growth is influenced by genetic factors and environmental cues. Genotype-by-environment interactions are governed by complex genetic epistatic networks that are subject to natural selection. Here we describe a novel epistatic interaction modulating growth in response to temperature common to 2 Arabidopsis recombinant inbred line (RIL) populations (Ler ؋ Kas-2 and Ler ؋ Kond). At 14°C, lines with specific allele combinations at interacting loci (incompatible interactions) have severe growth defects. These lines exhibit deregulated cell death programs and enhanced disease resistance. At 20°C, growth defects are suppressed, but a positive trait of enhanced resistance is retained. Mapping of 1 interacting QTL to a cluster of RPP1-like TIR-NB-LRR genes on chromosome 3 is consistent with our finding that environmentally conditioned epistasis depends on activation of the salicylic acid (SA) stress signaling pathway. The nature of the epistatic interaction conforms to the Dobzhansky-Muller model of genetic incompatibility with incomplete penetrance for reproductive isolation. Variation in fitness of different incompatible lines reveals the presence of additional modifiers in the genetic background. We propose that certain interacting loci lead to an optimal balance between growth and resistance to pathogens by modulating SA signaling under specific environments. This could allow the accumulation of additional incompatibilities before reaching complete reproductive isolation.natural variation ͉ Dobzhansky-Muller interactions ͉ growth ͉ temperature ͉ TIR-NB-LRR

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

“…Genetic mapping of stunted growth and necrotic phenotypes for a small subset of these crosses using laboratory strains such as Col and Ler as one of the parents implicated epistasis between a few loci involved in pathogen defense (Bomblies et al, 2007;Alcázar et al, 2009). These stunted and necrotic phenotypes are likely to have negative effects on fitness, such as we observed here, but relative fitness (fruit and seed production) of the F 1 has not been quantified for most of the crosses reported in Bomblies et al (2007).…”

“…Subsequent quantitative trait loci (QTL) mapping using Col as one of the parental lines indicated that the genetic basis of necrosis was due to negative epistatic interactions involving 2-4 loci (Bomblies et al, 2007). Similar interactions, mapped to approximately the same regions, were found in a study of the genetic basis of necrosis in two different recombinant inbred line mapping populations with Ler as a parental line (Alcázar et al, 2009).…”

“…For example, Fenster and Galloway (2000) found that the magnitude of heterosis varied with planting site. In addition, hybrid necrosis found in Arabidopsis was partially alleviated at warm (23°C) temperatures (Bomblies et al, 2007;Alcázar et al, 2009;Smith et al, 2011). In wide crosses, it is difficult to identify a single relevant environment in which to measure fitness, and it was not feasible for us to replicate the experiment across four or even two parental environments.…”

Chromosomal Location of HWA1 and HWA2, Complementary Hybrid Weakness Genes in Rice

“…We fine-mapped HWC2 gene in rice, and narrowed down the area of interest to 19 kb, identifying five candidate genes, one of which encodes an NB-LRR protein (Kuboyama et al 2009). Alcázar et al (2009) fine mapped a causal gene of incompatibility or hybrid breakdown to a cluster of TIR-NB-LRR genes in Arabidopsis. Yamamoto et al (2010) reported that hbd3, a causal gene controlling hybrid breakdown in rice, is located on the cluster of NB-LRR genes.…”

Arabidopsisand relatives as models for the study of genetic and genomic incompatibilities

“…Similar to the F 1 cases, these plants were strongly resistant to pathogen attack, and this depended on the defence hormone salicylic acid (SA). Remarkably, one of the responsible genes appears to be a distinct allelic variant at the same TIR-NB-LRR cluster as DM2 (Alcázar et al 2009). Since there are over 100 NB-LRR loci in the A. thaliana genome, this might indicate that not all of these are equally likely to cause hybrid problems.…”