Analysis of a Plant Complex Resistance Gene Locus Underlying Immune-Related Hybrid Incompatibility and Its Occurrence in Nature

Abstract

Mechanisms underlying speciation in plants include detrimental (incompatible) genetic interactions between parental alleles that incur a fitness cost in hybrids. We reported on recessive hybrid incompatibility between an Arabidopsis thaliana strain from Poland, Landsberg erecta (Ler), and many Central Asian A. thaliana strains. The incompatible interaction is determined by a polymorphic cluster of Toll/interleukin-1 receptor-nucleotide binding-leucine rich repeat (TNL) RPP1 (Recognition of Peronospora parasitica1)-like genes in Ler and alleles of the receptor-like kinase Strubbelig Receptor Family 3 (SRF3) in Central Asian strains Kas-2 or Kond, causing temperature-dependent autoimmunity and loss of growth and reproductive fitness. Here, we genetically dissected the RPP1-like Ler locus to determine contributions of individual RPP1-like Ler (R1–R8) genes to the incompatibility. In a neutral background, expression of most RPP1-like Ler genes, except R3, has no effect on growth or pathogen resistance. Incompatibility involves increased R3 expression and engineered R3 overexpression in a neutral background induces dwarfism and sterility. However, no individual RPP1-like Ler gene is sufficient for incompatibility between Ler and Kas-2 or Kond, suggesting that co-action of at least two RPP1-like members underlies this epistatic interaction. We find that the RPP1-like Ler haplotype is frequent and occurs with other Ler RPP1-like alleles in a local population in Gorzów Wielkopolski (Poland). Only Gorzów individuals carrying the RPP1-like Ler haplotype are incompatible with Kas-2 and Kond, whereas other RPP1-like alleles in the population are compatible. Therefore, the RPP1-like Ler haplotype has been maintained in genetically different individuals at a single site, allowing exploration of forces shaping the evolution of RPP1-like genes at local and regional population scales.

Chromosome-level assembly ofArabidopsis thalianaLerreveals the extent of translocation and inversion polymorphisms

“…Gene absence/presence polymorphisms have been connected to phenotypic variation (1) and genetic incompatibilities (51)(52)(53)(54) before, but the genome-wide extent of hundreds of polymorphic genes in both genomes was surprisingly high, even though we only looked at low-copy differences. The functional classes, which were enriched among the duplicated genes, included defense-related genes, which can have a selective advantage when duplicated because they can evolve race-specific resistances exemplified by the RPP1 locus where Ler has a 70-kb additional sequence including several strain-specific genes (1,55).…”

“…It is broadly known as Ler-0, which is an abbreviation for its accession code La-1 and a mutation in the ERECTA gene. In 1957, George Rédei, at the University of Missouri-Columbia, irradiated La-1 samples, which were provided by Friedrich Laibach and were collected in Landsberg an der Warthe (now called Gorzów Wielkopolski), Poland, where Ler-0-related genotypes are still present (1). Some seeds of the original batch were irradiated with X-rays, resulting, among others, in the isolation of the erecta (er) mutant (2,3).…”

Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector

“…So-called 'deadly mix' (DM) genes at the RPP1 locus have been shown to specify hybrid incompatibility in the Arabidopsis ecotypes Ler, Uk-1 and Bla-1 in specific crosses with other ecotypes (Alc azar et al, 2009(Alc azar et al, , 2014Chae et al, 2014). To determine whether hybrid incompatibility and immunity functions are encoded by related members of each respective RPP1 locus, we constructed a phylogeny of locus members with both known and unknown function.…”

“…Three other RPP1 loci, from Ler, Uk-1 and Bla-1, which are not associated with disease resistance, but play a role in hybrid incompatibility, have also been completely resolved (Alc azar et al, 2009(Alc azar et al, , 2014Chae et al, 2014). These loci were referred to as 'deadly mix2' (DM2) as they are able to activate an autoimmune response in a hybrid background, after crosses with certain incompatible ecotypes.…”

“…RPP1 is encoded by a complex genetic locus, whose rapid evolution has led to additional NLR variants across Arabidopsis ecotypes, some of which may also function in Hpa resistance T€ or et al, 1994;Botella et al, 1998;Gordon, 2002). Interestingly, several Arabidopsis ecotypes contain complex RPP1 loci with homologs activating deleterious auto-immune responses in incompatible hybrid crosses, indicating functional diversification of RPP1 locus members (Bomblies et al, 2007;Alc azar et al, 2009Alc azar et al, , 2014Chae et al, 2014).…”