Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature

PLoS Genet. 2014 Dec 11;10(12):e1004848. doi: 10.1371/journal.pgen.1004848. eCollection 2014 Dec.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Arabidopsis / genetics*
  • Arabidopsis / immunology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cloning, Molecular
  • DNA, Plant / genetics
  • Disease Resistance / genetics
  • Evolution, Molecular
  • Gene Expression Regulation, Plant*
  • Gene Silencing
  • Genetic Loci*
  • Genetic Variation
  • Genotype
  • Haplotypes
  • Hybridization, Genetic*
  • Phylogeny
  • Plant Immunity / genetics*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Transgenes

Substances

  • Arabidopsis Proteins
  • DNA, Plant
  • Protein Serine-Threonine Kinases
  • SRF3 protein, Arabidopsis

Grant support

The authors acknowledge funding support from Deutsche Forschungsgemeinschaft ‘SFB680’, the Max Planck Society and the European Research Council (AdG IMMUNEMESIS). MK and JEP are members of the Cluster of Excellence on Plant Sciences (CEPLAS). RA acknowledges further funding support from the Ramón y Cajal Program (RYC-2011-07847) of the Ministerio de Ciencia e Innovación (Spain), the BFU2013-41337-P grant of the Programa Estatal de Fomento de la Investigación Científica y Técnica de Excelencia (Ministerio de Economía y Competitividad, Spain) and a Marie Curie Career Integration Grant (DISEASENVIRON, PCIG10-GA-2011-303568) of the European Union. RA is member of the Grup de Recerca Consolidat 2014 SGR-920 of the Generalitat de Catalunya. MvR is a student of the International Max-Planck Research School (IMPRS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.