title: 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.
authors.affiliation: Department of Natural Products, Plant Biology and Soil Science, Laboratory of Plant Physiology, Faculty of Pharmacy. University of Barcelona, Barcelona, Spain; Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Rubén
authors.initials: R
authors.lastname: Alcázar
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Marcel
authors.initials: M
authors.lastname: von Reth
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
authors.forename: Jaqueline
authors.initials: J
authors.lastname: Bautor
authors.affiliation: Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
authors.forename: Eunyoung
authors.initials: E
authors.lastname: Chae
authors.affiliation: Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
authors.forename: Detlef
authors.initials: D
authors.lastname: Weigel
authors.affiliation: Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Cluster of Excellence on Plant Sciences (CEPLAS), Germany.
authors.forename: Maarten
authors.initials: M
authors.lastname: Koornneef
authors.affiliation: Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Cluster of Excellence on Plant Sciences (CEPLAS), Germany.
authors.forename: Jane E
authors.initials: JE
authors.lastname: Parker
mesh_terms: D000483:Alleles; D017360:Arabidopsis / Q000235:genetics* / Q000276:immunology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D003001:Cloning, Molecular; D018744:DNA, Plant / Q000235:genetics; D060467:Disease Resistance / Q000235:genetics; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant; D020868:Gene Silencing; D056426:Genetic Loci; D014644:Genetic Variation; D005838:Genotype; D006239:Haplotypes; D006824:Hybridization, Genetic; D010802:Phylogeny; D057865:Plant Immunity / Q000235:genetics*; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D019076:Transgenes
chemical_list: D029681:Arabidopsis Proteins; D018744:DNA, Plant; D017346:Protein Serine-Threonine Kinases; C554519:SRF3 protein, Arabidopsis