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PMID: 25503786 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

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

PLoS genetics ·Vol. 10 ·No. 12 ·2014-12-00 ·Pages e1004848

Alcázar R, von Reth M, Bautor J, Chae E, Weigel D, Koornneef M, Parker JE

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.

MeSH Terms
Alleles Arabidopsis/genetics,immunology Arabidopsis Proteins/genetics,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,metabolism Transgenes
Chemicals
Arabidopsis Proteins DNA, Plant Protein Serine-Threonine Kinases SRF3 protein, Arabidopsis
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Alcázar Rubén
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.
von Reth Marcel
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.
Bautor Jaqueline
Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
Chae Eunyoung
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
Weigel Detlef
Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
Koornneef Maarten
Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Cluster of Excellence on Plant Sciences (CEPLAS), Germany.
Parker Jane E
Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany; Cluster of Excellence on Plant Sciences (CEPLAS), Germany.
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Article Info
Journal
PLoS genetics
Abbr.
PLoS Genet
ISSN
1553-7404
DOI
10.1371/journal.pgen.1004848
Published
2014-12-00
Epub
2014-00-11
Pages
e1004848
Language
English
Region
United States
NLM ID
101239074
PMCID
PMC4263378
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.pgen.1004848 PMC Full Text View journal details
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