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

Alcázar R, von Reth M, Bautor J, Chae E, Weigel D, Koornneef M, Parker JE - PLoS Genet. (2014)

Bottom Line: In a neutral background, expression of most RPP1-like Ler genes, except R3, has no effect on growth or pathogen resistance.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.

View Article: PubMed Central - PubMed

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.

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.

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Genetic diversity of the RPP1-like locus in the Gorzów population.(A) Neighbor-joining tree showing the genome-wide genetic diversity among Gw accessions, estimated from a set of 149 genome-wide SNPs. Boxes represent genes within the RPP1-like haplotype (R1 to R8, with R8 the closest to the tree) conserved with Ler (red) differing from Ler (gray), or absent (white), based on amplification and sequencing of RPP1-like genes with specific primers designed for the RPP1-like Ler cluster. Accessions carrying the RPP1-like Ler haplotype are highlighted in red. Accessions used for crosses with Kas-2 or Kond and their compatibility/incompatibility outcome are indicated. (B) Neighbor-joining tree of RPP1-like genes in Gw− and Kas-2 showing extensive allelic variation. Phylogeny is based in sequencing RPP1-like genes in Gw− individuals (Gw-31, Gw-44, Gw-55 and Gw-99) and Kas-2.
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pgen-1004848-g006: Genetic diversity of the RPP1-like locus in the Gorzów population.(A) Neighbor-joining tree showing the genome-wide genetic diversity among Gw accessions, estimated from a set of 149 genome-wide SNPs. Boxes represent genes within the RPP1-like haplotype (R1 to R8, with R8 the closest to the tree) conserved with Ler (red) differing from Ler (gray), or absent (white), based on amplification and sequencing of RPP1-like genes with specific primers designed for the RPP1-like Ler cluster. Accessions carrying the RPP1-like Ler haplotype are highlighted in red. Accessions used for crosses with Kas-2 or Kond and their compatibility/incompatibility outcome are indicated. (B) Neighbor-joining tree of RPP1-like genes in Gw− and Kas-2 showing extensive allelic variation. Phylogeny is based in sequencing RPP1-like genes in Gw− individuals (Gw-31, Gw-44, Gw-55 and Gw-99) and Kas-2.

Mentions: In May 2011, we traced the origin of Ler (Landsberg an der Warthe, Germany 1939) [37] to the area of Gorzów Wielkopolski (Poland) (S9 Figure). There we collected 167 individuals (named Gorzów, Gw), which were genotyped using 149 genome-wide SNPs [38]. With these markers, we could distinguish at least 44 different multi-locus haplotypes (Figs. 5 and 6A) which shared 58–72% SNPs with Ler. This is well above the mode of ∼44% seen for arbitrary pairs of worldwide accessions [39]. Three Gw individuals (1.8% of the entire sample) carried heterozygous alleles at various markers across the genome including the RPP1-like cluster, suggesting that outcrossing occurs between local accessions, as previously observed [40]. Structure [41] and PCA analyses of Gw individuals and other accessions originally from neighboring countries (Austria, Czech Republic and Germany), as well as more geographically distant accessions (The Netherlands, Russia and former Soviet Union, and Central Asia), confirmed that the Gw population is most closely related to other Central European A. thaliana accessions and that, with K = 3 and above, forms a distinct group (S10 Figure).


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

Alcázar R, von Reth M, Bautor J, Chae E, Weigel D, Koornneef M, Parker JE - PLoS Genet. (2014)

Genetic diversity of the RPP1-like locus in the Gorzów population.(A) Neighbor-joining tree showing the genome-wide genetic diversity among Gw accessions, estimated from a set of 149 genome-wide SNPs. Boxes represent genes within the RPP1-like haplotype (R1 to R8, with R8 the closest to the tree) conserved with Ler (red) differing from Ler (gray), or absent (white), based on amplification and sequencing of RPP1-like genes with specific primers designed for the RPP1-like Ler cluster. Accessions carrying the RPP1-like Ler haplotype are highlighted in red. Accessions used for crosses with Kas-2 or Kond and their compatibility/incompatibility outcome are indicated. (B) Neighbor-joining tree of RPP1-like genes in Gw− and Kas-2 showing extensive allelic variation. Phylogeny is based in sequencing RPP1-like genes in Gw− individuals (Gw-31, Gw-44, Gw-55 and Gw-99) and Kas-2.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263378&req=5

pgen-1004848-g006: Genetic diversity of the RPP1-like locus in the Gorzów population.(A) Neighbor-joining tree showing the genome-wide genetic diversity among Gw accessions, estimated from a set of 149 genome-wide SNPs. Boxes represent genes within the RPP1-like haplotype (R1 to R8, with R8 the closest to the tree) conserved with Ler (red) differing from Ler (gray), or absent (white), based on amplification and sequencing of RPP1-like genes with specific primers designed for the RPP1-like Ler cluster. Accessions carrying the RPP1-like Ler haplotype are highlighted in red. Accessions used for crosses with Kas-2 or Kond and their compatibility/incompatibility outcome are indicated. (B) Neighbor-joining tree of RPP1-like genes in Gw− and Kas-2 showing extensive allelic variation. Phylogeny is based in sequencing RPP1-like genes in Gw− individuals (Gw-31, Gw-44, Gw-55 and Gw-99) and Kas-2.
Mentions: In May 2011, we traced the origin of Ler (Landsberg an der Warthe, Germany 1939) [37] to the area of Gorzów Wielkopolski (Poland) (S9 Figure). There we collected 167 individuals (named Gorzów, Gw), which were genotyped using 149 genome-wide SNPs [38]. With these markers, we could distinguish at least 44 different multi-locus haplotypes (Figs. 5 and 6A) which shared 58–72% SNPs with Ler. This is well above the mode of ∼44% seen for arbitrary pairs of worldwide accessions [39]. Three Gw individuals (1.8% of the entire sample) carried heterozygous alleles at various markers across the genome including the RPP1-like cluster, suggesting that outcrossing occurs between local accessions, as previously observed [40]. Structure [41] and PCA analyses of Gw individuals and other accessions originally from neighboring countries (Austria, Czech Republic and Germany), as well as more geographically distant accessions (The Netherlands, Russia and former Soviet Union, and Central Asia), confirmed that the Gw population is most closely related to other Central European A. thaliana accessions and that, with K = 3 and above, forms a distinct group (S10 Figure).

Bottom Line: In a neutral background, expression of most RPP1-like Ler genes, except R3, has no effect on growth or pathogen resistance.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.

View Article: PubMed Central - PubMed

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.

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.

Show MeSH
Related in: MedlinePlus