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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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Effects of R3 expression with different allelic combinations at SRF3 and QTL5.Expression of RPP1-like Ler genes determined by qRT-PCR in different Ler/Kas-2 recombinant inbred lines (RIL) carrying homozygous allelic combinations at RPP1-like/SRF3/QTL5 loci: Ler/Ler/Kas-2 (AAB), Ler/Kas-2/Ler (ABA), Ler/Kas-2/Kas-2 (ABB). AAB and ABA represent compatible allele combinations, whereas ABB triggers incompatibility. The ABB eds1-2 line carrying an EDS1 loss-of-function mutation is described in [31]. Values are relative to Ler and the mean ± SD of three biological replicates each using three technical replicates. Significant differences in the gene expression between Ler and different genotypes using Student's t-test are indicated by asterisks: *P<0.05, **P<0.01, ***P<0.005.
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pgen-1004848-g003: Effects of R3 expression with different allelic combinations at SRF3 and QTL5.Expression of RPP1-like Ler genes determined by qRT-PCR in different Ler/Kas-2 recombinant inbred lines (RIL) carrying homozygous allelic combinations at RPP1-like/SRF3/QTL5 loci: Ler/Ler/Kas-2 (AAB), Ler/Kas-2/Ler (ABA), Ler/Kas-2/Kas-2 (ABB). AAB and ABA represent compatible allele combinations, whereas ABB triggers incompatibility. The ABB eds1-2 line carrying an EDS1 loss-of-function mutation is described in [31]. Values are relative to Ler and the mean ± SD of three biological replicates each using three technical replicates. Significant differences in the gene expression between Ler and different genotypes using Student's t-test are indicated by asterisks: *P<0.05, **P<0.01, ***P<0.005.

Mentions: The RPP1-like Ler locus is incompatible with homozygous Kas-2 alleles at SRF3 and a third locus (QTL5) involved in HI with Kas-2 [31]. Because RPP1-like Ler R3 overexpression causes enhanced immunity in a neutral background, we asked whether allelic variation at the SRF3 and QTL5 interacting loci affect expression of genes within the RPP1-like Ler locus. For this, we measured expression of individual RPP1-like Ler genes in Ler/Kas-2 recombinant inbred lines (RILs) [36] carrying incompatible (RPP1-like/SRF3/QTL5: Ler/Kas-2/Kas-2) or compatible combinations of alleles at RPP1, SRF3 and QTL5 (Ler/Ler/Kas-2 and Ler/Kas-2/Ler) (Fig. 3). Expression analyses showed that RPP1-like Ler R3 transcript levels were significantly (≥2.0-fold) higher in RILs carrying incompatible alleles (Fig. 3). Also, R3 transcriptional up-regulation did not occur in an incompatible Ler/Kas-2 line carrying the eds1-2 mutation (Fig. 3). These results underscore the relationship between incompatibility and RPP1-like Ler R3 expression inferred from the amiRNA analysis (Fig. 1B), and suggest that incompatibility involves EDS1-dependent upregulation of RPP1-like Ler R3.


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)

Effects of R3 expression with different allelic combinations at SRF3 and QTL5.Expression of RPP1-like Ler genes determined by qRT-PCR in different Ler/Kas-2 recombinant inbred lines (RIL) carrying homozygous allelic combinations at RPP1-like/SRF3/QTL5 loci: Ler/Ler/Kas-2 (AAB), Ler/Kas-2/Ler (ABA), Ler/Kas-2/Kas-2 (ABB). AAB and ABA represent compatible allele combinations, whereas ABB triggers incompatibility. The ABB eds1-2 line carrying an EDS1 loss-of-function mutation is described in [31]. Values are relative to Ler and the mean ± SD of three biological replicates each using three technical replicates. Significant differences in the gene expression between Ler and different genotypes using Student's t-test are indicated by asterisks: *P<0.05, **P<0.01, ***P<0.005.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004848-g003: Effects of R3 expression with different allelic combinations at SRF3 and QTL5.Expression of RPP1-like Ler genes determined by qRT-PCR in different Ler/Kas-2 recombinant inbred lines (RIL) carrying homozygous allelic combinations at RPP1-like/SRF3/QTL5 loci: Ler/Ler/Kas-2 (AAB), Ler/Kas-2/Ler (ABA), Ler/Kas-2/Kas-2 (ABB). AAB and ABA represent compatible allele combinations, whereas ABB triggers incompatibility. The ABB eds1-2 line carrying an EDS1 loss-of-function mutation is described in [31]. Values are relative to Ler and the mean ± SD of three biological replicates each using three technical replicates. Significant differences in the gene expression between Ler and different genotypes using Student's t-test are indicated by asterisks: *P<0.05, **P<0.01, ***P<0.005.
Mentions: The RPP1-like Ler locus is incompatible with homozygous Kas-2 alleles at SRF3 and a third locus (QTL5) involved in HI with Kas-2 [31]. Because RPP1-like Ler R3 overexpression causes enhanced immunity in a neutral background, we asked whether allelic variation at the SRF3 and QTL5 interacting loci affect expression of genes within the RPP1-like Ler locus. For this, we measured expression of individual RPP1-like Ler genes in Ler/Kas-2 recombinant inbred lines (RILs) [36] carrying incompatible (RPP1-like/SRF3/QTL5: Ler/Kas-2/Kas-2) or compatible combinations of alleles at RPP1, SRF3 and QTL5 (Ler/Ler/Kas-2 and Ler/Kas-2/Ler) (Fig. 3). Expression analyses showed that RPP1-like Ler R3 transcript levels were significantly (≥2.0-fold) higher in RILs carrying incompatible alleles (Fig. 3). Also, R3 transcriptional up-regulation did not occur in an incompatible Ler/Kas-2 line carrying the eds1-2 mutation (Fig. 3). These results underscore the relationship between incompatibility and RPP1-like Ler R3 expression inferred from the amiRNA analysis (Fig. 1B), and suggest that incompatibility involves EDS1-dependent upregulation of RPP1-like Ler R3.

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