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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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Incompatible phenotypes derived from the cross of Gw+/Kas-2 and Gw+/Kond accessions.Gw+ individuals were crossed to Kas-2 and Kond and their F2 progenies screened for the occurrence of incompatible phenotypes at 14–16°C (see S5 Table). Dwarf plants on the left of each cross carry homozygous Gw (Ler) alleles at RPP1-like locus and homozygous SRF3 Kas-2 or Kond alleles, which are not present in normal sized sister F2 plants from the same cross (right). Incompatibility is absent in the cross of Gw− accessions with Kas-2 or Kond (Gw-160 as representative; see S5 Table).
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pgen-1004848-g007: Incompatible phenotypes derived from the cross of Gw+/Kas-2 and Gw+/Kond accessions.Gw+ individuals were crossed to Kas-2 and Kond and their F2 progenies screened for the occurrence of incompatible phenotypes at 14–16°C (see S5 Table). Dwarf plants on the left of each cross carry homozygous Gw (Ler) alleles at RPP1-like locus and homozygous SRF3 Kas-2 or Kond alleles, which are not present in normal sized sister F2 plants from the same cross (right). Incompatibility is absent in the cross of Gw− accessions with Kas-2 or Kond (Gw-160 as representative; see S5 Table).

Mentions: Having found that the RPP1-like haplotype is maintained within genetically different individuals from a local Gorzów population, we determined whether it also conditions incompatibility with Kas-2 and Kond. Therefore 13 Gw+ individuals belonging to 10 mutlilocus-haplotype groups (Gw-7, Gw-59, Gw-80/81, Gw-87, Gw-89, Gw-91/92, Gw-98, Gw-108, Gw-117 and Gw-152) and three Gw− controls (Gw-31, Gw-99 and Gw-160) were crossed to Kas-2 and Kond and equal numbers of F2 populations generated (S5 Table). Approximately 250 F2 plants per population were then scored for the segregation of incompatible phenotypes at 14–16°C. We detected the incompatibility in all crosses derived from Gw+ individuals with Kas-2 and Kond (S5 Table; Fig. 7). Incompatible F2 individuals always carried Gw (Ler) homozygous alleles at the RPP1-like locus and Kas-2 or Kond homozygous alleles at SRF3 (S5 Table). The data are consistent with involvement of at least two recessive loci in the Gw+/Kas-2 and Gw+/Kond incompatibilities. By contrast, F2 plants derived from crosses of Gw− with Kas-2 did not display HI at 14–16°C (Fig. 7 and S5 Table). These results show that Gw+ individuals carrying the RPP1-like Ler haplotype are incompatible with Kas-2 and Kond. Therefore, the incompatibility reported between Ler/Kas-2 and Ler/Kond can be extended to a population scale.


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)

Incompatible phenotypes derived from the cross of Gw+/Kas-2 and Gw+/Kond accessions.Gw+ individuals were crossed to Kas-2 and Kond and their F2 progenies screened for the occurrence of incompatible phenotypes at 14–16°C (see S5 Table). Dwarf plants on the left of each cross carry homozygous Gw (Ler) alleles at RPP1-like locus and homozygous SRF3 Kas-2 or Kond alleles, which are not present in normal sized sister F2 plants from the same cross (right). Incompatibility is absent in the cross of Gw− accessions with Kas-2 or Kond (Gw-160 as representative; see S5 Table).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004848-g007: Incompatible phenotypes derived from the cross of Gw+/Kas-2 and Gw+/Kond accessions.Gw+ individuals were crossed to Kas-2 and Kond and their F2 progenies screened for the occurrence of incompatible phenotypes at 14–16°C (see S5 Table). Dwarf plants on the left of each cross carry homozygous Gw (Ler) alleles at RPP1-like locus and homozygous SRF3 Kas-2 or Kond alleles, which are not present in normal sized sister F2 plants from the same cross (right). Incompatibility is absent in the cross of Gw− accessions with Kas-2 or Kond (Gw-160 as representative; see S5 Table).
Mentions: Having found that the RPP1-like haplotype is maintained within genetically different individuals from a local Gorzów population, we determined whether it also conditions incompatibility with Kas-2 and Kond. Therefore 13 Gw+ individuals belonging to 10 mutlilocus-haplotype groups (Gw-7, Gw-59, Gw-80/81, Gw-87, Gw-89, Gw-91/92, Gw-98, Gw-108, Gw-117 and Gw-152) and three Gw− controls (Gw-31, Gw-99 and Gw-160) were crossed to Kas-2 and Kond and equal numbers of F2 populations generated (S5 Table). Approximately 250 F2 plants per population were then scored for the segregation of incompatible phenotypes at 14–16°C. We detected the incompatibility in all crosses derived from Gw+ individuals with Kas-2 and Kond (S5 Table; Fig. 7). Incompatible F2 individuals always carried Gw (Ler) homozygous alleles at the RPP1-like locus and Kas-2 or Kond homozygous alleles at SRF3 (S5 Table). The data are consistent with involvement of at least two recessive loci in the Gw+/Kas-2 and Gw+/Kond incompatibilities. By contrast, F2 plants derived from crosses of Gw− with Kas-2 did not display HI at 14–16°C (Fig. 7 and S5 Table). These results show that Gw+ individuals carrying the RPP1-like Ler haplotype are incompatible with Kas-2 and Kond. Therefore, the incompatibility reported between Ler/Kas-2 and Ler/Kond can be extended to a population scale.

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