Cell: NLRs as hotspots of deleterious epistasis

Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis

Species-wide Genetic Incompatibility Analysis Identifies Immune Genes as Hot Spots of Deleterious Epistasis

Eunyoung Chae, Kirsten Bomblies, Sang-Tae Kim, Darya Karelina, Maricris Zaidem, Stephan Ossowski, Carmen Martín-Pizarro, Roosa A.E. Laitinen, Beth A. Rowan, Hezi Tenenboim, Sarah Lechner, Monika Demar, Anette Habring-Müller, Christa Lanz, Gunnar Rätsch, Detlef Weigel

Cell, published online November 20, 2014

Highlights

  • A species-wide genetic analysis identifies incompatibility hot spots in the genome
  • Antagonistic epistasis involving plant NLR immune receptors is a common cause
  • Polymorphic NLR tandem arrays can generate multiple incompatibility alleles
  • Deleterious epistasis limits the accessible space of immune receptor combinations

Summary
Intraspecific genetic incompatibilities prevent the assembly of specific alleles into single genotypes and influence genome- and species-wide patterns of sequence variation. A common incompatibility in plants is hybrid necrosis, characterized by autoimmune responses due to epistatic interactions between natural genetic variants. By systematically testing thousands of F1 hybrids of Arabidopsis thaliana strains, we identified a small number of incompatibility hot spots in the genome, often in regions densely populated by nucleotide-binding domain and leucine-rich repeat (NLR) immune receptor genes. In several cases, these immune receptor loci interact with each other, suggestive of conflict within the immune system. A particularly dangerous locus is a highly variable cluster of NLR genes, DM2, which causes multiple independent incompatibilities with genes that encode a range of biochemical functions, including NLRs. Our findings suggest that deleterious interactions of immune receptors limit the combinations of favorable disease resistance alleles accessible to plant genomes.