Plants can defend themselves against a wide array of enemies, yet one of the most striking observations is the variability in the effectiveness of such defences, both within and between species. Some of this variation can be explained by conflicting pressures from pathogens with different modes of attack1. A second explanation comes from an evolutionary tug of war, in which pathogens adapt to evade detection, until the plant has evolved new recognition capabilities for pathogen invasion2-5. If selection is, however, sufficiently strong, susceptible hosts should remain rare. That this is not the case is best justified by costs incurred from constitutive defences in a pest free environment6-11. Using a combination of forward genetics and genome-wide association analyses, we demonstrate that allelic diversity at a single locus, ACCELERATED CELL DEATH 6 (ACD6)12,13, underpins dramatic pleiotropic differences in both vegetative growth and resistance to microbial infection and herbivory among natural Arabidopsis thaliana strains. A hyperactive ACD6 allele, compared to the reference allele, strongly enhances resistance to a broad range of pathogens from different phyla, but at the same time slows the production of new leaves and greatly reduces the biomass of mature leaves. This allele segregates at intermediate frequency both throughout the worldwide range of A. thaliana and within local populations, consistent with this allele providing substantial fitness benefits despite its drastic impact on growth.

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 hotspots in the genome, often in regions densely populated by 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, DANGEROUS MIX2 (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 at the front lines of host-pathogen co-evolution limit the combinations of favorable disease resistance alleles accessible to plant genomes.

Several key processes in plant development are regulated by TCP transcription factors. CYCLOIDEA-like (CYC-like) TCP domain proteins have been shown to control flower symmetry in distantly related plant lineages. Gerbera hybrida, a member of one of the largest clades of angiosperms, the sunflower family (Asteraceae), is an interesting model for developmental studies because its elaborate inflorescence comprises different types of flowers that have specialized structures and functions. The morphological differentiation of flower types involves gradual changes in flower size and symmetry that follow the radial organization of the densely packed inflorescence. Differences in the degree of petal fusion further define the distinct shapes of the Gerbera flower types. To study the role of TCP transcription factors during specification of this complex inflorescence organization, we characterized the CYC-like homolog GhCYC2 from Gerbera. The expression of GhCYC2 follows a gradient along the radial axis of the inflorescence. GhCYC2 is expressed in the marginal, bilaterally symmetrical ray flowers but not in the centermost disk flowers, which are nearly radially symmetrical and have significantly less fused petals. Overexpression of GhCYC2 causes disk flowers to obtain morphologies similar to ray flowers. Both expression patterns and transgenic phenotypes suggest that GhCYC2 is involved in differentiation among Gerbera flower types, providing the first molecular evidence that CYC-like TCP factors take part in defining the complex inflorescence structure of the Asteraceae, a major determinant of the family's evolutionary success.CYCLOIDEA ͉ flower development ͉ evo-devo ͉ organ fusion

As Arabidopsis thaliana is increasingly employed in evolutionary and ecological studies, it is essential to understand patterns of natural genetic variation and the forces that shape them. Previous work focusing mostly on global and regional scales has demonstrated the importance of historical events such as long-distance migration and colonization. Far less is known about the role of contemporary factors or environmental heterogeneity in generating diversity patterns at local scales. We sampled 1,005 individuals from 77 closely spaced stands in diverse settings around Tübingen, Germany. A set of 436 SNP markers was used to characterize genome-wide patterns of relatedness and recombination. Neighboring genotypes often shared mosaic blocks of alternating marker identity and divergence. We detected recent outcrossing as well as stretches of residual heterozygosity in largely homozygous recombinants. As has been observed for several other selfing species, there was considerable heterogeneity among sites in diversity and outcrossing, with rural stands exhibiting greater diversity and heterozygosity than urban stands. Fine-scale spatial structure was evident as well. Within stands, spatial structure correlated negatively with observed heterozygosity, suggesting that the high homozygosity of natural A. thaliana may be partially attributable to nearest-neighbor mating of related individuals. The large number of markers and extensive local sampling employed here afforded unusual power to characterize local genetic patterns. Contemporary processes such as ongoing outcrossing play an important role in determining distribution of genetic diversity at this scale. Local “outcrossing hotspots” appear to reshuffle genetic information at surprising rates, while other stands contribute comparatively little. Our findings have important implications for sampling and interpreting diversity among A. thaliana accessions.

Recombination during meiosis shapes the complement of alleles segregating in the progeny of hybrids, and has important consequences for phenotypic variation. We examined allele frequencies, as well as crossover (XO) locations and frequencies in over 7000 plants from 17 F 2 populations derived from crosses between 18 Arabidopsis thaliana accessions. We observed segregation distortion between parental alleles in over half of our populations. The potential causes of distortion include variation in seed dormancy and lethal epistatic interactions. Such a high occurrence of distortion was only detected here because of the large sample size of each population and the number of populations characterized. Most plants carry only one or two XOs per chromosome pair, and therefore inherit very large, non-recombined genomic fragments from each parent. Recombination frequencies vary between populations but consistently increase adjacent to the centromeres. Importantly, recombination rates do not correlate with whole-genome sequence differences between parental accessions, suggesting that sequence diversity within A. thaliana does not normally reach levels that are high enough to exert a major influence on the formation of XOs. A global knowledge of the patterns of recombination in F 2 populations is crucial to better understand the segregation of phenotypic traits in hybrids, in the laboratory or in the wild.