Further information
Detlef Weigel, Max Planck Institute for Developmental Biology, Tübingen, Germany, presents this Darwin Lecture on: “Evolutionary tradeoffs, plant immunity and speciation”.
Abstract: The inconstancy of the environment places organisms under competing evolutionary pressures, particularly sessile organisms like plants. Allelic variants beneficial in one setting might be detrimental under different circumstances. Plants vary greatly in their ability to resist microbial or animal attack, and this is thought to reflect fitness costs in the absence of pathogens or predators. We have found that allelic diversity at a single locus, ACCELERATED CELL DEATH 6 (ACD6), underpins dramatic variation in both vegetative growth and resistance to microbial infection and herbivory in Arabidopsis thaliana. An ACD6 allele with increased activity, compared to the reference allele, strongly enhances resistance to a 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.
Another example of a potential evolutionary trade-off is provided by our work on hybrid necrosis, which has been observed in many intra- and interspecific plant crosses. Many cases share phenotypic similarities, suggesting a common underlying mechanism across a wide range of species. We have shown that several independent A. thaliana cases result from two-gene epistatic interactions that trigger autoimmune-like responses, and that behave as expected for Dobzhansky-Muller incompatibilities. Molecular analysis has revealed two recurrent themes: the causal genes often occur in polymorphic clusters and most encode disease resistance genes, which are the most divergent genes in plant genomes. This both explains the autoimmune phenotype, and provides a rationale for hybrid necrosis being so common. Our findings thus suggest that the extreme allelic diversity of disease resistance genes, presumably due to pathogen pressures, may frequently result in misinterpretation of endogenous plant proteins as pathogen-derived. That plant immune-system genes are involved in hybrid necrosis moreover implicate selective forces related to host-pathogen conflict as potential causes for the evolution of gene-flow barriers in plants.
Our work in this area is greatly aided by our discovery of whole-genome sequence variation, originally using ultra-high density oligonucleotide arrays, and more recently second-generation sequencing. We have been advocating a 1001 Genomes project for A. thaliana (see http://1001genomes.org), and we have already sequenced 84 wild strains from this species. I might briefly touch on some of the results from these efforts as well.
Supported by the Max Planck Society, ERA-PG ARABRAS, EU FP6 AGRON-OMICS and SIROCCO, and a Gottfried Wilhelm Leibniz Award of the DFG.