Coselected genes determine adaptive variation in herbivore resistance throughout the native range of Arabidopsis thaliana

Benjamin Brachi; Christopher G. Meyer; Romain Villoutreix; Alexander Platt; Timothy C. Morton; Fabrice Roux; Joy Bergelson

doi:10.1073/pnas.1421416112

Edited by Trudy F. C. Mackay, North Carolina State University, Raleigh, NC, and approved February 20, 2015 (received for review November 8, 2014)

Significance

How organisms adapt to the biotic and abiotic environment is a major question in evolutionary biology that addresses how natural selection shapes biodiversity. Using mass spectrometry, we characterized natural variation in major defense molecules, aliphatic glucosinolates, in hundreds of ecotypes of the model plant Arabidopsis thaliana, spanning the native range of the species. Using extensive genomic resources and field experiments, we provide strong evidence that populations are adapted to local herbivore communities along a striking longitudinal cline. In addition, we show that only a few genes of strong effect govern this natural variation and that alleles at these genes, located on different chromosomes, appear to have coevolved through epistatic selection.

Abstract

The “mustard oil bomb” is a major defense mechanism in the Brassicaceae, which includes crops such as canola and the model plant Arabidopsis thaliana. These plants produce and store blends of amino acid-derived secondary metabolites called glucosinolates. Upon tissue rupture by natural enemies, the myrosinase enzyme hydrolyses glucosinolates, releasing defense molecules. Brassicaceae display extensive variation in the mixture of glucosinolates that they produce. To investigate the genetics underlying natural variation in glucosinolate profiles, we conducted a large genome-wide association study of 22 methionine-derived glucosinolates using A. thaliana accessions from across Europe. We found that 36% of among accession variation in overall glucosinolate profile was explained by genetic differentiation at only three known loci from the glucosinolate pathway. Glucosinolate-related SNPs were up to 490-fold enriched in the extreme tail of the genome-wide FST scan, indicating strong selection on loci controlling this pathway. Glucosinolate profiles displayed a striking longitudinal gradient with alkenyl and hydroxyalkenyl glucosinolates enriched in the West. We detected a significant contribution of glucosinolate loci toward general herbivore resistance and lifetime fitness in common garden experiments conducted in France, where accessions are enriched in hydroxyalkenyls. In addition to demonstrating the adaptive value of glucosinolate profile variation, we also detected long-distance linkage disequilibrium at two underlying loci, GS-OH and GS-ELONG. Locally cooccurring alleles at these loci display epistatic effects on herbivore resistance and fitness in ecologically realistic conditions. Together, our results suggest that natural selection has favored a locally adaptive configuration of physically unlinked loci in Western Europe.

Footnotes

↵¹B.B. and C.G.M. contributed equally to this work.
↵²To whom correspondence should be addressed. Email: jbergels{at}uchicago.edu.

Author contributions: B.B., C.G.M., and J.B. designed research; B.B., C.G.M., R.V., and F.R. performed research; A.P. and T.C.M. contributed new reagents/analytic tools; B.B. and C.G.M. analyzed data; and B.B., C.G.M., and J.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1421416112/-/DCSupplemental.

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