Both social and engineering factors must be further explored and scrutinized across the globe—as should notions of justice related to flooding impacts and responses.
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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
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.
Coselected genes confer herbivore defense
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- Comparison of the Relative Potential for Epigenetic and Genetic Variation To Contribute to Trait Stability
- Network-Guided Discovery of Extensive Epistasis between Transcription Factors Involved in Aliphatic Glucosinolate Biosynthesis
- Autopolyploidization, geographic origin, and metabolome evolution in Arabidopsis thaliana
- A Global Coexpression Network Approach for Connecting Genes to Specialized Metabolic Pathways in Plants
- Quantitative Resistance: More Than Just Perception of a Pathogen
- Network-Guided GWAS Improves Identification of Genes Affecting Free Amino Acids
- Systems genetics of plant adaptation to environmental stresses
- Genome-Wide Association Mapping and Genomic Prediction Elucidate the Genetic Architecture of Morphological Traits in Arabidopsis
- Cytonuclear interactions affect adaptive traits of the annual plant Arabidopsis thaliana in the field
- Natural Variation of Plant Metabolism: Genetic Mechanisms, Interpretive Caveats, and Evolutionary and Mechanistic Insights
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