Natural genetic variation in Arabidopsis thaliana defense metabolism genes modulates field fitness

• Published in: eLife Vol. 4
• Main Authors: Kerwin, Rachel, Feusier, Julie, Corwin, Jason, Rubin, Matthew, Lin, Catherine, Muok, Alise, Larson, Brandon, Li, Baohua, Joseph, Bindu, Francisco, Marta, Copeland, Daniel, Weinig, Cynthia, Kliebenstein, Daniel J
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 13.04.2015; eLife Sciences Publications, Ltd
• Subjects: Alleles; Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis thaliana; Cloning; Ecology; Ecotype; Environment; Evolution; fitness; Flowers - genetics; Gene-Environment Interaction; Genes, Plant; Genetic diversity; Genetic Fitness; Genetic Loci; Genetic Pleiotropy; Genetic Variation; Genomics and Evolutionary Biology; Genotype & phenotype; Genotypes; glucosinolate; Glucosinolates; Glucosinolates - biosynthesis; Haplotypes - genetics; herbivory; Laboratories; Mutation; Natural selection; natural variation; Nutrition research; Pathogens; Phenotype; plant defense; Plant Leaves - genetics; Polymorphism, Genetic; Principal Component Analysis; Quantitative Trait, Heritable; Reproductive fitness; ecology; evolutionary biology; plant defense; fitness; glucosinolates; natural variation; herbivory; genomics; arabidopsis
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.05604

Natural populations persist in complex environments, where biotic stressors, such as pathogen and insect communities, fluctuate temporally and spatially. These shifting biotic pressures generate heterogeneous selective forces that can maintain standing natural variation within a species. To directly test if genes containing causal variation for the Arabidopsis thaliana defensive compounds, glucosinolates (GSL) control field fitness and are therefore subject to natural selection, we conducted a multi-year field trial using lines that vary in only specific causal genes. Interestingly, we found that variation in these naturally polymorphic GSL genes affected fitness in each of our environments but the pattern fluctuated such that highly fit genotypes in one trial displayed lower fitness in another and that no GSL genotype or genotypes consistently out-performed the others. This was true both across locations and within the same location across years. These results indicate that environmental heterogeneity may contribute to the maintenance of GSL variation observed within Arabidopsis thaliana. ‘Genetic variation’ describes the naturally occurring differences in DNA sequences that are found among individuals of the same species. These genetic differences arise from random mutations and may be passed on to their offspring. Some of these mutations may improve the ability of an individual to survive and reproduce—known as fitness—and are likely to become more common in the population. Other mutations may reduce an individual's fitness and are likely to be lost. However, it is believed that most of the mutations will have no effect on the fitness of individuals. It is not known why many of these ‘neutral’ genetic differences are maintained in populations. Some researchers have proposed that they are kept by chance and that there is no direct advantage to the population of keeping them unless these neutral mutations later become beneficial. However, other researchers think that the genetic variation itself may improve the fitness of the population by allowing it to quickly adapt to changes in the environment. Arabidopsis thaliana is a small plant that lives in many different environments and has high levels of genetic variation in many of its physical traits. One of these traits is the production of molecules called glucosinolates, which help the plants to defend against herbivores and infection by microbes. Previous studies have suggested that variation in the genes that make glucosinolates may improve the fitness of A. thaliana populations. To test this idea, Kerwin et al. carried out a field trial using A. thaliana plants that were genetically identical except for some of the genes involved in the production of glucosinolates. Kerwin et al. grew the plants in several different environments over several years. The field trial shows that variation in these genes affected the fitness of the plants in each of the different environments. However, the fitness benefit depended on the environment, and no single gene variant provided the best fitness across all environments, or over all the years of the trial. Kerwin et al.'s findings suggest that changes in the environment may contribute to the maintenance of genetic variation in the genes that make glucosinolates. This raises the questions of how many other genes in plants (or other species such as humans) have genetic variation that contributes to fitness across varied environments; and how can this link be tested in natural settings.