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Arabidopsis Thaliana and Its Wild Relatives: a Model System for Ecology and Evolution

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Arabidopsis Thaliana and Its Wild Relatives: a Model System for Ecology and Evolution Review TRENDS in Ecology & Evolution Vol.16 No.12 December 2001 693 Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution Thomas Mitchell-Olds The postgenomics era will bring many changes to ecology and evolution. diploids with eight chromosome pairs. Evolutionary Information about genomic sequence and function provides a new foundation and ecological studies have focused on A. lyrata ssp. for organismal biology. The crucifer Arabidopsis thaliana and its wild relatives lyrata in North America, A. lyrata ssp. petraea and will play an important role in this synthesis of genomics and ecology. We A. halleri in Europe, and A. halleri ssp. gemmifera discuss the need for model systems in ecology, the biology and relationships in Japan. (Earlier literature refers to these taxa as of crucifers, and the molecular resources available for these experiments. The Arabis lyrata, Cardaminopsis petraea, C. halleri scientific potential of this model system is illustrated by several recent studies and Arabis gemmifera, respectively.) Species are in plant–insect interactions, developmental plasticity, comparative genomics interfertile within this group of closely related N = 8 and molecular evolution. taxa. Chromosome number is reduced to N = 5 in A. thaliana, so diploid mapping crosses with wild There is a rich history of field studies on many species relatives are impossible5. However, Arabidopsis in diverse environments in plant ecology and suecica is believed to be an allotetraploid derived from evolution. Molecular methods are sufficiently A. thaliana and A. arenosa. advanced that we can now study the function and Previous taxonomic treatments of Arabis do not evolution of genes that are important in ecology; for constitute a natural classification, because various example, those that control responses to temperature, distantly related species have been included in this drought, pathogens, insects and other environmental grouping2–4, and future taxonomic work is needed in challenges. However, studies in molecular ecology this area. Arabis refers to at least two distantly and evolution require large initial investments in related but natural groups: N = 7 species in North molecular technologies. To be cost effective, these America, and N = 8 species of Arabis sensu stricto in investments must be shared among multiple Eurasia and North America. Arabis alpina is the type laboratories and funding sources. Equally important, species of the genus Arabis, which is distantly related individual investigators can achieve more in-depth to Arabidopsis. This group of N = 8 Arabis spp. is biological understanding when they build upon found in Eurasia, East Africa, northern California previous studies from a research community that and southern Oregon2,4. shares the tools and resources of model organisms. Approximately 50 named species of Arabis, such as Clearly, no single species or model system can address A. holboellii and A. drummondii, are found in North the diverse range of ecological and evolutionary America. This group has a basal number of N = 7 questions of current interest. Nevertheless, the chromosomes, and might be reclassified as genus crucifer Arabidopsis thaliana and its wild relatives Boechera based on taxonomic considerations4. The provide a model system that has a vast array of group is closely related to Arabidopsis, and molecular tools1, genetic resources and biological reproduces by self-pollination, outcrossing or information that can be used to address fundamental APOMIXIS6,7 (see Glossary). Taxa from diverse habitats questions in ecology and evolution (Table 1). can be cross fertilized, so it is feasible to map quantitative trait loci (QTLs) that control local Systematics adaptation to biotic and abiotic factors. Arabidopsis thaliana belongs to the Cruciferae (family Agriculturally important crucifers include Brassicaceae, Capparales). Over the past 40 million Brassica8 and Raphanus. Oilseed rape (canola) years, ~3000 crucifer species have radiated to many consists of varieties of B. napus and B. rapa. habitats worldwide2. Recent molecular and Horticultural crops include European cabbage, morphological studies have outlined systematic cauliflower and brussel sprouts (B. oleracea), Asian Thomas Mitchell-Olds Dept of Genetics and relationships across the Brassicaceae (Fig. 1), and vegetables such as Chinese cabbage and bok choy 2–4 Evolution, Max-Planck across the closest relatives of Arabidopsis . The (B. rapa), and radish (Raphanus spp.). Because Institute of Chemical genus Arabidopsis contains about ten species that are these weedy annuals are widely distributed in Ecology, Winzerlaer native to Eurasia, North Africa and North America. agricultural and other disturbed habitats, they have Strasse 10, 07745 Jena, Germany. The closest wild relatives of A. thaliana (Fig. 2) include featured in many ecological and evolutionary e-mail: [email protected] A. lyrata and A. halleri, which are self-incompatible studies. Rapid cycling genotypes are also useful for http://tree.trends.com 0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02291-1 694 Review TRENDS in Ecology & Evolution Vol.16 No.12 December 2001 Table 1. Examples of ecological and evolutionary questions that can be recombination is apparent in nucleotide addressed using model systems polymorphisms segregating among individuals. Questions Refs Species of Arabidopsis and Arabis have evolved a • What genes are responsible for ecologically important variation? 17 broad range of life-history, developmental and Why are they polymorphic? physiological traits that adapt them to a wide variety of Are quantitative trait locus alleles young, deleterious and spatially restricted, habitats. Combined with molecular tools and biological or are they old widespread polymorphisms contributing to local adaptation? information from A. thaliana, researchers can address • How often do disease resistance genes evolve via an arms race of sequential 18 many ecological questions in these species. Although SELECTIVE SWEEPS, versus ancient polymorphisms maintained by A. thaliana is common in agricultural fields and BALANCING SELECTION? • What ecological processes influence breeding system evolution and the 6 disturbed sites in the temperate zones, it is also found frequency of outcrossing, inbreeding, or asexual reproduction? in undisturbed rocky sites and forest openings • Is plasticity adaptive? 37 (T. Mitchell-Olds and M. Clauss, unpublished). Do developmental responses to environmental conditions increase fitness? Significant isolation by distance across its native range Have these responses been shaped by natural selection? suggests that populations of A. thaliana in Europe and • Can expression profiling identify candidate genes that influence insect 42,44 9 resistance, drought tolerance, flowering time and other ecologically Asia predate human agricultural disturbance , hence important traits in natural populations? they have long ecological and evolutionary histories in Does natural selection promote adaptive evolution of these loci? association with insects, pathogens, competitors and • How do polyploids differ ecologically and physiologically from their 5 abiotic environmental factors. diploid relatives? Among closely related taxa, A. lyrata grows on How are these differences shaped by natural selection? sand dunes, riverbanks, cliffs, or forest understorey in • What is the genetic basis of speciation? 29,50 Does sexual selection of pollen-stigma recognition genes influence sites with low densities of competing species (Fig. 3). reproductive isolation? By contrast, A. halleri thrives in perennial meadows What is the role of gene duplications in interspecific genomic incompatibility? under intense competition with grasses and forbs, as • What is the relative importance of changes in gene regulation versus 14,34 well as in heavy metal-contaminated sites. These protein function within and among species? short-lived perennial species inhabit primarily mesic Have these evolutionary changes resulted from neutral genetic drift or from natural selection? environments. Elsewhere, species of North American • Do neutral molecular markers predict patterns of ecologically important 51 Arabis inhabit deserts and xeric grassland, whereas variation in rare plants? other Arabis taxa grow in cold, wet, or high elevation What is the molecular basis of adaptively important polymorphisms in sites (Fig. 3). In some areas of western North America, endangered species? Arabis spp. can be studied in pristine environments that are largely free of human disturbance. laboratory research. Brassicas are the closest A broad geographical range is important for model agricultural relatives of Arabidopsis, so comparative systems in plant ecology, so that field populations will genomics should provide applied benefits. However, be readily accessible to many researchers. Arabidopsis because these species are ancient polyploids8, and its wild relatives fulfill this need3,12. Arabidopsis molecular studies can be far more complex than in thaliana is widely distributed in North Africa, Eurasia diploid Arabidopsis. and North America. Arabidopsis lyrata is found in Canada, the American Midwest and East Coast, UK, Geography and environments Scandinavia, central Europe, and parts of Asia. A recent study of molecular markers in 142 accessions Arabidopsis halleri ranges from France to Taiwan. sampled from the native range of A. thaliana found N = 7 Arabis
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