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      Arabidopsis halleri: a perennial model system for studying population differentiation and local adaptation

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          Abstract

          Local adaptation is assumed to occur when populations differ in a phenotypic trait or a set of traits, and such variation has a genetic basis. Here, we introduce Arabidopsis halleri and its life history as a perennial model system to study population differentiation and local adaptation. Studies on altitudinal adaptation have been conducted in two regions: Mt. Ibuki in Japan and the European Alps. Several studies have demonstrated altitudinal adaptation in ultraviolet-B (UV-B) tolerance, leaf water repellency against spring frost and anti-herbivore defences. Studies on population differentiation in A. halleri have also focused on metal hyperaccumulation and tolerance to heavy metal contamination. In these study systems, genome scans to identify candidate genes under selection have been applied. Lastly, we briefly discuss how RNA-Seq can broaden phenotypic space and serve as a link to underlying mechanisms. In conclusion, A. halleri provides us with opportunities to study population differentiation and local adaptation, and relate these to the genetic systems underlying target functional traits.

          Abstract

          One of the most fascinating observations on plants in natural habitats is the spatial co-variation between functional traits and natural environments. Here, we introduce a small perennial clonal herb, Arabidopsis halleri and its life history as a model system to study local adaptation along environmental gradients. Many studies using this species have addressed altitudinal adaptation in diverse functional traits and population differentiation in response to heavy metal contamination in soils. The species provides us with opportunities to study population differentiation and local adaptation, and relate these to the genetic systems underlying target functional traits using recent molecular tools.

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          The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana.

          To take complete advantage of information on within-species polymorphism and divergence from close relatives, one needs to know the rate and the molecular spectrum of spontaneous mutations. To this end, we have searched for de novo spontaneous mutations in the complete nuclear genomes of five Arabidopsis thaliana mutation accumulation lines that had been maintained by single-seed descent for 30 generations. We identified and validated 99 base substitutions and 17 small and large insertions and deletions. Our results imply a spontaneous mutation rate of 7 x 10(-9) base substitutions per site per generation, the majority of which are G:C-->A:T transitions. We explain this very biased spectrum of base substitution mutations as a result of two main processes: deamination of methylated cytosines and ultraviolet light-induced mutagenesis.
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            A map of local adaptation in Arabidopsis thaliana.

            Local adaptation is critical for species persistence in the face of rapid environmental change, but its genetic basis is not well understood. Growing the model plant Arabidopsis thaliana in field experiments in four sites across the species' native range, we identified candidate loci for local adaptation from a genome-wide association study of lifetime fitness in geographically diverse accessions. Fitness-associated loci exhibited both geographic and climatic signatures of local adaptation. Relative to genomic controls, high-fitness alleles were generally distributed closer to the site where they increased fitness, occupying specific and distinct climate spaces. Independent loci with different molecular functions contributed most strongly to fitness variation in each site. Independent local adaptation by distinct genetic mechanisms may facilitate a flexible evolutionary response to changing environment across a species range.
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              Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4.

              Little is known about the types of mutations underlying the evolution of species-specific traits. The metal hyperaccumulator Arabidopsis halleri has the rare ability to colonize heavy-metal-polluted soils, and, as an extremophile sister species of Arabidopsis thaliana, it is a powerful model for research on adaptation. A. halleri naturally accumulates and tolerates leaf concentrations as high as 2.2% zinc and 0.28% cadmium in dry biomass. On the basis of transcriptomics studies, metal hyperaccumulation in A. halleri has been associated with more than 30 candidate genes that are expressed at higher levels in A. halleri than in A. thaliana. Some of these genes have been genetically mapped to broad chromosomal segments of between 4 and 24 cM co-segregating with Zn and Cd hypertolerance. However, the in planta loss-of-function approaches required to demonstrate the contribution of a given candidate gene to metal hyperaccumulation or hypertolerance have not been pursued to date. Using RNA interference to downregulate HMA4 (HEAVY METAL ATPASE 4) expression, we show here that Zn hyperaccumulation and full hypertolerance to Cd and Zn in A. halleri depend on the metal pump HMA4. Contrary to a postulated global trans regulatory factor governing high expression of numerous metal hyperaccumulation genes, we demonstrate that enhanced expression of HMA4 in A. halleri is attributable to a combination of modified cis-regulatory sequences and copy number expansion, in comparison to A. thaliana. Transfer of an A. halleri HMA4 gene to A. thaliana recapitulates Zn partitioning into xylem vessels and the constitutive transcriptional upregulation of Zn deficiency response genes characteristic of Zn hyperaccumulators. Our results demonstrate the importance of cis-regulatory mutations and gene copy number expansion in the evolution of a complex naturally selected extreme trait. The elucidation of a natural strategy for metal hyperaccumulation enables the rational design of technologies for the clean-up of metal-contaminated soils and for bio-fortification.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                AoB Plants
                AoB Plants
                aobpla
                AoB Plants
                Oxford University Press (US )
                2041-2851
                December 2019
                27 November 2019
                27 November 2019
                : 11
                : 6
                : plz076
                Affiliations
                Center for Ecological Research, Kyoto University , Hirano, Otsu, Shiga, Japan
                Author notes
                Article
                plz076
                10.1093/aobpla/plz076
                6899346
                31832127
                db99b386-f3f6-4246-90d1-ede616a14f35
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Annals of Botany Company.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 July 2019
                : 22 October 2019
                : 26 November 2019
                : 08 December 2019
                Page count
                Pages: 13
                Funding
                Funded by: Japan Science and Technology Agency 10.13039/501100002241
                Award ID: JPMJCR15O1
                Funded by: Japan Society for the Promotion of Science 10.13039/501100001691
                Award ID: 19H01001
                Categories
                Special Issue: The Ecology and Genetics of Population Differentiation in Plants

                Plant science & Botany
                altitudinal adaptation,clonal propagation,common garden experiment,genome scan,life history,metalliferous habitat,perennial,rna-seq

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