Taming the wild: resolving the gene pools of non-model Arabidopsis lineages

BMC Evolutionary Biology Taming the wild: resolving the gene pools of non-model Arabidopsis lineages Nora Hohmann 0 Roswitha Schmickl 0 Tzen-Yuh Chiang Magdalena Luanov Filip Kol Karol Marhold Marcus A Koch 0 0 Centre for Organismal Studies (COS) Heidelberg, Heidelberg University , Heidelberg 69120 , Germany Background: Wild relatives in the genus Arabidopsis are recognized as useful model systems to study traits and evolutionary processes in outcrossing species, which are often difficult or even impossible to investigate in the selfing and annual Arabidopsis thaliana. However, Arabidopsis as a genus is littered with sub-species and ecotypes which make realizing the potential of these non-model Arabidopsis lineages problematic. There are relatively few evolutionary studies which comprehensively characterize the gene pools across all of the Arabidopsis supra-groups and hypothesized evolutionary lineages and none include sampling at a world-wide scale. Here we explore the gene pools of these various taxa using various molecular markers and cytological analyses. Results: Based on ITS, microsatellite, chloroplast and nuclear DNA content data we demonstrate the presence of three major evolutionary groups broadly characterized as A. lyrata group, A. halleri group and A. arenosa group. All are composed of further species and sub-species forming larger aggregates. Depending on the resolution of the marker, a few closely related taxa such as A. pedemontana, A. cebennensis and A. croatica are also clearly distinct evolutionary lineages. ITS sequences and a population-based screen based on microsatellites were highly concordant. The major gene pools identified by ITS sequences were also significantly differentiated by their homoploid nuclear DNA content estimated by flow cytometry. The chloroplast genome provided less resolution than the nuclear data, and it remains unclear whether the extensive haplotype sharing apparent between taxa results from gene flow or incomplete lineage sorting in this relatively young group of species with Pleistocene origins. Conclusions: Our study provides a comprehensive overview of the genetic variation within and among the various taxa of the genus Arabidopsis. The resolved gene pools and evolutionary lineages will set the framework for future comparative studies on genetic diversity. Extensive population-based phylogeographic studies will also be required, however, in particular for A. arenosa and their affiliated taxa and cytotypes. Chloroplast; Cytology; Evolution; ITS; Microsatellites; Systematics; Taxonomy - Background Arabidopsis: life in the fast lane Less than a decade ago Arabidopsis and its poorly known relatives was the title chosen to introduce the closest relatives of Arabidopsis thaliana to a broader readership [1]. This review summarized both the systematics and taxonomy of the genus and also the ecologically important traits to be studied in A. thalianas wild relatives. Its necessity was obvious because until 1999, a huge number of species (60) were recognized in Arabidopsis in the traditional sense. Arabidopsis taxonomical history was compiled in detail more than 10 years ago [2,3], and nine Arabidopsis species with several subspecies were recognized by this time. Based on this work and unraveling the evolutionary history of the genus Arabis [4-7], which differs morphologically from Arabidopsis only in the position of the cotyledons relative to the radicle in the seeds, a new systematic concept was presented 10-15 years ago [4,8,9]. Several species and subspecies have since been added either because molecular studies provided new resolution [10] or because description of new species [11] led to changes in their respective taxonomic rank (species, subspecies, variety) [11-17]. Arabidopsis has been estimated to comprise of at least nine species and six subspecies [8], or up to 13 (or even more) species and nine subspecies [18] depending on the taxonomic approach and the identifier. The most recent studies, e.g. on A. arenosa and its segregates [19], and taxonomic entities within the genus Arabidopsis are summarized in Table 1. Note that few of them will probably not be considered in future either because of insufficient diagnostic morphological characters or because they do not represent monophyletic lineages. Table 1 Arabidopsis species diversity and taxonomy Arabidopsis arenosa species aggregate Arabidopsis arenosa (L.) Lawalre subsp. arenosa (2n = 32) subsp. arenosa var. intermedia (Kovats) Hayek (2n = 32) subsp. borbasii (Zapaowicz) OKane & Al-Shehbaz (2n = 32) Arabidopsis arenosa, unclear taxonomic treatment (2n = 16) Arabidopsis carpatica, nom. prov. (2n = 16) Arabidopsis neglecta (Schultes) OKane & Al-Shehbaz subsp. neglecta (2n = 16) subsp. robusta, nom. prov. (2n = 32) Arabidopsis nitida, nom. prov. (2n = 16) Arabidopsis petrogena (A. Kern) V.I. Dorof. subsp. petrogena (2n = 16) subsp. exoleta, nom. prov. (2n = 32) Arabidopsis lyrata lineage Arabidopsis lyrata subsp. lyrata (L.) OKane & Al-Shehbaz Arabidopsis lyrata subsp. petraea (L.) OKane & Al-Shehbaz = A. petraea (L.) V.I. Dorof. Arabidopsis petraea subsp. umbrosa (Turcz. Ex Steud.) (2n = 16) Elven & D.F. Murray Arabidopsis petraea subsp. septentrionalis (N. Busch) (2n = 32) Elven & D.F. Murray Arabidopsis arenicola (Richardson ex Hook.) Al-Shehbaz et al. (2n = 16) Arabidopsis halleri lineage Arabidopsis halleri subsp. halleri (L.) OKane & Al-Shehbaz (2n = 16) Arabidopsis halleri subsp. dacica (Heuff.) Kolnk (2n = 16) Arabidopsis halleri subsp. gemmifera (Matsum.) OKane & Al-Shehbaz (2n = 16) Arabidopsis halleri subsp. ovirensis (Wulfen) A. P. Iljinsk. (2n = 16) (2n = 32) (2n = 26) Species diversity of Arabidopsis thalianas relatives. Information on taxonomy, chromosome number, ploidy level and geographic distribution is provided. Carpathians (alpine ranges) Carpathians (alpine ranges, only occasionally in lower altitudes) Carpathians (mountain ranges, middle to subalpine altitudes) Arctic NE Asia, Siberia, Alaska, Canada Arctic NE Europe, European Russia to Siberia Arctic Canada and Greenland Japan, winterannual (coastal, lowland) Fennoscandinavia and the Baltic region (2n = 32) Boreal Alasca, Canada, E Siberia, Russian Far East, Korea, Japan, Russian Arabidopsis taxa [17], however, may be considered more carefully in future, based on current morphological and molecular analysis (Koch et al., unpublished data). Monophyly is generally accepted among Arabidopsis taxa by plant scientists at present. However, considering that A. thaliana is a model system taxonomic recognition of new species as Arabidopsis is acknowledged much faster than comparable systematic-taxonomic changes in other genera. One such contrary example from the Brassicaceae family is the genus Noccaea which includes important model species for heavy metal tolerance and hyperaccumulation. Noccaea caerulescens required more than 30 years to be recognized appropriately within the correct evolu (...truncated)