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Comparative Gene Mapping in Arabidopsis Lyrata Chromosomes 1 and 2 and the Corresponding A Genet. Res., Camb. (2006), 87, pp. 75–85. f 2006 Cambridge University Press 75 doi:10.1017/S0016672306008020 Printed in the United Kingdom Comparative gene mapping in Arabidopsis lyrata chromosomes 1 and 2 and the corresponding A. thaliana chromosome 1: recombination rates, rearrangements and centromere location BENGT HANSSON1 #, AKIRA KAWABE1,SONJAPREUSS1, HELMI KUITTINEN2 AND DEBORAH CHARLESWORTH1* 1Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK 2 Department of Biology, PL 3000, FIN-90014 University of Oulu, Finland (Received 7 November 2005 and in revised form 23 December 2006) Summary To add detail to the genetic map of Arabidopsis lyrata, and compare it with that of A. thaliana, we have developed many additional markers in the A. lyrata linkage groups, LG1 and LG2, corresponding to A. thaliana chromosome 1. We used a newly developed method for marker development for single nucleotide polymorphisms present in gene sequences, plus length differences, to map genes in an A. lyrata family, including variants in several genes close to the A. thaliana centromere 1, providing the first data on the location of an A. lyrata centromere; we discuss the implications for the evolution of chromosome 1 of A. thaliana. With our larger marker density, large rearrangements between the two Arabidopsis species are excluded, except for a large inversion on LG2. This was previously known in Capsella; its presence in A. lyrata suggests that, like most other rearrangements, it probably arose in the A. thaliana lineage. Knowing that marker orders are similar, we can now compare homologous, non-rearranged map distances to test the prediction of more frequent crossing-over in the more inbreeding species. Our results support the previous conclusion of similar distances in the two species for A. lyrata LG1 markers. For LG2 markers, the distances were consistently, but non-significantly, larger in A. lyrata. Given the two species’ large DNA content difference, the similarity of map lengths, particularly for LG1, suggests that crossing-over is more frequent across comparable physical distances in the inbreeder, A. thaliana, as predicted. 1. Introduction has a DNA content about 50% higher (Johnston et al., 2005). Most likely, the weedy life-history of Genetic mapping is of evident importance in any A. thaliana has selected for this reduction, but other species of ecological or genetic interest, and molecular factors may have contributed. For instance, trans- markers are providing the ability to map ever more posable elements (TEs) may have come to lower species. The availability of the complete genome se- equilibrium abundances, in response to the species’ quence of Arabidopsis thaliana now makes it possible high selfing rate, as predicted from theoretical models to begin studies of genome evolution in the genus of TE abundance (Charlesworth & Charlesworth, Arabidopsis. It is well known that A. thaliana is a plant 1995; Wright et al., 2001; Wright & Schoen, 1999; with a small DNA content (Arumuganathan & Earle, Devos et al., 2002). In addition, loss of genomic DNA 1991), with a haploid genome of about 0.16 pico- may have occurred in chromosome rearrangements. grams (Bennett et al., 2003), or about 157 Mbp, and it It is clearly of great interest to know how these is likely that this is due to loss of DNA since the split changes in DNA content evolved, the time periods from related species, since the close relative, A. lyrata, involved, and how they affect recombination rates. Recombination rate differences may evolve quite * Corresponding author. Tel: +44 131 6505751. Fax: +44 131 quickly. Recombination hotspots differ between 6506564. e-mail: [email protected] # Present address: Department of Animal Ecology, Lund Uni- humans and chimpanzees (Winckler et al., 2005), and versity, Ecology Building, 22362 Lund, Sweden. genetic map distances differ between Drosophila Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 25 Sep 2021 at 07:13:14, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0016672306008020 B. Hansson et al. 76 species (e.g. True et al., 1996). Even strains of the in the mapped Arabidopsis and related species, but same species may differ. Within Arabidopsis thaliana, marker densities are low and rearrangements in some crossover frequencies differ between strains (Sanchez- regions may be missed (Kuittinen et al., 2004; Moran et al., 2002). Some general patterns have also Yogeeswaran et al., 2005; Koch & Kiefer, 2005; been observed cytologically in recombination rates, Boivin et al., 2004). particularly the greater chiasma frequency of in- To understand genome evolution and its conse- breeding species compared with outcrossing relatives quences for sequence diversity, data are needed about (Arroyo, 1975; Garber, 1956; Zarchi et al., 1972; both genetic and physical maps. These are available Grant, 1958; Rees, 1961). There are some reasons for A. thaliana, from the genome sequence together for expecting this difference, since some models that with mapping studies (Lister & Dean, 1993; select for recombination lead to higher recombination Copenhaver et al., 1997; Alonso-Blanco et al., 1998), when the population is inbreeding (Charlesworth but detailed comparisons with A. lyrata will require et al., 1977, 1979; Hedrick et al., 1978). Alternatively, mapping of densely spaced markers, and physical large diversity (i.e. greater sequence differences be- mapping information (which should become available tween alleles) in outcrossers has been suggested to from the forthcoming genome sequencing of this inhibit recombination (Borts & Haber, 1987), though species). Here, we describe mapping of 35 additional the divergence will generally not be enough for this to markers in the A. lyrata chromosomes corresponding be likely, and this interpretation is also contradicted to linkage groups 1 and 2 (LG1 and LG2 of Kuittinen by evidence that duplicate genes (paralogues) within et al., 2004), which are jointly homologous to A. yeast genomes can continue to undergo gene conver- thaliana chromosome 1 (Kuittinen et al., 2004; sion until their sequences have diverged considerably Yogeeswaran et al., 2005; Koch & Kiefer, 2005; (Gao & Innan, 2004). Boivin et al., 2004). Most of our markers were devel- To our knowledge, no previous studies have tested oped using a new approach named ‘ASP’ (see descrip- whether the expected chiasma frequency differences tion below), which uses allele-specific primers based between inbreeders and outcrossers are reflected in on coding sequences of identified genes in A. thaliana recombination distances estimated genetically. The (Hansson & Kawabe, 2005). Using genic markers genus Arabidopsis offers an excellent opportunity to allows comparisons between the genetic maps, which begin to test this. Its chromosome evolution is also is necessary for studying chromosome evolution. of interest, since A. thaliana, with 2n=2x=10 chro- In combination with the previously mapped markers mosomes, has several chromosome fusions relative to in Kuittinen et al. (2004), we now have 55 markers other related species, with 2n=2x=16 (Lysak et al., on A. lyrata LG1 and LG2 markers. The orthologous 2003). Closely related species are known, including A. thaliana genes are distributed across the whole of the outcrossing species A. lyrata, which is estimated, chromosome 1. Our mapping confirms the general using a molecular clock, to have split from A. thaliana conclusions of the previous maps that marker orders roughly 5 MYA ago. The self-compatible species, are similar in the two Arabidopsis species, with the Capsella rubella, is more distantly related, but still exception of a few genes with two copies in A. lyrata split recently enough to be a suitable outgroup for but only one in A. thaliana, and a large inversion inferring the directions of evolutionary changes on LG2. Our greater marker density excludes all (Koch et al., 2000). except small rearrangements, so that we can now Fusions are known to be common in inbreeders compare map distances without the danger that large (Lande, 1984; Charlesworth, 1992), and two sparse rearrangements might be present in the regions com- maps of A. lyrata (Kuittinen et al., 2004; pared. Our study supports in more detail the previous Yogeeswaran et al., 2005; Koch & Kiefer, 2005) de- conclusion (Kuittinen et al., 2004) that distances of duced that several fusions have occurred in A. thali- the markers on A. lyrata LG1, and perhaps also LG2, ana, accounting for this species’ five chromosomes, are similar between the two species. Finally, the simi- versus the eight chromosomes of A. lyrata and other larity of gene orders in the two species suggests that closely related species. One fusion joins the lower arm it may be possible to identify the centromere locations of two ancestral acrocentric chromosomes (corre- in A. lyrata, and we also describe evidence for puta- sponding to the A. lyrata chromosomes 1 and 2), tive centromere locations in one of the two linkage forming A. thaliana chromosome 1, and two others groups studied, and discuss the implications for the formed the long arms of the A. thaliana chromosomes evolution of chromosome 1 of A. thaliana. 2 and 5. Reciprocal translocations also occurred between chromosome arms. Large tracts of genome 2. Materials and methods should nevertheless be syntenic, unless rearrange- (i) Materials ments within the major chromosome arm regions have followed these events. Most chromosome arms DNA samples were used from the A. lyrata subsp. indeed have the same gene content, in the same order, petraea mapping family of Kuittinen et al. (2004). In Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 25 Sep 2021 at 07:13:14, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0016672306008020 Comparative gene mapping in Arabidopsis lyrata and A. thaliana 77 what follows, we refer to the species as A.
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