Comparative genome analyses of Arabidopsis spp.: Inferring chromosomal rearrangement events in the evolutionary history of A. thaliana

Abstract

Comparative genome analysis is a powerful tool that can facilitate the reconstruction of the evolutionary history of the genomes of modern-day species. The model plant Arabidopsis thaliana with its n = 5 genome is thought to be derived from an ancestral n = 8 genome. Pairwise comparative genome analyses of A. thaliana with polyploid and diploid Brassicaceae species have suggested that rapid genome evolution, manifested by chromosomal rearrangements and duplications, characterizes the polyploid, but not the diploid, lineages of this family. In this study, we constructed a low-density genetic linkage map of Arabidopsis lyrata ssp. lyrata (A. l. lyrata; n = 8, diploid), the closest known relative of A. thaliana (MRCA ∼5 Mya), using A. thaliana-specific markers that resolve into the expected eight linkage groups. We then performed comparative Bayesian analyses using raw mapping data from this study and from a Capsella study to infer the number and nature of rearrangements that distinguish the n = 8 genomes of A. l. lyrata and Capsella from the n = 5 genome of A. thaliana. We conclude that there is strong statistical support in favor of the parsimony scenarios of 10 major chromosomal rearrangements separating these n = 8 genomes from A. thaliana. These chromosomal rearrangement events contribute to a rate of chromosomal evolution higher than previously reported in this lineage. We infer that at least seven of these events, common to both sets of data, are responsible for the change in karyotype and underlie genome reduction in A. thaliana.[Supplemental material is available online at www.genome.org. The following individuals kindly provided reagents, samples, or unpublished information as indicated in the paper: C. Langley.]Comparative genome analysis can be a powerful tool to address questions pertaining to the evolution of the structure of genomes (Paterson and Bennetzen 2001). In plant families that include model taxa, such as the Brassicaceae, the Solanaceae, and the Poaceae, comparative mapping studies allow evolutionary inferences related to the nature and number of rearrangements that distinguish the genomes of the model species from those of their less well-studied relatives (Bonierbale et al. 1988;Ahn and Tanksley 1993;Prince et al. 1993;Chittendan et al. 1994;Kurata et al. 1994;Periera et al. 1994;Lagercrantz and Lydiate 1996;Gale and Devos 1998;Lagercrantz 1998;Doganlar et al. 2002). Not only do such inferences facilitate the transfer of knowledge from model taxa to their relatives, but they also provide insight into the process of genome restructuring that can lead to reproductive isolation and ultimately speciation (Rieseberg 2001;Hall et al. 2002). The larger the number of taxa analyzed within a family, the more comprehensive the information is for inferring the nature of ancestral genomes and the evolutionary history that led to the speciation of the members of that family.The Brassicaceae (or Cruciferae) is a dicot family divided into 13 tribes with a total of 360 genera (Al-Shehbaz 1973) including th...

Mechanisms of chromosome number reduction inArabidopsis thalianaand related Brassicaceae species

“…1C). Our data show that the centromeres of AT2 and AT3 retained the same position as in AK3 and AK5 and confirm that chromosomes AT2 and AT3 have been formed by a reciprocal translocation between AK3 and AK5, as indicated previously (7,8,11). Within AK4, no pericentric inversion involving the top arm was found by FISH with pools subdividing this region.…”

“…For A. lyrata, chromosome painting confirmed the pattern of genome colinearity derived from the A. thaliana͞A. lyrata genetic maps (7,8). Moreover, we present new insights as to the centromere positions within the ancestral karyotype and the role of specific inversion and translocation events during chromosome number reduction from n ϭ 8 to n ϭ 5 in A. thaliana.…”

“…To address the chromosomes that correspond to the linkage groups (LGs) of A. lyrata (7,8), multicolor CCP was applied to its pachytene chromosomes. A. thaliana BAC contigs arranged according to the eight LGs (Fig.…”

“…9) and on DNA sequence-derived phylogenetic trees (10), an ancestral karyotype with 8 chromosomes has been inferred. It has been suggested that the karyotype of A. thaliana descended from the ancestral karyotype by two reciprocal translocations, three chromosome fusions, and at least three inversions (8,11).…”

The genome of the mesopolyploid crop species Brassica rapa

“…For example, A. thaliana has experienced two genome duplications since its divergence from Carica, with rapid DNA sequence divergence, extensive gene loss, and fractionation of ancestral gene order eroding the resemblance of A. thaliana to ancestral Brassicales 1 . In the past few million years alone, A. thaliana has experienced a ~30% reduction in genome size 2 and 9-10 chromosomal rearrangements 3,4 that differentiate it from its sister species A. lyrata which retains near-perfect collinearity with representatives of a different genus, Capsella rubella.…”