Island species radiation and karyotypic stasis in Pachycladonallopolyploids

Abstract

BackgroundPachycladon (Brassicaceae, tribe Camelineae) is a monophyletic genus of ten morphologically and ecogeographically differentiated, and presumably allopolyploid species occurring in the South Island of New Zealand and in Tasmania. All Pachycladon species possess ten chromosome pairs (2n = 20). The feasibility of comparative chromosome painting (CCP) in crucifer species allows the origin and genome evolution in this genus to be elucidated. We focus on the origin and genome evolution of Pachycladon as well as on its genomic relationship to other crucifer species, particularly to the allopolyploid Australian Camelineae taxa. As species radiation on islands is usually characterized by chromosomal stasis, i.e. uniformity of chromosome numbers/ploidy levels, the role of major karyotypic reshuffling during the island adaptive and species radiation in Pachycladon is investigated through whole-genome CCP analysis.ResultsThe four analyzed Pachycladon species possess an identical karyotype structure. The consensual ancestral karyotype is most likely common to all Pachycladon species and corroborates the monophyletic origin of the genus evidenced by previous phylogenetic analyses. The ancestral Pachycladon karyotype (n = 10) originated through an allopolyploidization event between two genomes structurally resembling the Ancestral Crucifer Karyotype (ACK, n = 8). The primary allopolyploid (apparently with n = 16) has undergone genome reshuffling by descending dysploidy toward n = 10. Chromosome "fusions" were mediated by inversions, translocations and centromere inactivation/loss. Pachycladon chromosome 3 (PC3) resulted from insertional fusion, described in grasses. The allopolyploid ancestor originated in Australia, from the same or closely related ACK-like parental species as the Australian Camelineae allopolyploids. However, the two whole-genome duplication (WGD) events were independent, with the Pachycladon WGD being significantly younger. The long-distance dispersal of the diploidized Pachycladon ancestor to New Zealand was followed by the Pleistocene species radiation in alpine habitats and characterized by karyotypic stasis.ConclusionsKaryotypic stasis in Pachycladon suggests that the insular species radiation in this genus proceeded through homoploid divergence rather than through species-specific gross chromosomal repatterning. The ancestral Pachycladon genome originated in Australia through an allopolyploidization event involving two closely related parental genomes, and spread to New Zealand by a long-distance dispersal. We argue that the chromosome number decrease mediated by inter-genomic reshuffling (diploidization) could provide the Pachycladon allopolyploid founder with an adaptive advantage to colonize montane/alpine habitats. The ancestral Pachycladon karyotype remained stable during the Pleistocene adaptive radiation into ten different species.

A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History

“…In Brassicaceae, mesopolyploid WGDs postdating the a-WGD most likely accelerated diversification and species radiation in the Brassiceae (Lysak et al, 2005), the New Zealand and Australian Microlepidieae (Mandáková et al, 2010a(Mandáková et al, , 2010b, Heliophileae (Mandáková et al, 2012), Biscutelleae (C. Geiser, T. Mandáková, N. Arrigo, M.A. Lysak, and C. Parisod, unpublished results), Thelypodieae (Burrell et al, 2011), Leavenworthia (Cardamineae; Haudry et al, 2013), and possibly in Physarieae (Lysak et al, 2009).…”

“…To date, four tribes (Heliophileae [Mandáková et al, 2012], Microlepidieae [Joly et al, 2009;Mandáková et al, 2010aMandáková et al, , 2010b, Brassiceae and Brassicas [Lysak et al, 2005;Wang et al, 2011;Cheng et al, 2013], and Biscutelleae [C. Geiser, T. Mandáková, N. Arrigo, M.A. Lysak, and C. Parisod, unpublished results]) and the genus Leavenworthia (Haudry et al, 2013) have been shown to be mesopolyploids, which have undergone post-At-a polyploidizations.…”

The More the Merrier: Recent Hybridization and Polyploidy in Cardamine

“…Whereas the centromere of the insertion chromosome is maintained and that of the recipient chromosome is inactivated in grasses, in C. pratensis, the centromere of the insertion chromosome is lost and the centromere of the recipient chromosome remains functional. In Brassicaceae, NCFs have been previously documented as mediating chromosome number decreases in the ancestral genomes of Pachycladon (Mandáková et al, 2010a) and Hornungia but not as a mechanism responsible for intraspecific chromosome number variation. Our data explain the extensive intraspecific karyological variation in the C. pratensis species complex (Lövkvist, 1956;Ku cera et al, 2005) as the combination of intraspecific descending dysploidy and hybridization resulting in series of dysploid chromosome numbers deviating from the multiples of the ancestral base number (x = 8).…”

“…The recently established techniques, such as massive parallel sequencing and CCP, as well as detailed FISH/GISH analyses have highlighted several cases where the examination of the allopolyploid genomes revealed their complex origin and extensive intraspecific variability (Kantama et al, 2007;Xiong et al, 2011;Chester et al, 2012). Chromosome numbers increase due to repetitive cycles of wholegenome duplication (i.e., auto-and allopolyploidy) and decrease through fusion-like chromosome translocations during the genome diploidization process Arrigo and Barker, 2012;Mandáková et al, 2010aMandáková et al, , 2010b. Multispecies hybridization, exemplified here by Cardamine, and aneuploidy (Comai, 2005;Henry et al, 2005;Considine et al, 2012) may further modify chromosome numbers.…”

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

“…Similarly, recent genome sequencing of Leavenworthia alabamica (Haudry et al, 2013), Camelina sativa (Kagale et al, 2014), and Brassica oleracea (Liu et al, 2014;Parkin et al, 2014) have uncovered more recent neo/mesopolyploidy events that formed the basis for the evolution of their hexaploid genomes. Comparative cytogenetic and molecular phylogenetic analyses have unveiled additional mesopolyploidy events in a few Australian and New Zealand crucifer genera belonging to the Microlepidieae and Heliophileae tribes that are endemic to Namibia and South Africa (Joly et al, 2009;Mandáková et al, 2010aMandáková et al, , 2010bMandáková et al, , 2012, implying a key role for recurring mesopolyploidy events in the diversification of the Brassicaceae. These data and the substantial numerical expansion of the chromosome complement from the base ancestral karyotype across the Brassicaceae suggest that the neo/mesopolyploidy events revealed so far could represent a fraction of the total.…”