Genome evolution in Arabidopsis/Brassica: conservation and divergence of ancient rearranged segments and their breakpoints

Abstract

Since the tetraploidization of the Arabidopsis thaliana ancestor 30-35 million years ago (Mya), a wave of chromosomal rearrangements have modified its genome architecture. The dynamics of this process is unknown, as it has so far been impossible to date individual rearrangement events. In this paper, we present evidence demonstrating that the majority of rearrangements occurred before the Arabidopsis-Brassica split 20-24 Mya, and that the segmental architecture of the A. thaliana genome is predominantly conserved in Brassica. This finding is based on the conservation of four rearrangement breakpoints analysed by fluorescence in situ hybridization (FISH) and RFLP mapping of three A. thaliana chromosomal regions. For this purpose, 95 Arabidopsis bacterial artificial chromosomes (BACs) spanning a total of 8.25 Mb and 81 genetic loci for 36 marker genes were studied in the Brassica oleracea genome. All the regions under study were triplicated in the B. oleracea genome, confirming the hypothesis of Brassica ancestral genome triplication. However, whilst one of the breakpoints was conserved at one locus, it was not at the two others. Further comparison of their organization may indicate that the evolution of the hexaploid Brassica progenitor proceeded by several events, separated in time. Genetic mapping and reprobing with rDNA allowed assignment of the regions to particular Brassica chromosomes. Based on this study of regional organization and evolution, a new insight into polyploidization/diploidization cycles is proposed.

Ancestral Chromosomal Blocks Are Triplicated in Brassiceae Species with Varying Chromosome Number and Genome Size

“…The absence of the genome triplication in Calepina and Conringia species (n 5 7, 8) suggested the placement of these genera outside the tribe Brassiceae (Lysak et al, 2005). Similar to the previous study, three different ancestral blocks (J, M, and N) were found to be triplicated in the B. oleracea (n 5 9) complement upon CCP analysis (Ziolkowski et al, 2006). Hence, cytogenetic data corroborate the results of genetic mapping studies and provide strong evidence for the occurrence of an ancient whole-genome triplication event defining the tribe Brassiceae as a natural monophyletic lineage (Lysak et al, 2005;Lysak and Lexer, 2006).…”

“…Three homeologous copies of block F found in Brassiceae species studied herein are in agreement with genetic mapping data (Parkin et al, 2005, and refs. therein) and provide further evidence for the ancient triplication of the Brassiceae genomes as previously shown for ancestral block U in a number of Brassiceae taxa (Lysak et al, 2005) and for blocks J, M, and N in B. oleracea (Ziolkowski et al, 2006). .…”

Fast Diploidization in Close Mesopolyploid Relatives ofArabidopsis

“…The unexpectedly detected WGD shared by the diploid Australian crucifer species is analogous to the mesopolyploid whole-genome triplication discerned in the tribe Brassiceae by comparative genetic mapping (Lagercrantz and Lydiate, 1996;Parkin et al, 2005) and by comparative cytogenetic analysis (Lysak et al, 2005(Lysak et al, , 2007Ziolkowski et al, 2006). Several lineagespecific WGD events thus far documented across the angiosperms (Tang et al, 2008;Jaillon et al, 2009;Soltis et al, 2009) represent only the tip of the iceberg, as potential other WGD events remain uncovered.…”

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

“…In addition to the ancient paleopolyploidy events (a, b, and g WGD), a further peak at Ks = 0.38 (Figure 2; Supplemental Table 4) was found in the B. rapa distribution, representing the now well documented mesopolyploidy event (Parkin et al, 2005;Ziolkowski et al, 2006;Wang et al, 2011). Similarly, mixture model analyses of the Ks distributions of L. alabamica and C. sativa also revealed the presence of a major peak at Ks = 0.33 and 0.09, respectively ( Figure 2C), which represent the independent hexaploidy events experienced by these species (Haudry et al, 2013;Kagale et al, 2014).…”

“…The genome of A. thaliana revealed compelling evidence for remnants of at least three paleopolyploidy events, known as a, b, and g WGDs (Bowers et al, 2003), that are shared by all crucifer taxa (Haudry et al, 2013). Additionally, early comparative genetic mapping (Parkin et al, 2005) and cytogenetic studies (Lysak et al, 2005;Ziolkowski et al, 2006), as well as the recent whole-genome sequencing of Brassica rapa (Wang et al, 2011) have identified an additional later mesopolyploidy (wholegenome triplication) event in diploid Brassicas. Using Bayesian approaches and fossil information as age constraints, the age of the triplication event has now been estimated to be 22.5 million years (Beilstein et al, 2010).…”