Idahoa and Subularia: Hidden polyploid origins of two enigmatic genera of crucifers.

PREMISE: The monotypic Idahoa (I. scapigera) and the bispecific Subularia (S. aquatica and S. monticola) belong to Brassicaceae with unclear phylogenetic relationships and no tribal assignment. To fill this knowledge gap, we investigated these species and their closest relatives by combining cytogenomic and phylogenomic methods. METHODS: We used whole plastome sequences in maximum likelihood and Bayesian inference analyses. We tested the phylogenetic informativeness of shared genomic repeats. We combined nuclear gene tree reconciliation and comparative chromosome painting (CCP) to examine the occurrence of past whole-genome duplications (WGDs). RESULTS: The plastid data set corroborated the sister relationship between Idahoa and Subularia within the crucifer Lineage V but failed to resolve consistent topologies using both inference methods. The shared repetitive sequences provided conflicting pwhylogenetic signals. CCP analysis unexpectedly revealed that Idahoa (2n = 16) has a diploidized mesotetraploid genome, whereas two Subularia species (2n = 28 and 30) have diploidized mesoctoploid genomes. Several ancient allopolyploidy events have also been detected in closely related taxa (Chamira circaeoides, Cremolobeae, Eudemeae, and Notothlaspideae). CONCLUSIONS: Our results suggest that the contentious phylogenetic placement of Idahoa and Subularia is best explained by two WGDs involving one or more shared parental genomes. The newly identified mesopolyploid genomes highlight the challenges of studying plant clades with complex polyploidy histories and provide a better framework for understanding genome evolution in the crucifer family.

Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention.

Hybridization and polyploidy followed by genome-wide diploidization had a significant impact on the diversification of land plants. The ancient At-α whole-genome duplication (WGD) preceded the diversification of crucifers (Brassicaceae). Some genera and tribes also experienced younger, mesopolyploid WGDs concealed by subsequent genome diploidization. Here we tested if multiple base chromosome numbers originated due to genome diploidization after independent mesopolyploid WGDs and how diploidization affected post-polyploid gene retention. Sixteen species representing 10 Brassicaceae tribes were analyzed by comparative chromosome painting and/or whole-transcriptome analysis of gene age distributions and phylogenetic analyses of gene duplications. Overall, we found evidence for at least 13 independent mesopolyploidies followed by different degrees of diploidization across the Brassicaceae. New mesotetraploid events were uncovered for the tribes Anastaticeae, Iberideae and Schizopetaleae, and mesohexaploid WGDs for Cochlearieae and Physarieae. In contrast, we found convergent patterns of gene retention and loss among these independent WGDs. Our combined analyses of genomic data for Brassicaceae indicate that extant chromosome number variation in many plant groups, and especially monophyletic taxa with multiple base chromosome numbers, can result from clade-specific genome duplications followed by diploidization. Our observation of parallel gene retention and loss across multiple independent WGDs provides one of the first multi-species tests of the predictability of patterns of post-polyploid genome evolution.