Plant Journal 108: 1768–1785.
Whole-genome duplications (WGDs) and chromosome rearrangements (CRs) play the key role in driving the diversification and evolution of plant lineages. Although the direct link between WGDs and plant diversification is well documented, relatively few studies focus on the evolutionary significance of CRs. The cruciferous tribe Thlaspideae represents an ideal model system to address the role of large-scale chromosome alterations in genome evolution, as most Thlaspideae species share the same diploid chromosome number (2n = 2x = 14). Here we constructed the genome structure in 12 Thlaspideae species, including field pennycress (Thlaspi arvense) and garlic mustard (Alliaria petiolata). We detected and precisely characterized genus- and species-specific CRs, mostly pericentric inversions, as the main genome-diversifying drivers in the tribe. We reconstructed the structure of seven chromosomes of an ancestral Thlaspideae genome, identified evolutionary stable chromosomes versus chromosomes prone to CRs, estimated the rate of CRs, and uncovered an allohexaploid origin of garlic mustard from diploid taxa closely related to A. petiolata and Parlatoria cakiloidea. Furthermore, we performed detailed bioinformatic analysis of the Thlaspideae repeatomes, and identified repetitive elements applicable as unique species- and genus-specific barcodes and chromosome landmarks. This study deepens our general understanding of the evolutionary role of CRs, particularly pericentric inversions, in plant genome diversification, and provides a robust base for follow-up whole-genome sequencing efforts.