Convergent Patterns of Karyotype Evolution Underlying Karyotype Uniformity in Conifers

Adv Sci (Weinh). 2024 Dec 25:e2411098. doi: 10.1002/advs.202411098. Online ahead of print.

Abstract

Karyotype diversity plays an important role in speciation and diversification. However, gymnosperms, particularly conifers, exhibit remarkable karyotype uniformity. To explore the evolutionary processes shaping karyotypes in gymnosperms, the karyotype evolutionary history is reconstructed through comparative genomic analyses. Synteny analysis confirms the absence of ancient polyploidy in conifers and its rarity across the gymnosperms as a whole. Further analysis reveals convergent patterns of reciprocal translocations between nonhomologous chromosomes in conifer genomes. Centromeric-centromeric reciprocal translocations (CRTs) have been identified as the primary mechanism of karyotype evolution in conifers, while telomeric-centromeric reciprocal translocations (TRTs) significantly contributed to descending dysploidy within Cupressales. A graph-based method is utilized to infer the detailed evolutionary pathways from the proto-gymnosperm karyotype (n = 12) to modern conifer karyotypes (n = 11-12). In conclusion, the scarcity of both polyploidy and dysploidy contributes to the karyotype uniformity of gymnosperms and potentially also to their lower species richness compared to angiosperms. However, the pervasive CRTs and occasional TRTs underlie this "apparent uniformity", supporting the "karyotype orthoselection" hypothesis. This study provides new insights into the mechanisms maintaining karyotype uniformity in conifers and the role of karyotype evolution in their diversification.

Keywords: conifers; descending dysploidy; karyotype evolution; polyploidy; proto‐gymnosperm karyotype; reciprocal translocations; synteny analysis.