Mitoplastomic discordance in Brassicaceae phylogenomics confirms the complex evolutionary history of the family

Abstract

Background and aims: The phylogeny of the Brassicaceae family has traditionally been inferred from plastid and nuclear DNA. However, early studies were limited by the availability of genetic markers and incomplete taxon sampling. Recent phylogenomic studies, leveraging more densely sampled nuclear and plastid datasets, have resolved many taxonomic uncertainties. These studies either targeted complete plastomes or provided extensive representation of the nuclear genome. Nevertheless, substantial cytonuclear discordance, poorly resolved backbone relationships, and challenges placing 'rogue taxa' have left unresolved questions about deeper relationships, notably of the family's five supertribes. In this context, we performed the first phylogenomic analysis of the slower-evolving, maternally inherited mitogenome, which presents a promising avenue for resolving deeper phylogenetic nodes.

Methods: Using published mitogenomes from nine Brassicaceae species, we generated a mitogenomic reference file to recover mitogenomic sequencing read data from Hendriks et al. (2023). Subsequently, we reconstructed a codon-aware mitogenomic supermatrix, alongside updated nuclear (281 genes) and plastome (76 genes) supermatrices, and inferred family-wide maximum likelihood phylogenies from each of these three genomes. Congruence among the resulting phylogenies was thoroughly assessed.

Key results: We present the first densely sampled family-wide mitogenomic Brassicaceae phylogeny, including 167 species, 145 genera (40% of the family), and 40 tribes (69% of the family), and the first family-wide phylogenomic comparison based on all three plant genomes. While cytonuclear discordance was evident, we also uncovered strong phylogenomic discordance between the two organellar genomes-mitogenome and plastome-coined here as 'mitoplastomic discordance'. Our findings offer new insights into placing several rogue and previously unplaced taxa.

Conclusions: Phylogenomic discordance in Brassicaceae was more pervasive than expected. While bifurcating phylogenies offer clear evolutionary hypotheses, they do not fully capture evolutionary complexities. Our results have implications for understanding Brassicaceae evolution, taxonomy, and systematics, shedding light on processes like hybridisation and genome duplication, commonly resulting in evolutionary reticulation.

Keywords: Brassicaceae; Cruciferae; cytonuclear discordance; mitogenomics; mitoplastomic discordance; mustard family; phylogenomics; rogue taxaa.