Complex reticulation in backbone subfamily relationships in Leguminosae

Authors: STAI, JACOB - Iowa State University; CARDINAL-MCTEAGUE, WARREN - University Of British Columbia; BRUNEAU, ANNE - University Of Montreal; Cannon, Steven

Submitted to: bioRxiv
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/16/2024
Publication Date: 8/16/2024
Citation: Stai, J.S., Cardinal-Mcteague, W., Bruneau, A., Cannon, S.B. 2024. Complex reticulation in backbone subfamily relationships in Leguminosae. bioRxiv. https://doi.org/10.1101/2024.07.12.603319.
DOI: https://doi.org/10.1101/2024.07.12.603319

Interpretive Summary: The legume plant family is the third largest plant family, with more than 20,000 species, and approximately two dozen crops, including oil seeds such as soybean and peanut, forage crops such as clover and alfalfa, and tree crops such as tamarind and carob. Determining the origins and diversification patterns of this family is important for understanding the relationships among the diverse species within the family and how agriculturally important characteristics have evolved. The research here describes the order and timing of early divisions of the legume family into six subfamilies; and also the relative timing of genome doubling events that occurred in the same timeframe as the early diversification. A key conclusion is that at least one of the subfamilies (the Caesalpinioideae, containing species such as honeylocust and Kentucky coffeetree) resulted from a merger of two early legume species that had likely diverged for several million years. This kind of merger of distinct species, called allopolyploidy, may help explain some of the unusual diversity seen in this subfamily. This type of merger also has implications for the way species are analyzed and compared. This basic understanding is important for understanding other allopolyploid crop species such as peanut, cotton, canola, and wheat.

Technical Abstract: Contradictory lines of evidence have made it difficult to resolve the phylogenetic history of the legume diversification era; this is true for the backbone topology, and for the number and timing of whole genome duplications (WGDs). By analyzing the transcriptomic data for 473 gene families in 76 species covering all six accepted legume subfamilies, we assessed the phylogenetic relationships of the legume backbone and uncovered evidence of independent whole genome duplications in each of the six legume subfamilies. Three subfamilies — Cercidoideae, Dialioideae, and Caesalpinioideae — bear evidence of an allopolyploid duplication pattern suggestive of ancient hybridization. In Cercidoideae and Dialioideae, the hybridization appears to be within-subfamily, with the basal genera Cercis and Poeppigia appearing to be unduplicated descendants of one of the parental lineages; in Caesalpinioideae, the hybridization appears to involve a member of the Papilionoid lineage, and some other lineage, potentially extinct. Three independent lines of evidence, consisting of a concatenated superalignment, concordance factor analysis of the set of gene family alignments and topologies, and direct inference of reticulation events via maximum pseudolikelihood implemented by PhyloNet, converged on a single backbone hypothesis and the above hypotheses of reticulate evolution.