Complex but Clear Allopolyploid Pattern of Subtribe Tussilagininae (Asteraceae: Senecioneae) Revealed by Robust Phylogenomic Evidence, with Development of a Novel Homeolog-Sorting Pipeline

Abstract

Polyploidy is a significant mechanism in eukaryotic evolution and is particularly prevalent in the plant kingdom. However, our knowledge about this phenomenon and its effects on evolution remains limited. A major obstacle to the study of polyploidy is the great difficulty in untangling the origins of allopolyploids. Due to the drastic genome changes and the erosion of allopolyploidy signals caused by the combined effects of hybridization and complex post-polyploid diploidization processes, resolving the origins of allopolyploids has long been a challenging task. Here we revisit this issue with the interesting case of subtribe Tussilagininae (Asteraceae: Senecioneae) and by developing HomeoSorter, a new pipeline for network inferences by phasing homeologs to parental subgenomes. The pipeline is based on the basic idea of a previous study but with major changes to address the scaling problem and implement some new functions. With simulated data, we demonstrate that HomeoSorter works efficiently on genome-scale data and has high accuracy in identifying polyploid patterns and assigning homeologs. Using HomeoSorter, the maximum pseudo-likelihood model of Phylonet, and genome-scale data, we further address the complex origin of Tussilagininae, a speciose group (ca. 45 genera and 710 species) characterized by having high base chromosome numbers (mainly x = 30, 40). In particular, the inferred patterns are strongly supported by the chromosomal evidence. Tussilagininae is revealed to comprise two large groups with successive allopolyploid origins: Tussilagininae s.s. (mainly x = 30) and the Gynoxyoid group (x = 40). Two allopolyploidy events first give rise to Tussilagininae s.s., with the first event occurring between the ancestor of subtribe Senecioninae (x = 10) and a lineage (highly probably with x = 10) related to the Brachyglottis alliance, and the resulting hybrid lineage crossing with the ancestor of Chersodoma (x = 10) and leading to Tussilagininae s.s. Then, after early diversification, the Central American group (mainly x = 30) of Tussilagininae s.s., is involved in a third allopolyploidy event with, again, the Chersodoma lineage and produces the Gynoxyoid group. Our study highlights the value of HomeoSorter and the homeolog-sorting approach in polyploid phylogenetics. With rich species diversity and clear evolutionary patterns, Tussilagininae s.s. and the Gynoxyoid group are also excellent models for future investigations of polyploidy.