Whole-genome microsynteny-based phylogeny of angiosperms

Abstract Plant genomes are generally very complex and dynamic structures, and vary greatly in size, organization, and architecture. This is mainly due to the often-excessive numbers of transposable and repetitive elements, as well as to the fact that many plants are ancient or recent polyploids. Such (recurrent) whole-genome duplications are usually followed by genomic rearrangements, gene transpositions and gene loss, making local gene order-based phylogenetic inference particularly challenging. Nevertheless, microsynteny, i.e. the conservation of local gene content and order, has been recognized as a valuable and alternative phylogenetic character to sequence-based characters (nucleotides or amino acids) for the inference of phylogenetic trees, but to date its application for reconstructing larger phylogenies has been, for several reasons, limited. Here, by combining synteny network analysis, matrix representation, and maximum likelihood, we have reconstructed a microsynteny-based phylogenetic tree for more than 120 available high-quality plant genomes, representing more than 50 different plant families and 30 plant orders within the angiosperms. Comparisons with sequence alignment-based trees and current phylogenetic classifications show that we reconstruct very accurate and robust phylogenies, albeit with sometimes important alternative sister-group relationships. For instance, our synteny-based tree positioned Vitales as early-diverging eudicots, Saxifragales belongs to superasterids, and magnoliids as sister to monocots. We discuss how synteny-based phylogeny can be complementary to traditional methods and could provide additional insights into some long-standing controversial phylogenetic relationships.