Whole-genome microsynteny-based phylogeny of angiosperms

Plant genomes vary greatly in size, organization, and architecture. Such structural differences may be highly relevant for inference of genome evolution dynamics and phylogeny. Indeed, microsynteny—the conservation of local gene content and order—is recognized as a valuable source of phylogenetic information, but its use for the inference of large phylogenies has been limited. Here, by combining synteny network analysis, matrix representation, and maximum likelihood phylogenetic inference, we provide a way to reconstruct phylogenies based on microsynteny information. Both simulations and use of empirical data sets show our method to be accurate, consistent, and widely applicable. As an example, we focus on the analysis of a large-scale whole-genome data set for angiosperms, including more than 120 available high-quality genomes, representing more than 50 different plant families and 30 orders. Our ‘microsynteny-based’ tree is largely congruent with phylogenies proposed based on more traditional sequence alignment-based methods and current phylogenetic classifications but differs for some long-contested and controversial relationships. For instance, our synteny-based tree finds Vitales as early diverging eudicots, Saxifragales within superasterids, and magnoliids as sister to monocots. We discuss how synteny-based phylogenetic inference can complement traditional methods and could provide additional insights into some long-standing controversial phylogenetic relationships.

Analysis of the Coptis chinensis genome reveals the diversification of protoberberine-type alkaloids

Chinese goldthread (Coptis chinensis Franch.), a member of the Ranunculales, represents an important early-diverging eudicot lineage with diverse medicinal applications. Here, we present a high-quality chromosome-scale genome assembly and annotation of C. chinensis. Phylogenetic and comparative genomic analyses reveal the phylogenetic placement of this species and identify a single round of ancient whole-genome duplication (WGD) shared by the Ranunculaceae. We characterize genes involved in the biosynthesis of protoberberine-type alkaloids in C. chinensis. In particular, local genomic tandem duplications contribute to member amplification of a Ranunculales clade-specific gene family of the cytochrome P450 (CYP) 719. The functional versatility of a key CYP719 gene that encodes the (S)-canadine synthase enzyme involved in the berberine biosynthesis pathway may play critical roles in the diversification of other berberine-related alkaloids in C. chinensis. Our study provides insights into the genomic landscape of early-diverging eudicots and provides a valuable model genome for genetic and applied studies of Ranunculales.

The evolution of euAPETALA2 genes in vascular plants: from plesiomorphic roles in sporangia to acquired functions in ovules and fruits

The field of evolutionary developmental biology (evo-devo) can help address how morphological novelties evolve, a key question in evolutionary biology. In Arabidopsis thaliana, APETALA2 (AP2) plays a role in the development of key plant innovations including seeds, flowers, and fruits. AP2 belongs to the APETALA2/ETHYLENE RESPONSIVE ELEMENT BINDING FACTOR (AP2/ERF) family which has members in all viridiplantae, making it one of the oldest and most diverse gene lineages. One key subclade, present across vascular plants is the euAPETALA2 (euAP2) clade, whose founding member is AP2. We reconstructed the evolution of the euAP2 gene lineage in vascular plants to better understand its impact on the morphological evolution of plants, identifying seven major duplication events. We also performed spatio-temporal expression analyses of euAP2/TOE3 genes focusing on less explored vascular plant lineages, including ferns, gymnosperms, early diverging angiosperms and early diverging eudicots. Altogether, our data suggest that euAP2 genes originally contributed to spore and sporangium development, and were subsequently recruited to ovule, fruit and floral organ development. Finally, euAP2 protein sequences are highly conserved, therefore, changes in the role of euAP2 during development are most likely due to changes in regulatory regions.

Whole-genome microsynteny-based phylogeny of angiosperms

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.