Abstract

Chloranthales remain the last major mesangiosperm lineage without a nuclear genome assembly. We therefore assemble a high-quality chromosome-level genome of Chloranthus spicatus to resolve enigmatic evolutionary relationships, as well as explore patterns of genome evolution among the major lineages of mesangiosperms (eudicots, monocots, magnoliids, Chloranthales, and Ceratophyllales). We find that synteny is highly conserved between genomic regions of Amborella, Vitis, and Chloranthus. We identify an ancient single whole-genome duplication (WGD) (κ) prior to the divergence of extant Chloranthales. Phylogenetic inference shows Chloranthales as sister to magnoliids. Furthermore, our analyses indicate that ancient hybridization may account for the incongruent phylogenetic placement of Chloranthales + magnoliids relative to monocots and eudicots in nuclear and chloroplast trees. Long genes and long introns are found to be prevalent in both Chloranthales and magnoliids compared to other angiosperms. Overall, our findings provide an improved context for understanding mesangiosperm relationships and evolution and contribute a valuable genomic resource for future investigations.

Highlights

  • Chloranthales remain the last major mesangiosperm lineage without a nuclear genome assembly

  • Chloranthus spicatus has a genome size of 2.97 Gb based on K-mer analysis (Supplementary Fig. 2, Supplementary Data 1); the individual sequenced had a heterozygosity rate of 0.99%, which is possibly associated with the obligate outcrossing system of this species[31]

  • The results showed tandem (23, 33.3%), whole-genome duplication (WGD) (18, 26.1%), and transposition (21, 30.4%) duplication events contributed to the expansion of Terpene synthases (TPSs) in C. spicatus, with only a few proximal repeats (7, 10.1%)

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Summary

Introduction

Chloranthales remain the last major mesangiosperm lineage without a nuclear genome assembly. Decades of effort have established a phylogenetic framework that identifies major angiosperm groups and clarifies their evolutionary relationships (e.g.1,3–5, and references in supplementary Fig. 1). In this framework, Amborellales, Nymphaeales, and Austrobaileyales form a grade (ANA grade)[6,7] of successive sisters to all other living angiosperms. Plastid trees yield magnoliids as the sister to a clade of monocots and eudicots, this placement is not always well supported[1] This incongruence between nuclear and plastid gene trees may reflect the evolutionary complexity of Mesangiospermae, perhaps due to incomplete lineage sorting and/or hybridization during their rapid radiation[12]

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