Insights into angiosperm evolution, floral development and chemical biosynthesis from the Aristolochia fimbriata genome

John E Bowers,Yiheng Hu,Xiaoliang Wang,Hao Wu ,Xiaohong Yan ,Kunpeng Li,Claude W Depamphilis,Hongzhi Kong,Stefan Wanke,Lumei Liu,Ran Zhao,Peng Xu,Yuannian Jiao,Jinpeng Wang,Douglas E Soltis,Pamela S Soltis,Hongyan Shan,Liuyu Qin,Xin Yi,James H Leebens‐Mack

doi:10.1038/s41477-021-00990-2

Abstract

Aristolochia, a genus in the magnoliid order Piperales, has been famous for centuries for its highly specialized flowers and wide medicinal applications. Here, we present a new, high-quality genome sequence of Aristolochia fimbriata, a species that, similar to Amborella trichopoda, lacks further whole-genome duplications since the origin of extant angiosperms. As such, the A. fimbriata genome is an excellent reference for inferences of angiosperm genome evolution, enabling detection of two novel whole-genome duplications in Piperales and dating of previously reported whole-genome duplications in other magnoliids. Genomic comparisons between A. fimbriata and other angiosperms facilitated the identification of ancient genomic rearrangements suggesting the placement of magnoliids as sister to monocots, whereas phylogenetic inferences based on sequence data we compiled yielded ambiguous relationships. By identifying associated homologues and investigating their evolutionary histories and expression patterns, we revealed highly conserved floral developmental genes and their distinct downstream regulatory network that may contribute to the complex flower morphology in A. fimbriata. Finally, we elucidated the genetic basis underlying the biosynthesis of terpenoids and aristolochic acids in A. fimbriata.

Highlights

Aristolochia, a genus in the magnoliid order Piperales, has been famous for centuries for its highly specialized flowers and wide medicinal applications
Given that Amborella and Nymphaea exhibit similar genome organization patterns that differ from those of the A. fimbriata genome, we propose that the separated genomic regions were ancestral and either a fusion event occurred before the divergence of monocots and magnoliids followed by a further fission event in the common ancestor of Laurales and Magnoliales or parallel evolution in the Piperales and monocots led to similar fusions
We found that the fusion pattern of the A1-A2 and B1-B2 is common in magnoliids and monocots, while the A1-A2 is connected with C1 in the genomes of Amborella, N. colorata and eudicots

Summary

Introduction

Aristolochia, a genus in the magnoliid order Piperales, has been famous for centuries for its highly specialized flowers and wide medicinal applications. We present a new, high-quality genome sequence of Aristolochia fimbriata, a species that, similar to Amborella trichopoda, lacks further whole-genome duplications since the origin of extant angiosperms. Genomic comparisons between A. fimbriata and other angiosperms facilitated the identification of ancient genomic rearrangements suggesting the placement of magnoliids as sister to monocots, whereas phylogenetic inferences based on sequence data we compiled yielded ambiguous relationships. The major mesangiosperm lineages are the eudicot, monocot and magnoliid clades, which make up approximately 75, 22 and 3% of angiosperm species diversity, respectively, and are the product of an ancient, rapid radiation[1,3]

Methods

Results

Conclusion