Recurrent gene duplication in the angiosperm tribe Delphinieae (Ranunculaceae) inferred from intracellular gene transfer events and heteroplasmic mutations in the plastid matK gene

Seongjun Park,Boram An,Seonjoo Park

doi:10.1038/s41598-020-59547-6

Abstract

The study of intracellular gene transfer may allow for the detection of interesting evolutionary processes such as ancient polyploidization. We compared 24 plastid genomes (plastomes) from tribe Delphinieae, one from tribe Nigelleae and one from tribe Ranunculeae, including five newly sequenced genomes. The functional transfers of the plastids rpl32 and rps16 to the nucleus in tribe Delphinieae were identified. Unexpectedly, we discovered multiple divergent copies of the nuclear-encoded plastid rpl32 in the genus Aconitum. Phylogenetic and synonymous substitution rate analyses revealed that the nuclear-encoded plastid rpl32 underwent two major duplication events. These ancient gene duplication events probably occurred via multiple polyploidization events in Aconitum between 11.9 and 24.7 Mya. Furthermore, our sequence rate analysis indicated that the eight plastid-encoded rpl subunits in Aconitum had a significantly accelerated evolutionary rate compared to those in other genera, suggesting that highly divergent paralogs targeted to the plastid may contribute to an elevated rate of evolution in plastid rpl genes. In addition, heteroplasmy of the plastid matK from two Aconitum species suggested the existence of potentially functional plastid maturases in its plastome. Our results provide insight into the evolutionary history of the tribe Delphinieae.

Highlights

Gene duplication (GD) has played an important role in eukaryotic evolution by generating evolutionary novelty[1]
We generated complete plastome sequences for five species (Aconitum pseudolaeve, Consolida orientalis, Delphinium maackianum, Staphisagria macrosperma, and Nigella damascena) to improve plastome sampling in tribe Delphinieae. Combining these data with previously published plastomes, we examined the phylogenetic distribution of gene losses and identified functional transfers to the nucleus via intracellular gene transfer (IGT) or gene substitution
The complete plastomes for four species (A. pseudolaeve, C. orientalis, D. maackianum, and S. macrosperma) from tribe Delphinieae and N. damascena from tribe Nigelleae were determined by paired-end Illumina reads with deep coverages, ranging from 372x to 1,004x (Supplementary Table S1 and Supplementary Fig. S1)

Summary

Introduction

Gene duplication (GD) has played an important role in eukaryotic evolution by generating evolutionary novelty[1]. We generated complete plastome sequences for five species (Aconitum pseudolaeve, Consolida orientalis, Delphinium maackianum, Staphisagria macrosperma, and Nigella damascena) to improve plastome sampling in tribe Delphinieae. Combining these data with previously published plastomes, we examined the phylogenetic distribution of gene losses and identified functional transfers to the nucleus via IGT or gene substitution. These surveys revealed multiple copies of the nuclear-encoded rpl[32] among Aconitum species, suggesting at least one GD event in the genus. We evaluated the functional properties of the truncated plastid-encoded matK gene

Methods

Results

Discussion

Conclusion