Complete plastome sequence of Thalictrum coreanum (Ranunculaceae) and transfer of the rpl32 gene to the nucleus in the ancestor of the subfamily Thalictroideae.

Seongjun Park,Seonjoo Park,Robert K Jansen

doi:10.1186/s12870-015-0432-6

Seongjun Park, Seonjoo Park + Show 1 more

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https://doi.org/10.1186/s12870-015-0432-6

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Abstract

BackgroundPlastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but molecular evidence for recent functional gene transfers among seed plants have only been documented for the four genes accD, infA, rpl22, and rpl32.ResultsThe complete plastid genome of Thalictrum coreanum, the first from the subfamily Thalictroideae (Ranunculaceae), was sequenced and revealed the losses of two genes, infA and rpl32. The functional transfer of these two genes to the nucleus in Thalictrum was verified by examination of nuclear transcriptomes. A survey of the phylogenetic distribution of the rpl32 loss was performed using 17 species of Thalictrum and representatives of related genera in the subfamily Thalictroideae. The plastid-encoded rpl32 gene is likely nonfunctional in members of the subfamily Thalictroideae (Aquilegia, Enemion, Isopyrum, Leptopyrum, Paraquilegia, and Semiaquilegia) including 17 Thalictrum species due to the presence of indels that disrupt the reading frame. A nuclear-encoded rpl32 with high sequence identity was identified in both Thalictrum and Aquilegia. The phylogenetic distribution of this gene loss/transfer and the high level of sequence similarity in transit peptides suggest a single transfer of the plastid-encoded rpl32 to the nucleus in the ancestor of the subfamily Thalictroideae approximately 20–32 Mya.ConclusionsThe genome sequence of Thalictrum coreanum provides valuable information for improving the understanding of the evolution of plastid genomes within Ranunculaceae and across angiosperms. Thalictrum is unusual among the three sequenced Ranunculaceae plastid genomes in the loss of two genes infA and rpl32, which have been functionally transferred to the nucleus. In the case of rpl32 this represents the third documented independent transfer from the plastid to the nucleus with the other two transfers occurring in the unrelated angiosperm families Rhizophoraceae and Salicaceae. Furthermore, the transfer of rpl32 provides additional molecular evidence for the monophyly of the subfamily Thalictroideae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0432-6) contains supplementary material, which is available to authorized users.

Highlights

Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis
Plastome of Thalictrum coreanum The Thalictrum coreanum plastome is 155,088 bp with a pair of inverted repeats (IRs) of 26,403 bp separated by a small single copy (SSC) region of 17,549 bp and a large single copy (LSC) region of 84,733 bp (Figure 1A and Table 1)
IRb of T. coreanum and M. saniculifolia extends into the LSC to include the N-terminal portion of rps19, generating a truncated rps19 fragment in IRa

Summary

Introduction

Plastids originated from cyanobacteria and the majority of the ancestral genes were lost or functionally transferred to the nucleus after endosymbiosis. Comparative genomic investigations have shown that gene transfer from plastids to the nucleus is an ongoing evolutionary process but molecular evidence for recent functional gene transfers among seed plants have only been documented for the four genes accD, infA, rpl, and rpl. Successful functional gene transfers from the plastid to the nucleus in seed plants have been documented for only four genes: infA in multiple lineages [7], rpl in Fabaceae and Fagaceae [8,9], rpl in Rhizophoraceae and Salicaceae [10,11] and accD in Trifolium [12,13]. In addition to functional gene transfers, movement of DNA fragments from the plastid to the nucleus is common among flowering plants (referred to as NUPTs; nuclear plastid DNA) [1,14], and the proportion of NUPTs differs considerably among species [15,16]

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