Complete plastid genomes from Ophioglossum californicum, Psilotum nudum, and Equisetum hyemale reveal an ancestral land plant genome structure and resolve the position of Equisetales among monilophytes.

Felix Grewe,Wenhu Guo,Emily A Gubbels,Jeffrey P Mower,A Katie Hansen

doi:10.1186/1471-2148-13-8

Felix Grewe, Wenhu Guo + Show 3 more

Open Access

https://doi.org/10.1186/1471-2148-13-8

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Journal: BMC evolutionary biology	Publication Date: Jan 11, 2013
Citations: 142	License type: cc-by

Affiliation: University of Nebraska–Lincoln

Abstract

BackgroundPlastid genome structure and content is remarkably conserved in land plants. This widespread conservation has facilitated taxon-rich phylogenetic analyses that have resolved organismal relationships among many land plant groups. However, the relationships among major fern lineages, especially the placement of Equisetales, remain enigmatic.ResultsIn order to understand the evolution of plastid genomes and to establish phylogenetic relationships among ferns, we sequenced the plastid genomes from three early diverging species: Equisetum hyemale (Equisetales), Ophioglossum californicum (Ophioglossales), and Psilotum nudum (Psilotales). A comparison of fern plastid genomes showed that some lineages have retained inverted repeat (IR) boundaries originating from the common ancestor of land plants, while other lineages have experienced multiple IR changes including expansions and inversions. Genome content has remained stable throughout ferns, except for a few lineage-specific losses of genes and introns. Notably, the losses of the rps16 gene and the rps12i346 intron are shared among Psilotales, Ophioglossales, and Equisetales, while the gain of a mitochondrial atp1 intron is shared between Marattiales and Polypodiopsida. These genomic structural changes support the placement of Equisetales as sister to Ophioglossales + Psilotales and Marattiales as sister to Polypodiopsida. This result is augmented by some molecular phylogenetic analyses that recover the same relationships, whereas others suggest a relationship between Equisetales and Polypodiopsida.ConclusionsAlthough molecular analyses were inconsistent with respect to the position of Marattiales and Equisetales, several genomic structural changes have for the first time provided a clear placement of these lineages within the ferns. These results further demonstrate the power of using rare genomic structural changes in cases where molecular data fail to provide strong phylogenetic resolution.

Highlights

Plastid genome structure and content is remarkably conserved in land plants
Most plastid genomes have a quadripartite structure involving a large single-copy (LSC) and a small single-copy (SSC) region separated by two copies of an inverted repeat (IR)
Static vs. dynamic plastome structural evolution in monilophytes The three chloroplast DNA sequences from Ophioglossum californicum, Psilotum nudum, and Equisetum hyemale (Figure 1) have a typical circularly mapping structure containing the LSC and SSC separated by two IRs

Summary

Introduction

Plastid genome structure and content is remarkably conserved in land plants. This widespread conservation has facilitated taxon-rich phylogenetic analyses that have resolved organismal relationships among many land plant groups. Genomes from diverse land plant lineages—including seed plants, ferns, lycophytes, hornworts, mosses, and liverworts —have a similar repertoire of genes that generally encode for proteins involved in photosynthesis or gene expression The order of these plastid genes has remained consistent for most species, such that large syntenic tracks can be identified between genomes. Most plastid genomes have a quadripartite structure involving a large single-copy (LSC) and a small single-copy (SSC) region separated by two copies of an inverted repeat (IR) These generalities apply to most land plants, exceptions certainly exist, such as the convergent loss of photosynthetic genes from parasitic plants [4,5,6] or ndh genes from several lineages [7,8], the highly rearranged genomes of some species [9,10,11], and the independent loss of one copy of the IR in several groups [8,11,12,13]. Recent molecular and morphological evidence unequivocally support the inclusion of horsetails in ferns sensu lato (Monilophyta or Moniliformopses), which encompasses whisk ferns and ophioglossoid ferns (Psilotopsida), marattioid ferns (Marattiopsida), and leptosporangiate ferns (Polypodiopsida) [16,18,21]

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