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. 2010 Oct 23:10:321.
doi: 10.1186/1471-2148-10-321.

Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages

Kenneth G Karol  1 , Kathiravetpillai Arumuganathan, Jeffrey L Boore, Aaron M Duffy, Karin D E Everett, John D Hall, S Kellon Hansen, Jennifer V Kuehl, Dina F Mandoli, Brent D Mishler, Richard G Olmstead, Karen S Renzaglia, Paul G Wolf
Affiliations

Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages

Kenneth G Karol et al. BMC Evol Biol. .

Abstract

Background: Despite considerable progress in our understanding of land plant phylogeny, several nodes in the green tree of life remain poorly resolved. Furthermore, the bulk of currently available data come from only a subset of major land plant clades. Here we examine early land plant evolution using complete plastome sequences including two previously unexamined and phylogenetically critical lineages. To better understand the evolution of land plants and their plastomes, we examined aligned nucleotide sequences, indels, gene and nucleotide composition, inversions, and gene order at the boundaries of the inverted repeats.

Results: We present the plastome sequences of Equisetum arvense, a horsetail, and of Isoetes flaccida, a heterosporous lycophyte. Phylogenetic analysis of aligned nucleotides from 49 plastome genes from 43 taxa supported monophyly for the following clades: embryophytes (land plants), lycophytes, monilophytes (leptosporangiate ferns + Angiopteris evecta + Psilotum nudum + Equisetum arvense), and seed plants. Resolution among the four monilophyte lineages remained moderate, although nucleotide analyses suggested that P. nudum and E. arvense form a clade sister to A. evecta + leptosporangiate ferns. Results from phylogenetic analyses of nucleotides were consistent with the distribution of plastome gene rearrangements and with analysis of sequence gaps resulting from insertions and deletions (indels). We found one new indel and an inversion of a block of genes that unites the monilophytes.

Conclusions: Monophyly of monilophytes has been disputed on the basis of morphological and fossil evidence. In the context of a broad sampling of land plant data we find several new pieces of evidence for monilophyte monophyly. Results from this study demonstrate resolution among the four monilophytes lineages, albeit with moderate support; we posit a clade consisting of Equisetaceae and Psilotaceae that is sister to the "true ferns," including Marattiaceae.

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Figures

Figure 1
Figure 1
Gene maps of the Equisetum arvense and Isoetes flaccida plastomes. The inverted repeats (IRA and IRB) which separate the genome into the large (LSC) and small (SSC) single copy regions are indicated on the inner cycle along with the nucleotide content (G/C dark grey, A/T light grey). Genes shown on the outside of the outer circle are transcribed clockwise and those on the inside counter clockwise. Gene boxes are color coded by functional group as shown in the key. An asterisk (*) denotes genes with introns and a psi (ψ) denotes pseudogenes.
Figure 2
Figure 2
Comparison of plastome maps of early diverging land plant lineages showing major structural changes. Two mosses (Pp = Physcomitrella patens and Sr = Syntrichia ruralis), a hornwort (Af = Anthoceros formosae), four lycophytes (Hl = Huperzia lucidula, If = Isoetes flaccida, Sm = Selaginella moellendorffii and Su = Selaginella uncinata) and a monilophyte (Ea = Equisetum arvense) are compared. The liverwort Marchantia polymorpha shares a similar gene order with Sr, Af and Hl (not shown). Inverted repeat regions are depicted with grey boxes. Inversions and translocations are shown with arrows and solid or dashed lines respectively. The monilophyte-specific inversion shown for Ea is detailed in Fig. 3. Gene colors follow the key in Fig. 1.
Figure 3
Figure 3
Monilophyte-specific inversion. Detailed view of an inversion found only in monilophyte taxa (solid black lines and grey shadow) and a second inversion found only in Adiantum capillus-veneris and Alsophila spinulosa (dashed black lines), which together represent a large clade comprising about 90% of extant fern species diversity. Additional gene loss and movements are shown with arrows (SSC = gene translocated to small single copy). The lycophyte gene order and orientation in this region is similar to that of bryophytes and seed plants (not shown). Note that the ~5 kb region between trnE and trnY unique to Equisetum arvense contains no significant open reading frames when subjected to ORF Finder (http://www.ncbi.nlm.nih.gov/gorf/gorf.html). Gene colors follow the key in Fig. 1.
Figure 4
Figure 4
Genes found in the inverted repeat of seed-free land plants. A liverwort (Mp = Marchantia polymorpha), two mosses (Pp = Physcomitrella patens and Sr = Syntrichia ruralis), a hornwort (Af = Anthoceros formosae), four lycophytes (Hl = Huperzia lucidula, If = Isoetes flaccida, Sm = Selaginella moellendorffii and Su = Selaginella uncinata) and five monilophytes (Ac = Adiantum capillus-veneris, Ae = Angiopteris evecta, As = Alsophila spinulosa, Ea = Equisetum arvense, Pn = Psilotum nudum) are compared for inverted repeat (IR) gene content, including new plastomes reported here. The figure is organized so that IRA, the small single copy (SSC) and IRB are presented top to bottom. Grey boxes denote genes found in the IR and white boxes denote genes found in the large single copy or SSC. Genes in square brackets are those partially encoded in the IR. Genes in bold emphasize that gene order within the leptosporangiate ferns have been reorganized relative to other plants [37,38].
Figure 5
Figure 5
Phylogenetic results using nucleotide data. A) Cladogram based on ML analysis (-ln = 473022.24372) of 49 gene sequences from all 43 plastomes sampled (Table 1). Mapped non-homoplastic indels are shown in yellow circles. Numbers in grey circles are indels identified with a more restrictive taxon sampling that were difficult to score across all charophycean green algae and land plants. B) Phylogram based on ML analysis (-ln = 442145.83514) of gene sequences, excluding the two Selaginella species. C) Phylogram based on ML analysis (-ln = 436696.62372) of gene sequences, excluding the three gnetophyte taxa (Ephedra equisetina, Gnetum parvifolium and Welwitschia mirabilis). ML phylogenetic results (-ln = 405904.24872) that excluded Selaginella spp. and gnetophytes were similar in topology to b (not shown). Numbers above the branches are ML bootstrap proportions and numbers below are Bayesian posterior probabilities in this order: all taxa included/Selaginella spp. excluded/gnetophytes excluded/Selaginella spp. and gnetophytes excluded. The asterisk (*) in c indicates the ML bootstrap proportion for Marchantia polymorpha sister to the remaining land plants found in bootstrap analyses that included all taxa, though the best ML tree recovered a sister relationship of M. polymorpha with the mosses Physcomitrella patens and Syntrichia ruralis. Boxes and dashed lines indicate the relative position of monilophytes (light grey) and lycophytes (dark grey).
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