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. 2014 Feb 17:14:23.
doi: 10.1186/1471-2148-14-23.

From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes

Brad R Ruhfel  1 , Matthew A Gitzendanner, Pamela S Soltis, Douglas E Soltis, J Gordon Burleigh
Affiliations

From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes

Brad R Ruhfel et al. BMC Evol Biol. .

Abstract

Background: Next-generation sequencing has provided a wealth of plastid genome sequence data from an increasingly diverse set of green plants (Viridiplantae). Although these data have helped resolve the phylogeny of numerous clades (e.g., green algae, angiosperms, and gymnosperms), their utility for inferring relationships across all green plants is uncertain. Viridiplantae originated 700-1500 million years ago and may comprise as many as 500,000 species. This clade represents a major source of photosynthetic carbon and contains an immense diversity of life forms, including some of the smallest and largest eukaryotes. Here we explore the limits and challenges of inferring a comprehensive green plant phylogeny from available complete or nearly complete plastid genome sequence data.

Results: We assembled protein-coding sequence data for 78 genes from 360 diverse green plant taxa with complete or nearly complete plastid genome sequences available from GenBank. Phylogenetic analyses of the plastid data recovered well-supported backbone relationships and strong support for relationships that were not observed in previous analyses of major subclades within Viridiplantae. However, there also is evidence of systematic error in some analyses. In several instances we obtained strongly supported but conflicting topologies from analyses of nucleotides versus amino acid characters, and the considerable variation in GC content among lineages and within single genomes affected the phylogenetic placement of several taxa.

Conclusions: Analyses of the plastid sequence data recovered a strongly supported framework of relationships for green plants. This framework includes: i) the placement of Zygnematophyceace as sister to land plants (Embryophyta), ii) a clade of extant gymnosperms (Acrogymnospermae) with cycads + Ginkgo sister to remaining extant gymnosperms and with gnetophytes (Gnetophyta) sister to non-Pinaceae conifers (Gnecup trees), and iii) within the monilophyte clade (Monilophyta), Equisetales + Psilotales are sister to Marattiales + leptosporangiate ferns. Our analyses also highlight the challenges of using plastid genome sequences in deep-level phylogenomic analyses, and we provide suggestions for future analyses that will likely incorporate plastid genome sequence data for thousands of species. We particularly emphasize the importance of exploring the effects of different partitioning and character coding strategies.

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Figures

Figure 1
Figure 1
Box plots of percent GC content in the ntAll and ntNo3rd data sets as well as in the first, second, and third codon positions of the ntAll data set.
Figure 2
Figure 2
Box plots of percent GC content in seed plants (Spermatophyta; on left) and the data set as a whole (Viridiplantae; on right) in the ntAll and ntNo3rd data sets as well as the first, second, and third codon positions of the ntAll data set. For each pair of box plots, values for seed plants (Spermatophyta) are on the left, and values for all green plant taxa (Viridiplantae) are on the right.
Figure 3
Figure 3
Correlation between percent GC nucleotide content in the ntAll matrix and percent of amino acids in the AA matrix that are coded for by GC-rich codons (G, A, R, and P).
Figure 4
Figure 4
Correlation between percent GC nucleotide content in the ntAll matrix and percent of amino acids in the AA matrix that are coded for by AT-rich codons (F, Y, M, I, N, and K).
Figure 5
Figure 5
Fifty percent maximum likelihood majority-rule bootstrap consensus summary tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. Terminals with a triangle represent collapsed clades with > 2 taxa. Note position of Lycopodiophyta as sister to Spermatophyta is likely caused by base composition bias (see text). See Figures 9, 10, 11, 12, 13, and 14 for the complete tree and Additional file 1 for taxonomy. Lami. = Lamiidae; Campanuli. = Campanulidae; Lyco. = Lycopodiophyta.
Figure 6
Figure 6
Fifty percent maximum likelihood majority-rule bootstrap consensus summary tree of Viridiplantae inferred from the first and second codon positions (ntNo3rd) analysis. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 38,898 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. Terminals with a triangle represent collapsed clades with > 2 taxa. See Additional file 4 for the complete tree and Additional file 1 for taxonomy. Lami. = Lamiidae; Campanuli. = Campanulidae.
Figure 7
Figure 7
Fifty percent maximum likelihood majority-rule bootstrap consensus summary tree of Viridiplantae inferred from the RY-coded (RY) analysis. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. Terminals with a triangle represent collapsed clades with > 2 taxa. See Additional file 5 for the complete tree and Additional file 1 for taxonomy. Lami. = Lamiidae; Campanuli. = Campanulidae.
Figure 8
Figure 8
Fifty percent maximum likelihood majority-rule bootstrap consensus summary tree of Viridiplantae inferred from the amino acid (AA) analysis. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 19,449 AAs; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. Terminals with a triangle represent collapsed clades with > 2 taxa. See Additional file 6 for the complete tree and Additional file 1 for taxonomy. Lami. = Lamiidae; Campanuli. = Campanulidae.
Figure 9
Figure 9
Fifty percent maximum likelihood majority-rule bootstrap consensus tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Portion of tree showing Chlorophyta, Chlorokybophyceae, Mesostigmatophyceae, Charophyceae, Coleochaetophyceae, Zygnematophyceae, Marchantiophyta, Bryophyta, and Anthocerotophyta. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. See also Figure 5 for a summary tree of major Viridiplantae clades and Additional file 1 for taxonomy. Tree continued in Figure 10.
Figure 10
Figure 10
Fifty percent maximum likelihood majority-rule bootstrap consensus tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Portion of tree showing Monilophyta, Lycopodiophyta, and Acrogymnospermae. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. See also Figure 5 for a summary tree of major Viridiplantae clades and Additional file 1 for taxonomy. Note position of Lycopodiophyta as sister to Spermatophyta is likely caused by base composition bias (see text). Tree continued in Figures 9 and 11.
Figure 11
Figure 11
Fifty percent maximum likelihood majority-rule bootstrap consensus tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Portion of tree showing Amborellales, Nymphaeales, Austrobaileyales, Chloranthales, and Magnoliidae. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. See also Figure 5 for a summary tree of major Viridiplantae clades and Additional file 1 for taxonomy. Tree continued in Figures 10 and 12.
Figure 12
Figure 12
Fifty percent maximum likelihood majority-rule bootstrap consensus tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Portion of tree showing Monocotyledoneae. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. See also Figure 5 for a summary tree of major Viridiplantae clades and Additional file 1 for taxonomy. Tree continued in Figures 11 and 13.
Figure 13
Figure 13
Fifty percent maximum likelihood majority-rule bootstrap consensus tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Portion of tree showing Ceratophyllales, Ranunculales, Sabiaceae, Proteales, Trochodendrales, Buxales, Gunnerales, and Superasteridae. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. See also Figure 5 for a summary tree of major Viridiplantae clades and Additional file 1 for taxonomy. Tree continued in Figures 12 and 14.
Figure 14
Figure 14
Fifty percent maximum likelihood majority-rule bootstrap consensus tree of Viridiplantae inferred from the all nucleotide positions (ntAll) analysis. Portion of tree showing Dilleniaceae and Superrosidae. Data set derived from 78 protein-coding genes of the plastid genome (ntax = 360; 58,347 bp; missing data ~15.6%). Bootstrap support values ≥ 50% are indicated. See also Figure 5 for a summary tree of major Viridiplantae clades and Additional file 1 for taxonomy. Tree continued in Figure 13.
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