Abstract
BackgroundThe Viridiplantae comprise two major phyla: the Streptophyta, containing the charophycean green algae and all land plants, and the Chlorophyta, containing the remaining green algae. Despite recent progress in unravelling phylogenetic relationships among major green plant lineages, problematic nodes still remain in the green tree of life. One of the major issues concerns the scaly biflagellate Mesostigma viride, which is either regarded as representing the earliest divergence of the Streptophyta or a separate lineage that diverged before the Chlorophyta and Streptophyta. Phylogenies based on chloroplast and mitochondrial genomes support the latter view. Because some green plant lineages are not represented in these phylogenies, sparse taxon sampling has been suspected to yield misleading topologies. Here, we describe the complete chloroplast DNA (cpDNA) sequence of the early-diverging charophycean alga Chlorokybus atmophyticus and present chloroplast genome-based phylogenies with an expanded taxon sampling.ResultsThe 152,254 bp Chlorokybus cpDNA closely resembles its Mesostigma homologue at the gene content and gene order levels. Using various methods of phylogenetic inference, we analyzed amino acid and nucleotide data sets that were derived from 45 protein-coding genes common to the cpDNAs of 37 green algal/land plant taxa and eight non-green algae. Unexpectedly, all best trees recovered a robust clade uniting Chlorokybus and Mesostigma. In protein trees, this clade was sister to all streptophytes and chlorophytes and this placement received moderate support. In contrast, gene trees provided unequivocal support to the notion that the Mesostigma + Chlorokybus clade represents the earliest-diverging branch of the Streptophyta. Independent analyses of structural data (gene content and/or gene order) and of subsets of amino acid data progressively enriched in slow-evolving sites led us to conclude that the latter topology reflects the true organismal relationships.ConclusionIn disclosing a sister relationship between the Mesostigmatales and Chlorokybales, our study resolves the long-standing debate about the nature of the unicellular flagellated ancestors of land plants and alters significantly our concepts regarding the evolution of streptophyte algae. Moreover, in predicting a richer chloroplast gene repertoire than previously inferred for the common ancestor of all streptophytes, our study has contributed to a better understanding of chloroplast genome evolution in the Viridiplantae.
Highlights
The Viridiplantae comprise two major phyla: the Streptophyta, containing the charophycean green algae and all land plants, and the Chlorophyta, containing the remaining green algae
Six monophyletic groups are currently recognized in the Charophyceae: the Mesostigmatales [4] represented by Mesostigma viride, a scaly biflagellate that has long been thought to be a member of the Prasinophyceae [5]; the Chlorokybales represented as well by a single species (Chlorokybus atmophyticus); the Klebsormidiales (3 genera, 45 spp.); the Zygnematales (~ 50 genera, ~ 6,000 spp.); the Coleochaetales (3 genera, 20 spp.); and the Charales (6 genera, 81 spp.) [6]
Structural genomic features The Chlorokybus chloroplast DNA (cpDNA) sequence maps as a circular molecule of 152,254 bp with an overall A+T content of 63.8% (Figure 1). While this size is in the range expected for a streptophyte or chlorophyte genome, the nucleotide composition deviates slightly from the range (67.5–73.8% A+T) previously reported for streptophyte algae [8] and is most similar to the A+T content found for the ulvophyte Pseudendoclonium akinetum (62.3%) and the chlorophycean alga Scenedesmus obliquus (67.2%) [23]
Summary
The Viridiplantae comprise two major phyla: the Streptophyta, containing the charophycean green algae and all land plants, and the Chlorophyta, containing the remaining green algae. A phylogeny based on four genes from three cellular compartments (the nuclear 18S rRNA gene, the chloroplast atpB and rbcL and the mitochondrial nad5) supports the notions that the Charales are sister to land plants and that charophycean green algae evolved progressively toward a more elaborated cellular complexity, occurring sequentially as biflagellated unicells, cubical packets of two, four or eight non-flagellated cells (sarcinoid morphology), unbranched/branched filaments and complex branched thalli with parenchymatous tissue [4,7] In this four-gene tree, inferred using the glaucocystophyte Cyanophora paradoxa and chlorophyte green algae as outgroup, the deepest branch is occupied by the Mesostigmatales, the Chlorokybales emerge just after the Mesostigmatales, the Zygnematales are resolved as the divergence, and the Coleochaetales are sister to the clade uniting the Charales and land plants. The finding that Mesostigma shares more ESTs with land plants than with the chlorophyte Chlamydomonas reinhardtii [18] as well as the discoveries of a multigene family (BIP2-like sequences) [19] and a GapA/B gene duplication [18,20] restricted to Mesostigma and streptophytes were interpreted as compelling evidence for the affiliation of this unicellular biflagellate with the Streptophyta
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
