Verdigellas peltata Seaweed in the order Palmophyllales, such as the specimen shown here, live at great depth.
The green plants (Viridiplantae) are an ancient group of eukaryotes comprising two main clades: the Chlorophyta, which includes a wide diversity of green algae, and the Streptophyta, which consists of freshwater green algae and the land plants. The early-diverging lineages of the Viridiplantae comprise unicellular algae, and multicellularity has evolved independently in the two clades. Recent molecular data have revealed an unrecognized early-diverging lineage of green plants, the Palmophyllales, with a unique form of multicellularity, and typically found in deep water. The phylogenetic position of this enigmatic group, however, remained uncertain. Here we elucidate the evolutionary affinity of the Palmophyllales using chloroplast genomic, and nuclear rDNA data. Phylogenetic analyses firmly place the palmophyllalean Verdigellas peltata along with species of Prasinococcales (prasinophyte clade VI) in the deepest-branching clade of the Chlorophyta. The small, compact and intronless chloroplast genome (cpDNA) of V. peltata shows striking similarities in gene content and organization with the cpDNAs of Prasinococcales and the streptophyte Mesostigma viride, indicating that cpDNA architecture has been extremely well conserved in these deep-branching lineages of green plants. The phylogenetic distinctness of the Palmophyllales-Prasinococcales clade, characterized by unique ultrastructural features, warrants recognition of a new class of green plants, Palmophyllophyceae class. nov.
|Figure 4: Plastid tree of green plants showing the phylogenetic position of the new class Palmophyllophyceae.|
Class Palmophyllophyceae Leliaert et al. class. nov.
Description: Marine green algae. Cells planktonic, solitary or in loose colonies, or cells grouped in a gelatinous matrix forming benthic macroscopic thalli. Cells spherical or subspherical, lacking flagella and organic body scales, with a single cup-shaped chloroplast enclosing a mitochondrion, nucleus, and large Golgi body. Cell surrounded by a cell wall, with or without pores. Chloroplast surrounded by two membranes, with chlorophylls a and b, with or without pyrenoid. Cell division by unequal binary fission. Strongly supported clade in plastid multi-gene and nuclear ribosomal DNA phylogenetic analyses.
Order Palmophyllales Zechman et al. 2010.
Family Palmophyllaceae Zechman et al. 2010.
Genera Palmophyllum Kützing (type genus), Verdigellas D.L. Ballantine & J.N. Norris, Palmoclathrus Womersley.
Order Prasinococcales Guillou et al.2014.
Description: Marine planktonic green algae. Cells solitary or forming loose colonies. Cells spherical or subspherical, lacking flagella and organic body scales, with a thin cell wall surrounded by a thick ellipsoidal gelatinous capsule, or with a thick, multi-layered cell wall without gelatinous capsule. Cells with a single cup-shaped chloroplast enclosing a mitochondrion, nucleus, and large Golgi body. Chloroplast with a large pyrenoid surrounded by a starch sheath; pyrenoid matrix penetrated by a bifurcate extension of the cytoplasm and the mitochondrion. Cell division by unequal binary fission in which one of the daughter cells retains the parent wall, while the other is released with a newly produced cell wall. Main pigments include chlorophylls a and b, prasinoxanthin, Mg-2,4-divinylphaeoporphyrin a5 monomethylester (MgDVP), uriolide, and micromonol.
Family Prasinococcaceae Leliaert fam. nov.
Genera Prasinococcus H. Miyashita & M. Chihara (type genus) and Prasinoderma T. Hasegawa & M. Chihara.
Nomenclatural notes: The order Prasinococcales was originally described by Chadefaud (1960) for the single species Halosphaera viridis (descriptive order name according to article 16.1 of the International Code of Nomenclature (ICN)). Since Halosphaera is now considered a member of the Pyramimonadales, Prasinococcales Chadefaud is a synonym of Pyramimonadales. More recently, Guillou et al. (2004) used the name Prasinococcales to label “prasinophyte clade VI”, which includes Prasinococcus (Miyashita et al. 1993) and Prasinoderma (Hasegawa et al. 1996). In the interpretation of Guillou et al.11, which is different from Chadefaud, Prasinococcales is an automatically typified name according to article 16.1 of the ICN, with type Prasinococcus. Because Guillou et al. (2004) did not provide a description for the order, we provide one here. Although the family Prasinococcaceae is flagged as an accepted family name in the Global Biodiversity Information Facility (GBIF: www.gbif.org) and in AlgaeBase (algaebase.org), the name has never been described nor validly published, hence the formal description in this paper.
We provide solid phylogenetic evidence that the enigmatic Palmophyllales together with the Prasinococcales form the deepest-branching clade of the Chlorophyta, which we describe as a new class, the Palmophyllophyceae. Our phylogenetic results improve our understanding of morphological evolution in the green plants. Until present, the early-diverging lineages of the Chlorophyta (the prasinophytes) were only known to comprise unicellular planktonic algae. Our results point to an independent origin of macroscopic growth and multicellularity outside of the core Chlorophyta. Our study also contributes to a better understanding of plastid genome evolution in green plants. The small, compact and intronless cpDNA of Verdigellas peltata shows remarkable similarities in gene content and organization with the cpDNAs of Prasinococcales and the streptophyte Mesostigma viride, indicating that cpDNA architecture has been extremely well conserved in the early-branching lineages of green plants.
Frederik Leliaert, Ana Tronholm, Claude Lemieux, Monique Turmel, Michael S. DePriest, Debashish Bhattacharya, Kenneth G. Karol, Suzanne Fredericq, Frederick W. Zechman and Juan M. Lopez-Bautista. 2016. Chloroplast Phylogenomic Analyses Reveal the Deepest-Branching Lineage of the Chlorophyta, Palmophyllophyceae class. nov.. Scientific Reports. 6, Article number: 25367. DOI: 10.1038/srep25367
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