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. 2020 Sep;4(9):1220-1231.
doi: 10.1038/s41559-020-1221-7. Epub 2020 Jun 22.

The genome of Prasinoderma coloniale unveils the existence of a third phylum within green plants

Linzhou Li #  1   2 , Sibo Wang #  1   3 , Hongli Wang  1   4 , Sunil Kumar Sahu  1 , Birger Marin  5 , Haoyuan Li  1 , Yan Xu  1   4 , Hongping Liang  1   4 , Zhen Li  6 , Shifeng Cheng  1 , Tanja Reder  5 , Zehra Çebi  5 , Sebastian Wittek  5 , Morten Petersen  3 , Barbara Melkonian  5   7 , Hongli Du  8 , Huanming Yang  1 , Jian Wang  1 , Gane Ka-Shu Wong  1   9 , Xun Xu  1   10 , Xin Liu  1 , Yves Van de Peer  11   12   13 , Michael Melkonian  14   15 , Huan Liu  16   17
Affiliations

The genome of Prasinoderma coloniale unveils the existence of a third phylum within green plants

Linzhou Li et al. Nat Ecol Evol. 2020 Sep.

Erratum in

Abstract

Genome analysis of the pico-eukaryotic marine green alga Prasinoderma coloniale CCMP 1413 unveils the existence of a novel phylum within green plants (Viridiplantae), the Prasinodermophyta, which diverged before the split of Chlorophyta and Streptophyta. Structural features of the genome and gene family comparisons revealed an intermediate position of the P. coloniale genome (25.3 Mb) between the extremely compact, small genomes of picoplanktonic Mamiellophyceae (Chlorophyta) and the larger, more complex genomes of early-diverging streptophyte algae. Reconstruction of the minimal core genome of Viridiplantae allowed identification of an ancestral toolkit of transcription factors and flagellar proteins. Adaptations of P. coloniale to its deep-water, oligotrophic environment involved expansion of light-harvesting proteins, reduction of early light-induced proteins, evolution of a distinct type of C4 photosynthesis and carbon-concentrating mechanism, synthesis of the metal-complexing metabolite picolinic acid, and vitamin B1, B7 and B12 auxotrophy. The P. coloniale genome provides first insights into the dawn of green plant evolution.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Phylogenetic analysis of P. coloniale.
a, Light micrograph of P. coloniale. b, The phylogenetic tree was constructed using the maximum-likelihood method in RAxML and MrBayes based on a concatenated sequence alignment of 256 single-copy genes (500 bootstraps). c, The basal divergence of the new phylum Prasinodermophyta, as revealed by analyses of complete nuclear- and plastid-encoded rRNA operons from 109 Archaeplastida. The rRNA dataset comprised 8,818 aligned positions and contained representatives of all major lineages of Rhodoplantae (seven classes), Glaucoplantae (four genera) and Viridiplantae (three divisions with several classes) including embryophytes. Shown is the RAxML phylogeny (GTRGAMMA model); the three support values at branches are RAxML/IQ-TREE bootstrap percentages/Bayesian posterior probabilities. Bold branches received maximal support (100/100/1).
Fig. 2
Fig. 2. Comparative analysis of P. coloniale and other Chlorophyta.
a, Venn diagram showing unique and shared orthogroups among P. coloniale, C. atmophyticus, M. commoda and C. paradoxa. Gene numbers are given in parentheses. b, Percentages of proteins found among Viridiplantae (red), Chlorophyta-specific (blue) and Streptophyta-specific (green) based on the classification given in OrthoFinder. Species abbreviations are listed in Supplementary Table 32. c, PCA of the type and number of Pfam domains of all genes across the Viridiplantae. d, Box-and-whisker plots depicting distributions of the lengths of exons and introns in selected Viridiplantae.
Fig. 3
Fig. 3. Phylogenetic tree of the LHC antenna protein superfamily.
The tree is derived from a MAFFT alignment and was constructed using IQ-TREE (see Methods) with the model of sequence evolution suggested by the programme. Bootstrap values (500 replicates) ≥50% are shown. The LHC superfamily can be divided into ten clades, marked by different colours; the LHC genes of P. coloniale are highlighted in red. The coloured circles on the outer ring denote the distribution of the different LHC subfamilies in the respective taxa. The TUC clade comprises Trebouxiophyceae, Ulvophyceae and Chlorophyceae (all in Chlorophyta). ELIP, early light-induced protein; SEP, two-helix stress-enhanced protein; OHP, one-helix protein; PSBS, the photosystem II subunit S; RedCAP, red lineage chlorophyll a/b-binding (CAB)-like protein.
Fig. 4
Fig. 4. CCMs in P. coloniale.
a, Maximum-likelihood phylogeny of CA proteins in P. coloniale. b, Proposed CCMs in which inorganic carbon is assimilated by P. coloniale based on predicted protein localizations. A brown arrow denotes that a reaction occurs only in P. coloniale, and a grey dotted arrow denotes a reaction that exists in Mamiellophyceae. MA, malic acid; MDH, malate dehydrogenase; ME, malic enzyme; Pyr, pyruvate; 3-PGA, 3-phosphoglyceric acid; PPDK, pyruvate, phosphate dikinase; RuBisCO, ribulose-1,5-bisphosphate carboxylase oxygenase; TCA, tricarboxylic acid cycle.
Fig. 5
Fig. 5. Analysis of peptidoglycan biosynthesis and flagellar proteins derived from the P. coloniale genome.
a, Distribution of proteins involved in the peptidoglycan biosynthetic pathway across Archaeplastida. b, Distribution of key flagellar proteins across Viridiplantae and Glaucoplantae.
Fig. 6
Fig. 6. Comparison of de novo NAD+ and quinolinate biosynthesis genes.
a, Distribution of genes related to the de novo NAD+ and quinolinate biosynthetic pathways in P. coloniale (orange) as compared with Rhodoplantae (red), Glaucoplantae (purple), early-diverging Chlorophyta (blue), early-diverging Streptophyta (green) and bacteria (brown). Solid circles denote the presence of homologues in each clade. TDO/IDO, tryptophan-/indoleamine 2,3-dioxygenase; AFM, arylformamidase; KMO, kynurenine 3-monooxygenase; KYU, kynureninase; HAAO, 3-hydroxyanthranilate 3,4-dioxygenase; ACMSD, 2-amino-3-carboxymuconate-6-semialdehyde decarboxylase; AO, l-aspartate oxidase; QS, quinolinate synthase. b, A gene fusion architecture between KYU and HAAO of P. coloniale; the left and right parts are the KYU and HAAO genes, respectively. A comparison of sequence similarity of various KYU and HAAO genes from different organisms is shown.
Extended Data Fig. 1
Extended Data Fig. 1. A physical map of the P. coloniale genome.
Outer ring: The 22 chromosomes were labeled from Chr1 to Chr22. Inner rings 2–5 (from outside to inside): Illumina sequencing depth colored in light green (y-axis min-max: 0–592). PacBio sequencing depth colored in light purple (y-axis min-max: 0–67). GC content of P. coloniale chromosomes in light blue (y-axis min-max: 0–80.0). The gene number distribution of P. coloniale colored in red (y-axis min-max: 0–38). The slide window of inner rings 2–5 is 5,000 bp. Inner rings 6–15: Genes shared between P. coloniale and other early-diverging viridiplant genomes, from outside to inside. M. viride, C. atmophyticus, K. nitens, C. braunii and M. endlicherianum (green), M. commoda, M. pusilla, B. prasinos, O. lucimarinus and O. tauri (blue).
Extended Data Fig. 2
Extended Data Fig. 2. The impact of a severely reduced taxon sampling in rRNA phylogenies on the placement of the Prasinodermophyta.
(a). RAxML phylogeny of 23 Archaeplastida/Plantae, for which genome sequences have been determined. As an exception, the Gonium genome project did not cover both rRNA operons, and thus, Gonium was replaced by the closely related Yamagishiella. For similar reasons, Micromonas pusilla was replaced by M. bravo. The Prasinodermophyta, represented only by Prasinoderma coloniale, was resolved as sister to the Mamiellales (Mamiellophyceae) with maximal support. This artificial placement (that is Prasinoderma coloniale diverging within the Chlorophyta) gained high support by bootstrapping (numbers in red color). (b). Splitting the long branch of Prasinoderma coloniale by addition of Prasinococcus capsulatus did not change the artificial placement of the Prasinodermophyta, but reduced the bootstrap support for the artificial branches (numbers in red color). (c). When the long branch of the Mamiellales was subdivided by addition of Monomastix sp. and Pyramimonas parkeae, the Mamiellophyceae/Pyramimonadophyceae-clade diverged independently, and the Prasinodermophyta attained a basally diverging position within Viridiplantae. However, the support for the basal divergence of the Prasinodermophyta was relatively low (numbers in blue color). (d). Further addition of only two taxa, Dolichomastix tenuilepis and Cymbomonas tetramitiformis, was sufficient to raise the bootstrap support for the monophyly of the Chlorophyta (to the exclusion of Prasinodermophyta; 94%), and the monophyly of Chlorophyta+Streptophyta (again to the exclusion of Prasinodermophyta; 89%) to high values (numbers in blue color), comparable to the 109-taxa rRNA phylogeny (Fig. 1c), and the genome/transcriptome tree (Fig. 1b). Taxon sampling for resolving the phylogenetic position of the Prasinodermophyta is thus saturated with only 28 sequences of Archaeplastidae/Plantae.
Extended Data Fig. 3
Extended Data Fig. 3. Comparison of genome characteristics across Viridiplantae.
Genome size, average gene size, the percentage of the coding sequence, average gene density, average exon number per gene and total exon number among early-diverging lineages of Chlorophyta and Streptophyta compared to P. coloniale.
Extended Data Fig. 4
Extended Data Fig. 4. The phylogenetic tree of WRKY domain.
Prasinoderma’s WRKY domain is marked in light green color. WRKY domains I CTD and I NTD represent the C- and N-terminal domains of a single WRKY gene, each domain is monophyletic comprising both Streptophyta and Chlorophyta. This suggests that the common ancestor of Chlorophyta and Streptophyta had this configuration. Interestingly, P. coloniale has four gene copies with a total of six WRKY domains (Supplementary Fig. 13). Two of the gene copies display both N- and C-terminal WRKY domains, the other two have only N-terminal WRKY domains. The phylogenetic tree (Supplementary Fig. 13) placed three WRKY domains in clade I CTD (two C-terminal and one N-terminal WRKY domain), the other N-terminal WRKY domains of P. coloniale could not be positioned in one of the 8 WRKY domain subfamilies. We suggest that the I CTD subfamily is ancestral in the Viridiplantae and the N-terminal WRKY domains originated by domain duplication and shuffling.
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