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. 2020 Feb;6(2):95-106.
doi: 10.1038/s41477-019-0560-3. Epub 2019 Dec 16.

Genomes of early-diverging streptophyte algae shed light on plant terrestrialization

Sibo Wang #  1   2   3 , Linzhou Li #  1   4   5 , Haoyuan Li  1   2 , Sunil Kumar Sahu  1   4 , Hongli Wang  1   2 , Yan Xu  1   6 , Wenfei Xian  1   2 , Bo Song  1   2 , Hongping Liang  1   6 , Shifeng Cheng  1   2 , Yue Chang  1   2 , Yue Song  1   2 , Zehra Çebi  7 , Sebastian Wittek  7 , Tanja Reder  7 , Morten Peterson  3 , Huanming Yang  1   2 , Jian Wang  1   2 , Barbara Melkonian  7   8 , Yves Van de Peer  9   10 , Xun Xu  1   2 , Gane Ka-Shu Wong  11   12 , Michael Melkonian  13   14 , Huan Liu  15   16   17 , Xin Liu  18   19   20
Affiliations

Genomes of early-diverging streptophyte algae shed light on plant terrestrialization

Sibo Wang et al. Nat Plants. 2020 Feb.

Abstract

Mounting evidence suggests that terrestrialization of plants started in streptophyte green algae, favoured by their dual existence in freshwater and subaerial/terrestrial environments. Here, we present the genomes of Mesostigma viride and Chlorokybus atmophyticus, two sister taxa in the earliest-diverging clade of streptophyte algae dwelling in freshwater and subaerial/terrestrial environments, respectively. We provide evidence that the common ancestor of M. viride and C. atmophyticus (and thus of streptophytes) had already developed traits associated with a subaerial/terrestrial environment, such as embryophyte-type photorespiration, canonical plant phytochrome, several phytohormones and transcription factors involved in responses to environmental stresses, and evolution of cellulose synthase and cellulose synthase-like genes characteristic of embryophytes. Both genomes differed markedly in genome size and structure, and in gene family composition, revealing their dynamic nature, presumably in response to adaptations to their contrasting environments. The ancestor of M. viride possibly lost several genomic traits associated with a subaerial/terrestrial environment following transition to a freshwater habitat.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Comparative genome profile of M. viride and C. atmophyticus.
a, This phylogenetic tree was constructed by maximum likelihood based on the concatenated sequences of single-copy genes, while species-specific gene duplicates were excluded from the analysis. A k-means clustering of gene families based on the gene abundance of each species is shown in the right-hand panel; each column represents a family and each row represents one species. b, Differential interference contrast micrographs showing M. viride (left) and C. atmophyticus (right). c, Venn diagrams showing the number of gene families shared among M. viride, C. atmophyticus and a representative rhodophyte, streptophyte or chlorophyte. d, Significant increases and decreases in gene families; filled red circles, triangles and rhombi denote function enrichment of significant increased gene families in the KEGG pathway, while empty symbols denote function enrichment of significant decreased gene families in the KEGG pathway. Details of these functions are shown in the right-hand panel. e, Percentages of total proteins found in both algae and embryophytes (red), proteins shared among algae (purple) and proteins shared among embryophytes (green) based on the classification given in Orthofinder. f, Principal component analysis of the type and number of Pfam domains.
Fig. 2
Fig. 2. Analysis of TF genes and phytohormone signalling pathways in M. viride and C. atmophyticus.
a, Using a HMMER approach for the respective genomes, the numbers of TFs and TRs were identified using the TAPscan database v.2 (for details see Methods). b, Illustrative phylogenetic representation of the predicted gain (green) and loss (orange) of plant TFs in streptophyte algae. c, Presence/absence of the main phytohormone signalling pathways deduced from the genomes of M. viride and C. atmophyticus. Coloured boxes indicate the presence of genes in the pathways, white boxes their absence. All searches were done using HMM (1 × 10–10). Purple-lined ellipses denote genes identified in M. viride but not in C. atmophyticus, while the green-lined ellipse denotes a gene identified in C. atmophyticus but not in M. viride. d, The maximum-likelihood method was used to draw the phylogenetic tree of the PIN and PIN-related homologues to understand their origin among Streptophyta.
Fig. 3
Fig. 3. Phylogenetic distribution of enzymes involved in cell wall biosynthesis in M. viride and C. atmophyticus.
a, Phylogenetic tree of CESA and CSL (GT2 family). The tree was constructed using the maximum-likelihood method. b, Left: summary of the gains and losses of cell wall biosynthetic genes mapped on the phylogenetic tree. Right: copy number of the respective cell wall biosynthetic genes. HG, homogalacturonan; XGA, xylogalacturonan; RGI and RGII, rhamnogalacturonan I and II; AGP, arabinogalactan protein; GSL, glucan synthase-like.
Fig. 4
Fig. 4. Analysis of flagellar genes and their phylogenetic distribution.
The phylogenomic tree (left) was constructed using a maximum-likelihood method based on the concatenated sequences of single-copy genes from different representative algal lineages. The horizontal bar chart (middle) denotes the number of putative orthologues to 398 Chlamydomonas conserved flagellar proteins; the pink horizontal bar represents the number of structure-related flagellar genes (individual genes listed at the top of the right panel), while the green area represents the number of flagella-associated genes. The right panel shows the key structure-related flagellar proteins in six categories. The circle size is proportional to the copy number of putative orthologous genes found in the respective species.
Fig. 5
Fig. 5. Distribution of EF-1α, EF-like and plant phytochromes.
a, Maximum likelihood was used to infer the phylogenetic tree. Right: representative EF-1α and EF-like motifs, from red algae to embryophytes. ‘Other Streptophyta’ represents C. atmophyticus, Klebsormidiophyceae, Coleochaetophyceae, Charophyceae and Zygnematophyceae. b, Left: simplified phylogenic tree of phytochromes across cyanobacteria, glaucophytes, prasinophytes and streptophyte algae is shown. Right: complete domain structures of the phytochrome proteins. PHYX1/PHYX2 represent the sister lineage to p-PHY. The phytochromes from glaucophytes and cyanobacteria are represented by g-PHY and c-PHY, respectively.
Extended Data Fig. 1
Extended Data Fig. 1. The KEGG distribution of unique proteins in M. viride (blue) and C. atmophyticus (pink).
The x-axis indicates the number of genes in a specific category in the respective species. The metabolism pathway is shown on the y-axis.
Extended Data Fig. 2
Extended Data Fig. 2. Sequence conservation of various phytohormone receptor genes in representative species.
Each cell shows a pairwise sequence alignment between a known Arabidopsis protein receptor (top) and the best BLAST hit (E-value
Extended Data Fig. 3
Extended Data Fig. 3. Analysis of the conserved flagellar proteome in flagellate and non-flagellate organisms and the distribution of key flagellar proteins.
Key structure-related flagellar proteins in flagellate and non-flagellate algal species in different lineages. The phylogenetic tree on the left panel was constructed using maximum-likelihood method based on the concatenated sequences of single-copy genes from these genomes, after excluding the species-specific gene duplications. The presence (filled circle) or absence (empty circle) of putative orthologs to conserved flagellar proteins is shown on right panel [Based on Reciprocal Blast Hit (RBH) method with Cut-off value of e-5]. The histogram on the lower panel shows the differential expression level of these important structure-related flagellar proteins.
Extended Data Fig. 4
Extended Data Fig. 4. Distribution of EF-1α and EF-like motifs.
Maximum Likelihood was used to infer the phylogenetic tree of the EF-1α and EF-like homologs to understand their phylogenetic distribution. The right panel displays the representative EF-1α and EF-like motifs from red algae to embryophytes. The tree derived from a MAFFT alignment and constructed using IQ-TREE (see Methods). Bootstrap values (500 replicates) ≥50% are shown.
Extended Data Fig. 5
Extended Data Fig. 5. Phylogenetic tree of phytochrome.
Maximum Likelihood was used to infer the phylogenetic tree of the phytochrome. The tree derived from a MAFFT alignment and constructed using RAxML (see Methods). Bootstrap values (500 replicates) ≥50% are shown.
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