Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution.

The transition to a terrestrial environment, termed terrestrialization, is generally regarded as a pivotal event in the evolution and diversification of the land plant flora that changed the surface of our planet. Through phylogenomic studies, a group of streptophyte algae, the Zygnematophyceae, have recently been recognized as the likely sister group to land plants (embryophytes). Here, we report genome sequences and analyses of two early diverging Zygnematophyceae (Spirogloea muscicola gen. nov. and Mesotaenium endlicherianum) that share the same subaerial/terrestrial habitat with the earliest-diverging embryophytes, the bryophytes. We provide evidence that genes (i.e., GRAS and PYR/PYL/RCAR) that increase resistance to biotic and abiotic stresses in land plants, in particular desiccation, originated or expanded in the common ancestor of Zygnematophyceae and embryophytes, and were gained by horizontal gene transfer (HGT) from soil bacteria. These two Zygnematophyceae genomes represent a cornerstone for future studies to understand the underlying molecular mechanism and process of plant terrestrialization.

Plastid Genome Evolution of Two Colony-Forming Benthic Ochrosphaera neapolitana Strains (Coccolithales, Haptophyta).

Coccolithophores are well-known haptophytes that produce small calcium carbonate coccoliths, which in turn contribute to carbon sequestration in the marine environment. Despite their important ecological role, only two of eleven haptophyte plastid genomes are from coccolithophores, and those two belong to the order Isochrysidales. Here, we report the plastid genomes of two strains of Ochrosphaera neapolitana (Coccolithales) from Spain (CCAC 3688 B) and the USA (A15,280). The newly constructed plastid genomes are the largest in size (116,906 bp and 113,686 bp, respectively) among all the available haptophyte plastid genomes, primarily due to the increased intergenic regions. These two plastid genomes possess a conventional quadripartite structure with a long single copy and short single copy separated by two inverted ribosomal repeats. These two plastid genomes share 110 core genes, six rRNAs, and 29 tRNAs, but CCAC 3688 B has an additional CDS (ycf55) and one tRNA (trnL-UAG). Two large insertions at the intergenic regions (2 kb insertion between ycf35 and ycf45; 0.5 kb insertion in the middle of trnM and trnY) were detected in the strain CCAC 3688 B. We found the genes of light-independent protochlorophyllide oxidoreductase (chlB, chlN, and chlL), which convert protochlorophyllide to chlorophyllide during chlorophyll biosynthesis, in the plastid genomes of O. neapolitana as well as in other benthic Isochrysidales and Coccolithales species, putatively suggesting an evolutionary adaptation to benthic habitats.

Chromosome-level genome of Pedinomonas minor (Chlorophyta) unveils adaptations to abiotic stress in a rapidly fluctuating environment.

The Pedinophyceae (Viridiplantae) comprise a class of small uniflagellate algae with a pivotal position in the phylogeny of the Chlorophyta as the sister group of the 'core chlorophytes'. We present a chromosome-level genome assembly of the freshwater type species of the class, Pedinomonas minor. We sequenced the genome using Pacbio, Illumina and Hi-C technologies, performed comparative analyses of genome and gene family evolution, and analyzed the transcriptome under various abiotic stresses. Although the genome is relatively small (55 Mb), it shares many traits with core chlorophytes including number of introns and protein-coding genes, messenger RNA (mRNA) lengths, and abundance of transposable elements. Pedinomonas minor is only bounded by the plasma membrane, thriving in temporary habitats that frequently dry out. Gene family innovations and expansions and transcriptomic responses to abiotic stresses have shed light on adaptations of P. minor to its fluctuating environment. Horizontal gene transfers from bacteria and fungi have possibly contributed to the evolution of some of these traits. We identified a putative endogenization site of a nucleocytoplasmic large DNA virus and hypothesized that endogenous viral elements donated foreign genes to the host genome, their spread enhanced by transposable elements, located at gene boundaries in several of the expanded gene families.

Insights into the Evolution of Hydroxyproline-Rich Glycoproteins from 1000 Plant Transcriptomes.

The carbohydrate-rich cell walls of land plants and algae have been the focus of much interest given the value of cell wall-based products to our current and future economies. Hydroxyproline-rich glycoproteins (HRGPs), a major group of wall glycoproteins, play important roles in plant growth and development, yet little is known about how they have evolved in parallel with the polysaccharide components of walls. We investigate the origins and evolution of the HRGP superfamily, which is commonly divided into three major multigene families: the arabinogalactan proteins (AGPs), extensins (EXTs), and proline-rich proteins. Using motif and amino acid bias, a newly developed bioinformatics pipeline, we identified HRGPs in sequences from the 1000 Plants transcriptome project (www.onekp.com). Our analyses provide new insights into the evolution of HRGPs across major evolutionary milestones, including the transition to land and the early radiation of angiosperms. Significantly, data mining reveals the origin of glycosylphosphatidylinositol (GPI)-anchored AGPs in green algae and a 3- to 4-fold increase in GPI-AGPs in liverworts and mosses. The first detection of cross-linking (CL)-EXTs is observed in bryophytes, which suggests that CL-EXTs arose though the juxtaposition of preexisting SPn EXT glycomotifs with refined Y-based motifs. We also detected the loss of CL-EXT in a few lineages, including the grass family (Poaceae), that have a cell wall composition distinct from other monocots and eudicots. A key challenge in HRGP research is tracking individual HRGPs throughout evolution. Using the 1000 Plants output, we were able to find putative orthologs of Arabidopsis pollen-specific GPI-AGPs in basal eudicots.

Shared features and reciprocal complementation of the Chlamydomonas and Arabidopsis microbiota.

Microscopic algae release organic compounds to the region immediately surrounding their cells, known as the phycosphere, constituting a niche for colonization by heterotrophic bacteria. These bacteria take up algal photoassimilates and provide beneficial functions to their host, in a process that resembles the establishment of microbial communities associated with the roots and rhizospheres of land plants. Here, we characterize the microbiota of the model alga Chlamydomonas reinhardtii and reveal extensive taxonomic and functional overlap with the root microbiota of land plants. Using synthetic communities derived from C. reinhardtii and Arabidopsis thaliana, we show that phycosphere and root bacteria assemble into taxonomically similar communities on either host. We show that provision of diffusible metabolites is not sufficient for phycosphere community establishment, which additionally requires physical proximity to the host. Our data suggest the existence of shared ecological principles driving the assembly of the A. thaliana root and C. reinhardtii phycosphere microbiota, despite the vast evolutionary distance between these two photosynthetic organisms.

The Draft Genome of Coelastrum proboscideum (Sphaeropleales, Chlorophyta).

Coelastrum proboscideum Bohlin, 1896 (Sphaeropleales, Scenedesmaceae, Chlorophyta) is a coenobial species with cosmopolitan distribution in diverse freshwater habitats. Coelastrum spp. are widely tested for biotechnological applications such as carotenoid and lipid production, and in bioremediation of wastewater. Here, we report the draft genome of C. proboscideum var. dilatatum strain SAG 217-2. The final assembly comprised 125,935,854 bp with over 8357 scaffolds. The whole-genome data is publicly available in the Nucleotide Sequence Archive (CNSA) of China National GeneBank (CNGB) (https://db.cngb.org/cnsa/) under the accession number CNA0014153.

Author Correction: The genome of Prasinoderma coloniale unveils the existence of a third phylum within green plants.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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

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.

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

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.

The Draft Genome of Hariotina reticulata (Sphaeropleales, Chlorophyta) Provides Insight into the Evolution of Scenedesmaceae.

Hariotina reticulata P. A. Dangeard 1889 (Sphaeropleales, Chlorophyta) is a common member of the summer phytoplankton of meso- to highly eutrophic water bodies with a worldwide distribution. Here, we report the draft whole-genome shotgun sequencing of H. reticulata strain SAG 8.81. The final assembly comprises 107,596,510bp with over 15,219 scaffolds (>100bp). This whole-genome project is publicly available in the CNSA (https://db.cngb.org/cnsa/) of CNGBdb under the accession number CNP0000705.

The Draft Genome of the Small, Spineless Green Alga Desmodesmus costato-granulatus (Sphaeropleales, Chlorophyta).

Desmodesmus costato-granulatus (Skuja) Hegewald 2000 (Sphaeropleales, Chlorophyta) is a small, spineless green alga that is abundant in the freshwater phytoplankton of oligo- to eutrophic waters worldwide. It has a high lipid content and is considered for sustainable production of diverse compounds, including biofuels. Here, we report the draft whole-genome shotgun sequencing of D. costato-granulatus strain SAG 18.81. The final assembly comprises 48,879,637bp with over 4,141 scaffolds. This whole-genome project is publicly available in the CNSA (https://db.cngb.org/cnsa/) of CNGBdb under the accession number CNP0000701.

A Re-investigation of Sarcinochrysis marina (Sarcinochrysidales, Pelagophyceae) from its Type Locality and the Descriptions of Arachnochrysis, Pelagospilus, Sargassococcus and Sungminbooa genera nov.

Systematists increasingly use molecular markers to identify species; however, most microalgae were described before gene sequencing and type specimens were often ink drawings. Cryptic speciation and biogeographic isolation are other potential problems when anchoring an old species name with a modern gene sequence. Therefore when biological type material is absent, the best approach is to recollect the alga from the type locality and sequence genes. Sarcinochrysis marina, described in 1930 by Geitler from the Canary Islands, Spain, is the oldest Pelagophyceae genus. Geitler used two cultures in his study, but these cultures no longer exist. We re-isolated S. marina from the type locality near Las Palmas, Gran Canaria. Furthermore, we included additional Pelagophyceae strains that were isolated from natural habitats for this study or were obtained from culture collections. We produced 85 sequences, representing the nuclear-encoded SSU rRNA and the plastid-encoded rbcL, psaA, psaB, psbA, and psbC genes. The sequences were used to infer maximum likelihood phylogenetic trees. We anchored the name Sarcinochrysis marina using the Las Palmas isolate, and we described four new genera (Arachnochrysis, Pelagospilus, Sargassococcus, Sungminbooa) and nine new species in the Sarcinochrysidales. We also described a new family, Chrysocystaceae, based upon molecular phylogenetic analyses.

10KP: A phylodiverse genome sequencing plan.

Understanding plant evolution and diversity in a phylogenomic context is an enormous challenge due, in part, to limited availability of genome-scale data across phylodiverse species. The 10KP (10,000 Plants) Genome Sequencing Project will sequence and characterize representative genomes from every major clade of embryophytes, green algae, and protists (excluding fungi) within the next 5 years. By implementing and continuously improving leading-edge sequencing technologies and bioinformatics tools, 10KP will catalogue the genome content of plant and protist diversity and make these data freely available as an enduring foundation for future scientific discoveries and applications. 10KP is structured as an international consortium, open to the global community, including botanical gardens, plant research institutes, universities, and private industry. Our immediate goal is to establish a policy framework for this endeavor, the principles of which are outlined here.