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

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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 C ₄ photosynthesis and carbon-concentrating mechanism, synthesis of the metal-complexing metabolite picolinic acid, and vitamin B ₁, B ₇ and B ₁₂ auxotrophy. The P. coloniale genome provides first insights into the dawn of green plant evolution.

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One thousand plant transcriptomes and the phylogenomics of green plants

James Leebens-Mack, Michael S Barker, Eric J Carpenter … (2019)

Green plants (Viridiplantae) include around 450,000–500,000 species 1,2 of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life.

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The timescale of early land plant evolution

Jennifer L Morris, Mark Puttick, James Clark … (2018)

Significance Establishing the timescale of early land plant evolution is essential to testing hypotheses on the coevolution of land plants and Earth’s System. Here, we establish a timescale for early land plant evolution that integrates over competing hypotheses on bryophyte−tracheophyte relationships. We estimate land plants to have emerged in a middle Cambrian–Early Ordovocian interval, and vascular plants to have emerged in the Late Ordovician−Silurian. This timescale implies an early establishment of terrestrial ecosystems by land plants that is in close accord with recent estimates for the origin of terrestrial animal lineages. Biogeochemical models that are constrained by the fossil record of early land plants, or attempt to explain their impact, must consider a much earlier, middle Cambrian–Early Ordovician, origin.

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The Ectocarpus genome and the independent evolution of multicellularity in brown algae.

J. Mark Cock, Lieven Sterck, Pierre Rouzé … (2010)

Brown algae (Phaeophyceae) are complex photosynthetic organisms with a very different evolutionary history to green plants, to which they are only distantly related. These seaweeds are the dominant species in rocky coastal ecosystems and they exhibit many interesting adaptations to these, often harsh, environments. Brown algae are also one of only a small number of eukaryotic lineages that have evolved complex multicellularity (Fig. 1). We report the 214 million base pair (Mbp) genome sequence of the filamentous seaweed Ectocarpus siliculosus (Dillwyn) Lyngbye, a model organism for brown algae, closely related to the kelps (Fig. 1). Genome features such as the presence of an extended set of light-harvesting and pigment biosynthesis genes and new metabolic processes such as halide metabolism help explain the ability of this organism to cope with the highly variable tidal environment. The evolution of multicellularity in this lineage is correlated with the presence of a rich array of signal transduction genes. Of particular interest is the presence of a family of receptor kinases, as the independent evolution of related molecules has been linked with the emergence of multicellularity in both the animal and green plant lineages. The Ectocarpus genome sequence represents an important step towards developing this organism as a model species, providing the possibility to combine genomic and genetic approaches to explore these and other aspects of brown algal biology further.

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Contributors

Yves Van de Peer:

ORCID: http://orcid.org/0000-0003-4327-3730

yves.vandepeer@psb.vib-ugent.be

Michael Melkonian: michael.melkonian@uni-koeln.de

Huan Liu:

ORCID: http://orcid.org/0000-0003-3909-0931

liuhuan@genomics.cn

Journal

Journal ID (nlm-ta): Nat Ecol Evol

Journal ID (iso-abbrev): Nat Ecol Evol

Title: Nature Ecology & Evolution

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2397-334X

Publication date (Electronic): 22 June 2020

Publication date PMC-release: 22 June 2020

Publication date (Print): 2020

Volume: 4

Issue: 9

Pages: 1220-1231

Affiliations

[1 ]GRID grid.21155.32, ISNI 0000 0001 2034 1839, State Key Laboratory of Agricultural Genomics, BGI-Shenzhen, ; Shenzhen, China

[2 ]GRID grid.5170.3, ISNI 0000 0001 2181 8870, Department of Biotechnology and Biomedicine, , Technical University of Denmark, ; Lyngby, Denmark

[3 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Department of Biology, , University of Copenhagen, ; Copenhagen, Denmark

[4 ]BGI Education Center, University of Chinese Academy of Sciences, Shenzhen, China

[5 ]GRID grid.6190.e, ISNI 0000 0000 8580 3777, Institute for Plant Sciences, Department of Biological Sciences, University of Cologne, ; Cologne, Germany

[6 ]GRID grid.5342.0, ISNI 0000 0001 2069 7798, Department of Plant Biotechnology and Bioinformatics (Ghent University) and Center for Plant Systems Biology, ; Ghent, Belgium

[7 ]GRID grid.5718.b, ISNI 0000 0001 2187 5445, Central Collection of Algal Cultures, Faculty of Biology, , University of Duisburg-Essen, ; Essen, Germany

[8 ]GRID grid.79703.3a, ISNI 0000 0004 1764 3838, School of Biology and Biological Engineering, , South China University of Technology, ; Guangzhou, China

[9 ]GRID grid.17089.37, Department of Biological Sciences and Department of Medicine, , University of Alberta, ; Edmonton, Alberta Canada

[10 ]GRID grid.21155.32, ISNI 0000 0001 2034 1839, Guangdong Provincial Key Laboratory of Genome Read and Write, BGI-Shenzhen, ; Shenzhen, China

[11 ]GRID grid.27871.3b, ISNI 0000 0000 9750 7019, College of Horticulture, , Nanjing Agricultural University, ; Nanjing, China

[12 ]GRID grid.49697.35, ISNI 0000 0001 2107 2298, Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, , University of Pretoria, ; Pretoria, South Africa

Author information

Sunil Kumar Sahu http://orcid.org/0000-0002-4742-9870

Birger Marin http://orcid.org/0000-0002-4287-2099

Zhen Li http://orcid.org/0000-0001-8920-9270

Gane Ka-Shu Wong http://orcid.org/0000-0001-6108-5560

Xun Xu http://orcid.org/0000-0002-5338-5173

Xin Liu http://orcid.org/0000-0003-3256-2940

Yves Van de Peer http://orcid.org/0000-0003-4327-3730

Huan Liu http://orcid.org/0000-0003-3909-0931

Article

Publisher ID: 1221

DOI: 10.1038/s41559-020-1221-7

PMC ID: 7455551

PubMed ID: 32572216

SO-VID: b677cf6c-e59d-4ea7-9775-fa179dd6f018

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 12 June 2019

Date accepted : 12 May 2020

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Keywords: evolutionary genetics,molecular evolution,phylogenetics,taxonomy,evolutionary biology

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Keywords: evolutionary genetics, molecular evolution, phylogenetics, taxonomy, evolutionary biology

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

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Pensoft Biodiversity

Most cited references 76

One thousand plant transcriptomes and the phylogenomics of green plants

The timescale of early land plant evolution

The Ectocarpus genome and the independent evolution of multicellularity in brown algae.

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