A phylogenomically informed five-order system for the closest relatives of land plants

Sebastian Hess; Shelby K Williams; Anna Busch; Iker Irisarri; Charles F Delwiche; Sophie de Vries; Tatyana Darienko; Andrew J Roger; John M Archibald; Henrik Buschmann; Klaus von Schwartzenberg; Jan de Vries

doi:10.1016/j.cub.2022.08.022

A phylogenomically informed five-order system for the closest relatives of land plants

Curr Biol. 2022 Oct 24;32(20):4473-4482.e7. doi: 10.1016/j.cub.2022.08.022. Epub 2022 Sep 1.

Authors

Affiliations

¹ Institute for Zoology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany. Electronic address: sebastian.hess@uni-koeln.de.
² Department of Biochemistry and Molecular Biology, Dalhousie University, 5850 College St., Halifax NS B3H 4R2, Canada.
³ Institute for Zoology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany.
⁴ University of Goettingen, Institute for Microbiology and Genetics, Department of Applied Bioinformatics, Goldschmidtstr. 1, 37077 Goettingen, Germany; University of Goettingen, Campus Institute Data Science (CIDAS), Goldschmidstr. 1, 37077 Goettingen, Germany.
⁵ Cell Biology and Molecular Genetics, University of Maryland-College Park, College Park, MD, USA.
⁶ University of Goettingen, Institute for Microbiology and Genetics, Department of Applied Bioinformatics, Goldschmidtstr. 1, 37077 Goettingen, Germany.
⁷ University of Applied Sciences Mittweida, Faculty of Applied Computer Sciences and Biosciences, Section Biotechnology and Chemistry, Molecular Biotechnology, Technikumplatz 17, 09648 Mittweida, Germany.
⁸ Universität Hamburg, Institute of Plant Science and Microbiology, Microalgae and Zygnematophyceae Collection Hamburg (MZCH) and Aquatic Ecophysiology and Phycology, Ohnhorststr. 18, 22609 Hamburg, Germany.
⁹ University of Goettingen, Institute for Microbiology and Genetics, Department of Applied Bioinformatics, Goldschmidtstr. 1, 37077 Goettingen, Germany; University of Goettingen, Campus Institute Data Science (CIDAS), Goldschmidstr. 1, 37077 Goettingen, Germany; University of Goettingen, Goettingen Center for Molecular Biosciences (GZMB), Department of Applied Bioinformatics, Goldschmidtstr. 1, 37077 Goettingen, Germany. Electronic address: devries.jan@uni-goettingen.de.

Abstract

The evolution of streptophytes had a profound impact on life on Earth. They brought forth those photosynthetic eukaryotes that today dominate the macroscopic flora: the land plants (Embryophyta).¹ There is convincing evidence that the unicellular/filamentous Zygnematophyceae-and not the morphologically more elaborate Coleochaetophyceae or Charophyceae-are the closest algal relatives of land plants.^2-6 Despite the species richness (>4,000), wide distribution, and key evolutionary position of the zygnematophytes, their internal phylogeny remains largely unresolved.⁷^,⁸ There are also putative zygnematophytes with interesting body plan modifications (e.g., filamentous growth) whose phylogenetic affiliations remain unknown. Here, we studied a filamentous green alga (strain MZCH580) from an Austrian peat bog with central or parietal chloroplasts that lack discernible pyrenoids. It represents Mougeotiopsis calospora PALLA, an enigmatic alga that was described more than 120 years ago⁹ but never subjected to molecular analyses. We generated transcriptomic data of M. calospora strain MZCH580 and conducted comprehensive phylogenomic analyses (326 nuclear loci) for 46 taxonomically diverse zygnematophytes. Strain MZCH580 falls in a deep-branching zygnematophycean clade together with some unicellular species and thus represents a formerly unknown zygnematophycean lineage with filamentous growth. Our well-supported phylogenomic tree lets us propose a new five-order system for the Zygnematophyceae and provides evidence for at least five independent origins of true filamentous growth in the closest algal relatives of land plants. This phylogeny provides a robust and comprehensive framework for performing comparative analyses and inferring the evolution of cellular traits and body plans in the closest relatives of land plants.

Keywords: Charophyta; conjugating green algae; conjugatophyceae; multicellularity; phylogenomics; plant evolution; plant terrestrialization; streptophyte algae.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Biological Evolution
Charophyceae* / genetics
Embryophyta* / genetics
Phylogeny
Plants
Soil
Streptophyta*

Substances

Soil