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

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

Medicine

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65 Citas (Scopus)

Resumen

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.

Idioma original	English
Páginas (desde-hasta)	4473-4482.e7
Publicación	Current Biology
Volumen	32
N.º	20
DOI	https://doi.org/10.1016/j.cub.2022.08.022
Estado	Published - oct. 24 2022

Nota bibliográfica

Funding Information:
This work was funded by the German Research Foundation grants 283693520 (Research Fellowship) and 417585753 ( Emmy Noether Programme ) both to S.H., grants 440231723 (VR 132/4-1) to J.d.V. and 440540015 (BU 2301/6-1) to H.B. within the framework of the Priority Programme “ MAdLand – Molecular Adaptation to Land: Plant Evolution to Change” ( SPP 2237 ), and grant 410739858 in the frame of the project CharMod to K.v.S.; J.d.V. further thanks the European Research Council for funding under the European Union’s Horizon 2020 research and innovation programme (Grant Agreement No. 852725 ; ERC-StG “TerreStriAL”). We thank Richard McCourt ( Drexel University ) and the Herbarium of the Academy of Natural Sciences of Philadelphia (PH) for destructive sampling of material from Mesogerron fluitans, and Elke Woelken ( Universität Hamburg ) for excellent support in electron microscopy.

Funding Information:
This work was funded by the German Research Foundation grants 283693520 (Research Fellowship) and 417585753 (Emmy Noether Programme) both to S.H. grants 440231723 (VR 132/4-1) to J.d.V. and 440540015 (BU 2301/6-1) to H.B. within the framework of the Priority Programme “MAdLand – Molecular Adaptation to Land: Plant Evolution to Change” (SPP 2237), and grant 410739858 in the frame of the project CharMod to K.v.S.; J.d.V. further thanks the European Research Council for funding under the European Union's Horizon 2020 research and innovation programme (Grant Agreement No. 852725; ERC-StG “TerreStriAL”). We thank Richard McCourt (Drexel University) and the Herbarium of the Academy of Natural Sciences of Philadelphia (PH) for destructive sampling of material from Mesogerron fluitans, and Elke Woelken (Universität Hamburg) for excellent support in electron microscopy. Conceptualization, S.H. J.d.V.; investigation, S.H. S.K.W. A.B. I.I. S.d.V. H.B. K.v.S. J.d.V.; writing – original draft, S.H. I.I. and J.d.V.; writing – review and editing, all authors; visualization, S.H. A.B. I.I. and J.d.V.; and funding acquisition, S.H. and J.d.V. The authors declare no competing interests.

Publisher Copyright:
© 2022 The Author(s)

ASJC Scopus Subject Areas

General Neuroscience
General Biochemistry,Genetics and Molecular Biology
General Agricultural and Biological Sciences

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title = "A phylogenomically informed five-order system for the closest relatives of land plants",

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.",

author = "Sebastian Hess and Williams, {Shelby K.} and Anna Busch and Iker Irisarri and Delwiche, {Charles F.} and {de Vries}, Sophie and Tatyana Darienko and Roger, {Andrew J.} and Archibald, {John M.} and Henrik Buschmann and {von Schwartzenberg}, Klaus and {de Vries}, Jan",

note = "Funding Information: This work was funded by the German Research Foundation grants 283693520 (Research Fellowship) and 417585753 ( Emmy Noether Programme ) both to S.H., grants 440231723 (VR 132/4-1) to J.d.V. and 440540015 (BU 2301/6-1) to H.B. within the framework of the Priority Programme “ MAdLand – Molecular Adaptation to Land: Plant Evolution to Change” ( SPP 2237 ), and grant 410739858 in the frame of the project CharMod to K.v.S.; J.d.V. further thanks the European Research Council for funding under the European Union{\textquoteright}s Horizon 2020 research and innovation programme (Grant Agreement No. 852725 ; ERC-StG “TerreStriAL”). We thank Richard McCourt ( Drexel University ) and the Herbarium of the Academy of Natural Sciences of Philadelphia (PH) for destructive sampling of material from Mesogerron fluitans, and Elke Woelken ( Universit{\"a}t Hamburg ) for excellent support in electron microscopy. Funding Information: This work was funded by the German Research Foundation grants 283693520 (Research Fellowship) and 417585753 (Emmy Noether Programme) both to S.H. grants 440231723 (VR 132/4-1) to J.d.V. and 440540015 (BU 2301/6-1) to H.B. within the framework of the Priority Programme “MAdLand – Molecular Adaptation to Land: Plant Evolution to Change” (SPP 2237), and grant 410739858 in the frame of the project CharMod to K.v.S.; J.d.V. further thanks the European Research Council for funding under the European Union's Horizon 2020 research and innovation programme (Grant Agreement No. 852725; ERC-StG “TerreStriAL”). We thank Richard McCourt (Drexel University) and the Herbarium of the Academy of Natural Sciences of Philadelphia (PH) for destructive sampling of material from Mesogerron fluitans, and Elke Woelken (Universit{\"a}t Hamburg) for excellent support in electron microscopy. Conceptualization, S.H. J.d.V.; investigation, S.H. S.K.W. A.B. I.I. S.d.V. H.B. K.v.S. J.d.V.; writing – original draft, S.H. I.I. and J.d.V.; writing – review and editing, all authors; visualization, S.H. A.B. I.I. and J.d.V.; and funding acquisition, S.H. and J.d.V. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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doi = "10.1016/j.cub.2022.08.022",

language = "English",

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T1 - A phylogenomically informed five-order system for the closest relatives of land plants

AU - Hess, Sebastian

AU - Williams, Shelby K.

AU - Busch, Anna

AU - Irisarri, Iker

AU - Delwiche, Charles F.

AU - de Vries, Sophie

AU - Darienko, Tatyana

AU - Roger, Andrew J.

AU - Archibald, John M.

AU - Buschmann, Henrik

AU - von Schwartzenberg, Klaus

AU - de Vries, Jan

N1 - Funding Information: This work was funded by the German Research Foundation grants 283693520 (Research Fellowship) and 417585753 ( Emmy Noether Programme ) both to S.H., grants 440231723 (VR 132/4-1) to J.d.V. and 440540015 (BU 2301/6-1) to H.B. within the framework of the Priority Programme “ MAdLand – Molecular Adaptation to Land: Plant Evolution to Change” ( SPP 2237 ), and grant 410739858 in the frame of the project CharMod to K.v.S.; J.d.V. further thanks the European Research Council for funding under the European Union’s Horizon 2020 research and innovation programme (Grant Agreement No. 852725 ; ERC-StG “TerreStriAL”). We thank Richard McCourt ( Drexel University ) and the Herbarium of the Academy of Natural Sciences of Philadelphia (PH) for destructive sampling of material from Mesogerron fluitans, and Elke Woelken ( Universität Hamburg ) for excellent support in electron microscopy. Funding Information: This work was funded by the German Research Foundation grants 283693520 (Research Fellowship) and 417585753 (Emmy Noether Programme) both to S.H. grants 440231723 (VR 132/4-1) to J.d.V. and 440540015 (BU 2301/6-1) to H.B. within the framework of the Priority Programme “MAdLand – Molecular Adaptation to Land: Plant Evolution to Change” (SPP 2237), and grant 410739858 in the frame of the project CharMod to K.v.S.; J.d.V. further thanks the European Research Council for funding under the European Union's Horizon 2020 research and innovation programme (Grant Agreement No. 852725; ERC-StG “TerreStriAL”). We thank Richard McCourt (Drexel University) and the Herbarium of the Academy of Natural Sciences of Philadelphia (PH) for destructive sampling of material from Mesogerron fluitans, and Elke Woelken (Universität Hamburg) for excellent support in electron microscopy. Conceptualization, S.H. J.d.V.; investigation, S.H. S.K.W. A.B. I.I. S.d.V. H.B. K.v.S. J.d.V.; writing – original draft, S.H. I.I. and J.d.V.; writing – review and editing, all authors; visualization, S.H. A.B. I.I. and J.d.V.; and funding acquisition, S.H. and J.d.V. The authors declare no competing interests. Publisher Copyright: © 2022 The Author(s)

PY - 2022/10/24

Y1 - 2022/10/24

N2 - 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.

AB - 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.

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

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