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Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds

View ORCID ProfileAndrea Del Cortona, Christopher J. Jackson, View ORCID ProfileFrançois Bucchini, View ORCID ProfileMichiel Van Bel, Sofie D’hondt, View ORCID ProfilePavel Škaloud, View ORCID ProfileCharles F. Delwiche, View ORCID ProfileAndrew H. Knoll, View ORCID ProfileJohn A. Raven, View ORCID ProfileHeroen Verbruggen, View ORCID ProfileKlaas Vandepoele, View ORCID ProfileOlivier De Clerck, View ORCID ProfileFrederik Leliaert
doi: https://doi.org/10.1101/668475
Andrea Del Cortona
aDepartment of Biology, Phycology Research Group, Ghent University, Krijgslaan 281, 9000 Ghent, Belgium
bDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium
cVIB Center for Plant Systems Biology, Technologiepark 71, 9052 Zwijnaarde, Belgium
dBioinformatics Institute Ghent, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium
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  • For correspondence: andrea.delcortona@gmail.com klaas.vandepoele@psb.vib-ugent.be olivier.declerck@ugent.be frederik.leliaert@meisebotanicgarden.be
Christopher J. Jackson
eSchool of Biosciences, University of Melbourne, Melbourne, Victoria, Australia
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François Bucchini
bDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium
cVIB Center for Plant Systems Biology, Technologiepark 71, 9052 Zwijnaarde, Belgium
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Michiel Van Bel
bDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium
cVIB Center for Plant Systems Biology, Technologiepark 71, 9052 Zwijnaarde, Belgium
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Sofie D’hondt
aDepartment of Biology, Phycology Research Group, Ghent University, Krijgslaan 281, 9000 Ghent, Belgium
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Pavel Škaloud
fDepartment of Botany, Faculty of Science, Charles University, Benátská 2, CZ-12800 Prague 2, Czech Republic
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Charles F. Delwiche
gDepartment of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD 20742, USA
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  • ORCID record for Charles F. Delwiche
Andrew H. Knoll
hDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, 02138, USA
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John A. Raven
iDivision of Plant Sciences, University of Dundee at the James Hutton Institute, Dundee, DD2 5DA, UK
jSchool of Biological Sciences, University of Western Australia (M048), 35 Stirling Highway, WA 6009, Australia
kClimate Change Cluster, University of Technology, Ultimo, NSW 2006, Australia
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Heroen Verbruggen
eSchool of Biosciences, University of Melbourne, Melbourne, Victoria, Australia
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Klaas Vandepoele
bDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium
cVIB Center for Plant Systems Biology, Technologiepark 71, 9052 Zwijnaarde, Belgium
dBioinformatics Institute Ghent, Ghent University, Technologiepark 71, 9052 Zwijnaarde, Belgium
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  • For correspondence: andrea.delcortona@gmail.com klaas.vandepoele@psb.vib-ugent.be olivier.declerck@ugent.be frederik.leliaert@meisebotanicgarden.be
Olivier De Clerck
aDepartment of Biology, Phycology Research Group, Ghent University, Krijgslaan 281, 9000 Ghent, Belgium
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  • ORCID record for Olivier De Clerck
  • For correspondence: andrea.delcortona@gmail.com klaas.vandepoele@psb.vib-ugent.be olivier.declerck@ugent.be frederik.leliaert@meisebotanicgarden.be
Frederik Leliaert
aDepartment of Biology, Phycology Research Group, Ghent University, Krijgslaan 281, 9000 Ghent, Belgium
lMeise Botanic Garden, Nieuwelaan 38, 1860 Meise, Belgium
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  • For correspondence: andrea.delcortona@gmail.com klaas.vandepoele@psb.vib-ugent.be olivier.declerck@ugent.be frederik.leliaert@meisebotanicgarden.be
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Abstract

The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focusses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations, with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that the unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified following recolonization of benthic environments that became increasingly available as sea ice retreated. An increased supply of nutrients and biotic interactions such as grazing pressure has likely triggered the independent evolution of macroscopic growth via different strategies, including both true multicellularity, and multiple types of giant celled forms.

Significance Statement Green seaweeds are important primary producers along coastlines worldwide, and likely played a key role in the evolution of animals. To understand their origin and diversification, we resolve key relationships among extant green algae using a phylotranscriptomic approach. We calibrate our tree using available fossil data, to reconstruct important evolutionary events such as transitions to benthic environments, and evolution of macroscopic growth. We estimate green seaweeds to have originated in the late Tonian/Cryogenian Period, followed by a marked Ordovician diversification of macroscopic forms. This ancient proliferation of green seaweeds likely modified shallow marine ecosystems, which set off an evolutionary arms race between ever larger seaweeds and grazers.

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Posted June 12, 2019.
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Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds
Andrea Del Cortona, Christopher J. Jackson, François Bucchini, Michiel Van Bel, Sofie D’hondt, Pavel Škaloud, Charles F. Delwiche, Andrew H. Knoll, John A. Raven, Heroen Verbruggen, Klaas Vandepoele, Olivier De Clerck, Frederik Leliaert
bioRxiv 668475; doi: https://doi.org/10.1101/668475
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Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds
Andrea Del Cortona, Christopher J. Jackson, François Bucchini, Michiel Van Bel, Sofie D’hondt, Pavel Škaloud, Charles F. Delwiche, Andrew H. Knoll, John A. Raven, Heroen Verbruggen, Klaas Vandepoele, Olivier De Clerck, Frederik Leliaert
bioRxiv 668475; doi: https://doi.org/10.1101/668475

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