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Evolution and cytological diversification of the green seaweeds (Ulvophyceae)

Ellen Cocquyt UGent, Heroen Verbruggen UGent, Frédérik Leliaert UGent and Olivier De Clerck UGent (2010) MOLECULAR BIOLOGY AND EVOLUTION. 27(9). p.2052-2061
abstract
The Ulvophyceae, one of the four classes of the Chlorophyta, is of particular evolutionary interest because it features an unrivaled morphological and cytological diversity. Morphological types range from unicells and simple multicellular filaments to sheet-like and complex corticated thalli. Cytological layouts range from typical small cells containing a single nucleus and chloroplast to giant cells containing millions of nuclei and chloroplasts. In order to understand the evolution of these morphological and cytological types, the present paper aims to assess whether the Ulvophyceae are monophyletic and elucidate the ancient relationships among its orders. Our approach consists of phylogenetic analyses (maximum likelihood and Bayesian inference) of seven nuclear genes, small subunit nuclear ribosomal DNA and two plastid markers with carefully chosen partitioning strategies, and models of sequence evolution. We introduce a procedure for fast site removal (site stripping) targeted at improving phylogenetic signal in a particular epoch of interest and evaluate the specificity of fast site removal to retain signal about ancient relationships. From our phylogenetic analyses, we conclude that the ancestral ulvophyte likely was a unicellular uninucleate organism and that macroscopic growth was achieved independently in various lineages involving radically different mechanisms: either by evolving multicellularity with coupled mitosis and cytokinesis (Ulvales--Ulotrichales and Trentepohliales), by obtaining a multinucleate siphonocladous organization where every nucleus provides for its own cytoplasmic domain (Cladophorales and Blastophysa), or by developing a siphonous organization characterized by either one macronucleus or millions of small nuclei and cytoplasmic streaming (Bryopsidales and Dasycladales). We compare different evolutionary scenarios giving rise to siphonous and siphonocladous cytologies and argue that these did not necessarily evolve from a multicellular or even multinucleate state but instead could have evolved independently from a unicellular ancestor.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
NUCLEAR, CELLS, ACETABULARIA, ULTRASTRUCTURE, CHLOROPHYTA, ALGAE, SEQUENCE DATA, PHYLOGENETIC TREE SELECTION, Ulvophyceae, Chlorophyta, green algae, evolution, multigene phylogeny, fast site removal, MITOCHONDRIAL, SUPPORT
journal title
MOLECULAR BIOLOGY AND EVOLUTION
Mol. Biol. Evol.
volume
27
issue
9
pages
2052 - 2061
Web of Science type
Article
Web of Science id
000281184100008
JCR category
GENETICS & HEREDITY
JCR impact factor
5.51 (2010)
JCR rank
20/154 (2010)
JCR quartile
1 (2010)
ISSN
0737-4038
DOI
10.1093/molbev/msq091
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1105214
handle
http://hdl.handle.net/1854/LU-1105214
date created
2011-01-20 08:23:26
date last changed
2016-12-19 15:46:19
@article{1105214,
  abstract     = {The Ulvophyceae, one of the four classes of the Chlorophyta, is of particular evolutionary interest because it features an unrivaled morphological and cytological diversity. Morphological types range from unicells and simple multicellular filaments to sheet-like and complex corticated thalli. Cytological layouts range from typical small cells containing a single nucleus and chloroplast to giant cells containing millions of nuclei and chloroplasts. In order to understand the evolution of these morphological and cytological types, the present paper aims to assess whether the Ulvophyceae are monophyletic and elucidate the ancient relationships among its orders. Our approach consists of phylogenetic analyses (maximum likelihood and Bayesian inference) of seven nuclear genes, small subunit nuclear ribosomal DNA and two plastid markers with carefully chosen partitioning strategies, and models of sequence evolution. We introduce a procedure for fast site removal (site stripping) targeted at improving phylogenetic signal in a particular epoch of interest and evaluate the specificity of fast site removal to retain signal about ancient relationships. From our phylogenetic analyses, we conclude that the ancestral ulvophyte likely was a unicellular uninucleate organism and that macroscopic growth was achieved independently in various lineages involving radically different mechanisms: either by evolving multicellularity with coupled mitosis and cytokinesis (Ulvales--Ulotrichales and Trentepohliales), by obtaining a multinucleate siphonocladous organization where every nucleus provides for its own cytoplasmic domain (Cladophorales and Blastophysa), or by developing a siphonous organization characterized by either one macronucleus or millions of small nuclei and cytoplasmic streaming (Bryopsidales and Dasycladales). We compare different evolutionary scenarios giving rise to siphonous and siphonocladous cytologies and argue that these did not necessarily evolve from a multicellular or even multinucleate state but instead could have evolved independently from a unicellular ancestor.},
  author       = {Cocquyt, Ellen and Verbruggen, Heroen and Leliaert, Fr{\'e}d{\'e}rik and De Clerck, Olivier},
  issn         = {0737-4038},
  journal      = {MOLECULAR BIOLOGY AND EVOLUTION},
  keyword      = {NUCLEAR,CELLS,ACETABULARIA,ULTRASTRUCTURE,CHLOROPHYTA,ALGAE,SEQUENCE DATA,PHYLOGENETIC TREE SELECTION,Ulvophyceae,Chlorophyta,green algae,evolution,multigene phylogeny,fast site removal,MITOCHONDRIAL,SUPPORT},
  language     = {eng},
  number       = {9},
  pages        = {2052--2061},
  title        = {Evolution and cytological diversification of the green seaweeds (Ulvophyceae)},
  url          = {http://dx.doi.org/10.1093/molbev/msq091},
  volume       = {27},
  year         = {2010},
}

Chicago
Cocquyt, Ellen, Heroen Verbruggen, Frédérik Leliaert, and Olivier De Clerck. 2010. “Evolution and Cytological Diversification of the Green Seaweeds (Ulvophyceae).” Molecular Biology and Evolution 27 (9): 2052–2061.
APA
Cocquyt, E., Verbruggen, H., Leliaert, F., & De Clerck, O. (2010). Evolution and cytological diversification of the green seaweeds (Ulvophyceae). MOLECULAR BIOLOGY AND EVOLUTION, 27(9), 2052–2061.
Vancouver
1.
Cocquyt E, Verbruggen H, Leliaert F, De Clerck O. Evolution and cytological diversification of the green seaweeds (Ulvophyceae). MOLECULAR BIOLOGY AND EVOLUTION. 2010;27(9):2052–61.
MLA
Cocquyt, Ellen, Heroen Verbruggen, Frédérik Leliaert, et al. “Evolution and Cytological Diversification of the Green Seaweeds (Ulvophyceae).” MOLECULAR BIOLOGY AND EVOLUTION 27.9 (2010): 2052–2061. Print.