[en] Chlamydomonas reinhardtii is a unicellular green alga whose lineage diverged from land plants over 1 billion years ago. It is a model system for studying chloroplast-based photosynthesis, as well as the structure, assembly, and function of eukaryotic flagella (cilia), which were inherited from the common ancestor of plants and animals, but lost in land plants. We sequenced the approximately 120-megabase nuclear genome of Chlamydomonas and performed comparative phylogenomic analyses, identifying genes encoding uncharacterized proteins that are likely associated with the function and biogenesis of chloroplasts or eukaryotic flagella. Analyses of the Chlamydomonas genome advance our understanding of the ancestral eukaryotic cell, reveal previously unknown genes associated with photosynthetic and flagellar functions, and establish links between ciliopathy and the composition and function of flagella.
Materials and methods and supplemental online (SOM) text are available as supporting material on Science Online.
E. H. Harris, Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 363 (2001).
L. C. Keller, E. P. Romijn, I. Zamora, J. R. Yates 3rd, W. F. Marshall, Curr. Biol. 15, 1090 (2005).
G. J. Pazour, N. Agrin, B. L. Walker, G. B. Witman, J. Med. Genet. 43, 62 (2006).
C. Vilchez, I. Garbayo, E. Markvicheva, F. Galvan, R. Leon, Bioresour. Technol. 78, 55 (2001).
M. L. Ghirardi et al., Annu. Rev. Plant Biol. 58, 71 (2007).
H. S. Yoon, J. D. Hackett, C. Ciniglia, G. Pinto, D. Bhattacharya, Mol. Biol. Evol. 21, 809 (2004).
J. B. Li et al., Cell 117, 541 (2004).
A. R. Grossman et al., Curr. Opin. Plant Biol. 10, 190 (2007).
Chlamydomonas reinhardtii v 3.0, DOE Joint Genome Institute, www.jgi.doe.gov/chlamy.
R. Storms, P. J. Hastings, Exp. Cell Res. 104, 39 (1977).
P. Kathir et al., Eukaryot. Cell 2, 362 (2003).
L. A. Rymarquis, J. M. Handley, M. Thomas, D. B. Stern, Plant Physiol. 137, 557 (2005).
M. Jain et al., Nucleic Acids Res. 35, 2074 (2007).
Q. Yuan et al., Plant Physiol. 138, 18 (2005).
M. Yandell et al., PLoS Comput Biol 2, e15 (2006).
B. Palenik et al., Proc. Natl. Acad. Sci. U.S.A. 104, 7705 (2007).
P. Schaap, Front. Biosci. 10, 1485 (2005).
E. Hasegawa, H. Hayashi, S. Asakura, R. Kamiya, Cell Motil. Cytoskeleton 8, 302 (1987).
S. M. Pasquale, U. W. Goodenough, J. Cell Biol. 105, 2279 (1987).
A. R. Gaillard, L. A. Fox, J. M. Rhea, B. Craige, W. S. Sale, Mol. Biol. Cell 17, 2626 (2006).
D. Gonzalez-Ballester, A. de Montaigu, J. J. Higuera, A. Galvan, E. Fernandez, Plant Physiol. 137, 522 (2005).
S. V. Pollock, W. Pootakham, N. Shibagaki, J. L. Moseley, A. R. Grossman, Photosynth. Res. 86, 475 (2005).
A. Grossman, H. Takahashi, Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 163 (2001).
S. Somlo, B. Ehrlich, Curr. Biol. 11(9), R356 (2001).
T. Avidor-Reiss et al., Cell 117, 527 (2004).
M. W. Gray, Curr. Opin. Genet. Dev. 9, 678 (1999).
D. Bhattacharya, H. S. Yoon, J. D. Hackett, Bioessays 26, 50 (2004).
P. Keeling, Protist 155, 3 (2004).
E. V. Armbrust et al., Science 306, 79 (2004).
Phaeodactylum tricornutum, v2.0, DOE Joint Genome Institute, www.jgi.doe.gov/phaeodactylum.
A. M. Duchêne et al., Proc. Natl. Acad. Sci. U.S.A. 102, 16484 (2005).
A. J. Perry, J. M. Hulett, V. A. Likic, T. Lithgow, P. R. Gooley, Curr. Biol. 16, 221 (2006).
A. J. Ytterberg, J. B. Peltier, K. J. van Wijk, Plant Physiol. 140, 984 (2006).
M. Schmidt et al., Plant Cell 18, 1908 (2006).
P. A. Vidi et al., J. Biol. Chem. 281, 11225 (2006).
M. J. Zylka, S. M. Reppert, Brain Res. Mol. Brain Res. 74, 175 (1999).
E. Sato et al., Biochemistry 43, 14189 (2004).
M. R. Lamb, S. K. Dutcher, C. K. Worley, C. L. Dieckmann, Genetics 153, 721 (1999).
T. Q. Do, A. Y. Hsu, T. Jonassen, P. T. Lee, C. F. Clarke, J. Biol. Chem. 276, 18161 (2001).
P. Zimmermann, M. Hirsch-Hoffmann, L. Hennig, W. Gruissem, Plant Physiol. 136, 2621 (2004).
G. J. Pazour, N. Agrin, J. Leszyk, G. B. Witman, J. Cell Biol. 170, 103 (2005).
E. T. O'Toole, T. H. Giddings, J. R. McIntosh, S. K. Dutcher, Mol. Biol. Cell 14, 2999 (2003).
D. L. Bernhard, K. S. Renzaglia, Bryologist 98, 52 (1995).
I. Manton, K. Kowallik, H. A. von Stosch, J. Cell Sci. 6, 131 (1970).
I. B. Heath, W. M. Darley, J. Phycol. 18, 51 (1972).
L. J. Briggs, J. A. Davidge, B. Wickstead, M. L. Ginger, K. Gull, Curr. Biol. 14, R611 (2004).
J. L. Rosenbaum, G. B. Witman, Nat. Rev. Mol. Cell Biol. 3, 813 (2002).
G. J. Pazour, B. L. Dickert, G. B. Witman, J. Cell Biol. 144, 473 (1999).
H. Qin, D. R. Diener, S. Geimer, D. G. Cole, J. L. Rosenbaum, J. Cell Biol. 164, 255 (2004).
S. J. Ansley et al., Nature 425, 628 (2003).
O. E. Blacque et al., Genes Dev. 18, 1630 (2004).
G. Ou et al., Mol. Biol. Cell 18, 1554 (2007).
F. D. Ciccarelli et al., Science 311, 1283 (2006).
P. J. Keeling et al., Trends Ecol. Evol. 20, 670 (2005).
L. Eichinger et al., Nature 435, 43 (2005).
We thank R. Howson for help with drawing figures, E. Begovic and S. Nicholls for comments on the manuscript. SM is supported by the grants NIH GM42143, DOE DE-FG02-04ER15529 USDA 2004-35318-1495. SP and DSR are funded by USDA and DOE, Joint Genome Institute. ARG is supported by USDA 2003-35100-13235, DOE DE-AC36-99GO10337 and the NSFfunded Chlamydomonas Genome Project, MCB 0235878. SJK was supported in part by a Ruth L. Kirschstein National Research Service Award GM07185. The authors declare they have no conflicts of interest. Genome assembly together with predicted gene models and and annotations were deposited at DDBJ/EMBL/GenBank under the project accession ABCN00000000. Since manual curation continues, some models or anotations are changing and the latest set of gene models and annotations is available from www.jgi.doe.gov/chlamy. The most recent set, which includes a number of changes compared with the frozen set used for this analysis, was submitted as the first version, ABCN01000000.