Sex determination in Chlamydomonas

Seminars in Cell and Developmental Biology

Volumn 18, Issue 3, 2007, Pages 350-361

  Goodenough, Ursula ^a   Lin, Huawen ^a   Lee, Jae Hyeok ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chlamydomonas; Chloroplast genome; Fertilization; Homeoprotein; Mating type

Indexed keywords

ALGAL GENETICS; AUTOSOME; CELL DIFFERENTIATION; CHLAMYDOMONAS REINHARDTII; GAMETE; GENE EXPRESSION; GENE LOCUS; GREEN ALGA; NONHUMAN; REVIEW; SEX DETERMINATION; ZYGOTE;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

EID: 34547655805     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2007.02.006     Document Type: Review

References (115)

1. Goodenough U.W. Chlamydomonas mating interactions. In: Dworkin M. (Ed). Microbial cell-cell interactions (1991), American Society for Microbiology, Washington, DC 71-112
2. Goodenough U.W., Armbrust E.V., Campbell A.M., and Ferris P.J. Molecular genetics of sexuality in Chlamydomonas. Ann Rev Plant Physiol Plant Mol Biol 46 (1995) 21-44
3. Beck C.F., and Haring M.A. Gametic differentiation of Chlamydomonas. Int Rev Cytol 168 (1996) 259-302
4. Pan J., and Snell W.J. Signal transduction during fertilization in the unicellular green alga, Chlamydomonas. Curr Opin Microbiol 3 (2000) 596-602
5. Pan J., Misamore M.J., Wang Q., and Snell W.J. Protein transport and signal transduction during fertilization in Chlamydomonas. Traffic 4 (2003) 452-459
6. Berney C., and Pawlowski J. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc Biol Sci 273 (2006) 1867-1872
7. Cavalier-Smith T., Brasier M., and Embley T.M. Introduction: how and when did microbes change the world?. Philos Trans R Soc Lond B: Biol Sci 361 (2006) 845-850
8. Ramesh M.A., Malik S.B., and Logsdon Jr. J.M. A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15 (2005) 185-191
9. Derelle E., Ferraz C., Rombauts S., Rouze P., Worden A.Z., Robbens S., et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103 (2006) 11647-11652
10. Harris E.H. The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use (1989), Academic Press, San Diego
11. Sager R., and Granick S. Nutritional control of sexuality in Chlamydomonas reinhardi. J Gen Physiol 37 (1954) 729-742
12. Ebersold W.T. Chlamydomonas reinhardi: heterozygous diploid strains. Science 157 (1967) 447
13. Galloway R.E., and Goodenough U.W. Genetic analysis of mating locus linked mutations in Chlamydomonas reinhardtii. Genetics 111 (1985) 447-461
14. Abe J., Kubo T., Takagi Y., Saito T., Miura K., Fukuzawa H., et al. The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii. Curr Genet 46 (2004) 304-315
15. Abe J., Kubo T., Saito T., and Matsuda Y. The regulatory networks of gene expression during the sexual differentiation of Chlamydomonas reinhardtii, as analyzed by mutants for gametogenesis. Plant Cell Physiol 46 (2005) 312-316
16. Gromoff E.D., and Beck C.F. Genes expressed during sexual differentiation of Chlamydomonas reinhardtii. Mol Genet Genom 241 (1993) 415-421
17. Gloeckner G., and Beck C.F. Genes involved in light control of sexual differentiation in Chlamydomonas reinhardtii. Genetics 141 (1995) 937-943
18. Gillham N.W. Uniparental inheritance in Chlamydomonas reinhardi. Am Nat 103 (1969) 355-388
19. Ferris P.J., and Goodenough U.W. The mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76 (1994) 1135-1145
20. Uyenoyama M.K. Evolution under tight linkage to mating type. New Phytologist 165 (2005) 63-70
21. Gallegos A., Jacobson D.J., Raju N.B., Skupski M.P., and Natvig D.O. Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma. Genetics 154 (2000) 623-633
22. Fraser J.A., Diezmann S., Subaran R.L., Allen A., Lengeler K.B., Dietrich F.S., et al. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2 (2004) e384
23. Hood M.E., Antonovics J., and Koskella B. Shared forces of sex chromosome evolution in haploid-mating and diploid-mating organisms: Microbotryum violaceum and other model organisms. Genetics 168 (2004) 141-146
24. Grewal S.I., and Klar A.J. A recombinationally repressed region between mat2 and mat3 loci shares homology to centromeric repeats and regulates directionality of mating-type switching in fission yeast. Genetics 146 (1997) 1221-1238
25. Ferris P.J., Armbrust E.V., and Goodenough U.W. Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160 (2002) 181-200
26. Lee N., Bakkeren G., Wong K., Sherwood J.E., and Kronstad J.W. The mating-type and pathogenicity locus of the fungus Ustilago hordei spans a 500-kb region. Proc Natl Acad Sci USA (1999) 15026-15031
27. Badrane H., and May G. The divergence-homogenization duality in the evolution of the b1 mating type gene of Coprinus cinereus. Mol Biol Evol 16 (1999) 975-986
28. Schartl M. Sex chromosome evolution in non-mammalian vertebrates. Curr Opin Genet Dev 14 (2004) 634-641
29. Graves J.A. Sex chromosome specialization and degeneration in mammals. Cell 124 (2006) 901-914
30. Martin N.C., and Goodenough U.W. Gametic differentiation in Chlamydomonas reinhardtii. I. Production of gametes and their fine structure. J Cell Biol 67 (1975) 587-605
31. Martin N.C., Chiang K.S., and Goodenough U.W. Turnover of chloroplast and cytoplasmic ribosomes during gametogenesis in Chlamydomonas reinhardi. Dev Biol 51 (1976) 190-201
32. Vallon O., Bulte L., Kuras R., Olive J., and Wollman F.A. Extensive accumulation of an extracellular l-amino-acid oxidase during gametogenesis of Chlamydomonas reinhardtii. Eur J Biochem 215 (1993) 351-360
33. Merchan F., van den Ende H., Fernandez E., and Beck C.F. Low-expression genes induced by nitrogen starvation and subsequent sexual differentiation in Chlamydomonas reinhardtii, isolated by the differential display technique. Planta 213 (2001) 309-317
34. Lin H., and Goodenough U.W. Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes MID and MTD1. Genetics 176 (2007) 913-925
35. Goodenough U.W., Detmers P.A., and Hwang C. Activation for cell fusion in Chlamydomonas: analysis of wild-type gametes and nonfusing mutants. J Cell Biol 92 (1982) 378-386
36. Ferris P.J., and Goodenough U.W. Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics 146 (1997) 859-869
37. Schnell R.A., and Lefebvre P.A. Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics 134 (1993) 737-747
38. Galvan A., and Fernandez E. Eukaryotic nitrate and nitrite transporters. Cell Mol Life Sci 58 (2001) 225-233
39. Schauser L., Roussis A., Stiller J., and Stougaard J. A plant regulator controlling development of symbiotic root nodules. Nature 402 (1999) 191-195
40. Schauser L., Wieloch W., and Stougaard J. Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60 (2005) 229-237
41. Borisov A.Y., Madsen L.H., Tsyganov V.E., Umehara Y., Voroshilova V.A., Batagov A.O., et al. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol 131 (2003) 1009-1017
42. Ferris P.J., Woessner J.P., and Goodenough U.W. A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol Biol Cell 7 (1996) 1235-1248
43. Misamore M.J., Gupta S., and Snell W.J. The Chlamydomonas Fus1 protein is present on the mating type plus fusion organelle and required for a critical membrane adhesion event during fusion with minus gametes. Mol Biol Cell 14 (2003) 2530-2542
44. Goodenough U.W., Hwang C., and Martin H. Isolation and genetic analysis of mutant strains of Chlamydomonas reinhardi defective in gametic differentiation. Genetics 82 (1976) 169-186
45. Goodenough U.W., Hwang C., and Warren A.J. Sex-limited expression of gene loci controlling flagellar membrane agglutination in the Chlamydomonas mating reaction. Genetics 89 (1978) 235-243
46. - mating-type locus of Chlamydomonas. Genetics 99 (1981) 41-47
47. Cooper J.B., Adair W.S., Mecham R.P., Heuser J.E., and Goodenough U.W. Chlamydomonas agglutinin is a hydroxyproline-rich glycoprotein. Proc Natl Acad Sci USA 80 (1983) 5898-5901
48. Goodenough U.W., Adair W.S., Collin-Osdoby P., and Heuser J.E. Structure of the Chlamydomonas agglutinin and related flagellar surface proteins in vitro and in situ. J Cell Biol 101 (1985) 924-941
49. Ferris P.J., Waffenschmidt S., Umen J.G., Lin H., Lee J.H., Ishida K., et al. Plus and minus sexual agglutinins from Chlamydomonas reinhardtii. Plant Cell 17 (2005) 597-615
50. Cassab G.I. Plant cell wall proteins. Ann Rev Plant Physiol Plant Mol Biol 49 (1998) 281-309
51. Goodenough U.W., and Heuser J.E. The Chlamydomonas cell wall and its constituent glycoproteins analyzed by the quick-freeze, deep-etch technique. J Cell Biol 101 (1985) 1550-1568
52. Goodenough U.W., and Heuser J.E. Molecular organization of cell-wall crystals from Chlamydomonas reinhardtii and Volvox carteri. J Cell Sci 90 (1988) 717-734
53. Goodenough U.W., Gebhart B., Mecham R.P., and Heuser J.E. Crystals of the Chlamydomonas reinhardtii cell wall: polymerization, depolymerization, and purification of glycoprotein monomers. J Cell Biol 103 (1986) 405-417
54. Goodenough U.W., and Heuser J.E. Deep-etch analysis of adhesion complexes between gametic flagellar membranes of Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 35 (1999) 756-767
55. Pasquale S.M., and Goodenough U.W. Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105 (1987) 2279-2292
56. Wilson N.F., O'Connell J.S., Lu M., and Snell W.J. Flagellar adhesion between mt(+) and mt(-) Chlamydomonas gametes regulates phosphorylation of the mt(+)-specific homeodomain protein GSP1. J Biol Chem 274 (1999) 34383-34388
57. Saito T., Small L., and Goodenough U.W. Activation of adenylyl cyclase in Chlamydomonas reinhardtii by adhesion and by heat. J Cell Biol 122 (1993) 137-147
58. Kurvari V., Zhang Y., Luo Y., and Snell W.J. Molecular cloning of a protein kinase whose phosphorylation is regulated by gametic adhesion during Chlamydomonas fertilization. Proc Natl Acad Sci USA 93 (1996) 39-43
59. Pan J., and Snell W.J. Regulated targeting of a protein kinase into an intact flagellum: an aurora/lpl1p-like protein kinase translocates from the cell body into the flagella during gamete activation in Chlamydomonas. J Biol Chem 275 (2000) 24106-24114
60. Wang Q., and Snell W.J. Flagellar adhesion between mating type plus and mating type minus gametes activates a flagellar protein-tyrosine kinase during fertilization in Chlamydomonas. J Biol Chem 278 (2003) 32936-32942
61. Wang Q., Pan J., and Snell W.J. Intraflagellar transport particles participate directly in cilium-generated signaling in Chlamydomonas. Cell 125 (2006) 549-562
62. Snell W.J., and Moore W.S. Aggregation-dependent turnover of flagellar adhesion molecules in Chlamydomonas gametes. J Cell Biol 84 (1980) 203-210
63. Saito T., Tsubo Y., and Matsuda Y. Synthesis and turnover of cell body-agglutinin as a pool of flagellar surface-agglutinin in Chlamydomonas reinhardii gamete. Arch Microbiol 142 (1985) 207-210
64. Goodenough U.W. Cyclic AMP enhances the sexual agglutinability of Chlamydomonas flagella. J Cell Biol 109 (1989) 247-252
65. Snell W.J., Pan J., and Wang Q. Cilia and flagella revealed from flagellar assembly in Chlamydomonas to human obesity disorders. Cell 117 (2004) 693-697
66. Kinoshita T., Fukuzawa H., Shimada T., Saito T., and Matsuda Y. Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii: similarity of functional domains to matrix metalloproteases. Proc Natl Acad Sci USA 89 (1992) 4693-4697
67. Matsuda Y. Topography of cell wall lytic enzyme in Chlamydomonas reinhardtii: form and location of the stored enzyme in vegetative cell and gamete. J Cell Biol 104 (1987) 321-329
68. Buchanan M.J., Imam S.H., Eskue W.A., and Snell W.J. Activation of the cell wall degrading protease, lysin, during sexual signalling in Chlamydomonas: the enzyme is stored as an inactive, higher relative molecular mass precursor in the periplasm. J Cell Biol 108 (1989) 199-207
69. Matsuda Y., Saito T., Yamaguchi T., and Kawase H. Cell wall lytic enzyme released by mating gametes of Chlamydomonas reinhardtii is a metalloprotease and digests the sodium perchlorate-insoluble component of cell wall. J Biol Chem 260 (1985) 6373-6377
70. Weiss R.L., Goodenough D.A., and Goodenough U.W. Membrane differentiations at sites specialized for cell fusion. J Cell Biol 72 (1977) 144-160
71. Goodenough U.W., and Weiss R.L. Interrelationships between microtubules, a striated fiber, and the gametic mating structure of Chlamydomonas reinhardi. J Cell Biol 76 (1978) 430-438
72. Goodenough U.W., and Weiss R.L. Gametic differentiation in Chlamydomonas reinhardtii. III. Cell wall lysis and microfilament-associated mating structure activation in wild-type and mutant strains. J Cell Biol 67 (1975) 623-637
73. Detmers P.A., Goodenough U.W., and Condeelis J. Elongation of the fertilization tubule in Chlamydomonas: new observations on the core microfilaments and the effect of transient intracellular signals on their structural integrity. J Cell Biol 97 (1983) 522-532
74. Wilson N.F., Foglesong M.J., and Snell W.J. The Chlamydomonas mating type plus fertilization tubule, a prototypic cell fusion organelle: isolation, characterization, and in vitro adhesion to mating type minus gametes. J Cell Biol 137 (1997) 1537-1553
75. Mori T., Kuroiwa H., Higashiyama T., and Kuroiwa T. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8 (2006) 64-71
76. Forest C.L., Goodenough D.A., and Goodenough U.W. Flagellar membrane agglutination and sexual signaling in the conditional gam-1 mutant of Chlamydomonas. J Cell Biol 79 (1978) 74-84
77. Davidson E.H. Genomic regulatory systems: development and evolution (2001), Academic Press, San Diego, CA
78. Minami S.A., and Goodenough U.W. Novel glycopolypeptide synthesis induced by gametic cell fusion in Chlamydomonas reinhardtii. J Cell Biol 77 (1978) 165-181
79. Ferris P.J., and Goodenough U.W. Transcription of novel genes, including a gene linked to the mating-type locus, induced by Chlamydomonas fertilization. Mol Cell Biol 7 (1987) 2360-2366
80. Woessner J.P., and Goodenough U.W. Molecular characterization of a zygote wall protein: an extensin-like molecule in Chlamydomonas reinhardtii. Plant Cell 1 (1989) 901-911
81. Uchida H., Kawano S., Sato N., and Kuroiwa T. Isolation and characterization of novel genes which are expressed during the very early stage of zygote formation in Chlamydomonas reinhardtii. Curr Genet 24 (1993) 296-300
82. Uchida H., Suzuki L., Anai T., Doi K., Takano H., Yamashita H., et al. A pair of invertedly repeated genes in Chlamydomonas reinhardtii encodes a zygote-specific protein whose expression is UV-sensitive. Curr Genet 36 (1999) 232-240
83. Suzuki L., Woessner J.P., Uchida H., Kuroiwa H., Yuasa Y., Waffenschmidt S., et al. A zygote-specific protein with hydroxyproline-rich glycoprotein domains and lectin-like domains involved in the assembly of the cell wall of Chlamydomonas reinhardtii (Chlorophyta). J Phycol 36 (2000) 571-583
84. Matters G.L., and Goodenough U.W. A gene/pseudogene tandem duplication encodes a cysteine-rich protein expressed during zygote development in Chlamydomonas reinhardtii. Mol Gen Genet 232 (1992) 81-88
85. Rodriguez H., Haring M.A., and Beck C.F. Molecular characterization of two light-induced, gamete-specific genes from Chlamydomonas reinhardtii that encode hydroxyproline-rich proteins. Mol Genet Genom 261 (1999) 267-274
86. Hoffmann X.-K., and Beck C.F. Mating-induced shedding of cell walls, removal of walls from vegetative cells, and osmotic stress induce presumed cell wall genes in Chlamydomonas. Plant Physiol 139 (2005) 999-1014
87. Kurvari V., Grishin N.V., and Snell W.J. A gamete-specific, sex-limited homeodomain protein in Chlamydomonas. J Cell Biol 143 (1998) 1971-1980
88. - gametes initiates zygote development without gamete fusion. Genes Dev 15 (2001) 2767-2777
89. Birky C.W. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92 (1995) 11331-11338
90. Kaneda H., Hayashi J., Takahama S., Taya C., Lindahl K.F., and Yonekawa H. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92 (1995) 4542-4546
91. Shitara H., Hayashi J.I., Takahama S., Kaneda H., and Yonekawa H. Maternal inheritance of mouse mtDNA in interspecific hybrids: segregation of the leaked paternal mtDNA followed by the prevention of subsequent paternal leakage. Genetics 148 (1998) 851-858
92. Sutovsky P., McCauley T.C., Sutovsky M., and Day B.N. Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol Reprod 68 (2003) 1793-1800
93. Thompson W.E., Ramalho-Santos J., and Sutovsky P. Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 69 (2003) 254-260
94. Kuroiwa T., Kawano S., Nishibayashi S., and Sato C. Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298 (1982) 481-483
95. Nishimura Y., Misumi O., Matsunaga S., Higashiyama T., Yokota A., and Kuroiwa T. The active digestion of uniparental chloroplast DNA in a single zygote of Chlamydomonas reinhardtii is revealed by using the optical tweezer. Proc Natl Acad Sci USA 96 (1999) 12577-12582
96. Umen J.G., and Goodenough U.W. Chloroplast DNA methylation and inheritance in Chlamydomonas. Genes Dev 15 (2001) 2585-2597
97. Sager R., and Lane D. Molecular basis of maternal inheritance. Proc Natl Acad Sci 69 (1972) 2410-2413
98. - chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev 16 (2002) 1116-1128
99. Gillham N.W., Boynton J.E., Johnson A.M., and Burkhart B.D. Mating type linked mutations which disrupt the uniparental transmission of chloroplast genes in Chlamydomonas. Genetics 115 (1987) 677-684
100. Armbrust E.V., Ibrahim A., and Goodenough U.W. A mating type-linked mutation that disrupts the uniparental inheritance of chloroplast DNA also disrupts cell-size control in Chlamydomonas. Mol Biol Cell 6 (1995) 1807-1818
101. Umen J.G., and Goodenough U.W. Control of cell division by a retinoblastoma protein homolog in Chlamydomonas. Genes Dev 15 (2001) 1652-1661
102. Wurtz E.A., Boynton J.E., and Gillham N.W. Perturbation of chloroplast DNA amounts and chloroplast gene transmission in Chlamydomonas reinhardtii by 5-fluorodeoxyuridine. Proc Natl Acad Sci USA 74 (1977) 4552-4556
103. Sager R., and Ramanis Z. The mechanism of maternal inheritance in Chlamydomonas: biochemical and genetic studies. Theor Appl Genet 43 (1973) 101-108
104. Balakirev M.Y., Tcherniuk S.O., Jaquinod M., and Chroboczek J. Otubains: a new family of cysteine proteases in the ubiquitin pathway. EMBO Rep 4 (2003) 517-522
105. Armbrust E.V., Ferris P.J., and Goodenough U.W. A mating type-linked gene cluster expressed in Chlamydomonas zygotes participates in the uniparental inheritance of the chloroplast genome. Cell 74 (1993) 801-811
106. Proschold T., Marin B., Schlosser U.G., and Melkonian M. Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152 (2001) 265-300
107. Mesland D.A.M. Mating in Chlamydomonas eugametos. Arch Microbiol 109 (1976) 31-35
108. Clark N.L., Aagaard J.E., and Swanson W.J. Evolution of reproductive proteins from animals and plants. Reproduction 131 (2006) 11-22
109. Coyne J.A., and Orr H.A. Speciation (2004), Sinauer, New York
110. Noor M.A., and Feder J.L. Speciation genetics: evolving approaches. Nat Rev Genet 7 (2006) 851-861
111. Stanley S.M. Clades versus clones in evolution: why we have sex. Science 190 (1975) 382
112. Wright S. The shifting balance theory and macrolevolution. Ann Rev Genet 16 (1982) 1-20
113. Coyne J., Barton N., and Turelli M. A critique of Sewall Wright's Shifting Balance theory of evolution. Evolution 51 (1997) 643-671
114. Peer K., and Taborsky M. Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sibling mating. Evolution 59 (2005) 317-323
115. Pröschold T., Marin B., Schlösser U.G., and Melknoian M. Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamyomonas Ehrenberg and Chloromonas Gobi, and description of OOgamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152 (2001) 265-300