Sequence of the Gonium pectorale mating locus reveals a complex and dynamic history of changes in volvocine algal mating haplotypes

G3: Genes, Genomes, Genetics

Volumn 6, Issue 5, 2016, Pages 1179-1189

  Hamaji, Takashi ^a   Mogi, Yuko ^b   Ferris, Patrick J ^c   Mori, Toshiyuki ^b   Miyagishima, Shinya ^d   Kabeya, Yukihiro ^d   Nishimura, Yoshiki ^a   Toyoda, Atsushi ^e   Noguchi, Hideki ^e   Fujiyama, Asao ^e   Olson, Bradley J S C ^f   Marriage, Tara N ^f   Nishii, Ichiro ^g   Umen, James G ^a   Nozaki, Hisayoshi ^b  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c The University of Arizona   (United States)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f KANSAS STATE UNIVERSITY   (United States)

^g NARA WOMEN'S UNIVERSITY   (Japan)

Author keywords

Chlamydomonas; Evolution; Genetics of Sex; Gonium; Mating locus; Volvox

Indexed keywords

CHLAMYDOMONAS; FERTILIZATION; GENETICS; HAPLOTYPE; MATING; SEXUAL DEVELOPMENT; STRUCTURE ACTIVITY RELATION; VOLVOX; BIOLOGY; CHROMOSOME WALKING; CLASSIFICATION; GENE EXPRESSION; GENETIC LINKAGE; GENOMICS; HIGH THROUGHPUT SEQUENCING; MOLECULAR EVOLUTION; PHYLOGENY; PLANT GENOME; PROCEDURES; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; SEX DETERMINATION PROCESS;

CHROMOSOME WALKING; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENETIC LINKAGE; GENOME, PLANT; GENOMICS; HAPLOTYPES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PHYLOGENY; QUANTITATIVE TRAIT LOCI; REPRODUCTION; SEX DETERMINATION PROCESSES; VOLVOX;

EID: 84966415489     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.026229     Document Type: Article

References (48)

1. Ahmed, S., J. M. Cock, E. Pessia, R. Luthringer, A. Cormier et al., 2014 A haploid system of sex determination in the brown alga Ectocarpus sp. Curr. Biol. 24: 1945-1957.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Bachtrog, D., M. Kirkpatrick, J. E. Mank, S. F. McDaniel, J. C. Pires et al., 2011 Are all sex chromosomes created equal? Trends Genet. 27: 350-357.
4. Charlesworth, D., and B. Charlesworth, 2010 Evolutionary biology: the origins of two sexes. Curr. Biol. 20: R519-R521.
5. Charlesworth, D., B. Charlesworth, and G. Marais, 2005 Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118-128.
6. Coleman, A. W., 2012 A comparative analysis of the Volvocaceae (Chlorophyta). J. Phycol. 48: 491-513.
7. De Hoff, P. L., P. Ferris, B. J. S. C. Olson, A. Miyagi, S. Geng et al., 2013 Species and population level molecular profiling reveals cryptic recombination and emergent asymmetry in the dimorphic mating locus of C. reinhardtii. PLoS Genet. 9: e1003724.
8. Ferris, P. J., and U. W. Goodenough, 1994 The mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76: 1135-1145.
9. Ferris, P. J., and U. W. Goodenough, 1997 Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics 146: 859-869.
10. Ferris, P., J. Woessner, and U. Goodenough, 1996 A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol. Biol. Cell 7: 1235-1248.
11. Ferris, P. J., C. Pavlovic, S. Fabry, and U. W. Goodenough, 1997 Rapid evolution of sex-related genes in Chlamydomonas. Proc. Natl. Acad. Sci. USA 94: 8634-8639.
12. Ferris, P. J., E. V. Armbrust, and U. W. Goodenough, 2002 Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160: 181-200.
13. Ferris, P., B. J. S. C. Olson, P. L. De Hoff, S. Douglass, D. Casero et al., 2010 Evolution of an expanded sex-determining locus in Volvox. Science 328: 351-354.
14. Gasteiger, E., A. Gattiker, C. Hoogland, I. Ivanyi, R. D. Appel et al., 2003 ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31: 3784-3788.
15. Geng, S., P. De Hoff, and J. G. Umen, 2014 Evolution of sexes from an ancestral mating-type specification pathway. PLoS Biol. 12: e1001904.
16. Goodenough, U., H. Lin, and J.-H. Lee, 2007 Sex determination in Chlamydomonas. Semin. Cell Dev. Biol. 18: 350-361.
17. Hamaji, T., P. J. Ferris, A. W. Coleman, S. Waffenschmidt, F. Takahashi et al., 2008 Identification of the minus-dominance gene ortholog in the mating-type locus of Gonium pectorale. Genetics 178: 283-294.
18. Hamaji, T., P. J. Ferris, I. Nishii, and H. Nozaki, 2009 Identification of the minus mating-type specific gene MTD1 from Gonium pectorale (Volvocales, Chlorophyta). J. Phycol. 45: 1310-1314.
19. Hamaji, T., P. J. Ferris, I. Nishii, Y. Nishimura, and H. Nozaki, 2013a Distribution of the sex-determining gene MID and molecular correspondence of mating types within the isogamous genus Gonium (Volvocales, Chlorophyta). PLoS One 8: e64385.
20. Hamaji, T., D. R. Smith, H. Noguchi, A. Toyoda, M. Suzuki et al., 2013b Mitochondrial and plastid genomes of the colonial green alga Gonium pectorale give insights into the origins of organelle DNA architecture within the Volvocales. PLoS One 8: e57177.
21. Hanschen, E. R., T. N.Marriage, P. J. Ferris, T. Hamaji, A. Toyoda, A. Fujiyama, R. Neme, H. Noguchi, Y. Minakuchi, M. Suzuki, H. Kawai-Toyooka, D. R. Smith, H. Sparks, J. Anderson, R. Bakarić, V. Luria, A. Karger, M. Kirschner, P. M. Durand, R. E. Michod, H. Nozaki, and B. J. S. C. Olson, 2016 Cell cycle regulation, group level adaptation, and the evolution of multicellularity. Nat. Commun. (in press).
22. Herron, M. D., and R. E. Michod, 2008 Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye. Evolution 62: 436-451.
23. Hiraide, R., H. Kawai-Toyooka, T. Hamaji, R. Matsuzaki, K. Kawafune et al., 2013 The evolution of male-female sexual dimorphism predates the gender-based divergence of the mating locus gene MAT3/RB. Mol. Biol. Evol. 30: 1038-1040.
24. Immler, S., and S. P. Otto, 2015 The evolution of sex chromosomes in organisms with separate haploid sexes. Evolution 69: 694-708.
25. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A.McGettigan et al., 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
26. Librado, P., and J. Rozas, 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
27. Lin, H., and U.W. Goodenough, 2007 Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics 176: 913-925.
28. Liu, Y.-G., and R. F. Whittier, 1995 Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25: 674-681.
29. McDaniel, S. F., K. M. Neubig, A. C. Payton, R. S. Quatrano, and D. J. Cove, 2013 Recent gene-capture on the UV sex chromosomes of the moss Ceratodon purpureus. Evolution 67: 2811-2822.
30. Merchant, S. S., S. E. Prochnik, O. Vallon, E. H. Harris, S. J. Karpowicz et al., 2007 The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250.
31. Misamore, M. J., S. Gupta, and W. J. Snell, 2003 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: 2530-2542.
32. Mogi, Y., T. Hamaji, M. Suzuki, P. Ferris, T. Mori et al., 2012 Evidence for tubular mating structures induced in each mating type of heterothallic Gonium pectorale (Volvocales, Chlorophyta). J. Phycol. 48: 670-674.
33. Nei, M., 1987 Molecular Evolutionary Genetics, Columbia University Press, New York, NY.
34. Nozaki, H., K. Misawa, T. Kajita, M. Kato, S. Nohara et al., 2000 Origin and evolution of the colonial Volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Mol. Phylogenet. Evol. 17: 256-268.
35. Nozaki, H., T. Mori, O. Misumi, S. Matsunaga, and T. Kuroiwa, 2006 Males evolved from the dominant isogametic mating type. Curr. Biol. 16: R1018-R1020.
36. Pasquale, S. M., and U. W. Goodenough, 1987 Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J. Cell Biol. 105: 2279-2292.
37. Prochnik, S. E., J. Umen, A. M. Nedelcu, A. Hallmann, S. M. Miller et al., 2010 Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329: 223-226.
38. Salamov, A. A., and V. V. Solovyev, 2000 Ab initio gene finding in Drosophila genomic DNA. Genome Res. 10: 516-522.
39. Sambrook, J., and D.W. Russell, 2001 Molecular cloning: a laboratory manual, NY Cold Spring Harbor Laboratory Press., Cold Spring Harbor, NY.
40. Setohigashi, Y., T. Hamaji, M. Hayama, R. Matsuzaki, and H. Nozaki, 2011 Uniparental inheritance of chloroplast DNA is strict in the isogamous Volvocalean Gonium. PLoS One 6: e19545.
41. Soderlund, C., W. Nelson, A. Shoemaker, and A. Paterson, 2006 SyMAP: A system for discovering and viewing syntenic regions of FPC maps. Genome Res. 16: 1159-1168.
42. Soderlund, C., M. Bomhoff, and W. M. Nelson, 2011 SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res. 39: e68.
43. Sun, S., Y.-P. Hsueh, and J. Heitman, 2012 Gene conversion occurs within the mating-type locus of Cryptococcus neoformans during sexual reproduction. PLoS Genet. 8: e1002810.
44. Umen, J. G., 2011 Evolution of sex and mating loci: an expanded view from Volvocine algae. Curr. Opin. Microbiol. 14: 634-641.
45. Yamada, T. K., T. Nakada, K. Miyaji, and H. Nozaki, 2006 Morphology and molecular phylogeny of Gonium multicoccum (Volvocales, Chlorophyceae) newly found in Japan. J. Jpn. Bot. 81: 139-147.
46. Yamato, K. T., K. Ishizaki, M. Fujisawa, S. Okada, S. Nakayama et al., 2007 Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc. Natl. Acad. Sci. USA 104: 6472-6477.
47. Yang, Z., 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586.
48. Yang, Z., and R. Nielsen, 2000 Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17: 32-43.