Journal of Plant Research

, Volume 130, Issue 3, pp 423–431 | Cite as

Sexual reproduction and sex determination in green algae

  • Hiroyuki SekimotoEmail author
JPR Symposium Fusion in Fertilization: Interdisciplinary Collaboration among Plant and Animal Scientists


The sexual reproductive processes of some representative freshwater green algae are reviewed. Chlamydomonas reinhardtii is a unicellular volvocine alga having two mating types: mating type plus (mt+) and mating type minus (mt), which are controlled by a single, complex mating-type locus. Sexual adhesion between the gametes is mediated by sex-specific agglutinin molecules on their flagellar membranes. Cell fusion is initiated by an adhesive interaction between the mt+ and mt mating structures, followed by localized membrane fusion. The loci of sex-limited genes and the conformation of sex-determining regions have been rearranged during the evolution of volvocine algae; however, the essential function of the sex-determining genes of the isogamous unicellular Chlamydomonas reinhardtii is conserved in the multicellular oogamous Volvox carteri. The sexual reproduction of the unicellular charophycean alga, Closterium peracerosum-strigosum-littorale complex, is also focused on here. The sexual reproductive processes of heterothallic strains are controlled by two multifunctional sex pheromones, PR-IP and PR-IP Inducer, which independently promote multiple steps in conjugation at the appropriate times through different induction mechanisms. The molecules involved in sexual reproduction and sex determination have also been characterized.


Closterium Chlamydomonas Sexual reproduction Sex determination 



This work was partly supported by Grants-in-Aid for Scientific Research (nos. 24370038, 25304012, 26650147, 15H05237, and 16H04836) from the Japan Society for the Promotion of Science, Grants-in-Aid for Scientific Research on Innovative Areas “Elucidating common mechanisms of allogenic authentication” (no. 24112713 to H.S.) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan. The work was also partly supprted by MEXT KAKENHI (221S0002).


  1. Abe J, Hori S, Tsuchikane Y, Kitao N, Kato M, Sekimoto H (2011) Stable nuclear transformation of the Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol 52:1676–1685. doi: 10.1093/pcp/pcr103 CrossRefPubMedGoogle Scholar
  2. Abe J, Hirano N, Komiya A, Kanda N, Fujiwara A, Hori S, Tsuchikane Y, Sekimoto H (2016a) Preparation of knockdown transformants of unicellular charophycean alga, Closterium peracerosum-strigosum-littorale complex. Bio-protocol 6:e1813CrossRefGoogle Scholar
  3. Abe J, Hori S, Sato M, Sekimoto H (2016b) Concanavalin A disrupts the release of fibrous material necessary for zygote formation of a unicellular charophycean alga, Closterium peracerosum-strigosum-littorale complex. Front Plant Sci 7:1040. doi: 10.3389/fpls.2016.01040 PubMedPubMedCentralGoogle Scholar
  4. Akatsuka S, Sekimoto H, Iwai H, Fukumoto R, Fujii T (2003) Mucilage secretion regulated by sex pheromones in Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol 44:1081–1087CrossRefPubMedGoogle Scholar
  5. Akatsuka S, Tsuchikane Y, Fukumoto R, Fujii T, Sekimoto H (2006) Physiological characterization of the sex pheromone protoplast-release-inducing protein from the Closterium peracerosum-strigosum-littorale complex (Charophyta). Phycol Res 54:116–121CrossRefGoogle Scholar
  6. Buchanan MJ, Imam SH, Eskue WA, Snell WJ (1989) 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 108:199–207CrossRefPubMedGoogle Scholar
  7. Cook PA (1963) Variation in vegetative and sexual morphology among the small curved species of Closterium. Phycologia 3:1–18CrossRefGoogle Scholar
  8. Ferris PJ, Goodenough UW (1994) The Mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76:1135–1145CrossRefPubMedGoogle Scholar
  9. Ferris PJ, Goodenough UW (1997) Mating type in Chlamydomonas is specified by mid, the minus-dominance gene. Genetics 146:859–869PubMedPubMedCentralGoogle Scholar
  10. Ferris PJ, Woessner JP, Goodenough UW (1996) A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol Biol Cell 7:1235–1248CrossRefPubMedPubMedCentralGoogle Scholar
  11. Ferris P, Armbrust EV, Goodenough UW (2002) Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160:181–200PubMedPubMedCentralGoogle Scholar
  12. Ferris P, Waffenschmidt S, Umen JG, Lin H, Lee J-H, Ishida K, Kubo T, Lau J, Goodenough UW (2005) Plus and minus sexual agglutinins from Chlamydomonas reinhardtii. Plant Cell 17:597–615CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ferris P, Olson BJ, De Hoff PL, Douglass S, Casero D, Prochnik S, Geng S, Rai R, Grimwood J, Schmutz J, Nishii I, Hamaji T, Nozaki H, Pellegrini M, Umen JG (2010) Evolution of an expanded sex-determining locus in Volvox. Science 328:351–354CrossRefPubMedPubMedCentralGoogle Scholar
  14. Geng S, De Hoff P, Umen JG (2014) Evolution of sexes from an ancestral mating-type specification pathway. PloS One 12:e1001904. doi: 10.1371/journal.pbio.1002055 CrossRefGoogle Scholar
  15. Goodenough UW (1989) Cyclic AMP enhances the sexual agglutinability of Chlamydomonas flagella. J Cell Biol 109:247–252CrossRefPubMedGoogle Scholar
  16. Graham LE, Graham JE, Wilcox LW (2009) Algae 2nd edn. Benjamin Cummings, San FranciscoGoogle Scholar
  17. Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20:125–151CrossRefPubMedGoogle Scholar
  18. Hamaji T, Ferris PJ, Coleman AW, Waffenschmidt S, Takahashi F, Nishii I, Nozaki H (2008) Identification of the minus-dominance gene ortholog in the mating-type locus of Gonium pectorale. Genetics 178:283–294CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hamaji T, Ferris PJ, Nishii I, Nishimura Y, Nozaki H (2013) Distribution of the sex-determining gene MID and molecular correspondence of mating types within the isogamous genus Gonium (Volvocales, Chlorophyta). PloS One 8:e64385. doi: 10.1371/journal.pone.0064385 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hamaji T, Lopez D, Pellegrini M, Umen J (2016a) Identification and characterization of a cis-regulatory element for zygotic gene expression in Chlamydomonas reinhardtii. G3 (Bethesda) 6:1541–1548. doi: 10.1534/g3.116.029181 CrossRefGoogle Scholar
  21. Hamaji T, Mogi Y, Ferris PJ, Mori T, Miyagishima S, Kabeya Y, Nishimura Y, Toyoda A, Noguchi H, Fujiyama A, Olson BJ, Marriage TN, Nishii I, Umen JG, Nozaki H (2016b) Sequence of the Gonium pectorale mating locus reveals a complex and dynamic history of changes in volvocine algal mating haplotypes. G3 (Bethesda) 6:1179–1189 doi: 10.1534/g3.115.026229 CrossRefPubMedCentralGoogle Scholar
  22. Hanschen ER, Marriage TN, Ferris PJ, Hamaji T, Toyoda A, Fujiyama A, Neme R, Noguchi H, Minakuchi Y, Suzuki M, Kawai-Toyooka H, Smith DR, Sparks H, Anderson J, Bakaric R, Luria V, Karger A, Kirschner MW, Durand PM, Michod RE, Nozaki H, Olson BJ (2016) The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity. Nat commun 7:11370. doi: 10.1038/ncomms1137 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Harris EH (1989) The Chlamydomonas Sourcebook: a comprehensive guide to biology and laboratory use. Academic Press, San DiegoGoogle Scholar
  24. Hirano N, Marukawa Y, Abe J, Hashiba S, Ichikawa M, Tanabe Y, Ito M, Nishii I, Tsuchikane Y, Sekimoto H (2015) A Receptor-like kinase, related with cell wall sensor of higher plants, is required for sexual reproduction in the unicellular charophycean alga, Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol 56:1456–1462CrossRefPubMedGoogle Scholar
  25. Hori S, Sekimoto H, Abe J (2012) Properties of cell surface carbohydrates in sexual reproduction of the Closterium peracerosum–strigosum–littorale complex (Zygnematophyceae, Charophyta). Phycol Res 60:254–260 doi: 10.1111/j.1440-1835.2012.00656.x CrossRefGoogle Scholar
  26. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N, Moriyama T, Ikeuchi M, Watanabe M, Wada H, Kobayashi K, Saito M, Masuda T, Sasaki-Sekimoto Y, Mashiguchi K, Awai K, Shimojima M, Masuda S, Iwai M, Nobusawa T, Narise T, Kondo S, Saito H, Sato R, Murakawa M, Ihara Y, Oshima-Yamada Y, Ohtaka K, Satoh M, Sonobe K, Ishii M, Ohtani R, Kanamori-Sato M, Honoki R, Miyazaki D, Mochizuki H, Umetsu J, Higashi K, Shibata D, Kamiya Y, Sato N, Nakamura Y, Tabata S, Ida S, Kurokawa K, Ohta H (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978. doi: 10.1038/ncomms4978 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hunnicutt GR, Kosfiszer MG, Snell WJ (1990) Cell body and flagellar agglutinins in Chlamydomonas reinhardtii: the cell body plasma membrane is a reservoir for agglutinins whose migration to the flagella is regulated by a functional barrier. J Cell Biol 111:1605–1616CrossRefPubMedGoogle Scholar
  28. Ichimura T (1973) The life cycle and its control in some species of Closterium, with special reference to the biological species problem. D. Sci. thesis, University of Tokyo, TokyoGoogle Scholar
  29. Ju C, Van de Poel B, Cooper ED, Thierer JH, Gibbons TR, Delwiche CF, Chang C (2015) Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat Plant 1:14004. doi: 10.1038/nplants.2014.4 CrossRefGoogle Scholar
  30. Kanaoka MM, Higashiyama T (2015) Peptide signaling in pollen tube guidance. Curr Opin Plant Biol 28:127–136. doi: 10.1016/j.pbi.2015.10.006 CrossRefPubMedGoogle Scholar
  31. Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353. doi: 10.1126/science.1065156 CrossRefPubMedGoogle Scholar
  32. Kinoshita T, Fukuzawa H, Shimada T, Saito T, Matsuda Y (1992) Primary structure and expression of a gamete lytic enzyme in Chlamydomonas reinhardtii: similarity of functional domains to matrix metalloproteases. Proc Natl Acad Sci USA 89:4693–4697CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lee JH, Huawen L, Joo S, Goodenough UW (2008) Early sexual origins of homeoprotein heterodimerization and evolution of the plant KNOX/BELL family. Cell 133:829–840CrossRefPubMedGoogle Scholar
  34. Lin H, Goodenough UW (2007) Gametogenesis in the Chlamydomonas reinhardtii minus mating type is controlled by two genes, MID and MTD1. Genetics 176:913–925CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lippert BE (1967) Sexual reproduction in Closterium moniliferum and Closterium ehrenbergii. J Phycol 3:182–198CrossRefPubMedGoogle Scholar
  36. Liu Y, Tewari R, Ning J, Blagborough AM, Garbom S, Pei J, Grishin NV, Steele RE, Sinden RE, Snell WJ, Billker O (2008) The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes Dev 22:1051–1068. doi: 10.1101/gad.1656508 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Liu Y, Misamore MJ, Snell WJ (2010) Membrane fusion triggers rapid degradation of two gamete-specific, fusion-essential proteins in a membrane block to polygamy in Chlamydomonas. Development 137:1473–1481. doi: 10.1242/dev.044743 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250. doi: 10.1126/science.1143609 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Misamore MJ, Gupta S, Snell WJ (2002) FUS1, the cell surface protein required for Chlamydomonas fertilization, contains invasin-like internal repeats and requires actin for its localization. Mol Biol Cell 13:625Google Scholar
  40. Misamore MJ, Gupta S, Snell WJ (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 14:2530–2542CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64–71. doi: 10.1038/ncb1345 CrossRefPubMedGoogle Scholar
  42. Noguchi T (1988) Numerical and structural changes in dictyosomes during zygospore germination of Closterium ehrenbergii. Protoplasma 147:135–142CrossRefGoogle Scholar
  43. Noguchi T, Ueda K (1985) Cell walls, plasma membranes, and dictyosomes during zygote maturation of Closterium ehrenbergii. Protoplasma 128:64–71CrossRefGoogle Scholar
  44. Nojiri T, Fujii T, Sekimoto H (1995) Purification and characterization of a novel sex pheromone that induces the release of another sex pheromone during sexual reproduction of the heterothallic Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol 36:79–84Google Scholar
  45. Nozaki H, Mori T, Misumi O, Matsunaga S, Kuroiwa T (2006) Males evolved from the dominant isogametic mating type. Curr Biol 16:R1018–R1020CrossRefPubMedGoogle Scholar
  46. Pan J, Snell WJ (2002) Kinesin-II is required for flagellar sensory transduction during fertilization in Chlamydomonas. Mol Biol Cell 13:1417–1426CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pasquale SM, Goodenough UW (1987) Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J Cell Biol 105:2279–2292CrossRefPubMedGoogle Scholar
  48. Pickett-Heaps JD, Fowke LC (1971) Conjugation in the desmid Closterium littorale. J Phycol 7:37–50Google Scholar
  49. Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–226CrossRefPubMedPubMedCentralGoogle Scholar
  50. Saito T, Tsubo Y, Matsuda Y (1985) Synthesis and turnover of cell body agglutinin as a pool of flagellar surface agglutinin in Chlamydomonas reinhardtii gamete. Arch Microbiol 142:207–210CrossRefGoogle Scholar
  51. Saito T, Small L, Goodenough UW (1993) Activation of adenylyl cyclase in Chlamydomonas reinhardtii by adhesion and by heat. J Cell Biol 122:137–147CrossRefPubMedGoogle Scholar
  52. Scofield S, Murray AH (2006) KNOX gene function in plant stem cell niches. Plant Mol Biol 60:929–946CrossRefPubMedGoogle Scholar
  53. Sekimoto H (2002) Production and secretion of a biologically active Closterium sex pheromone by Saccharomyces cerevisiae. Plant Physiol Biochem 40:789–794CrossRefGoogle Scholar
  54. Sekimoto H, Satoh S, Fujii T (1990) Biochemical and physiological properties of a protein inducing protoplast release during conjugation in the Closterium peracerosum-strigosum-littorale complex. Planta 182:348–354CrossRefPubMedGoogle Scholar
  55. Sekimoto H, Satoh S, Fujii T (1992) Biochemical and physiological properties of a gametic protoplast-release-inducing protein in Closterium. Korean. J Phycol 7:121–129Google Scholar
  56. Sekimoto H, Inoki Y, Fujii T (1993a) Detection and evaluation of an inducer of diffusible mating pheromone of heterothallic Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol 37:991–996Google Scholar
  57. Sekimoto H, Satoh S, Fujii T (1993b) Analysis of binding of biotinylated protoplast-release-inducing protein that induces release of gametic protoplasts in the Closterium peracerosum-strigosum-littorale complex. Planta 189:468–474CrossRefPubMedGoogle Scholar
  58. Sekimoto H, Sone Y, Fujii T (1994a) cDNA cloning of a 42-kilodalton subunit of protoplast-release-inducing protein from Closterium. Plant Physiol 104:1095–1096CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sekimoto H, Sone Y, Fujii T (1994b) A cDNA encoding a 19-kilodalton subunit of protoplast-release-inducing protein from Closterium. Plant Physiol 105:447CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sekimoto H, Sone Y, Fujii T (1994c) Regulation of expression of the genes for a sex pheromone by an inducer of the sex pheromone in the Closterium peracerosum-strigosum-littorale complex. Planta 193:137–144CrossRefPubMedGoogle Scholar
  61. Sekimoto H, Fukumoto R, Dohmae N, Takio K, Fujii T, Kamiya Y (1998) Molecular cloning of a novel sex pheromone responsible for the release of a different sex pheromone in Closterium peracerosum-strigosum-littorale complex. Plant Cell Physiol 39:1169–1175CrossRefPubMedGoogle Scholar
  62. Sekimoto H, Tanabe Y, Takizawa M, Ito N, Fukumoto R, Ito M (2003) Expressed sequence tags from the Closterium peracerosum-strigosum-littorale complex, a unicellular charophycean alga, in the sexual reproduction process. DNA Res 10:147–153CrossRefPubMedGoogle Scholar
  63. Sekimoto H, Tanabe Y, Tsuchikane Y, Shirosaki H, Fukuda H, Demura T, Ito M (2006) Gene expression profiling using cDNA microarray analysis of the sexual reproduction stage of the unicellular charophycean alga Closterium peracerosum-strigosum-littorale complex. Plant Physiol 141:271–279CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sekimoto H, Abe J, Tsuchikane Y (2012) New insights into the regulation of sexual reproduction in Closterium. Int Rev. Cell Mol Biol 297:309–338. doi: 10.1016/B978-0-12-394308-8.00014-5 Google Scholar
  65. Sekimoto H, Abe J, Tsuchikane Y (2014) Mechanism of sexual reproduction in fresh water microalgae. In: Ramawat KG, Merillon JM, Shivanna KR (eds.) Reproductive biology of plants. CRC Press, Boca Raton, pp 29–56CrossRefGoogle Scholar
  66. Snell WJ, Eskue WA, Buchanan MJ (1989) Regulated secretion of a serine protease that activates an extracellular matrix-degrading metalloprotease during fertilization in Chlamydomonas. J Cell Biol 109:1689–1694CrossRefPubMedGoogle Scholar
  67. Steele RE, Dana CE (2009) Evolutionary history of the HAP2/GCS1 gene and sexual reproduction in metazoans. PloS one 4:e7680. doi: 10.1371/journal.pone.0007680 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Timme RE, Bachvaroff TR, Delwiche CF (2012) Broad phylogenomic sampling and the sister lineage of land plants. PloS one 7:e29696. doi: 10.1371/journal.pone.0029696 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Tsuchikane Y, Ito M, Fujii T, Sekimoto H (2005) A sex pheromone, protoplast-release-inducing protein (PR-IP) Inducer, induces sexual cell division and production of PR-IP in Closterium. Plant Cell Physiol 46:1472–1476CrossRefPubMedGoogle Scholar
  70. Tsuchikane Y, Kokubun Y, Sekimoto H (2010a) Characterization and molecular cloning of conjugation-regulating sex pheromones in homothallic Closterium. Plant Cell Physiol 51:1515–1523CrossRefPubMedGoogle Scholar
  71. Tsuchikane Y, Sato M, Ootaki T, Kokubun Y, Nozaki H, Ito M, Sekimoto H (2010b) Sexual processes and phylogenetic relationships of a homothallic strain in the Closterium peracerosum-strigosum-littorale complex (Zygnematales, Charophyceae). J Phycol 46:278–284CrossRefGoogle Scholar
  72. Tsuchikane Y, Tsuchiya M, Hindak F, Nozaki H, Sekimoto H (2012) Zygospore formation between homothallic and heterothallic strains of Closterium. Sex Plant Reprod 25:1–9. doi: 10.1007/s00497-011-0174-z CrossRefPubMedGoogle Scholar
  73. von Besser K, Frank AC, Johnson MA, Preuss D (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133:4761–4769. doi: 10.1242/dev.02683 CrossRefGoogle Scholar
  74. Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA, Ruhfel BR, Wafula E, Der JP, Graham SW, Mathews S, Melkonian M, Soltis DE, Soltis PS, Miles NW, Rothfels CJ, Pokorny L, Shaw AJ, DeGironimo L, Stevenson DW, Surek B, Villarreal JC, Roure B, Philippe H, dePamphilis CW, Chen T, Deyholos MK, Baucom RS, Kutchan TM, Augustin MM, Wang J, Zhang Y, Tian Z, Yan Z, Wu X, Sun X, Wong GK, Leebens-Mack J (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci USA 111:E4859–E4868CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wong JL, Johnson MA (2010) Is HAP2-GCS1 an ancestral gamete fusogen? Trends Cell Biol 20:134–141. doi: 10.1016/j.tcb.2009.12.007 CrossRefPubMedGoogle Scholar
  76. Zhang YH, Snell WJ (1994) Flagellar adhesion-dependent regulation of Chlamydomonas adenylyl cyclase in vitro—a possible role for protein kinases in sexual signaling. J Cell Biol 125:617–624CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  1. 1.Department of Chemical and Biological Sciences, Faculty of ScienceJapan Women’s UniversityTokyoJapan

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