Cytoplasmic inheritance in green algae: patterns, mechanisms and relation to sex type

Journal of Plant Research volume 123, pages171–184(2010)Cite this article

Abstract

Cytological and genetic investigations of two major groups of green algae, chlorophyte and streptophyte green algae, show a predominance of uniparental inheritance of the plastid and mitochondrial genomes in most species. However, in some crosses of isogamous species of Ulva compressa, these genomes are transmitted from mt+, mt−, and both parents. In species with uniparental organelle inheritance, various mechanisms can eliminate organelles and their DNA during male gametogenesis or after fertilization. Concerning plastid inheritance, two major mechanisms are widespread in green algae: (1) digestion of plastid DNA during male gametogenesis, during fertilization, or after fertilization; and (2) disintegration or fusion of the plastid in the zygote. The first mechanism also eliminates the mitochondrial DNA in anisogamous and oogamous species. These mechanisms would ensure the predominantly uniparental inheritance of organelle genomes in green algae. To trace the evolutionary history of cytoplasmic inheritance in green algae, the relations between uniparental inheritance and sex type were considered in isogamous, anisogamous, and oogamous species using sex-specific features that might be nearly universal among Chlorophyta.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL (1990) Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 18:141–153

    Article  CAS  PubMed  Google Scholar 

  2. Aoyama H, Hagiwara Y, Misumi O, Kuroiwa T, Nakamura S (2006) Complete elimination of maternal mitochondrial DNA during meiosis resulting in the paternal inheritance of the mitochondrial genome in Chlamydomonas species. Protoplasma 228:231–242

    Article  CAS  PubMed  Google Scholar 

  3. Armbrust EV (1998) Uniparental inheritance of chloroplast genomes. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer, Dordrecht, pp 93–113

    Google Scholar 

  4. Baur E (1909) Das wesen und die rrblichkeitsverhaltnisse der “varietates albo-marginatae hort” von Pelargonium zonale. Zeit Vererbungsl 1:330–351

    Article  Google Scholar 

  5. Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004

    Article  CAS  PubMed  Google Scholar 

  6. Biebel P (1973) Morphology and life cycle of saccoderm desmids in culture. Nova Hedwigia 42:39–57

    Google Scholar 

  7. Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338

    Article  CAS  PubMed  Google Scholar 

  8. Birky CW Jr (2008) Uniparental inheritance of organelle genes. Curr Biol 18:R692–R695

    Article  CAS  PubMed  Google Scholar 

  9. Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW (1987) Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci USA 84:2391–2395

    Article  CAS  PubMed  Google Scholar 

  10. Bråten T (1971) The ultrastructure of fertilization and zygote formation in the green alga Ulva mutabilis Føyn. J Cell Biol 9:621–633

    Google Scholar 

  11. Bråten T (1973) Autoradiographic evidence for the rapid disintegration of one chloroplast in the zygote of the green alga Ulva mutabilis. J Cell Biol 12:385–389

    Google Scholar 

  12. Cavalier-Smith T (1970) Electron microscopic evidence for chloroplast fusion in zygotes of Chlamydomonas reinhardtii. Nature 228:333–335

    Article  CAS  PubMed  Google Scholar 

  13. Coleman AW, Maguire MJ (1982) A microspectrofluorometric analysis of nuclear and chloroplast DNA in Volvox. Dev Biol 94:441–450

    Article  CAS  PubMed  Google Scholar 

  14. Coleman AW, Maguire MJ (1983) Cytological detection of the basis of uniparental inheritance of plastid DNA in Chlamydomonas moewusii. Curr Genet 7:211–218

    Article  Google Scholar 

  15. Correns C (1909) Vererbungsversuche mit blaß-(gelb-)-grünen und buntblättrigen Sippen bei Mirabilis jalapa, Urtica pilulifera und Lunaria annua. Z Abst U Vererbl 1:291–329

    Article  Google Scholar 

  16. Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot 75:1443–1458

    Google Scholar 

  17. Creasey A, Mendis K, Carlton J, Williamson D, Wilson I, Carter R (1994) Maternal inheritance of extrachromosomal DNA in malaria parasites. Mol Biochem Parasitol 65:95–98

    Article  CAS  PubMed  Google Scholar 

  18. Ferris PJ, Goodenough UW (1994) The mating-type locus of Chlamydomonas reinhardtii contains highly rearranged DNA sequences. Cell 76:1135–1145

    Article  CAS  PubMed  Google Scholar 

  19. Ferris PJ, Armbrust EV, Goodenough UW (2002) Genetic structure of the mating-type locus of Chlamydomonas reinhardtii. Genetics 160:181–200

    CAS  PubMed  Google Scholar 

  20. Fjeld A (1971) Unequal contribution of the two gametes to the zygote in the isogameous multicellular alga Ulva mutabilis. Exp Cell Res 69:449–452

    Article  CAS  PubMed  Google Scholar 

  21. Friedmann I (1960) Gametes, fertilization and zygote development in Prasiola stipitata Suhr. I. Light microscopy. Nova Hedwigia 1:333–344

    Google Scholar 

  22. Fritsch FE (1956) The structure and reproduction of the algae, volume I. Cambridge University Press, Cambridge

  23. Gillham NW (1994) Organelle genes and genomes. Oxford University Press, New York

    Google Scholar 

  24. Goodenough UW, Weiss RL (1978) Interrelationships between microtubules, a striated fiber, and the gametic mating structure of Chlamydomonas reinhardti. J Cell Biol 76:430–438

    Article  CAS  PubMed  Google Scholar 

  25. Goodenough UW, Lin H, Lee JH (2007) Sex determination on Chlamydomonas. Sem Cell Dev Biol 18:350–361

    Article  CAS  Google Scholar 

  26. Graham LE (1993) Origin of land plants. Wiley, New York

    Google Scholar 

  27. Graham LE, Wilcox LW (2000) Algae. Prentice Hall, Upper Saddle River

    Google Scholar 

  28. 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 178:283–294

    Article  CAS  PubMed  Google Scholar 

  29. Hirai M, Arai M, Mori T, Miyagishima SY, Kawai S, Kita K, Kuroiwa T, Terenius O, Matsuoka H (2008) Male fertility of malaria parasites is determined by GCS1, a plant-type reproduction factor. Curr Biol 18:607–613

    Article  CAS  PubMed  Google Scholar 

  30. Holmes JA, Dutcher SK (1989) Cellular asymmetry in Chlamydomonas. J Cell Sci 94:273–285

    PubMed  Google Scholar 

  31. Holmes JA, Dutcher SK (1992) Genetic approaches to the study of cytoskeletal structure and function in Chlamydomonas. In: Menzel D (ed) The cytoskeleton of the algae. CRC Press, Boca Raton, pp 347–367

  32. Izumi Y, Ono K (1999) Changes in plastid DNA content during the life cycle of the hornwort Anthoceros punctatus L. Cytologia 64:37–44

    Google Scholar 

  33. Kagami Y, Mogi Y, Arai T, Yamamoto M, Kuwano K, Kawano S (2008) Sexuality and uniparental inheritance of chloroplast DNA in the isogamous green alga Ulva compressa (Ulvophyceae). J Phycol 44:691–702

    Article  CAS  Google Scholar 

  34. Kawano S (2008) Behavior of selfish DNA and sexuality. Plant Morphol 19:45–54 (in Japanese)

    Google Scholar 

  35. Kirk JTO, Tilney-Bassett RAE (1978) The plastids. Elsevier/North-Holland, Amsterdam

    Google Scholar 

  36. Korn RW (1969) Chloroplast inheritance in Cosmarium turpinii Breb. J Phycol 5:332–336

    Article  Google Scholar 

  37. Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62

    Article  CAS  Google Scholar 

  38. Kuroiwa T, Hori T (1986) Preferential digestion of male chloroplast nuclei and mitochondrial nuclei during gametogenesis of Bryopsis maxima Okamura. Protoplasma 133:85–87

    Article  Google Scholar 

  39. Kuroiwa T, Hori T (1990) Patterns of maternal inheritance and phylogeny of plants. In: Takahashi N (ed) Dynamic analysis of regulatory mechanisms in life cycle of higher plants. University of Tokyo Press, Tokyo, pp 149–188 (in Japanese)

    Google Scholar 

  40. Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298:481–483

    Article  CAS  PubMed  Google Scholar 

  41. Kuroiwa T, Enomoto S, Shihira-Ishikawa I (1985) Preferential destruction of chloroplast nucleoids in zygotes in green algae Dictyosphaeria cavernosa and Acetabularia calyculus. Experientia 41:1178–1179

  42. Kuroiwa H, Sugai M, Kuroiwa T (1988) Behavior of chloroplasts and chloroplast nuclei during spermatogenesis in the fern, Pteris vittata L. Protoplasma 146:89–100

    Article  Google Scholar 

  43. Kuroiwa T, Kawano S, Watanabe M, Hori T (1991) Preferential digestion of chloroplast DNA in male gametangia during the late stage of gametogenesis in the anisogamous alga Bryopsis maxima. Protoplasma 163:102–113

    Article  CAS  Google Scholar 

  44. Kuroiwa H, Nozaki H, Kuroiwa T (1993a) Preferential digestion of chloroplast nuclei in sperms before and during fertilization in Volvox carteri. Cytologia 58:281–291

    Google Scholar 

  45. Kuroiwa T, Uchida H, Hori T, Maegawa M (1993b) Preferential disappearance of chlorophyll preceding digestion of male-derived chloroplast DNA in young zygotes of Monostroma latissimum by a DAPI-epifluorescence microscopy and electron microscopy. Cytologia 58:331–336

    CAS  Google Scholar 

  46. Kurssanow L (1912) Über Befruchtung, Reifung und Keimung bei Zygnema. Flora 104:65–84

    Google Scholar 

  47. Lee RW, Langille B, Lemieux C, Boer PH (1990) Inheritance of mitochondrial and chloroplast genome markers in backcrosses of Chlamydomonas eugametos x Chlamydomonas moewusii hybrids. Curr Genet 17:73–76

    Article  Google Scholar 

  48. Lee SH, Motomura T, Ichimura T (2002) Light and electron microscopic observations of preferential destruction of chloroplast and mitochondrial DNA at early male gametogenesis of the anisogamous green alga Derbesia tenuissima (Chlorophyta). J Phycol 38:524–542

    Article  Google Scholar 

  49. Lewis IF (1925) A new conjugate from Woods Hole. Am J Bot 12:351–357

    Article  Google Scholar 

  50. Lewis LA, McCourt RM (2004) Green algae and the origin of land plants. Am J Bot 91:1535–1556

    Article  Google Scholar 

  51. Lippert BE (1967) Sexual reproduction in Closterium moniliferum and Closterium ehrenbergii. J Phycol 3:182–198

    Article  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. Melkonian M (1989) Flagellar apparatus ultrastructure in Mesostigma viride (Prasinophyceae). Plant Syst Evol 164:93–122

    Article  Google Scholar 

  54. Miyamura S (2003) Eyespot behavior during the fertilization of gametes in ulvalean alga Enteromorpha compressa (Linnaeus) Nees revealed by field emission scanning electron microscopy. Cytologia 68:173–176

    Article  Google Scholar 

  55. Miyamura S, Hori T (1997) Pyrenoid as a chloroplast nucleoid in Caulerpa. In: Bonotto S (ed) Proceedings of the Qingdao Symposium. Pollettino Del Museo Regionale Di Scienze Naturali, Torino, pp 225–238

  56. Miyamura S, Nagumo T (2007) Inheritance pattern of chloroplast DNA is correlated with gamete types based on sex-specific arrangement of the cell fusion site in Caulerpa (Ulvophyceae, Chlorophyta). Phycol Res 55:47–57

    Article  CAS  Google Scholar 

  57. Miyamura S, Kuroiwa T, Nagata T (1987) Disappearance of plastid and mitochondrial nucleoids during the formation of generative cells of higher plants revealed by fluorescence microscopy. Protoplasma 141:149–159

    Article  Google Scholar 

  58. Miyamura S, Sakaushi S, Hori T, Mitsuhashi F, Nagumo T (2005) Sex-specific cell surface structure of anisogametes: morphological changes during fertilization of Bryopsis maxima (Ulvophyceae, Chlorophyta) revealed by ultra-high resolution field emission scanning electron microscopy. J Phycol 41:114–125

    Article  Google Scholar 

  59. Moestrup Ø, Hori T (1989) Ultrastructure of the flagellar apparatus in Pyramimonas octopus (Prasinophyceae). II. Flagellar roots, connecting fibres, and numbering of individual flagella in green algae. Protoplasma 148:41–56

    Article  Google Scholar 

  60. Mogensen HL (1996) The how and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404

    Article  Google Scholar 

  61. Mogi Y, Kagami Y, Kuwano K, Miyamura S, Nagumo T, Kawano S (2008) Asymmetry of eyespot and mating structure position in Ulva compressa (Ulvales, Chlorophyta) revealed by a new field emission scanning electron microscopy method. J Phycol 44:1290–1299

    Article  Google Scholar 

  62. Mogi Y, Hatakeyama Y, Kuwano K, Miyamura S, Kawano S (2009) Patterns of organelle inheritance revealed by 12 interline crosses in Ulva compressa. Phycologia 48(Suppl):86

    Google Scholar 

  63. Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) Generative cell specific 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64–71

    Article  CAS  PubMed  Google Scholar 

  64. Moriyama Y, Kawano S (2003) Rapid, selective digestion of mitochondrial DNA in accordance with the matA hierarchy of multiallelic mating types in the mitochondrial inheritance of Physarum polycephalum. Genetics 164:963–975

    CAS  PubMed  Google Scholar 

  65. Myles DG (1978) The fine structure of fertilization in the fern Marsilea vestita. J Cell Sci 30:265–281

    CAS  PubMed  Google Scholar 

  66. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organelle DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65

    Article  CAS  PubMed  Google Scholar 

  67. Nakamura S, Ogawa K, Kuroiwa T (1987) Survey of Ca2+-dependent nuclease in green plants. Plant Cell Physiol 28:545–548

    CAS  Google Scholar 

  68. Nakayama T, Inouye I (2000) Ultrastructure of the biflagellate gametes of Collinsiella cava (Ulvophyceae, Chlorophyta). Phycol Res 48:63–73

    Article  Google Scholar 

  69. Nishimura Y, Misumi O, Matsunaga S, Higashiyama T, Yokota A, Kuroiwa T (1999) The active digestion of uniparental chloroplast DNA in a single zygote of Chlamydomonas reinhardtii is revealed by using the optical tweezers. Proc Natl Acad Sci USA 96:12577–12582

    Article  CAS  PubMed  Google Scholar 

  70. Nishimura Y, Misumi O, Kato K, Inada N, Higashiyama T, Momoyama Y, Kuroiwa T (2002) An mt+ gamete-specific nuclease that targets mt− chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev 16:1116–1128

    Article  CAS  PubMed  Google Scholar 

  71. Nishimura Y, Yoshida T, Naruse K, Yamada T, Sumi K, Mitani H, Higashiyama T, Kuroiwa T (2006) Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Natl Acad Sci USA 103:1382–1387

    Article  CAS  PubMed  Google Scholar 

  72. Nozaki H, Mori T, Misumi O, Matsunaga S, Kuroiwa T (2006) Males evolved from the dominant isogametic mating type. Curr Biol 16:R1018–R1020

    Article  CAS  PubMed  Google Scholar 

  73. Ogawa S (1982) Disintegration of chloroplasts during zygote formation in Spirogyra verruculosa. Bot Mag Tokyo 95:249–260

    Article  Google Scholar 

  74. Ogawa S (1988) Disappearance of chloroplast nucleoids during male gamete formation in Bryopsis plumosa (Hudson) C. Ag. (Chlorophyceae). Bot Gaz 149:25–29

    Article  Google Scholar 

  75. Ogawa S, Hirota K (2000) Disintegration of chloroplasts during zygote maturation in Closterium ehrenbergii (Zygnematales, Chlorophyta). Int J Plant Sci 161:609–614

    Article  CAS  Google Scholar 

  76. Peters AF, Scornet D, Müller DG, Kloareg B, Cock JM (2004) Inheritance of organelles in artificial hybrids of the isogamous multicellular chromist alga Ectocarpus siliculosus (Phaeophyceae). Eur J Phycol 39:235–242

    Article  Google Scholar 

  77. Sager R (1954) Mendelian and non-Mendelian inheritance of streptomycin resistance in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 40:356–363

    Article  CAS  PubMed  Google Scholar 

  78. Sears BB (1980) Elimination of plastids during spermatogenesis and fertilization in the plant kingdom. Plasmid 4:233–255

    Article  CAS  PubMed  Google Scholar 

  79. Smith GM (1950) The fresh-water algae of the United States. McGraw-Hill, New York

    Google Scholar 

  80. Stein JR (1958) A morphological and genetic study of Gonium pectorale. Am J Bot 45:388–397

    Article  Google Scholar 

  81. Suda S, Watanabe MM, Inouye I (1989) Evidence for sexual reproduction in the primitive green alga Nephroselmis olivacea (Prasinophyceae). J Phycol 25:596–600

    Article  Google Scholar 

  82. Suda S, Watanabe MM, Inouye I (2004) Electron microscopy of sexual reproduction in Nephroselmis olivacea (Prasinophyceae, Chlorophyta). Phycol Res 52:273–283

    Article  Google Scholar 

  83. Sugiyama M, Ito J, Aoyama S, Fukuda H (2000) Endonucleases. Plant Mol Biol 44:387–397

    Article  CAS  PubMed  Google Scholar 

  84. Sun GH, Uyeda TGP, Kuroiwa T (1988) Destruction of organelle nuclei during spermatogenesis in Chara corallina examined by staining with DAPI and anti-DNA antibody. Protoplasma 144:185–188

    Article  Google Scholar 

  85. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (1999) Ubiquitin tag for sperm mitochondria. Nature 402:371–372

    Article  CAS  PubMed  Google Scholar 

  86. Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G (2000) Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63:582–590

    Article  CAS  PubMed  Google Scholar 

  87. Whatley JM (1982) Ultrastructure of plastid inheritance: green algae to angiosperms. Biol Rev 57:527–569

    Article  Google Scholar 

  88. White DJ, Wolff JN, Pierson M, Gemmell NJ (2008) Revealing the hidden complexities of mtDNA inheritance. Mol Ecol 17:4925–4942

    Article  CAS  PubMed  Google Scholar 

  89. Worden AZ, Lee JH, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV, Foulon E, Grimwood J, Gundlach H, Henrissat B, Napoli C, McDonald SM, Parker MS, Rombauts S, Salamov A, Von Dassow P, Badger JH, Coutinho PM, Demir E, Dubchak I, Gentemann C, Eikrem W, Gready JE, John U, Lanier W, Lindquist EA, Lucas S, Mayer KFX, Moreau H, Not F, Otillar R, Panaud O, Pangilinan J, Paulsen I, Piegu B, Poliakov A, Robbens S, Schmutz J, Toulza E, Wyss T, Zelensky A, Zhou K, Armbrust EV, Bhattacharya D, Goodenough UW, Van de Peer Y, Grigoriev IV (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272

    Article  CAS  PubMed  Google Scholar 

  90. Xu J (2005) The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 48:951–995

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The author is greatly indebted to Prof. Tsuneyoshi Kuroiwa for the opportunity to write this article. I also thank Prof. Shigeyuki Kawano and Yuko Mogi for information about cytoplasmic inheritance in Ulva compressa. This work was partly supported by a KAKENHI Grant-in-Aid for Scientific Research (B) (No. 20370025).

Author information

Affiliations

  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Shinichi Miyamura

Authors
  1. Shinichi Miyamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shinichi Miyamura.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Miyamura, S. Cytoplasmic inheritance in green algae: patterns, mechanisms and relation to sex type. J Plant Res 123, 171–184 (2010). https://doi.org/10.1007/s10265-010-0309-6

Download citation

Keywords

  • Anisogamy
  • Cytoplasmic inheritance
  • Green algae
  • Isogamy
  • Oogamy
  • Sex