Review of cytological studies on cellular and molecular mechanisms of uniparental (maternal or paternal) inheritance of plastid and mitochondrial genomes induced by active digestion of organelle nuclei (nucleoids)

Journal of Plant Research

Volumn 123, Issue 2, 2010, Pages 207-230

  Kuroiwa, Tsuneyoshi ^a  

^a RIKKYO UNIVERSITY   (Japan)

Author keywords

Active digestion of DNA; Biparental inheritance; Maternal inheritance; Mitochondria; Organelle nuclei (nucleoid); Plastid (chloroplast); Uniparental inheritance

Indexed keywords

CIRCULAR DNA;

CYTOLOGY; EUKARYOTE; EVOLUTION; EXTRACHROMOSOMAL INHERITANCE; GENETICS; METABOLISM; MITOCHONDRIAL GENOME; PLASTID GENOME; REVIEW;

CYTOLOGICAL TECHNIQUES; DNA, CIRCULAR; EUKARYOTA; EVOLUTION; EXTRACHROMOSOMAL INHERITANCE; GENOME, MITOCHONDRIAL; GENOME, PLASTID;

EUKARYOTA;

EID: 77951499161     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10265-009-0306-9     Document Type: Review

References (116)

1. Ankel-Simons F, Cummins JM (1996) Misconceptions about mitochondria and mammalian fertilization implications for theories. Proc Natl Acad Sci USA 93: 13859-13863.
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. Protoplasma 228: 231-242.
3. Armbrust EV, Ferris PJ, Goodenough UW (1993) A mating type-linked gene cluster expressed in Chlamydomonas zygotes participates in the uniparental inheritance of the chloroplast genome. Cell 74: 801-811.
4. Avise JC, Giblin-Davidosom C, Laerm J, Patton JC, Lansman RA (1979) Mitochondrial DNA clones and matriarchal phylogeny within and among geographic populations of the pocket gopher, Geomys pinetis. Proc Natl Acad Sci USA 76: 6694-6698.
5. - origin in gametes and zygotes of Chlamydomonas. Curr Genet 20: 239-243.
6. Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92: 11331-11338.
7. Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts. Annu Rev Genet 35: 125-148.
8. Bolen PL, Grant DM, Swinton D, Boynton JE, Gillham NW (1982) Extensive methylation of chloroplasts DNA by a nuclear gene mutation does not affect chloroplast gene transmission in Chlamydomonas. Cell 28: 335-343.
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.
10. Burton WG, Roberts RJ, Myers PA, Sager R (1977) A site-specific single-strand endonuclease from the eukaryote Chlamydomonas. Proc Natl Acad Sci USA 7: 2687-2691.
11. Burton WG, Grabowy CT, Sager R (1979) Role of methylation in the modification and restriction of chloroplast DNA in Chlamydomonas. Proc Natl Acad Sci USA 76: 1390-1394.
12. Corriveau JS, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperms species. Am J Bot 75: 1443-1458.
13. Cosmides LM, Tooby J (1981) Cytoplasmic inheritance and intragenomic conflict. J Theor Biol 89: 83-129.
14. Dawid IB, Blackler AW (1972) Maternal and cytoplasmic inheritance of mitochondrial DNA in Xenopus. Dev Biol 29: 152-161.
15. Dujon B, Slonimski PP, Weil L (1974) Mitochondrial genetics. IX. A model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78: 415-437.
16. Feng TY, Chiang KS (1984) The persistence of maternal inheritance in Chlamydomonas despite hypomethylation of chloroplast DNA induced by inhibitors. Proc Natl Acad Sci USA 81: 3438-3442.
17. Gillham NW (1994) Organelle gene sand genomes. Oxford University Press, New York.
18. Gillham NW, Boynton JE, Harris EH (1991) Transmission of plastid genes. In: Nogorad L, Vasil IK (eds) The molecular biology of plastids. Academic, San Diego, pp 55-92.
19. Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352: 255-257.
20. Hagemann R (1992) Plastid genetics in higher plants. In: Herrmann R (ed) Cell organelles. Springer, Vienna, pp 66-96.
21. Hagemann R, Schroder MB (1989) The cytological basis of the plastid inheritance in angiosperm. Protoplasma 152: 57-64.
22. Hayashi JI, Yonekawa H, Gotoh O, Watanabe J, Tagashira Y (1978) Strictly maternal inheritance of rat mitochondrial DNA. Biochem Biophys Res Commun 84: 1032-1038.
23. Hecht NB (1984) Gene expression during spermatogenesis. Ann N Y Acad Sci 513: 90-101.
24. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T (2001) Pollen tube attraction by the synergid cell. Science 293: 1480-1483.
25. Hoeh WR, Blakley KH, Brown WM (1991) Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial DNA. Science 251: 1488-1490.
26. Hurst LD (1992) Intragenomic conflict as an evolutionary force. Proc R Soc Lond B Biol Sci 248: 135-140.
27. Hurst LD, Hamilton WD (1992) Cytoplasmic fusion and the nature of sexes. Proc R Soc Lond B Biol Sci 247: 189-194.
28. Hutchison CA, Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251: 536-538.
29. Jansen RP, de Boer K (1998) The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol 145: 81-88.
30. Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF, Yonekawa H (1995) Elimination of paternal mitochondrial DNA intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92: 4542-4546.
31. Kawano S, Kuroiwa T (1989) Transmission pattern of mitochondrial DNA during plasmodium formation in Physarum polycephalum. J Gen Microbiol 135: 1559-1566.
32. Kawano S, Anderson RW, Namba T, Kuroiwa T (1987) Polymorphism and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J Gen Microbiol 133: 3175-3182.
33. Kawano S, Takano H, Mori K, Kuroiwa T (1991) A mitochondrial plasmid that promotes mitochondrial fusion in Physarum polycephalum. Protoplasma 160: 167-169.
34. Kawano S, Takano H, Imai J, Mori K, Kuroiwa T (1993) A genetic system controlling mitochondrial fusion in the slime mould, Physarum polycephalum. Genetics 133: 213-224.
35. Kawano S, Takano H, Kuroiwa T (1995) Sexuality of mitochondria fusion, recombination and plasmid. Int Rev Cytol 161: 49-110.
36. Kirk JTO, Tilney-Bassett RAE (1978) The plastids: their chemistry, structure, growth, and inheritance, 2nd edn. Elsevier/North-Holland Biomedical, Oxford.
37. Kroon AM, de Vos WM, Bakker H (1978) The heterogeneity of rat-liver mitochondrial DNA. Biochim Biophys Acta 519: 269-273.
38. Kuriyama H, Takano H, Suzuki L, Uchida H, Kawano S, Kuroiwa H, Kuroiwa T (1999) Characterization of Chlamydomonas reinhardtii zygote-specific cDNAs that encode novel proteins containing ankyrin repeats and WW domains. Plant Physiol 119: 873-884.
39. 3H-uridine autoradiography of a central body in mitochondria. Exp Cell Res 78: 351-359.
40. Kuroiwa T (1974) Studies on mitochondrial structure and function in Physarum polycephalum III. Electron microscopy of a large amount of DNA released from a central body in mitochondria by trypsin digestion. J Cell Biol 63: 299-306.
41. Kuroiwa T (1982) Mitochondrial nuclei. Int Rev Cytol 75: 1-59.
42. Kuroiwa T (1985a) Chlamydomonas reinhardtii life cycle and maternal inheritance. Microbiol Sci 2: 272-273.
43. Kuroiwa T (1985b) Mechanism of maternal inheritance of chloroplast DNA-an active digestion hypothesis. Microbiol Sci 2: 267-270.
44. Kuroiwa T (1991) The replication, differentiation and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128: 1-62.
45. Kuroiwa T (1998) The primitive red algae Cyanidium caldarium and Cyanidioschyzone merolae as model system for investigating the dividing apparatus of mitochondria and plastids. BioEssays 20: 344-354.
46. Kuroiwa T (2010) 100 years since the discovery of non-Mendelian plastid phenotypes. J Plant Res. doi: 10. 1007/s10265-009-0283-z.
47. Kuroiwa T, Hori T (1986) Preferential digestion of male chloroplast and mitochondrial nuclei during gametogenesis of Bryopsis maxima. Protoplasma 133: 85-87.
48. Kuroiwa T, Nakamura S (1986) No effect of preferential digestion of chloroplast genome of male origin on chloroplast genome of female origin in young zygotes of Chlamydomonas reinhardtii as revealed by a video-intensified microscope photon counting system. Histochem Cytochem Acta 19: 95-102.
49. Kuroiwa T, Uchida H (1996) Organelle division and cytoplasmic inheritance origin and basis of the transmission of organelle genomes. Bioscience 46: 827-835.
50. Kuroiwa T, Suzuki T, Ogawa K, Kawano S (1981) The chloroplast nucleus: distribution, number, size and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant Cell Physiol 22: 381-396.
51. Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298: 481-483.
52. Kuroiwa T, Nakamura S, Sato C, Tsubo Y (1985a) Epifluorescent microscopic studies on the mechanism of preferential destruction of chloroplast nucleoids of male origin in young zygotes of Chlamydomonas reinhardtii. Protoplasma 125: 43-52.
53. Kuroiwa T, Enomoto S, Shihira-Ishikawa I (1985b) Preferential destruction of chloroplast nucleoids in zygotes in green algae Dictyosphaeria cavernosa and Acetabularia calyculus. Experientia 41: 1171-1179.
54. 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.
55. Kuroiwa T, Kawano S, Watanabe M, Hori T (1991a) Preferential digestion of chloroplast DNA in male gametangia during late stage of the gametogenesis in the anisogamous alga Bryopsis maxima. Protoplasma 163: 102-113.
56. Kuroiwa T, Fujie M, Mita T, Kuroiwa H (1991b) Application of embedding of samples in Technovit 7100 resin to observations of small amounts of DNA in the cellular organelles associated with cytoplasmic inheritance. Fluoresc Appl Tech 3: 23-25.
57. Kuroiwa H, Nozaki H, Kuroiwa T (1993) Preferential digestion of chloroplast nuclei in sperms just before fertilization in Volvox carteri. Cytologia 58: 281-291.
58. Kuroiwa T, Kuroiwa H, Mita T, Ohta N (1994) Cyanidium caldarium as a model cell for studying division of chloroplasts. In: Seckbach J (ed) Evolutionary pathways and enigmatic alga Cyanidium caldarium (Rhodophyta) and related cells. Kluwer, Dordrecht, pp 220-232.
59. Kuroiwa H, Ohta T, Fujie M, Kuroiwa T (1996) The studies on the development and three-dimensional reconstruction of giant mitochondria and nuclei in egg cells of Pelargonium zonale. Protoplasma 192: 235-244.
60. Kuroiwa T, Misumi O, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Yoshida Y, Hirooka S, Kuroiwa H (2008) Structure, function, and origin of vesicle, mitochondrial and plastid division machineries with emphasis on dynamin rings and electron-dense rings. Int Rev Cell Mol Biol 271: 97-141.
61. Mannella CA, Goewert RR, Lambowitz AM (1979) Characterization of variant Neurosporea crassa mitochondrial DNAs which contain tandem reiterations. Cell 18: 1197-1207.
62. Matagne RF, Michel-Wolwertz MR, Munaut C, Duyckaerts C, Sluse F (1989) Induction and characterization of mitochondrial DNA mutants in Chlamydomonas. J Cell Biol 108: 1221-1226.
63. Meland S, Johansen S, Johansen T, Haugli K, Haugli F (1991) Rapid disappearance of one parental mitochondrial genotype after isogamous mating in the myxomycete Physarum polycephalum. Curr Genet 19: 55-59.
64. Mirfakhrai M, Tanaka Y, Yanagisawa K (1990) Evidence for mitochondrial DNA polymorphism and uniparental inheritance in the cellular slime mold Polysphondylium pallidum: effect of intraspecies mating on mitochondrial DNA transmission. Genetics 124: 607-613.
65. Misumi O, Suzuki L, Nishimura Y, Sakai A, Kawano S, Kuroiwa H, Kuroiwa T (1999) Isolation and phenotypic characterization of Chlamydomonas reinhardtii mutants defective in chloroplast DNA segregation. Protoplasma 209: 273-282.
66. Miyakawa I, Aoi H, Sando N, Kuroiwa T (1984) Fluorescence microscopic studies of mitochondrial nucleoids during meiosis and sporulation in the yeast, Saccharomyces cerevisiae. J Cell Sci 66: 21-38.
67. 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.
68. Mogensen HL (1988) Exclusion of male mitochondria and plastids during syngamy in barley as a basis for maternal inheritance. Proc Natl Acad Sci USA 85: 2594-2597.
69. Moriyama Y, Kawano S (2003) Rapid, active 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.
70. Moriyama Y, Kawano S (2010) Maternal inheritance of mitochondria: multipolarity, multiallelism and hierarchical transmission of mitochondrial DNA in the true slime mold Physarum polycephalum. J Plant Res. doi: 10. 1007/s10265-009-0298-5.
71. Nagata N (2010) Mechanisms for independent cytoplasmic inheritance of mitochondria and plastids in angiosperms. J Plant Res. doi: 10. 1007/s10265-009-0293-x.
72. Nagata N, Sodmergen, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1997) Preferential degradation of plastid DNA with preservation of mitochondrial DNA in the sperm cells of Pelargonium zonale during pollen development. Protoplasma 197: 217-229.
73. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) A control of selective increase and decrease of organellar DNA in generative cells just after pollen mitosis one concerning cytoplasmic inheritance. Planta 209: 53-65.
74. Nakamura S (2010) Paternal inheritance of mitochondria in Chlamydomonas. J Plant Res. doi: 10. 1007/s10265-009-0295-8.
75. Nakamura S, Kuroiwa T (1989) Selective elimination of chloroplast DNA by 5-fluorodeoxyridine causing no effect on preferential digestion of male chloroplast nucleoids in Chlamydomonas. Eur J Cell Biol 48: 165-173.
76. Nakamura S, Sakihara M, Chibana H, Ikehara T, Kuroiwa T (1994) Mutations disturbing the condensation of plastid nucleoids in Chlamydomonas reinhardtii. Protoplasma 178: 111-118.
77. Nakamura S, Misumi O, Aoyama H, Voesik R, Kuroiwa T (2003) Monokaryotic chloroplast (moc) mutation has no effect on non-Mendelian transmission of chloroplast and mitochondrial DNA in Chlamydomonas. Protoplasma 22: 107-112.
78. Neale DB, Marshall KA, Sederoff RR (1989) Inheritance and evolution of conifer organelle genomes. In: Hanover JW, Keathley EE (eds) Genetic manipulation of woody plants. Plenum, New York, pp 252-264.
79. Nishimura Y (2010) Uniparental inheritance of cpDNA and the genetic control of sexual differentiation in Chlamydomonas reinhardtii. J Plant Res. doi: 10. 1007/s10265-009-0292-y.
80. Nishimura Y, Misumi O, Matsunaga S, Miyagishima S, 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 tweezer. Proc Natl Acad Sci USA 96: 12577-12582.
81. - chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev 16: 1116-1128.
82. Nishimura Y, Yoshinari 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.
83. Ogawa K, Kuroiwa T (1985a) Destruction of chloroplast nuclei of the male gamete by calcium and nuclease C in a cell model of Chlamydomonas reinhardtii. Plant Cell Physiol 26: 493-503.
84. Ogawa K, Kuroiwa T (1985b) Nuclease polymorphism of calcium-dependent nuclease in Chlamydomonas reinhardtii. Plant Cell Physiol 26: 481-491.
85. Ogawa K, Kuroiwa T (1985c) Purification of major isozymes of nuclease and production of active fragments by trypsin. Plant Cell Physiol 26: 1473-1484.
86. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Ito K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Dresselhaus T, Kanaoka MM, Sasaki N, Higashiyama T (2009) Defensin-like peptides LUREs are pollen tube attractants secreted from the synergid cell. Nature 458: 251-376.
87. Reilly JG, Thomas CA Jr (1980) Length polymorphisms, restriction site variation, and maternal inheritance of mitochondrial DNA of Drosophila melanogaster. Plasmid 3: 109-115.
88. Russell SD (1984) Ultrastructure of the sperm of Plumbago zeylanica: 2. Quantitative cytology and three-dimensional reconstruction. Planta 162: 385-391.
89. Russell SD (1989) Preferential fertilization in the synergid-lacking angiosperm Plumbago zeylanica. Phytomorphology 39: 1-20.
90. Sager R (1981) The application of DNA methylation studies to the analysis of chloroplast evolution. Ann N Y Acad Sci 361: 209-218.
91. Sager R, Lane D (1972) Molecular basis of maternal inheritance. Proc Natl Acad Sci USA 69: 2410-2413.
92. Saiki A, Matsumoto M, Katowgi J, Watanabe A, Onitake K (1997) Establishment of in vitro spermatogenesis from spermatocytes in the medaka, Oryzias latipes. Dev Growth Differ 39: 337-344.
93. Saito C, Nagata N, Sakai A, Mori K, Kuroiwa H, Kuroiwa T (2000) Unequal distribution of DNA-containing organelles in generative cells of Erythrina crista-galli (Fabaceae). Sex Plant Rep 12: 296-301.
94. Saito C, Nagata N, Sakai A, Mori K, Kuroiwa H, Kuroiwa T (2001) Behavior of plastid nucleoids during male gametogenesis in Plumbago auriculata. Protoplasma 216: 143-154.
95. Sakai A, Takano H, Kuroiwa T (2004) Structure, composition, function, and evolution of the organelle-nuclei in higher plants. Int Rev Cytol 23: 107-860.
96. Sano H, Grabowy CT, Sager R (1981) Differential activity of DNA methyltransferase in the life cycle of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 78: 3118-3122.
97. Sasaki N, Kuroiwa H, Nishitani C, Takano H, Higashiyama T, Kobayashi T, Shirai Y, Sakai A, Kawano S, Murakami-Murofushi K, Kuroiwa T (2003) Glom is a novel mitochondrial DNA packing protein in Physarum polycephalum and causes intense chromatin condensation without suppressing DNA function. Mol Biol Cell 14: 4758-4769.
98. Schwartz DC, Samad A (1997) Optical mapping approaches to molecular genomics. Curr Opin Biotechnol 8: 70-74.
99. Sears BB (1980) Elimination of plastids during spermatogenesis in the plant kingdom. Plasmid 4: 233-255.
100. Smith SE (1988) Biparental inheritance of organelles and its implications in crop improvement. Plant Breed Rev 6: 361-363.
101. Sodmergen, Suzuki T, Kawano S, Nakamura S, Tano S, Kuroiwa T (1992) Behavior of organelle nuclei (nucleoids) in generative and generative cells during maturation of pollen in Lilium longiflorum and Pelargonium zonale. Protoplasma 168: 73-81.
102. Sodmergen, Chen GH, Hu ZM, Guo FL, Guan XL (1995) Male gametophyte development in Plumbago zeylanica: cytoplasm localization and cell determination in the early generative cell. Protoplasma 186: 79-86.
103. Sun GH, Uyeda TQ, 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.
104. Suzuki L, Wocessner JP, Uchida H, Kuroiwa H, Yuasa Y, Walffenschmidt S, Goodenough UW, Kuroiwa T (2000) A zygote-specific protein with hydroxyproline-rich glycoprotein domains and lectin-like domains involved in the assembly of the cell wall of Chlamydomonas reinhardtii. J Phycol 36: 571-583.
105. Szmidt AE, Alden T, Hallgren JE (1987) Paternal inheritance of chloroplast DNA in Larix. Plant Mol Biol 9: 59-64.
106. Takano H, Onoue K, Kawano S (2010) Mitochondrial fusion and inheritance of the mitochondrial genome. J Plant Res. doi: 10. 1007/s10265-009-0268-y.
107. Takano H, Kawano S, Kuroiwa T (1992) Constitutive homologous recombination between the mitochondrial DNA and a linear mitochondrial plasmid in Physarum polycephalum. Curr Genet 22: 221-227.
108. Tanaka K, Oikawa K, Ohta N, Kuroiwa H, Kuroiwa T, Takahashi H (1996) Chloroplast RNA polymerase sigma subunit encoded by nuclear genome in a red alga. Science 272: 1841-1844.
109. Tsubo Y, Matsuda Y (1984) Transmission of chloroplast genes in crosses between Chlamydomonas reinhardtii diploids. Correlation with chloroplast nucleoid behavior in young zygotes. Curr Genet 8: 223-229.
110. Uchida H, Kawano S, Sato N, Kuroiwa T (1993) Isolation and characterization of novel genes which are expressed during the very early stage of zygote formation in Chlamydomonas reinhardtii. Curr Genet 24: 296-300.
111. Uchida H, Suzuki L, Anai T, Doi K, Takano H, Yamashita H, Oka T, Kawano S, Tomizawa K, Kawazu T, Kuroiwa T (1999) A pair of invertedly repeated genes in Chlamydomonas reinhardtii. Curr Genet 36: 232-240.
112. Umen JG, Goodenough UW (2001) Chloroplast DNA methylation and inheritance in Chlamydomonas. Genes Dev 15: 2585-2597.
113. Wegener D, Beck CF (1991) Identification of novel genes specifically expressed in Chlamydomonas reinhardtii zygotes. Plant Mol Biol 16: 937-946.
114. Whatley NF (1982) Ultrastructure of plastid inheritance: green algae to angiosperms. Biol Rev 57: 527-569.
115. Zhang Q, Sodmergen (2010) Why does biparental plastid inheritance revive in angiosperms? J Plant Res. doi: 10. 1007/s10265-009-0291-z.
116. Zouros E, Freeman KR, Oberhauser-Ball A, Pogson GH (1992) Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilis. Nature 359: 412-414.