Greening in the dark: Light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms

Journal of Photochemistry and Photobiology B: Biology

Volumn 43, Issue 2, 1998, Pages 87-100

  Armstrong, Gregory A ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Bacteriochlorophyll chlorophyll biosynthesis; Chloroplast development; Greening; Light independent protochlorophyllide oxidoreductase (DPOR); Nitrogenase; Plastid genome

Indexed keywords

BACTERIOCHLOROPHYLL; OXIDOREDUCTASE; PROTOCHLOROPHYLLIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; REVIEW;

EID: 0032524680     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1011-1344(98)00063-3     Document Type: Review

References (94)

1. [1] B.R. Green, D.G. Durnford, The chlorophyll-carotenoid proteins of oxygenic photosynthesis, Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 (1996) 685-714.
2. [2] J.P. Thornber, D.T. Morishige, S. Anandan, G.F. Peter, Chlorophyll-carotenoid proteins of higher plant thylakoids, in: H. Scheer (Ed.), Chlorophylls, CRC Press, Boca Raton, FL, 1991, pp. 549-585.
3. [3] D. von Wettstein, S. Gough, C.G. Kannangara, Chlorophyll Biosynthesis, Plant Cell 7 (1995) 1039-1057.
4. [4] H. Scheer, Chemistry of chlorophylls, in: H. Scheer (Ed.), Chlorophylls, CRC Press, Boca Raton, FL, 1991, pp. 3-30.
5. [5] R.J. Porra, Recent progress in porphyrin and chlorophyll biosynthesis, Photochem. Photobiol. 65 (1997) 492-516.
6. [6] C.A. Rebeiz, R. Parham, D.A. Fasoula, I.M. Ioannides, Chlorophyll a biosynthetic heterogeneity, in: D.J. Chadwick, K. Ackrill, The Biosynthesis of the Tetrapyrrole Pigments Wiley, Chichester, UK, 1994, pp. 177-193.
7. [7] U. Oster, C.E. Bauer, W. Rüdiger, Characterization of chlorophyll a and bacteriochlorophyll a synthases by heterologous expression in Escherichia coli, J. Biol. Chem. 272 (1997) 9671-9676.
8. [8] L. Bogorad, Chlorophyll biosynthesis, in: T.W. Goodwin (Ed.), Chemistry and Biochemistry of Plant Pigment, Academic Press, New York, NY, 1976, pp. 64-148.
9. [9] R. Schulz, H. Senger, Protochlorophyllide reductase: a key enzyme in the greening process, in: C. Sundqvist, M. Ryberg (Eds.), Pigment-Protein Complexes in Plastids: Synthesis and Assembly, Academic Press, New York, NY, 1993, pp. 179-218.
10. [10] Y. Fujita, Protochlorophyllide reduction: a key step in the greening of plants, Plant Cell Physiol, 37 (1996) 411-421.
11. [11] H. Y. Adamson, R.G. Hiller, J. Walmsley, Protochlorophyllide reduction and greening in angiosperms: an evolutionary perspective, J. Photochem. Photobiol. B: Biol. 41 (1997) 201-221.
12. [12] J.T.O. Kirk, R.A.E. Tilney-Bassett, The Plastids, Elsevier/North-Holland Biomedical Press, Amsterdam, Netherlands, 1978.
13. [13] A. Burgerstein, Über das Verhalten der Gymnospermen-Keimlinge im Lichte und im Dunkeln, Ber. Dtsch. Bot. Ges. 18 (1900) 168-184.
14. [14] D.P. Whittier, Dark-grown Psilotum, Am. Fern J. 78 (1988) 109-116.
15. [15] C.E. Bauer, D.W. Bollivar, J.Y. Suzuki, Genetic analyses of photopigment biosynthesis in eubacteria: a guiding light for algae and plants, J. Bacteriol. 175 (1993) 3919-3925.
16. [16] G. Laudi, M.L. Manzini, Chlorophyll content and plastid ultrastructure in leaflets of Metasequoia glyptostroboides, Protoplasma 84 (1975) 185-190.
17. [17] K. Ou, H. Adamson, Chlorophyll accumulation in cotyledons, hypocotyls and primary needles of Pinus pinea seedlings in light and dark, Physiol. Plant. 93 (1995) 719-724.
18. [18] P. Mariani, M.E. De Carli, N. Rascio, B. Baldan, G. Casadoro, G. Gennari, M. Bodner, W. Larcher, Synthesis of chlorophyll and photosynthetic competence in etiolated and greening seedlings of Larix decidua as compared with Picea abies, J. Plant Physiol. 137 (1990) 5-14.
19. [19] W.T. Griffiths, Reconstitution of chlorophyllide formation by isolated etioplast membranes, Biochem. J. 174 (1978) 681-692.
20. [20] K. Apel, H.J. Santel, T.E. Redlinger, H. Falk, The protochlorophyllide holochrome of barley (Hordeum vulgare L.): isolation and characterization of the NADPH-protochlorophyllide oxidoreductase, Eur. J. Biochem. 111 (1980) 251-258.
21. [21] W.T. Griffiths, Protochlorophyllide photoreduction, in: H. Scheer (Ed.), Chlorophylls, CRC Press, Boca Raton, FL, 1991, pp. 433-449.
22. [22] G.A. Armstrong, S. Runge, G. Frick, U. Sperling, K. Apel, Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana, Plant Physiol. 108 (1995) 1505-1517.
23. [23] H. Holtorf, S. Reinbothe, C. Reinbothe, B. Bereza, K. Apel, Two routes of chlorophyllide synthesis that are differentially regulated by light in barley, Proc. Natl. Acad. Sci. USA 92 (1995) 3254-3258.
24. [24] A.J. Spano, Z.H. He, M.P. Timko, NADPH:protochlorophyllide oxidoreductases in white pine (Pinus strobus) and loblolly pine (P. taeda), Mol. Gen. Genet. 236 (1992) 86-95.
25. [25] C. Forreiter, K. Apel, Light-independent and light-dependent protochlorophyllide-reducing activities and two distinct NADPH-protochlorophyllide oxidoreductase polypeptides in mountain pine (Pinus mugo), Planta 190 (1993) 536-545.
26. [26] J.D. Rowe, T.W. Griffiths, Protochlorophyllide reductase in photosynthetic prokaryotes and its role in chlorophyll synthesis, Biochem. J. 311 (1995) 411-424.
27. [27] J.Y. Suzuki, C.E. Bauer, A prokaryotic origin for light-dependent chlorophyll biosynthesis of plants, Proc. Natl. Acad. Sci. USA 92 (1995) 3749-3753.
28. [28] J. Li, M.P. Timko, Thepc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear gene for NADPH:protochlorophyllide oxidoreductase, Plant Mol. Biol. 30 (1996) 15-37.
29. [29] N. Lebedev, B. van Cleve, G. Armstrong, K. Apel, Chlorophyll synthesis in a deetiolated (det340) mutant of Arabidopsis without NADPH-protochlorophyllide (Pchlide) oxidoreductase (POR) A and photoactive Pchlide-F655, Plant Cell 7 (1995) 2081-2090.
30. [30] S. Reinbothe, S. Runge, C. Reinbothe, B. van Cleve, K. Apel, Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids, Plant Cell 7 (1995) 161-172.
31. [31] S. Runge, U. Sperling, G. Frick, K. Apel, G.A. Armstrong, Distinct roles for light-dependent NADPH:protochlorophyllide oxidoreductases (POR) A and B during greening in higher plants, Plant J. 9 (1996) 513-523.
32. [32] U. Sperling, B. van Cleve, G. Frick, K. Apel, G.A. Armstrong, Over-expression of light-dependent PORA or PORB in plants depleted of endogenous POR by far-red light enhances seedling survival in white light and protects against photooxidative damage, Plant J. 12 (1997) 649-658.
33. [33] U. Sperling, F. Franck, B. van Cleve, G. Frick, K. Apel and G.A. Armstrong, Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. Plant Cell, 10 (1998) 283-296.
34. [34] R. Sager, Inheritance in the green alga Chlamydomonas reinhardtii, Genetics 40 (1955) 476-489.
35. [35] C. Ford, W.-Y. Wang, Three new yellow loci in Chlamydomonas reinhardtii, Mol. Gen. Genet. 179 (1980) 259-263.
36. [36] C. Ford, W.-Y. Wang, Temperature sensitive yellow mutants of Chlamydomonas reinhardtii, Mol. Gen. Genet. 180 (1980) 5-10.
37. [37] C. Ford, S. Mitchell, W.-Y. Wang, Protochlorophyllide photoconversion mutants of Chlamydomonas reinhardtii, Mol. Gen. Genet. 184 (1981) 460-463.
38. [38] K. Ohyama, H. Fukuzawa, T. Kohchi, H. Shirai, T. Sano, S. Sano, K. Umesono, Y. Shiki, M. Takeuchi, Z. Chang, S.-I, Aota, H. Inokuchi, H. Ozeki, Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha, Nature 322 (1986) 572-574.
39. [39] K. Shinozaki, M. Ohme, M. Tanaka, T. Wakasugi, N. Hayashida, T. Matsubayashi, J. Chunwongse, J. Obokata, K. Yamaguchi-Shinozaki, C. Ohto, K. Torazawa, B.-Y. Meng, M. Sugita, H. Deno, T. Kamogashira, K. Yamada, J. Kusuda, F. Takaiwa, A. Kato, N. Tohdoh, H. Shimada, M. Sugiura, The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression, EMBO J.5 (1986) 2043-2049.
40. [40] J. Hiratsuka, H. Shimada, R. Whittier, T. Ishibashi, M. Sakamoto, M. Mori, C. Kondo, Y. Honji, C.-R. Sun, B.-Y. Meng, Y.-Q. Li, A. Kanno, Y. Nishizawa, A. Hirai, K. Shinozaki, M, Sugiura, The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals, Mol. Gen. Genet. 217 (1989) 185-194.
41. [41] Y. Fujita, Y. Takahashi, T. Kohchi, H. Ozeki, K. Ohyama, H. Matsubara, Identification of a novel nifH-like (frxC) protein in chloroplasts of the liverwort Marchantia polymorpha, Plant Mol. Biol. 13 (1989) 551-561.
42. [42] J.E. Hearst, M. Alberti, R.F. Doolittle, A putative nitrogenase reductase gene found in the nucleotide sequences from the photosynthetic gene cluster of R. capsulata, Cell 40 (1985) 219-220.
43. [43] Y. Fujita, Y. Takahashi, F. Shonai, Y. Ogura, H. Matsubara, Cloning, nucleotide sequence and differential expression of the nifH and nifH-like (frxC) genes from the filamentous cyanobacterium Plectonema boryanum, Plant Cell Physiol. 32 (1991) 1093-1106.
44. [44] J. Lidholm, P. Gustafsson, Homologues of the green algal gidA gene and the liverwort frxC gene are present on the chloroplast genomes of conifers. Plant Mol. Biol. 17 (1991) 787-798.
45. [45] C. Huang, X.-Q. Liu, Nucleotide sequence of the frxC, petB and trnL genes in the chloroplast genome of Chlamydomonas reinhardtii, Plant Mol. Biol. 18 (1992) 985-988.
46. [46] M. Alberti, D.H. Burke, J.E. Hearst, Structure and sequence of the photosynthesis gene cluster, in: R.E. Blankenship, M.T. Madigan, C.E. Bauer (Eds.), Advances in Photosynthesis, Volume 2: Anoxygenic Photosynthetic Bacteria, Kluwer Academic, Dordrecht, Netherlands, 1995, pp. 1083-1106.
47. [47] K.M. Zsebo, J.E. Hearst, Genetic-physical mapping of a photosynthetic gene cluster from R. capsulata, Cell 37 (1984) 937-947.
48. [48] S.A. Coomber, M. Chaudhri, A. Connor, G. Britton, C.N. Hunter, Localised transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides, Mol. Microbiol. 4 (1990) 977-989.
49. [49] Z. Yang, CE. Bauer, Rhodobacter capsulatus genes involved in early steps of the bacteriochlorophyll biosynthetic pathway, J. Bacteriol. 172 (1990) 5001-5010.
50. [50] D.H. Burke, M. Alberti, J.E. Hearst, bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants, J. Bacteriol. 175 (1993) 2414-2422.
51. [51] D.W. Bollivar, J.Y. Suzuki, J.T. Beatty, J.M. Dobrowolski, C.E. Bauer, Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus, J. Mol. Biol. 237 (1994) 622-640.
52. [52] D.C. Youvan, E.J. Bylina, M. Alberti, H. Begusch, J.E. Hearst, Nucleotide and deduced polypeptide sequences of the photosynthetic reaction-center, B870 antenna, and flanking polypeptides from R. capsulata, Cell 37 (1984) 949-957.
53. [53] J. Girard-Bascou, Mutations in four chloroplast loci of Chlamydomonas reinhardtii affecting the photosystem I reaction centers, Curr. Genet. 12 (1987) 483-488.
54. [54] C. Roitgrund, L.J. Mets, Localization of two novel chloroplast genome functions: trans-splicing of RNA and protochlorophyllide reduction, Curr. Genet. 17 (1990) 147-153.
55. [55] M. Goldschmidt-Clermont, Y. Choquet, J. Girard-Bascou, F. Michel, M. Schirmer-Rahire, J.-D. Rochaix, A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii, Cell 65 (1991) 135-143.
56. [56] Y. Ogura, M. Takemura, K. Oda, K. Yamato, E. Ohta, H. Fukuzawa, K. Ohyama, Cloning and nucleotide sequence of a frxC-ORF469 gene cluster of Synechocystis PCC6803: conservation with liverwort chloroplast frxC-ORF465 and nif operon, Biosci. Biotech. Biochem. 56 (1992) 788-793.
57. [57] Y. Choquet, M. Rahire, J. Girard-Bascou, J. Erickson, J.-D. Rochaix, A chloroplast gene is required for the light-independent accumulation of chlorophyll in Chlamydomonas reinhardtii, EMBO J. 11 (1992) 1697-1704.
58. [58] J.Y. Suzuki, C.E, Bauer, Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC), Plant Cell 4 (1992) 929-940.
59. [59] Y. Fujita, Y. Takahashi, M. Chuganji, H. Matsubara, The nifH-like (frxC) gene is involved in the biosynthesis of chlorophyll in the filamentous cyanobacterium Plectonema boryanum, Plant Cell Physiol. 33 (1992) 81-92.
60. [60] Y. Fujita, H. Matsumoto, Y. Takahashi, H. Matsubara, Identification of a nifDK-like gene (ORF467) involved in the biosynthesis of chlorophyll in the cyanobacterium Plectonema boryanum. Plant Cell Physiol. 34 (1993) 305-314.
61. [61] M. Richard, G. Bellemare, Nucleotide sequence of Chlamydomonas moewusii chloroplasttc tRNA Thr, Nucl. Acids Res. 18 (1990) 2061.
62. [62] J. Li, M. Goldschmidt-Clermont, M.P. Timko, Chloroplast-encoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii, Plant Cell 5 (1993) 1817-1829.
63. [63] X.-Q, Liu, H. Xu, C. Huang, Chloroplast chlB is required for light-independent chlorophyll accumulation in Chlamydomonas reinhardtii, Plant Mol. Biol. 23 (1993) 297-308.
64. [64] Y. Fujita, H. Takagi, T. Hase, Identification of the chlB gene product essential for light-independent chlorophyll biosynthesis in the cyano-bacterium Plectonema boryanum, Plant Cell Physiol. 37 (1996) 313-323.
65. [65] T. Wakasugi, J. Tsudsuki, S. Ito, K. Nakashima, T. Tsudsuki, M. Sugiura, Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii, Proc. Natl. Acad. Sci. USA 91 (1994) 9794-9798.
66. [66] V.L. Stirewalt, C.B. Michalowski, W. Löffelhardt, H.J. Bohnert, D.A. Bryant, Nucleotide sequence of the cyanelle genome from Cyanophora paradoxa. Plant Mol. Biol. Reptr. 13 (1995) 327-332.
67. [67] M. Reith, J. Munholland, Complete nucleotide sequence of the Porphyra purpurea chloroplast genome, Plant Mol. Biol. Reptr. 13 (1995) 333-345.
68. [68] J. Tsudzuki, K. Nakashima, M. Ito, T. Tsudzuki, M. Horihata, K. Satoh, K. Yoshinaga, T. Wakasugi. T. Nagai, M. Kapoor, M. Sugiura, Chloroplast genome structure of unicellular green alga Chlorella vulgaris C-27, in: P. Mathis (Ed.), Photosynthesis: From Light to Biosphere Vol. III, Kluwer Academic, Dordrecht, Netherlands, 1995 pp. 643-646.
69. [69] M. Kapoor, T. Wakasugi, K. Yoshinaga, M. Sugiura, The chloroplast chlL gene of the green alga Chlorella vulgaris C-27 contains a self-splicing group I intron, Mol. Gen. Genet. 250 (1996) 655-664.
70. [70] R.M. Maier, K. Neckermann, G.I. Igloi, H. Kössel, Complete sequence of the maize chloroplast genome: Gene content, hotspots of divergence and fine tuning of genetic information by transcript editing, J. Mol. Biol. 251 (1995) 614-628.
71. [71] K. V. Kowallik, B. Stoebe, I. Schaffran, U. Freier, The chloroplast genome of a chlorophyll a + c-containing alga, Odontella sinensis, Plant Mol. Biol. Reptr. 13 (1995) 336-342.
72. [72] R.B. Hallick, L. Hong, R.G. Drager, M.R. Favreau, A. Montfort, B. Orsat, A. Spielmann, E. Stutz, Complete sequence of Euglena gracilis chloroplast DNA, Nucl. Acids Res. 21 (1993) 3537-3544.
73. [73] K. Yamada, M. Matsuda, Y. Fujita, H. Matsubara, M. Sugai, A frxC homolog exists in the chloroplast DNAs from various pteridophytes and in gymnosperms, Plant Cell Physiol. 33 (1992) 325-327.
74. [74] K. Yamada, M. Matsuda, N. Yamamoto, The presence of a homologue of liverwort ORF289 (frxC) on the chloroplast genomes of pteridophytes and gymnosperms, in: N. Murata (Ed.), Research in Photosynthesise Vol. III, Kluwer Academic, Dordrecht, Netherlands, 1992, pp. 515-518.
75. [75] D.H. Burke, L. A. Raubeson, M. Alberti, J.E. Hearst, E.T. Jordan, S.A. Kirch, A.E.C. Valinski, D.S. Conant, D.B. Stein, The chlL (frxC) gene: phylogenetic distribution in vascular plants and DNA sequence from Polystichum acrostichoides (Pteridophyta) and Synechococcus sp. 7002 (Cyanobacteria), Pl. Syst. Evol. 187 (1993) 89-102.
76. [76] M. Richard, C. Tremblay, G. Bellemare, Chloroplastic genomes of Ginko biloba and Chlamydomonas moewusii contain a chlB gene encoding one subunit of a light-independent protochlorophyllide reductase, Curr. Genet. 26 (1994) 159-165.
77. [77] R. Boivin, M. Richard, D. Beauseigle, J. Bousquet, G. Bellemare, Phylogenetic inferences from chloroplast chlB gene sequences of Neprolepsis exaltata (Filicopsida), Ephreda altissima (Gnetopsida), and diverse land plants, Mol. Phylogenet. Evol. 6 (1996) 19-29.
78. [78] B. Karpinska, S. Karpinski, J.E. Hällgren, The chlB gene encoding a subunit of light-independent protochlorophyllide reductase is edited in chloroplasts of conifers, Curr. Genet. 31 (1997) 343-347.
79. [79] K. Yamada, Personal communication, 1996.
80. [80] H. Adamson, T. Griffiths, N. Packer, M. Sutherland, Light-independent accumulation of chlorophyll a and b and protochlorophyllide in green barley (Hordeum vulgare L.), Physiol. Plant, 64 (1985) 345-352.
81. [81] H. Adamson, N. Packer, J. Gregory, Chloroplast development and the synthesis of chlorophyll and protochlorophyllide in Zostera transferred to darkness. Planta 165 (1985) 469-476.
82. [82] J. Walmsley, H. Adamson, Chlorophyll accumulation and breakdown in light-grown barley transferred to darkness: effect of seedling age, Physiol. Plant. 77 (1989) 312-319.
83. 14C glutamic acid) evidence of dark chlorophyll synthesis in the absence of chlorophyll accumulation, Physiol. Plant. 77 (1994) 435-444.
84. [84] S. Takio, T. Satoh, Expression patterns of chloroplast genes involved in light-independent chlorophyll synthesis in liverwort cells, in: P. Mathis (Ed.), Photosynthesis: from Light to Biosphere Vol. III, Kluwer Academic, Dordrecht, Netherlands 1995, pp. 941-944.
85. [85] D.H. Burke, J.E. Hearst, A. Sidow, Early evolution of photosynthesis: clues from nitrogenase and chlorophyll iron proteins, Proc. Natl. Acad. Sci. USA 90 (1993) 7134-7138.
86. [86] J.W. Peters, K. Fischer, R.D. Dean, Nitrogenase structure and function: a biochemical-genetic perspective, Annu. Rev. Microbiol. 49 (1995) 335-366.
87. [87] D.H. Burke, M. Alberti, J.E. Hearst, The Rhodobacter capsulatus chlorin reductase-encoding locus, bchA, consists of three genes, bchX, bchY, and bchZ, J. Bacteriol. 175 (1993) 2407-2413.
88. [88] G.A. Peschek, B. Hinterstoisser, M. Wastyn, O. Kuntner, B. Pineau, A. Missbichler, J. Lang, Chlorophyll precursors in the plasma membrane of a cyanobacterium, Anacystis nidulans, J. Biol. Chem. 264 (1989) 11827-11832.
89. [89] J.Y. Suzuki, C.E. Bauer, Altered monovinyl and divinyl protochlorophyllide pools in bchJ mutants of Rhodobacter capsulatus, J. Biol. Chem. 270 (1995) 3732-3740.
90. [90] K. Shinohara, A. Murakami, Y. Fujita, Biochemical characteristics of thylakoid membranes in chloroplasts of dark-grown pine cotyledons, Plant Physiol. 98 (1992) 39-43.
91. [91] H. Drumm-Herrel, H. Mohr, Regulation by light of chlorophyll synthesis in the cotyledons of Scots pine (Pinus sylvestris) seedlings, Physiol. Plant. 91 (1994) 300-306.
92. 2 concentration and in chlorophyll biosynthesis, Plant Physiol. 108 (1995) 1461-1469.
93. [93] Q. Wu, W.F.J. Vermaas, Light-dependent chlorophyll a biosynthesis upon chlL deletion in wild-type and photosystem I-less strains of the cyanobacterium Synechocystis sp. PCC 6803, Plant Mol. Biol. 29 (1995) 933-945.
94. [94] C. Ford, S. Mitehell, W.-Y. Wang, Characterization of NADPH: protochlorophyllide photoconversion in the y-7 and pc-1 y-7 mutants of Chlamydomonas reinhardtii, Mol. Gen. Genet. 192 (1983) 290-292.