Molecular techniques to interrogate and edit the Chlamydomonas nuclear genome

Plant Journal

Volumn 82, Issue 3, 2015, Pages 393-412

  Jinkerson, Robert E ^a   Jonikas, Martin C ^a  

^a GEOPHYSICAL LABORATORY   (United States)

Author keywords

Chlamydomonas reinhardtii; genetics; genome editing; markers; molecular tools; nuclear genome; reporters; transformation

Indexed keywords

EPITOPES; GENES; MUTAGENESIS;

CHLAMYDOMONAS REINHARDTII; GENETICS; MARKERS; MOLECULAR TOOLS; NUCLEAR GENOMES; REPORTERS; TRANSFORMATION;

PROTEINS;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

GENETIC MARKER; MUTAGENIC AGENT;

CELL NUCLEUS; CHLAMYDOMONAS; CHROMOSOMAL MAPPING; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETIC PROCEDURES; GENETIC TRANSFORMATION; GENETICS; HOMOLOGOUS RECOMBINATION; MOLECULAR BIOLOGY; MUTAGENESIS; PLANT GENOME; PROCEDURES; RNA INTERFERENCE; TRANSGENIC PLANT;

CELL NUCLEUS; CHLAMYDOMONAS; CHROMOSOME MAPPING; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; GENE EXPRESSION REGULATION, PLANT; GENETIC MARKERS; GENETIC TECHNIQUES; GENOME, PLANT; HOMOLOGOUS RECOMBINATION; MOLECULAR BIOLOGY; MUTAGENESIS; MUTAGENS; PLANTS, GENETICALLY MODIFIED; RNA INTERFERENCE; TRANSFORMATION, GENETIC;

EID: 84929048842     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12801     Document Type: Article

References (193)

1. Aksoy, M., Pootakham, W., Pollock, S.V., Moseley, J.L., González-Ballester, D., and, Grossman, A.R., (2013) Tiered regulation of sulfur deprivation responses in Chlamydomonas reinhardtii and identification of an associated regulatory factor. Plant Physiol. 162, 195-211.
2. Alford, L.M., Mattheyses, A.L., Hunter, E.L., Lin, H., Dutcher, S.K., and, Sale, W.S., (2013) The Chlamydomonas mutant pf27 reveals novel features of ciliary radial spoke assembly. Cytoskeleton, 70, 804-818.
3. Annaluru, N., Muller, H., Mitchell, L.A., et al.,. (2014) Total synthesis of a functional designer eukaryotic chromosome. Science, 344, 55-58.
4. Auchincloss, A.H., Loroch, A.I., and, Rochaix, J.D., (1999) The argininosuccinate lyase gene of Chlamydomonas reinhardtii: cloning of the cDNA and its characterization as a selectable shuttle marker. Mol. Gen. Genet. 261, 21-30.
5. Babinger, P., Kobl, I., Mages, W., and, Schmitt, R., (2001) A link between DNA methylation and epigenetic silencing in transgenic Volvox carteri. Nucleic Acids Res. 29, 1261-1271.
6. Bellafiore, S., Ferris, P., Naver, H., Göhre, V., and, Rochaix, J.-D., (2002) Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell, 14, 2303-2314.
7. Bennoun, P., and, Levine, R.P., (1967) Detecting mutants that have impaired photosynthesis by their increased level of fluorescence. Plant Physiol. 42, 1284-1287.
8. Berthold, P., Schmitt, R., and, Mages, W., (2002) An engineered Streptomyces hygroscopicus aph 7 gene mediates dominant resistance against hygromycin B in Chlamydomonas reinhardtii. Protist, 153, 401-412.
9. Blaby, I.K., Blaby-Haas, C.E., Tourasse, N., et al.,. (2014) The Chlamydomonas genome project: a decade on. Trends Plant Sci. 19, 672-680.
10. - strain. Mol. Cell. Biol. 12, 5268-5279.
11. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A., and, Bonas, U., (2009) Breaking the code of DNA binding specificity of TAL-Type III effectors. Science, 326, 1509-1512.
12. Bowers, A.K., Keller, J.A., and, Dutcher, S.K., (2003) Molecular markers for rapidly identifying candidate genes in Chlamydomonas reinhardtii. ERY1 and ERY2 encode chloroplast ribosomal proteins. Genetics, 164, 1345-1353.
13. Brown, L.E., Sprecher, S.L., and, Keller, L.R., (1991) Introduction of exogenous DNA into Chlamydomonas reinhardtii by electroporation. Mol. Cell. Biol. 11, 2328-2332.
14. Camargo, A., Llamas, Á., Schnell, R.A., Higuera, J.J., González-Ballester, D., Lefebvre, P.A., Fernández, E., and, Galván, A., (2007) Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell, 19, 3491-3503.
15. Casas-Mollano, J.A., van Dijk, K., Eisenhart, J., and, Cerutti, H., (2007) SET3p monomethylates histone H3 on lysine 9 and is required for the silencing of tandemly repeated transgenes in Chlamydomonas. Nucleic Acids Res. 35, 939-950.
16. Casas-Mollano, J.A., Jeong, B.-R., Xu, J., Moriyama, H., and, Cerutti, H., (2008) The MUT9p kinase phosphorylates histone H3 threonine 3 and is necessary for heritable epigenetic silencing in Chlamydomonas. Proc. Natl Acad. Sci. USA, 105, 6486-6491.
17. Cerutti, H., and, Casas-Mollano, J.A., (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50, 81-99.
18. Cerutti, H., Johnson, A.M., Gillham, N.W., and, Boynton, J.E., (1997a) Epigenetic silencing of a foreign gene in nuclear transformants of Chlamydomonas. Plant Cell, 9, 925-945.
19. Cerutti, H., Johnson, A.M., Gillham, N.W., and, Boynton, J.E., (1997b) A eubacterial gene conferring spectinomycin resistance on Chlamydomonas reinhardtii: integration into the nuclear genome and gene expression. Genetics, 145, 97-110.
20. Croft, M.T., Moulin, M., Webb, M.E., and, Smith, A.G., (2007) Thiamine biosynthesis in algae is regulated by riboswitches. Proc. Natl Acad. Sci. USA, 104, 20770-20775.
21. 2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res. 20, 2959-2965.
22. Day, A., Schirmer-Rahire, M., Kuchka, M.R., Mayfield, S.P., and, Rochaix, J.D., (1988) A transposon with an unusual arrangement of long terminal repeats in the green alga Chlamydomonas reinhardtii. EMBO J. 7, 1917-1927.
23. Day, A., Debuchy, R., van Dillewijn, J., Purton, S., and, Rochaix, J.-D., (1990) Studies on the maintenance and expression of cloned DNA fragments in the nuclear genome of the green alga Chlamydomonas reinhardtii. Physiol. Plant. 78, 254-260.
24. Debuchy, R., Purton, S., and, Rochaix, J.D., (1989) The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J. 8, 2803-2809.
25. Decottignies, P., Lemarechal, P., Jacquot, J.P., Schmitter, J.M., and, Gadal, P., (1995) Primary structure and post-translational modification of ferredoxin-NADP reductase from Chlamydomonas reinhardtii. Arch. Biochem. Biophys. 316, 249-259.
26. Dent, R.M., Haglund, C.M., Chin, B.L., Kobayashi, M.C., and, Niyogi, K.K., (2005) Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol. 137, 545-556.
27. Diener, D., (2009) Analysis of cargo transport by IFT and GFP imaging of IFT in Chlamydomonas. In Methods in Cell Biology, Vol. 93 (, King, S.M., and, Pazour, G.J., eds). Burlington, MA: Academic Press, pp. 111-119.
28. van Dijk, K., Xu, H., and, Cerutti, H., (2006) Epigenetic silencing of transposons in the green alga Chlamydomonas reinhardtii. In Small RNAs-Analysis and Regulatory Functions (, Nellen, W., and, Hammann, C., eds). Berlin, Heidelberg, New York: Springer, pp. 159-178.
29. Dunahay, T.G., (1993) Transformation of Chlamydomonas reinhardtii with silicon carbide whiskers. Biotechniques, 15, 452-455, 457-458, 460.
30. Dutcher, S.K., Power, J., Galloway, R.E., and, Porter, M.E., (1991) Reappraisal of the genetic map of Chlamydomonas reinhardtii. J. Hered. 82, 295-301.
31. Dutcher, S.K., Li, L., Lin, H., Meyer, L., Giddings, T.H., Kwan, A.L., and, Lewis, B.L., (2012) Whole-genome sequencing to identify mutants and polymorphisms in Chlamydomonas reinhardtii. G3 (Bethesda), 2, 15-22.
32. Ebersold, W.T., (1956) Crossing over in Chlamydomonas reinhardtii. Am. J. Bot. 43, 408-410.
33. Eichler-Stahlberg, A., Weisheit, W., Ruecker, O., and, Heitzer, M., (2009) Strategies to facilitate transgene expression in Chlamydomonas reinhardtii. Planta, 229, 873-883.
34. Eversole, R.A., (1956) Biochemical mutants of Chlamydomonas reinhardtii. Am. J. Bot. 43, 404-407.
35. Ferris, P.J., (1989) Characterization of a Chlamydomonas transposon, Gulliver, resembling those in higher plants. Genetics, 122, 363-377.
36. Ferris, P.J., (1995) Localization of the nic-7, ac-29 and thi-10 genes within the mating-type locus of Chlamydomonas reinhardtii. Genetics, 141, 543-549.
37. Ferris, P.J., Woessner, J.P., and, Goodenough, U.W., (1996) A sex recognition glycoprotein is encoded by the plus mating-type gene fus1 of Chlamydomonas reinhardtii. Mol. Biol. Cell, 7, 1235-1248.
38. Fischer, N., and, Rochaix, J.D., (2001) The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii. Mol. Genet. Genomics, 265, 888-894.
39. Fuhrmann, M., Oertel, W., and, Hegemann, P., (1999) A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J. 19, 353-362.
40. Fuhrmann, M., Stahlberg, A., Govorunova, E., Rank, S., and, Hegemann, P., (2001) The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J. Cell Sci. 114, 3857-3863.
41. Fuhrmann, M., Hausherr, A., Ferbitz, L., Schödl, T., Heitzer, M., and, Hegemann, P., (2004) Monitoring dynamic expression of nuclear genes in Chlamydomonas reinhardtii by using a synthetic luciferase reporter gene. Plant Mol. Biol. 55, 869-881.
42. Galloway, R.E., and, Mets, L.J., (1984) Atrazine, bromacil, and diuron resistance in Chlamydomonas: a single non-mendelian genetic locus controls the structure of the thylakoid binding site. Plant Physiol. 74, 469-474.
43. Gao, H., Wright, D.A., Li, T., Wang, Y., Horken, K., Weeks, D.P., Yang, B., and, Spalding, M.H., (2014) TALE activation of endogenous genes in Chlamydomonas reinhardtii. Algal Res. 5, 52-60.
44. Gao, H., Wang, Y., Fei, X., Wright, D.A., and, Spalding, M.H., (2015) Expression activation and functional analysis of HLA3, a putative inorganic carbon transporter in Chlamydomonas reinhardtii. Plant J. 82, 1-11.
45. González-Ballester, D., de Montaigu, A., Galván, A., and, Fernández, E., (2005) Restriction enzyme site-directed amplification PCR: a tool to identify regions flanking a marker DNA. Anal. Biochem. 340, 330-335.
46. González-Ballester, D., Pootakham, W., Mus, F., et al.,. (2011) Reverse genetics in Chlamydomonas: a platform for isolating insertional mutants. Plant Methods, 7, 24.
47. Goodenough, U.W., Hwang, C., and, Martin, H., (1976) Isolation and genetic analysis of mutant strains of Chlamydomonas reinhardtii defective in gametic differentiation. Genetics, 82, 169-186.
48. Graham, J.E., Spanier, J.G., and, Jarvik, J.W., (1995) Isolation and characterization of Pioneer1, a novel Chlamydomonas transposable element. Curr. Genet. 28, 429-436.
49. Grant, D.M., Gillham, N.W., and, Boynton, J.E., (1980) Inheritance of chloroplast DNA in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 77, 6067-6071.
50. Griesbeck, C., Kobl, I., and, Heitzer, M., (2006) Chlamydomonas reinhardtii a protein expression system for pharmaceutical and biotechnological proteins. Mol. Biotechnol. 34, 213-223.
51. Grossman, A.R., Harris, E.E., Hauser, C., et al.,. (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot. Cell, 2, 1137-1150.
52. Gulis, G., Narasimhulu, K., Fox, L., and, Redding, K., (2008) Purification of His6-tagged photosystem I from Chlamydomonas reinhardtii. Photosynth. Res. 96, 51-60.
53. Gumpel, N., Rochaix, J.-D., and, Purton, S., (1994) Studies on homologous recombination in the green alga Chlamydomonas reinhardtii. Curr. Genet. 26, 438-442.
54. Hannon, M., Gimpel, J., Tran, M., Rasala, B., and, Mayfield, S., (2010) Biofuels from algae: challenges and potential. Biofuels, 1, 763-784.
55. Harris, E.H., (2009) Introduction to Chlamydomonas and its laboratory use. In The Chlamydomonas Sourcebook, Vol. 1 (, Harris, E.H., ed.). Oxford: Academic Press, pp. 1-444.
56. Hartnett, M.E., Newcomb, J.R., and, Hodson, R.C., (1987) Mutations in Chlamydomonas reinhardtii conferring resistance to the herbicide sulfometuron methyl. Plant Physiol. 85, 898-901.
57. Hawks, B.G., and, Lee, R.W., (1976) Methyl methanesulfonate mutagenesis of synchronized Chlamydomonas. Mutat. Res. 37, 221-228.
58. Heitzer, M., and, Zschoernig, B., (2007) Construction of modular tandem expression vectors for the green alga Chlamydomonas reinhardtii using the Cre/lox-system. Biotechniques, 43, 324-332.
59. Heitzer, M., Eckert, A., Fuhrmann, M., and, Griesbeck, C., (2007) Influence of codon bias on the expression of foreign genes in microalgae. In Transgenic Microalgae as Green Cell Factories, Vol. 616 (, Leõn, R., Galván, A.A., and, Fernández, E., eds). New York: Springer New York, pp. 46-53.
60. Huang, K., and, Beck, C.F., (2003) Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 100, 6269-6274.
61. Jacobson, B.S., (1957) Evidence for recovery from X-ray damage in Chlamydomonas. Radiat. Res. 7, 394-406.
62. Jeong, B.-R., Wu-Scharf, D., Zhang, C., and, Cerutti, H., (2002) Suppressors of transcriptional transgenic silencing in Chlamydomonas are sensitive to DNA-damaging agents and reactivate transposable elements. Proc. Natl Acad. Sci. USA, 99, 1076-1081.
63. Jiang, W., Zhou, H., Bi, H., Fromm, M., Yang, B., and, Weeks, D.P., (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41, e188.
64. Jiang, W., Brueggeman, A.J., Horken, K.M., Plucinak, T.M., and, Weeks, D.P., (2014) Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii. Eukaryot. Cell, 13, 1465-1469.
65. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., and, Charpentier, E., (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
66. Jinkerson, R.E., Subramanian, V., and, Posewitz, M.C., (2011) Improving biofuel production in phototrophic microorganisms with systems biology. Biofuels, 2, 125-144.
67. Jinkerson, R.E., Radakovits, R., and, Posewitz, M.C., (2013) Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered, 4, 37-43.
68. Kang, Y., and, Mitchell, D.R., (1998) An intronic enhancer is required for deflagellation-induced transcriptional regulation of a Chlamydomonas reinhardtii dynein gene. Mol. Biol. Cell, 9, 3085-3094.
69. Karcher, D., Köster, D., Schadach, A., Klevesath, A., and, Bock, R., (2009) The Chlamydomonas chloroplast HLP protein is required for nucleoid organization and genome maintenance. Mol. Plant, 2, 1223-1232.
70. Kataoka, M., Sato, R., and, Oshio, H., (1990) Isolation and partial characterization of mutant Chlamydomonas reinhardtii resistant to herbicides-23142. J. Pestic. Sci. 15, 449-451.
71. Kathir, P., LaVoie, M., Brazelton, W.J., Haas, N.A., Lefebvre, P.A., and, Silflow, C.D., (2003) Molecular map of the Chlamydomonas reinhardtii nuclear genome. Eukaryot. Cell, 2, 362-379.
72. Kilian, O., Benemann, C.S.E., Niyogi, K.K., and, Vick, B., (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc. Natl Acad. Sci. USA, 108, 21265-21269.
73. Kim, Y.G., Cha, J., and, Chandrasegaran, S., (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc. Natl Acad. Sci. USA, 93, 1156-1160.
74. Kim, K.-S., Kustu, S., and, Inwood, W., (2006) Natural history of transposition in the green alga Chlamydomonas reinhardtii: use of the AMT4 locus as an experimental system. Genetics, 173, 2005-2019.
75. Kim, S., Lee, Y.-C., Cho, D.-H., Lee, H.U., Huh, Y.S., Kim, G.-J., and, Kim, H.-S., (2014) A simple and non-invasive method for nuclear transformation of intact-walled Chlamydomonas reinhardtii. PLoS One, 9, e101018.
76. Kindle, K.L., (1990) High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 87, 1228-1232.
77. Kindle, K.L., Schnell, R.A., Fernandez, E., and, Lefebvre, P.A., (1989) Stable nuclear transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase. J. Cell Biol. 109, 2589-2601.
78. Komsic-Buchmann, K., Stephan, L.M., and, Becker, B., (2012) The SEC6 protein is required for contractile vacuole function in Chlamydomonas reinhardtii. J. Cell Sci. 125, 2885-2895.
79. Kong, F., Yamasaki, T., and, Ohama, T., (2014) Expression levels of domestic cDNA cassettes integrated in the nuclear genomes of various Chlamydomonas reinhardtii strains. J. Biosci. Bioeng. 117, 613-616.
80. Kovar, J.L., Zhang, J., Funke, R.P., and, Weeks, D.P., (2002) Molecular analysis of the acetolactate synthase gene of Chlamydomonas reinhardtii and development of a genetically engineered gene as a dominant selectable marker for genetic transformation. Plant J. 29, 109-117.
81. Kozminski, K.G., Diener, D.R., and, Rosenbaum, J.L., (1993) High level expression of nonacetylatable α-tubulin in Chlamydomonas reinhardtii. Cell Motil. Cytoskelet. 25, 158-170.
82. Krysan, P.J., Young, J.C., Tax, F., and, Sussman, M.R., (1996) Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport. Proc. Natl Acad. Sci. USA, 93, 8145-8150.
83. Kumar, S.V., Misquitta, R.W., Reddy, V.S., Rao, B.J., and, Rajam, M.V., (2004) Genetic transformation of the green alga-Chlamydomonas reinhardtii by Agrobacterium tumefaciens. Plant Sci. 166, 731-738.
84. Ladygin, V.G., and, Boutanaev, A.M., (2002) Transformation of Chlamydomonas reinhardtii CW-15 with the hygromycin phosphotransferase gene as a selectable marker. Russ. J. Genet. 38, 1009-1014.
85. Lauersen, K.J., Berger, H., Mussgnug, J.H., and, Kruse, O., (2013a) Efficient recombinant protein production and secretion from nuclear transgenes in Chlamydomonas reinhardtii. J. Biotechnol. 167, 101-110.
86. Lauersen, K.J., Vanderveer, T.L., Berger, H., Kaluza, I., Mussgnug, J.H., Walker, V.K., and, Kruse, O., (2013b) Ice recrystallization inhibition mediated by a nuclear-expressed and -secreted recombinant ice-binding protein in the microalga Chlamydomonas reinhardtii. Appl. Microbiol. Biotechnol. 97, 9763-9772.
87. Lauersen, K.J., Kruse, O., and, Mussgnug, J.H., (2015) Targeted expression of nuclear transgenes in Chlamydomonas reinhardtii with a versatile, modular vector toolkit. Appl. Microbiol. Biotechnol. 99, 3491-3503.
88. Lawrence, C.W., and, Holt, P.D., (1970) Effect of gamma radiation and alpha particles on gene recombination in Chlamydomonas reinhardtii. Mutat. Res. 10, 545-555.
89. Lechtreck, K.-F., Luro, S., Awata, J., and, Witman, G.B., (2009) HA-tagging of putative flagellar proteins in Chlamydomonas reinhardtii identifies a novel protein of intraflagellar transport complex B. Cell Motil. Cytoskelet. 66, 469-482.
90. Lee, R.W., and, Jones, R.F., (1973) Induction of Mendelian and non-Mendelian streptomycin resistant mutants during the synchronous cell cycle of Chlamydomonas reinhardtii. Mol. Gen. Genet. 121, 99-108.
91. Lee, R.W., and, Jones, R.F., (1976) Lethal and mutagenic effects of nitrosoguanidine on synchronized Chlamydomonas. Mol. Gen. Genet. 147, 283-289.
92. Lee, B., Choi, G.-G., Choi, Y.-E., Sung, M., Park, M., and, Yang, J.-W., (2014) Enhancement of lipid productivity by ethyl methane sulfonate-mediated random mutagenesis and proteomic analysis in Chlamydomonas reinhardtii. Korean J. Chem. Eng. 31, 1036-1042.
93. Levine, R.P., (1960a) Genetic control of photosynthesis in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 46, 972-978.
94. Levine, R.P., (1960b) A screening technique for photosynthetic mutants in unicellular algae. Nature, 188, 339-340.
95. L'Hernault, S.W., and, Rosenbaum, J.L., (1985) Chlamydomonas a-tubulin is posttranslationally modified by acetylation on the e-amino group of a lysine. Biochemistry, 24, 473-478.
96. Li, T., Liu, B., Spalding, M.H., Weeks, D.P., and, Yang, B., (2012a) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 30, 390-392.
97. Li, X., Moellering, E.R., Liu, B., Johnny, C., Fedewa, M., Sears, B.B., Kuo, M.-H., and, Benning, C., (2012b) A galactoglycerolipid lipase Is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell, 24, 4670-4686.
98. Lim, J.-M., Ahn, J.-W., Hwangbo, K., Choi, D.-W., Park, E.-J., Hwang, M.S., Liu, J.R., and, Jeong, W.-J., (2013) Development of cyan fluorescent protein (CFP) reporter system in green alga Chlamydomonas reinhardtii and macroalgae Pyropia sp. Plant Biotechnol. Rep. 7, 407-414.
99. Lin, H., Miller, M.L., Granas, D.M., and, Dutcher, S.K., (2013a) Whole genome sequencing identifies a deletion in protein phosphatase 2A that affects its stability and localization in Chlamydomonas reinhardtii. PLoS Genet. 9, e1003841.
100. Lin, H., Nauman, N., Albee, A., Hsu, S., and, Dutcher, S., (2013b) New mutations in flagellar motors identified by whole genome sequencing in Chlamydomonas. Cilia, 2, 14.
101. Loppes, R., (1968) Ethyl methanesulfonate: an effective mutagen in Chlamydomonas reinhardtii. Mol. Gen. Genet. 102, 229-231.
102. Lumbreras, V., Stevens, D.R., and, Purton, S., (1998) Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron. Plant J. 14, 441-447.
103. Lux, F.G., and, Dutcher, S.K., (1991) Genetic interactions at the FLA10 locus: suppressors and synthetic phenotypes that affect the cell cycle and flagellar function in Chlamydomonas reinhardtii. Genetics, 128, 549-561.
104. Mamedov, T., and, Yusibov, V., (2011) Green algae Chlamydomonas reinhardtii possess endogenous sialylated N-glycans. FEBS Open Bio, 1, 15-22.
105. Manuell, A.L., Beligni, M.V., Elder, J.H., Siefker, D.T., Tran, M., Weber, A., McDonald, T.L., and, Mayfield, S.P., (2007) Robust expression of a bioactive mammalian protein in Chlamydomonas chloroplast. Plant Biotechnol. J. 5, 402-412.
106. Mathieu-Rivet, E., Kiefer-Meyer, M.-C., Vanier, G., Ovide, C., Burel, C., Lerouge, P., and, Bardor, M., (2014) Protein N-glycosylation in eukaryotic microalgae and its impact on the production of nuclear expressed biopharmaceuticals. Front. Plant Sci. 5, 1-13.
107. Maul, J.E., Lilly, J.W., Cui, L., dePamphilis, C.W., Miller, W., Harris, E.H., and, Stern, D.B., (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell, 14, 2659-2679.
108. Mayfield, S.P., and, Kindle, K.L., (1990) Stable nuclear transformation of Chlamydomonas reinhardtii by using a C. reinhardtii gene as the selectable marker. Proc. Natl Acad. Sci. USA, 87, 2087-2091.
109. Mayfield, S.P., Manuell, A.L., Chen, S., Wu, J., Tran, M., Siefker, D., Muto, M., and, Marin-Navarro, J., (2007) Chlamydomonas reinhardtii chloroplasts as protein factories. Curr. Opin. Biotechnol. 18, 126-133.
110. Merchant, S.S., Prochnik, S.E., Vallon, O., et al.,. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science, 318, 245-250.
111. Meslet-Cladière, L., and, Vallon, O., (2011) Novel shuttle markers for nuclear transformation of the green alga Chlamydomonas reinhardtii. Eukaryot. Cell, 10, 1670-1678.
112. Meslet-Cladière, L., and, Vallon, O., (2012) A new method to identify flanking sequence tags in Chlamydomonas using 3′-RACE. Plant Methods, 8, 21.
113. Mets, L.J., and, Bogorad, L., (1971) Mendelian and uniparental alterations in erythromycin binding by plastid ribosomes. Science, 174, 707-709.
114. Mets, L.J., and, Geist, L.J., (1983) Linkage of a known chloroplast gene mutation to the uniparental genome of Chlamydomonas reinhardii. Genetics, 105, 559-579.
115. 2 production. Biochem. Biophys. Res. Commun. 417, 704-709.
116. Michelet, L., Zaffagnini, M., Vanacker, H., Le Maréchal, P., Marchand, C., Schroda, M., Lemaire, S.D., and, Decottignies, P., (2008) In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J. Biol. Chem. 283, 21571-21578.
117. Molnár, A., Schwach, F., Studholme, D.J., Thuenemann, E.C., and, Baulcombe, D.C., (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature, 447, 1126-1129.
118. Molnár, A., Bassett, A., Thuenemann, E., Schwach, F., Karkare, S., Ossowski, S., Weigel, D., and, Baulcombe, D., (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J. 58, 165-174.
119. Nekrasov, V., Staskawicz, B., Weigel, D., Jones, J.D.G., and, Kamoun, S., (2014) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 691-693.
120. Nelson, J.A., and, Lefebvre, P.A., (1995a) Targeted disruption of the NIT8 gene in Chlamydomonas reinhardtii. Mol. Cell. Biol. 15, 5762-5769.
121. Nelson, J.A.E., and, Lefebvre, P.A., (1995b) Transformation of Chlamydomonas reinhardtii. Methods Cell Biol. 47, 513-517.
122. Nelson, J.A., Savereide, P.B., and, Lefebvre, P.A., (1994) The CRY1 gene in Chlamydomonas reinhardtii: structure and use as a dominant selectable marker for nuclear transformation. Mol. Cell. Biol. 14, 4011-4019.
123. Neupert, J., Karcher, D., and, Bock, R., (2009) Generation of Chlamydomonas strains that efficiently express nuclear transgenes. Plant J. 57, 1140-1150.
124. Nguyen, R.L., Tam, L.-W., and, Lefebvre, P.A., (2005) The LF1 gene of Chlamydomonas reinhardtii encodes a novel protein required for flagellar length control. Genetics, 169, 1415-1424.
125. Ninomiya, Y., Suzuki, K., Ishii, C., and, Inoue, H., (2004) Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl Acad. Sci. USA, 101, 12248-12253.
126. O'Neill, B.M., Mikkelson, K.L., Gutierrez, N.M., Cunningham, J.L., Wolff, K.L., Szyjka, S.J., Yohn, C.B., Redding, K.E., and, Mendez, M.J., (2012) An exogenous chloroplast genome for complex sequence manipulation in algae. Nucleic Acids Res. 40, 2782-2792.
127. Oshio, H., Shibata, H., Mito, N., Yamamoto, M., Harris, E.H., Gillham, N.W., Boynton, J.E., and, Sato, R., (1993) Isolation and characterization of a Chlamydomonas reinhardtii mutant resistant to photobleaching herbicides. Z. Naturforsch. 43c, 339-344.
128. Pan, J., Wang, Q., and, Snell, W.J., (2004) An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev. Cell, 6, 445-451.
129. Pérez-Alegre, M., Dubus, A., and, Fernández, E., (2005) REM1, a new type of long terminal repeat retrotransposon in Chlamydomonas reinhardtii. Mol. Cell. Biol. 25, 10628-10638.
130. Periz, G., and, Keller, L.R., (1997) DNA elements regulating alpha1-tubulin gene induction during regeneration of eukaryotic flagella. Mol. Cell. Biol. 17, 3858-3866.
131. Petersen, J.L., and, Small, G.D., (2001) A gene required for the novel activation of a class II DNA photolyase in Chlamydomonas. Nucleic Acids Res. 29, 4472-4481.
132. Pfannenschmid, F., Wimmer, V.C., Rios, R.-M., Geimer, S., Kröckel, U., Leiherer, A., Haller, K., Nemcová, Y., and, Mages, W., (2003) Chlamydomonas DIP13 and human NA14: a new class of proteins associated with microtubule structures is involved in cell division. J. Cell Sci. 116, 1449-1462.
133. Plecenikova, A., Slaninova, M., and, Riha, K., (2014) Characterization of DNA repair deficient strains of Chlamydomonas reinhardtii generated by insertional mutagenesis. PLoS One, 9, e105482.
134. Posewitz, M.C., Smolinski, S.L., Kanakagiri, S., Melis, A., Seibert, M., and, Ghirardi, M.L., (2004) Hydrogen photoproduction is attenuated by disruption of an isoamylase gene in Chlamydomonas reinhardtii. Plant Cell, 16, 2151-2163.
135. Pratheesh, P.T., Vineetha, M., and, Kurup, G.M., (2014) An efficient protocol for the Agrobacterium-mediated genetic transformation of microalga Chlamydomonas reinhardtii. Mol. Biotechnol. 56, 507-515.
136. Randall, J., Warr, J.R., Hopkins, J.M., and, McVittie, A., (1964) A single-gene mutation of Chlamydomonas reinhardii affecting motility: a genetic and electron microscope study. Nature, 203, 912-914.
137. Randolph-Anderson, B.L., Sato, R., Johnson, A.M., Harris, E.H., Hauser, C.R., Oeda, K., Ishige, F., Nishio, S., Gillham, N.W., and, Boynton, J.E., (1998) Isolation and characterization of a mutant protoporphyrinogen oxidase gene from Chlamydomonas reinhardtii conferring resistance to porphyric herbicides. Plant Mol. Biol. 38, 839-859.
138. Rasala, B.A., and, Mayfield, S.P., (2011) The microalga Chlamydomonas reinhardtii as a platform for the production of human protein therapeutics. Bioengineered, 2, 50-54.
139. Rasala, B.A., Lee, P.A., Shen, Z., Briggs, S.P., Mendez, M., and, Mayfield, S.P., (2012) Robust expression and secretion of Xylanase1 in Chlamydomonas reinhardtii by fusion to a selection gene and processing with the FMDV 2A peptide. PLoS One, 7, e43349.
140. Rasala, B.A., Barrera, D.J., Ng, J., Plucinak, T.M., Rosenberg, J.N., Weeks, D.P., Oyler, G.A., Peterson, T.C., Haerizadeh, F., and, Mayfield, S.P., (2013) Expanding the spectral palette of fluorescent proteins for the green microalga Chlamydomonas reinhardtii. Plant J. 74, 545-556.
141. Rasala, B.A., Chao, S.-S., Pier, M., Barrera, D.J., and, Mayfield, S.P., (2014) Enhanced genetic tools for engineering multigene traits into green algae. PLoS One, 9, e94028.
142. Remacle, C., Cardol, P., Coosemans, N., Gaisne, M., and, Bonnefoy, N., (2006) High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc. Natl Acad. Sci. USA, 103, 4771-4776.
143. Reyon, D., Kirkpatrick, J., Sander, J., Zhang, F., Voytas, D., Joung, J.K., Dobbs, D., and, Coffman, C., (2011) ZFNGenome: a comprehensive resource for locating zinc finger nuclease target sites in model organisms. BMC Genom. 12, 83.
144. Rohr, J., Sarkar, N., Balenger, S., Jeong, B.-R., and, Cerutti, H., (2004) Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas. Plant J. 40, 611-621.
145. Ruecker, O., Zillner, K., Groebner-Ferreira, R., and, Heitzer, M., (2008) Gaussia-luciferase as a sensitive reporter gene for monitoring promoter activity in the nucleus of the green alga Chlamydomonas reinhardtii. Mol. Genet. Genomics, 280, 153-162.
146. Rymarquis, L.A., Handley, J.M., Thomas, M., and, Stern, D.B., (2005) Beyond complementation. Map-based cloning in Chlamydomonas reinhardtii. Plant Physiol. 137, 557-566.
147. Sager, R., (1954) Mendelian and non-Mendelian inheritance of streptomycin resistance in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 40, 356-363.
148. Schnell, R.A., and, Lefebvre, P.A., (1993) Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics, 134, 737-747.
149. Schoppmeier, J., Mages, W., and, Lechtreck, K.-F., (2005) GFP as a tool for the analysis of proteins in the flagellar basal apparatus of Chlamydomonas. Cell Motil. Cytoskelet. 61, 189-200.
150. Schroda, M., (2006) RNA silencing in Chlamydomonas: mechanisms and tools. Curr. Genet. 49, 69-84.
151. Schroda, M., Vallon, O., Wollman, F.-A., and, Beck, C.F., (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell, 11, 1165-1178.
152. Schroda, M., Blöcker, D., and, Beck, C.F., (2000) The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J. 21, 121-131.
153. Schroda, M., Beck, C.F., and, Vallon, O., (2002) Sequence elements within an HSP70 promoter counteract transcriptional transgene silencing in Chlamydomonas. Plant J. 31, 445-455.
154. Scranton, M.A., Ostrand, J.T., Fields, F.J., and, Mayfield, S.P., (2015) Chlamydomonas as a model for biofuels and bio-products production. Plant J. 82, 523-531.
155. Shalem, O., Sanjana, N.E., Hartenian, E., et al.,. (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science, 343, 84-87.
156. Shan, Q., Wang, Y., Li, J., et al.,. (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31, 686-688.
157. Shao, N., and, Bock, R., (2008) A codon-optimized luciferase from Gaussia princeps facilitates the in vivo monitoring of gene expression in the model alga Chlamydomonas reinhardtii. Curr. Genet. 53, 381-388.
158. Shimogawara, K., Fujiwara, S., Grossman, A., and, Usuda, H., (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics, 148, 1821-1828.
159. Silflow, C.D., LaVoie, M., Tam, L.-W., Tousey, S., Sanders, M., Wu, W.-C., Borodovsky, M., and, Lefebvre, P.A., (2001) The Vfl1 protein in Chlamydomonas localizes in a rotationally asymmetric pattern at the distal ends of the basal bodies. J. Cell Biol. 153, 63-74.
160. Sineshchekov, O.A., Jung, K.-H., and, Spudich, J.L., (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 99, 8689-8694.
161. Sizova, I.A., Lapina, T.V., Frolova, O.N., Alexandrova, N.N., Akopiants, K.E., and, Danilenko, V.N., (1996) Stable nuclear transformation of Chlamydomonas reinhardtii with a Streptomyces rimosus gene as the selective marker. Gene, 181, 13-18.
162. Sizova, I., Fuhrmann, M., and, Hegemann, P., (2001) A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene, 277, 221-229.
163. Sizova, I., Greiner, A., Awasthi, M., Kateriya, S., and, Hegemann, P., (2013) Nuclear gene targeting in Chlamydomonas using engineered zinc-finger nucleases. Plant J. 73, 873-882.
164. Sodeinde, O.A., and, Kindle, K.L., (1993) Homologous recombination in the nuclear genome of Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 90, 9199-9203.
165. Soria-Guerra, R.E., Ramírez-Alonso, J.I., Ibáñez-Salazar, A., Govea-Alonso, D.O., Paz-Maldonado, L.M.T., Bañuelos-Hernández, B., Korban, S.S., and, Rosales-Mendoza, S., (2013) Expression of an HBcAg-based antigen carrying angiotensin II in Chlamydomonas reinhardtii as a candidate hypertension vaccine. Plant Cell, Tissue Organ Cult. 116, 133-139.
166. 2. Proc. Natl Acad. Sci. USA, 101, 7787-7792.
167. Specht, E.A., Nour-Eldin, H.H., Hoang, K.T.D., and, Mayfield, S.P., (2015) An improved ARS2-derived nuclear reporter enhances the efficiency and ease of genetic engineering in Chlamydomonas. Biotechnol. J. 10, 473-479.
168. Stevens, D.R., Purton, S., and, Rochaix, J.D., (1996) The bacterial phleomycin resistance geneble as a dominant selectable marker in Chlamydomonas. Mol. Gen. Genet. 251, 23-30.
169. Suarez, J.V., Banks, S., Thomas, P.G., and, Day, A., (2014) A new F131V mutation in Chlamydomonas phytoene desaturase locates a cluster of norflurazon resistance mutations near the FAD-binding site in 3D protein models. PLoS One, 9, e99894.
170. Sugiura, M., Inoue, Y., and, Minagawa, J., (1998) Rapid and discrete isolation of oxygen-evolving His-tagged photosystem II core complex from Chlamydomonas reinhardtii by Ni2+ affinity column chromatography. FEBS Lett. 426, 140-144.
171. Tam, L.W., and, Lefebvre, P.A., (1993) Cloning of flagellar genes in Chlamydomonas reinhardtii by DNA insertional mutagenesis. Genetics, 135, 375-384.
172. Tenenboim, H., Smirnova, J., Willmitzer, L., Steup, M., and, Brotman, Y., (2014) VMP1-deficient Chlamydomonas exhibits severely aberrant cell morphology and disrupted cytokinesis. BMC Plant Biol. 14, 121.
173. Terashima, M., Freeman, E.S., Jinkerson, R.E., and, Jonikas, M.C., (2015) A fluorescence-activated cell sorting-based strategy for rapid isolation of high-lipid Chlamydomonas mutants. Plant J. 81, 147-159.
174. Townsend, J.A., Wright, D.A., Winfrey, R.J., Fu, F., Maeder, M.L., Joung, J.K., and, Voytas, D.F., (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature, 459, 442-445.
175. Trippens, J., Greiner, A., Schellwat, J., Neukam, M., Rottmann, T., Lu, Y., Kateriya, S., Hegemann, P., and, Kreimer, G., (2012) Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii. Plant Cell, 24, 4687-4702.
176. Tulin, F., and, Cross, F.R., (2014) A microbial avenue to cell cycle control in the plant superkingdom. Plant Cell, 26, 4019-4038.
177. Vartak, V., and, Bhargava, S., (1997) Characterization of a norflurazon-resistant mutant of Chlamydomonas reinhardtii. Weed Sci. 45, 374-377.
178. Wang, S.-C., Schnell, R.A., and, Lefebvre, P.A., (1998) Isolation and characterization of a new transposable element in Chlamydomonas reinhardtii. Plant Mol. Biol. 38, 681-687.
179. Warr, J.R., McVittie, A., Randall, J., and, Hopkins, J.M., (1966) Genetic control of flagellar structure in Chlamydomonas reinhardii. Genet. Res. 7, 335-351.
180. Wiedenheft, B., Sternberg, S.H., and, Doudna, J.A., (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature, 482, 331-338.
181. Wiseman, A., Gillham, N.W., and, Boynton, J.E., (1977) Nuclear mutations affecting mitochondrial structure and function in Chlamydomonas. J. Cell Biol. 73, 56-77.
182. Work, V.H., Radakovits, R., Jinkerson, R.E., Meuser, J.E., Elliott, L.G., Vinyard, D.J., Laurens, L.M.L., Dismukes, G.C., and, Posewitz, M.C., (2010) Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukaryot. Cell, 9, 1251-1261.
183. Wu-Scharf, D., Jeong, B.-R., Zhang, C., and, Cerutti, H., (2000) Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science, 290, 1159-1162.
184. Yamano, T., Iguchi, H., and, Fukuzawa, H., (2013) Rapid transformation of Chlamydomonas reinhardtii without cell-wall removal. J. Biosci. Bioeng. 115, 691-694.
185. Yoshihara, C., Inoue, K., Schichnes, D., Ruzin, S., Inwood, W., and, Kustu, S., (2008) An Rh1-GFP fusion protein is in the cytoplasmic membrane of a white mutant strain of Chlamydomonas reinhardtii. Mol. Plant, 1, 1007-1020.
186. Zäuner, S., Jochum, W., Bigorowski, T., and, Benning, C., (2012) A cytochrome b5-containing plastid-located fatty acid desaturase from Chlamydomonas reinhardtii. Eukaryot. Cell, 11, 856-863.
187. Zhang, C., Wu-Scharf, D., Jeong, B.-R., and, Cerutti, H., (2002) A WD40-repeat containing protein, similar to a fungal co-repressor, is required for transcriptional gene silencing in Chlamydomonas. Plant J. 31, 25-36.
188. Zhang, R., Patena, W., Armbruster, U., Gang, S.S., Blum, S.R., and, Jonikas, M.C., (2014) High-throughput genotyping of green algal mutants reveals random distribution of mutagenic insertion sites and endonucleolytic cleavage of transforming DNA. Plant Cell, 26, 1398-1409.
189. Zhao, T., Li, G., Mi, S., Li, S., Hannon, G.J., Wang, X.-J., and, Qi, Y., (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev. 21, 1190-1203.
190. Zhao, T., Wang, W., Bai, X., and, Qi, Y., (2009) Gene silencing by artificial microRNAs in Chlamydomonas. Plant J. 58, 157-164.
191. Zhou, H., Liu, B., Weeks, D.P., Spalding, M.H., and, Yang, B., (2014) Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice. Nucleic Acids Res. 42, 10903-10914.
192. Zorin, B., Hegemann, P., and, Sizova, I., (2005) Nuclear-gene targeting by using single-stranded DNA avoids illegitimate DNA integration in Chlamydomonas reinhardtii. Eukaryot. Cell, 4, 1264-1272.
193. Zorin, B., Lu, Y., Sizova, I., and, Hegemann, P., (2009) Nuclear gene targeting in Chlamydomonas as exemplified by disruption of the PHOT gene. Gene, 432, 91-96.