What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses

Journal of Cell Science

Volumn 125, Issue 8, 2012, Pages 1865-1875

  Dorrell, Richard G ^a   Howe, Christopher J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Chloroplast; Endosymbiotic gene transfer; Kleptoplast; Photosymbiont

Indexed keywords

ARTICLE; CELL LINEAGE; CELL MATURATION; CHLOROPLAST; CRYPTOMIONAD; CYANOPHAGE; DIATOM; DINOFLAGELLATE; EUKARYOTE; GENE TRANSFER; GREEN ALGA; HAPTOPHYTA; MOLECULAR BIOLOGY; NONHUMAN; OXIDATIVE STRESS; PHOTOSYNTHESIS; PRIORITY JOURNAL; RED ALGA; SYMBIONT; SYMBIOSIS; XANTHOPHYTE;

ANIMALS; CHLOROPLASTS; EUKARYOTA; GENE TRANSFER, HORIZONTAL; PHOTOSYNTHESIS; SYMBIOSIS;

CILIOPHORA; DINOPHYCEAE; DINOPHYSIS; EUKARYOTA; MYRIONECTA RUBRA; OPISTHOBRANCHIA; PAULINELLA CHROMATOPHORA; PROKARYOTA; RHIZARIA;

EID: 84863100082     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.102285     Document Type: Article

References (111)

1. Allen, J. F. (1993). Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol. 165, 609-631.
2. Allen, J. F. (2003). The function of genomes in bioenergetic organelles. Philos. Trans. R. Soc. Biol. 358, 19-37.
3. Archibald, J. M. and Lane, C. E. (2009). Going, going, not quite gone: nucleomorphs as a case study in nuclear genome reduction. J. Heredity 100, 582-590.
4. Archibald, J. M., Rogers, M. B., Toop, M., Ishida, K. and Keeling, P. J. (2003). Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. USA 100, 7678-7683.
5. Balint, I., Bhattacharya, J., Perelman, A., Schatz, D., Moskovitz, Y., Keren, N. and Schwarz, R. (2006). Inactivation of the extrinsic subunit of photosystem II, PsbU, in Synechococcus PCC 7942 results in elevated resistance to oxidative stress. FEBS Lett. 580, 2117-2122.
6. Balk, J. and Lobreaux, S. (2005). Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci. 10, 324-331.
7. Ball, S., Colleoni, C., Cenci, U., Raj, J. N. and Tirtiaux, C. (2011). The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J. Exp. Bot. 62, 1775-1801.
8. Barkan, A. (2011). Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol. 155, 1520-1532.
9. Barth, P., Lagoutte, B. and Sétif, P. (1998). Ferredoxin reduction by photosystem I from Synechocystis sp. PCC 6803: toward an understanding of the respective roles of subunits PsaD and PsaE in ferredoxin binding. Biochemistry. 37, 16233-16241.
10. Beck, C. F. (2005). Signaling pathways from the chloroplast to the nucleus. Planta 222, 743-756.
11. Bentley, F. K., Luo, H., Dilbeck, P., Burnap, R. L. and Eaton-Rye, J. J. (2008). Effects of Inactivating psbM and psbT on Photodamage and Assembly of Photosystem II in Synechocystis sp PCC 6803. Biochemistry. 47, 11637-11646.
12. Berney, C. and Pawlowski, J. (2006). A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc. R. Soc. B. Biol. Sci. 273, 1867-1872.
13. Bodyl, A., Mackiewicz, P. and Stiller, J. W. (2010). Comparative genomic studies suggest that the cyanobacterial endosymbionts of the amoeba Paulinella chromatophora possess an import apparatus for nuclear-encoded proteins. Plant Biol. 12, 639-649.
14. Busch, A. and Hippler, M. (2011). The structure and function of eukaryotic photosystem I. Biochim. Biophys. Acta Bioenerget. 1807, 864-877.
15. Carreto, J. I. and Carignan, M. O. (2011). Mycosporine-like amino acids: relevant secondary metabolites. chemical and ecological aspects. Mar. Drugs 9, 387-446.
16. Chauvat, F., Rouet, P., Bottin, H. and Boussac, A. (1989). Mutagenesis by random cloning of an Escherichia coli kanamycin resistance geen into the genome of the cyanobacterium Synechocystis PCC 803: selection of mutants defective in photosynthesis. Mol. Gen. Genet. 216, 51-59.
17. Chitnis, P. R. (2001). Photosystem I: Function and Physiology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 593-626.
18. Chitnis, P. R., Reilly, P. A., Miedel, M. C. and Nelson, N. (1989a). Structure and targeted mutagenesis of the gene encoding 8-kDa subunit of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 264, 18374-18380.
19. Chitnis, P. R., Reilly, P. A. and Nelson, N. (1989b). Insertional inactivation of the gene encoding subunit II of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. J. Biol. Chem. 264, 18381-18385.
20. Curtis, N. E., Pierce, S. K., Massey, S. E., Schwartz, J. A. and Maugel, T. K. (2007). Newly metamorphosed Elysia clarki juveniles feed on and sequester chloroplasts from algal species different from those utilized by adult slugs. Mar. Biol. 150, 797-806.
21. Curtis, N. E., Schwartz, J. A. and Pierce, S. K. (2010). Ultrastructure of sequestered chloroplasts in sacoglossan gastropods with differing abilities for plastid uptake and maintenance. Invert. Biol. 129, 297-308.
22. DeSalvo, M. K., Sunagawa, S., Fisher, P. L., Voolstra, C. R., Iglesias-Prieto, R. and Medina, M. (2010). Coral host transcriptomic states are correlated with Symbiodinium genotypes. Mol. Ecol. 19, 1174-1186.
23. Deusch, O., Landan, G., Roettger, M., Gruenheit, N., Kowallik, K. V., Allen, J. F., Martin, W. and Dagan, T. (2008). Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol. Biol. Evol. 25, 748-761.
24. Dorrell, R. G. and Smith, A. G. (2011). Do red and green make brown? perspectives on plastid acquisitions within the chromalveolates. Eukaryot. Cell 10, 856-868.
25. Escalera, L., Reguera, B., Takishita, K., Yoshimatsu, S., Koike, K. and Koike, K. (2011). Cyanobacterial endosymbionts in the benthic dinoflagellate Sinophysis canaliculata (Dinophysiales, Dinophyceae). Protist 162, 304-314.
26. Gabrielsen, T. M., Minge, M. A., Espelund, M., Tooming-Klunderud, A., Patil, V., Nederbragt, A. J., Otis, C., Turmel, M., Shalchian-Tabrizi, K., Lemieux, C. et al. (2011). Genome evolution of a tertiary dinoflagellate plastid. PLoS ONE 6, e19132.
27. Garcia-Cuetos, L., Moestrup, O., Hansen, P. J. and Daugbjerg, N. (2010). The toxic dinoflagellate Dinophysis acuminata harbors permanent chloroplasts of cryptomonad origin, not kleptochloroplasts. Harmful Algae 9, 25-38.
28. Gast, R. J., Moran, D.M., Dennett, M. R. and Caron, D. A. (2007). Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Env. Microbiol. 9, 39-45.
29. Gong, X. M., Agalarov, R., Brettel, K. and Carmeli, C. (2003). Control of electron transport in photosystem I by the iron-sulfur cluster FX in response to intra- and intersubunit interactions. J. Biol. Chem. 278, 19141-19150.
30. Green, B. R. (2011). Chloroplast genomes of photosynthetic eukaryotes. Plant J. 66, 34-44.
31. Green, B. J., Fox, T. C. and Rumpho, M. E. (2005). Stability of isolated algal chloroplasts that participate in a unique mollusc/kleptoplast association. Symbiosis 40, 31-40.
32. Haendeler, K., Grzymbowski, Y. P., Krug, P. J. and Waegele, H. (2009). Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life. Front. Zool. 6, 28.
33. Hanekamp, T. and Thorsness, P. E. (1996). Inactivation of YME2/RNA12, which encodes an integral inner mitochondrial membrane protein, causes increased escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 2764-2771.
34. Herrmann, K. M. and Weaver, L. M. (1999). The shikimate pathway. Ann. Rev. Plant Physiol. Plant Mol. Biol. 50, 473-503.
35. Hoefnagel, M. H. N., Atkin, O. K. and Wiskich, J. T. (1998). Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim. Biophys. Acta Bioenerget. 1366, 235-255.
36. Howe, C. J., Barbrook, A. C., Nisbet, R. E. R., Lockhart, P. J. and Larkum, A. W. D. (2008a). The origin of plastids. Philos. Trans. R. Soc. Biol. 363, 2675-2685.
37. Howe, C. J., Nisbet, R. E. R. and Barbrook, A. C. (2008b). The remarkable chloroplast genome of dinoflagellates. J. Exp. Bot. 59, 1035-1045.
38. Imanian, B., Pombert, J. F. and Keeling, P. J. (2010). The complete plastid genomes of the two 'dinotoms' Durinskia baltica and Kryptoperidinium foliaceum. PLoS ONE 5, e10711.
39. Ishida, K. and Green, B. R. (2002). Second- and third-hand chloroplasts in dinoflagellates: phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proc. Natl. Acad. Sci. USA 99, 9294-9299.
40. Jansson, C., Debus, R. J., Osiewacz, H. D., Gurevitz, M. and McIntosh, L. (1987). Construction of an Obligate Photoheterotrophic Mutant of the Cyanobacterium Synechocystis 6803: Inactivation of the psbA Gene Family. Plant Physiol. 85, 1021-1025.
41. Jarvis, P. (2008). Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179, 257-285.
42. Jeanjean, R., Latifi, A., Matthijs, H. C. P. and Havaux, M. (2008). The PsaE subunit of photosystem I prevents light-induced formation of reduced oxygen species in the cyanobacterium Synechocystis sp PCC 6803. Biochim. Biophys. Acta Bioenerget. 1777, 308-316.
43. Jesus, B., Ventura, P. and Calado, G. (2010). Behaviour and a functional xanthophyll cycle enhance photo-regulation mechanisms in the solar-powered sea slug Elysia timida (Risso, 1818). J. Exp. Mar. Biol. Ecol. 395, 98-105.
44. Jiroutova, K., Koreny, L., Bowler, C. and Obornik, M. (2010). A gene in the process of endosymbiotic transfer. PLoS ONE 5, e13234.
45. Johnson, M. D. (2011a). Acquired phototrophy in ciliates: a review of cellular interactions and structural adaptations. J. Eukaryot. Microbiol. 58, 185-195.
46. Johnson, M. D. (2011b). The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Res. 107, 117-132.
47. Johnson, M. D., Tengs, T., Oldach, D. and Stoecker, D. K. (2006). Sequestration, performance, and functional control of cryptophyte plastids in the ciliate Myrionecta rubra (Ciliophora). J. Phycol. 42, 1235-1246.
48. Johnson, M. D., Oldach, D., Delwiche, C. F. and Stoecker, D. K. (2007). Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445, 426-428.
49. Kim, E. and Archibald, J. M. (2009). Diversity and evolution of plastids and their genomes. Plant Cell Monogr. 13, 1-39.
50. Kleine, T., Maier, U. G. and Leister, D. (2009). DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu. Rev. Plant Biol. 60, 115-138.
51. Kneip, C., Voss, C., Lockhart, P. J. and Maier, U. G. (2008). The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution. BMC Evol. Biol. 8, 30.
52. Komenda, J. and Barber, J. (1995). Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis. Biochemistry. 34, 9625-9631.
53. Larkum, A. W. D., Lockhart, P. J. and Howe, C. J. (2007). Shopping for plastids. Trends Plant Sci. 12, 189-195.
54. Lister, D. L., Bateman, J. M., Purton, S. and Howe, C. J. (2003). DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316, 33-38.
55. Lloyd, A. H. and Timmis, J. N. (2011). The origin and characterization of new nuclear genes originating from a cytoplasmic organellar genome. Mol. Biol. Evol. 28, 2019-2028.
56. Marin, B., Nowack, E. C. M. and Melkonian, M. (2005). A plastid in the making: Evidence for a second primary endosymbiosis. Protist 156, 425-432.
57. Martin, W. (2003). Gene transfer from organelles to the nucleus: Frequent and in big chunks. Proc. Natl. Acad. Sci. USA 100, 8612-8614.
58. Maruyama, S., Suzaki, T., Weber, A. P. M., Archibald, J. M. and Nozaki, H. (2011). Eukaryote-to-eukaryote gene transfer gives rise to genome mosaicism in euglenids. BMC Evol. Biol. 11, 105.
59. Minge, M. A., Shalchian-Tabrizi, K., Torresen, O. K., Takishita, K., Probert, I., Inagaki, Y., Klaveness, D. and Jakobsen, K. S. (2010). A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evol. Biol. 10, 191.
60. Minnhagen, S., Carvalho, W. F., Salomon, P. S. and Janson, S. (2008). Chloroplast DNA content in Dinophysis (Dinophyceae) from different cell cycle stages is consistent with kleptoplasty. Env. Microbiol. 10, 2411-2417.
61. Minnhagen, S., Kim, M., Salomon, P. S., Yih, W., Graneli, E. and Park, M. G. (2011). Active uptake of kleptoplastids by Dinophysis caudata from its ciliate prey Myrionecta rubra. Aquat. Microb. Ecol. 62, 99-108.
62. Miyagishima, S. (2011). Mechanism of Plastid Division: From a Bacterium to an Organelle. Plant Physiol. 155, 1533-1544.
63. Moustafa, A., Beszteri, B., Maier, U. G., Bowler, C., Valentin, K. and Bhattacharya, D. (2009). Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324, 1724-1726.
64. Murata, N., Takahashi, S., Nishiyama, Y. and Allakhverdiev, S. I. (2007). Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta. 1767, 414-421.
65. Naithani, S., Hou, J. M. and Chitnis, P. R. (2000). Targeted inactivation of the psaK1, psaK2 and psaM genes encoding subunits of Photosystem I in the cyanobacterium Synechocystis sp PCC 6803. Photosynthesis Res. 63, 225-236.
66. Nakayama, T. and Ishida, K. (2009). Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr. Biol. 19, 284-285.
67. Nakayama, T., Ikegami, Y., Nakayama, T., Ishida, K.-i., Inagaki, Y. and Inouye, I. (2011). Spheroid bodies in rhopalodiacean diatoms were derived from a single endosymbiotic cyanobacterium. J. Plant Res. 124, 93-97.
68. Nelson, N. and Yocum, C. F. (2006). Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 57, 521-565.
69. Nishiyama, Y., Los, D. A. and Murata, N. (1999). PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol. 120, 301-308.
70. Nishiyama, Y., Allakhverdiev, S. I. and Murata, N. (2006). A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim. Biophys. Acta. 1757, 742-749.
71. Nosenko, T., Lidie, K. L., Van Dolah, F. M., Lindquist, E., Cheng, J. F. and Bhattacharya, D. (2006). Chimeric plastid proteome in the florida "red tide" dinoflagellate Karenia brevis. Mol. Biol. Evol. 23, 2026-2038.
72. Nowack, E. C. M. and Grossman, A. R. (2012). Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc. Natl. Acad. Sci. USA, 109, 5340-5345.
73. Nowack, E. C. M., Melkonian, M. and Gloeckner, G. (2008). Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18, 410-418.
74. Nowack, E. C. M., Vogel, H., Groth, M., Grossman, A. R., Melkonian, M. and Glockner, G. (2011). Endosymbiotic gene transfer and transcriptional regulation of transferred genes in Paulinella chromatophora. Mol. Biol. Evol. 28, 407-422.
75. Okamoto, N. and Inouye, I. (2006). Hatena arenicola gen. et sp nov., a katablepharid undergoing probable plastid acquisition. Protist 157, 401-419.
76. Parfrey, L.W., Lahr, D. J., Knoll, A. H. and Katz, L. A. (2011). Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl. Acad. Sci. USA 108, 13624-13629.
77. Park, M. G., Park, J. S., Kim, M. and Yih, W. (2008). Plastid dynamics during survival of Dinophysis caudata without its ciliate prey. J. Phycol. 44, 1154-1163.
78. Patron, N. J., Waller, R. F. and Keeling, P. J. (2006). A tertiary plastid uses genes from two endosymbionts. J. Mol. Biol. 357, 1373-1382.
79. Pelletreau, K. N., Bhattacharya, D., Price, D. C., Worful, J. M., Moustafa, A. and Rumpho, M. E. (2011). Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiol. 155, 1561-1565.
80. Pierce, S. K., Massey, S. E., Hanten, J. J. and Curtis, N. E. (2003). Horizontal transfer of functional nuclear genes between multicellular organisms. Biol. Bull. 204, 237-240.
81. Pierce, S. K., Curtis, N. E. and Schwartz, J. A. (2010). Chlorophyll synthesis by a sea slug (Elysia chlorotica). Integrat. Comparat. Biol. 50, 137.
82. Prechtl, J., Kneip, C., Lockhart, P., Wenderoth, K. and Maier, U. G. (2004). Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol. Biol. Evol. 21, 1477-1481.
83. Reith, M. and Munholland, J. (1995). Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol. Biol. Rep. 13, 333-335.
84. Reyes-Prieto, A., Yoon, H. S., Moustafa, A., Yang, E. C., Andersen, R. A., Boo, S. M., Nakayama, T., Ishida, K. and Bhattacharya, D. (2010). Differential gene retention in plastids of common recent origin. Mol. Biol. Evol. 27, 1530-1537.
85. Richly, E. and Leister, D. (2004). NUPTs in sequenced eukaryotes and their genomic organization in relation to NUMTs. Mol. Biol. Evol. 21, 1972-1980.
86. Rumpho, M. E., Worful, J. M., Lee, J., Kannan, K., Tyler, M. S., Bhattacharya, D., Moustafa, A. and Manhart, J. R. (2008). Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc. Natl. Acad. Sci. USA 105, 17867-17871.
87. Rumpho, M. E., Pochareddy, S., Worful, J. M., Summer, E. J., Bhattacharya, D., Pelletreau, K. N., Tyler, M. S., Lee, J., Manhart, J. R. and Soule, K. M. (2009). Molecular characterization of the calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Mol. Plant 2, 1384-1396.
88. Rumpho, M. E., Pelletreau, K. N., Moustafa, A. and Bhattacharya, D. (2011). The making of a photosynthetic animal. J. Exp. Biol. 214, 303-311.
89. Schmitt, V. and Waegele, H. (2011). Behavioural adapatations in relation to long-term retention of endosymbiotic chloroplasts in the sea slug Elysia timida (Opisthobranchia, Sacoglossa). Thalass. 27, 225-238.
90. Schnitzler, C. E. and Weis, V. M. (2010). Coral larvae exhibit few measurable transcriptional changes during the onset of coral-dinoflagellate endosymbiosis. Mar. Genom. 3, 107-116.
91. Schwartz, J. A., Curtis, N. E. and Pierce, S. K. (2010). Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol. Biol. 37, 29-37.
92. Shen, J. R., Ikeuchi, M. and Inoue, Y. (1997). Analysis of the psbU gene encoding the 12-kDa extrinsic protein of photosystem II and studies on its role by deletion mutagenesis in Synechocystis sp. PCC 6803. J. Biol. Chem. 272, 17821-17826.
93. Shen, J. R., Qian, M., Inoue, Y. and Burnap, R. L. (1998). Functional characterization of Synechocystis sp. PCC 6803 Delta psbU and Delta psbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37, 1551-1558.
94. Sheppard, A. E., Ayliffe, M. A., Blatch, L., Day, A., Delaney, S. K., Khairul-Fahmy, N., Li, Y., Madesis, P., Pryor, A. J. and Timmis, J. N. (2008). Transfer of plastid DNA to the nucleus is elevated during male gametogenesis in tobacco. Plant Physiol. 148, 328-336.
95. Sheppard, A. E., Madesis, P., Lloyd, A. H., Day, A., Ayliffe, M. A. and Timmis, J. N. (2011). Introducing an RNA editing requirement into a plastid-localised transgene reduces but does not eliminate functional gene transfer to the nucleus. Plant Mol. Biol. 76, 299-309.
96. Shi, L. X. and Schroder, W. P. (2004). The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta Bioenerget. 1608, 75-96.
97. Smart, L. B., Anderson, S. L. and McIntosh, L. (1991). Targeted genetic inactivation of the photosystem I reaction center in the cyanobacterium Synechocystis sp. PCC 6803. EMBO J. 10, 3289-3296.
98. Smith, D. R., Crosby, K. and Lee, R. W. (2011). Correlation between nuclear plastid DNA abundance and plastid number supports the limited transfer window hypothesis. Genom. Biol. Evol. 3, 365-371.
99. Stegemann, S., Hartmann, S., Ruf, S. and Bock, R. (2003). High-frequency gene transfer from the chloroplast genome to the nucleus. Proc. Natl. Acad. Sci. USA 100, 8828-8833.
100. Stoecker, D. K., Johnson, M. D., de Vargas, C. and Not, F. (2009). Acquired phototrophy in aquatic protists. Aquat. Microb. Ecol. 57, 279-310.
101. Sunagawa, S., Wilson, E. C., Thaler, M., Smith, M. L., Caruso, C., Pringle, J. R., Weis, V. M., Medina, M. and Schwarz, J. A. (2009). Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genom. 10, 258.
102. Thornton, L. E., Ohkawa, H., Roose, J. L., Kashino, Y., Keren, N. and Pakrasi, H. B. (2004). Homologs of plant PsbP and PsbQ proteins are necessary for regulation of photosystem II activity in the cyanobacterium Synechocystis 6803. Plant Cell 16, 2164-2175.
103. Thorsness, P. E., White, K. H. and Fox, T. D. (1993). Inactivation of Yme1, a member of the FtsH-Sec18-Pas1-Cdc48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 13, 5418-5426.
104. Voolstra, C. R., Schwarz, J. A., Schnetzer, J., Sunagawa, S., Desalvo, M. K., Szmant, A. M., Coffroth, M. A. and Medina, M. (2009). The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol. Ecol. 18, 1823-1833.
105. Waegele, H., Deusch, O., Haendeler, K., Martin, R., Schmitt, V., Christa, G., Pinzger, B., Gould, S. B., Dagan, T., Klussmann-Kolb, A. et al. (2011). Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Mol. Biol. Evol. 28, 699-706.
106. Weber, A. and Flugge, U. I. (2002). Interaction of cytosolic and plastidic nitrogen metabolism in plants. J. Exp. Bot. 53, 865-874.
107. Wisecaver, J. H. and Hackett, J. D. (2010). Transcriptome analysis reveals nuclearencoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genom. 11, 366.
108. Xu, Q., Hoppe, D., Chitnis, V. P., Odom, W. R., Guikema, J. A. and Chitnis, P. R. (1995). Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psaI reveals the function of psaI in the structural organization of psaL. J. Biol. Chem. 270, 16243-16250.
109. Yamaguchi, H., Nakayama, T., Kai, A. and Inouye, I. (2011). Taxonomy and phylogeny of a new kleptoplastidal dinoflagellate, Gymnodinium myriopyrenoides sp nov (Gymnodiniales, Dinophyceae), and its cryptophyte symbiont. Protist 162, 650-667.
110. Yokoyama, A., Takahashi, F., Kataoka, H., Hara, Y. and Nozaki, H. (2011). Evolutionary analyses of the nuclear-encoded photosynthetic gene psbO from tertiary plastid-conctaining algae in Dinophyta. J. Phycol. 47, 407-414.
111. Yuyama, I., Watanabe, T. and Takei, Y. (2011). Profiling differential gene expression of symbiotic and aposymbiotic corals using a high coverage gene expression profiling (HiCEP) analysis. Mar. Biotechnol. 13, 32-40.