Light-regulated photosynthetic gene expression and phosphoribulokinase enzyme activity in the heterokont alga vaucheria litorea (xanthophyceae) and its symbiotic molluskan partner elysia chlorotica (gastropoda)

Journal of Phycology

Volumn 48, Issue 2, 2012, Pages 373-383

  Soule, Kara M ^a   Rumpho, Mary E ^a  

^a UNIVERSITY OF MAINE   (United States)

Author keywords

Elysia chlorotica; Gene expression; Heterokont; Mollusk; Phosphoribulokinase; Photosynthesis; Plastid; Redox regulation; Symbiosis; Vaucheria litorea

Indexed keywords

ALGAE; ANIMALIA; ELYSIA CHLOROTICA; GASTROPODA; MOLLUSCA; OPISTHOBRANCHIA; VAUCHERIA LITOREA; XANTHOPHYCEAE;

EID: 84859430567     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2012.01111.x     Document Type: Article

References (80)

1. Allen, J. 2003. State transitions - a question of balance. Botany 299:1530-2.
2. Altschul, S. F., Gish, W., Miller, W., Meyers, E. W. & Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-10.
3. Ashby, M. K. & Houmard, J. H. 2006. Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution. Microbiol. Mol. Biol. Rev. 70:472-509.
4. Avilan, L., Gontero, B., Lebreton, S. & Ricard, J. 1997. Memory and imprinting effects in multienzyme complexes I. Isolation, dissociation, and reassociation of a phosphoribulokinase-glyceraldehyde-3-phosphate dehydrogenase complex from Chlamydomonas reinhardtii chloroplasts. Eur. J. Biochem. 246:78-84.
5. Avilan, L., Gontero, B., Lebreton, S. & Ricard, J. 2000. Thioredoxin activation of phosphoribulokinase in a bi-enzyme complex from Chlamydomonas reinhardtii chloroplasts. J. Biol. Chem. 275:9447-51.
6. Boggetto, N., Gontero, B. & Maberly, S. C. 2007. Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa. J. Phycol. 43:1227-35.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-54.
8. Buchanan, B. B. 1984. The ferredoxin/thioredoxin system: a key element in the regulatory function of light in photosynthesis. Bioscience 34:378-83.
9. 2 assimilation in oxygenic photosynthesis: the ferredoxin thioredoxin system. Perspective on its discovery, present status, and future development. Arch. Biochem. Biophys. 288:1-9.
10. Cattolico, R. A., Hariharan, T. & Johnson, P. J. 1998. Purification and characterization of phosphoribulokinase from the marine chromophytic alga Heterosigma carterae. Plant Physiol. 117:321-9.
11. Danon, A. & Mayfield, S. P. 1994a. Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266:1717-9.
12. Danon, A. & Mayfield, S. P. 1994b. ADP-dependent phosphorylation regulates RNA-binding in vitro: implications in light-modulated translation. EMBO J. 13:2227-35.
13. Doran, E. & Cattolico, R. A. 1997. Photoregulation of chloroplast gene transcription in the chromophytic alga Heterosigma carterae. Plant Physiol. 115:773-81.
14. Dunlap, J., Loros, J., Liu, Y. & Crosthwaite, S. 1999. Eukaryotica circadian systems: cycles in common. Cell 4:1-10.
15. Duplessis, M. R., Karol, K. G., Adman, E. T., Choi, L. Y. S., Jacobs, M. & Cattolico, R. A. 2007. Chloroplast His-to-Asp signal transduction: a potential mechanism for plastid gene regulation in Heterosigma akashiwo (Raphidophyceae). BMC Evol. Biol. 7:70.
16. Durnford, D. G., Price, J. A., McKim, S. M. & Sarchfield, M. L. 2003. Light-harvesting complex gene expression is controlled by both transcriptional and post-transcriptional mechanisms during photoacclimation in Chlamydomonas reinhardtii. Physiol. Plant. 118:193-205.
17. Escoubas, J. M., Lomas, M., LaRoche, J. & Falkowski, P. G. 1995. Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. U. S. A. 92:10237-41.
18. Gontero, B., Mulliert, G., Rault, M., Giudici-Orticoni, M. T. & Ricard, J. 1993. Structural and functional properties of a multi-enzyme complex from spinach chloroplasts. 2. Modulation of the kinetic properties of enzymes in the aggregated state. Eur. J. Biochem. 217:1075-82.
19. Goulard, F., Luning, K. & Jacobsen, S. 2004. Circadian rhythm of photosynthesis and concurrent oscillations of transcript abundance of photosynthetic genes in the marine red alga Grateloupia turuturu. Eur. J. Phycol. 39:431-7.
20. Graciet, E., Gans, P., Wedek, N., Lebreton, S., Camadro, J. M. & Gontero, B. 2003. The small protein CP12: a protein linker for supramolecular complex assembly. Biochemistry 42:8163-70.
21. Graves, D. A., Gibson, M. A. & Bleakney, J. S. 1979. The digestive diverticula of Alderia modesta and Elysia chlorotica. Veliger 21:415-22.
22. Green, B. J., Li, W.-Y., Manhart, J. R., Fox, T. C., Summer, E. J., Kennedy, R. A., Pierce, S. K. & Rumpho, M. E. 2000. Mollusc-algal chloroplast endosymbiosis: photosynthesis, thylakoid protein maintenance and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol. 124:331-42.
23. Gruber, A., Weber, T., Bartulos, C. R., Vugrinec, S. & Kroth, P. G. 2009. Intracellular distribution of the reductive and oxidative pentose phosphate pathways in two diatoms. J. Basic Microbiol. 49:58-72.
24. Hariharan, T., Johnson, P. J. & Cattolico, R. A. 1998. Purification and characterization of phosphoribulokinase from the marine chromophytic alga Heterosigma carterae. Plant Physiol. 117:321-9.
25. Hirasawa, M., Brandes, H. K., Hartman, F. C. & Knaff, D. B. 1998. Oxidation-reduction properties of the regulatory site of spinach phosphoribulokinase. Arch. Biochem. Biophys. 350:127-31.
26. Howard, T. P., Metodiev, M., Lloyd, J. C. & Raines, C. A. 2008. Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability. Proc. Natl. Acad. Sci. U. S. A. 105:4056-61.
27. Hwang, I., Chen, H. C. & Sheen, J. 2002. Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 129:500-15.
28. Imamura, A., Hanaki, N., Umeda, H., Makamura, A., Suzuki, A., Ueguchi, C. & Mizuno, T. 1998. Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 95:2691-6.
29. Ishizaki, Y., Tsunoyama, Y., Hatano, K., Ando, K., Kato, K., Shinmyo, A., Kobori, M., Takeba, G., Nakahira, Y. & Shiina, T. 2005. A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J. 42:133-44.
30. Iwasaki, H., Williams, S. B., Kitayama, Y., Ishiura, M., Golden, S. S. & Kondo, T. 2000. A kaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223-33.
31. Jacobs, M. A., Connell, L. & Cattolico, R. A. 1999. A conserved His-Asp signal response regulator-like gene in Heterosigma akashiwo. Plant Mol. Biol. 41:645-55.
32. Jacobsen, S., Luning, K. & Goulard, F. 2003. Circadian changes in relative abundance of two photosynthetic transcripts in the marine macroalga Kappaphycus alvarezii (Rhodophyta). J. Phycol. 39:888-96.
33. Jain, P. K., Kochhar, A., Khurana, J. P. & Tyagi, A. K. 1998. The psbO gene for 33-kDa precursor polypeptide of the oxygen-evolving complex in Arabidopsis thaliana- nucleotide sequence and control of its expression. DNA Res. 5:221-8.
34. Kanamaru, K., Nagashima, A., Fujiwara, M., Shimada, H., Shirano, Y., Nakabayashi, K., Shibata, D., Tanaka, K. & Takahashi, H. 2001. An Arabidopsis sigma factor (SIG2)-dependent expression of plastid-encoded tRNAs in chloroplasts. Plant Cell Physiol. 42:1034-43.
35. Kobayashi, D., Tamoi, M., Iwaki, T., Shigeoka, S. & Wadano, A. 2003. Molecular characterization and redox regulation of phosphoribulokinase from the cyanobacterium Synechococcus sp. PCC 7942. Plant Cell Physiol. 44:269-76.
36. Krause, K. & Krupinska, K. 2009. Nuclear regulators with a second home in organelles. Trends Plant Sci. 14:194-9.
37. Kroth, P. G., Chiovitti, A., Gruber, A., Martin-Jezequel, V., Mock, T., Parker, M. S., Stanley, M. S. et al. 2008. A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE 3:e1426.
38. Lebreton, S. & Gontero, B. 1999. Memory and imprinting in multienzyme complexes. Evidence for information transfer from glyceraldehyde-3-phosphate dehydrogenase to phosphoribulokinase under reduced state in Chlamydomonas reinhardtii. J. Biol. Chem. 274:20879-84.
39. Lebreton, S., Gontero, B., Avilan, L. & Ricard, J. 1997. Memory and imprinting effects in multienzyme complexes-II. Kinetics of the bienzyme complex from Chlamydomonas reinhardtii and hysteretic activation of chloroplast oxidized phosphoribulokinase. Eur. J. Biochem. 246:85-91.
40. Lemaire, S. D., Stein, M., Issakidis-Bourguet, E., Keryer, E., Benoit, V., Pineau, B., Gerard-Hirne, C., Miginiac-Maslow, M. & Jacquot, J. P. 1999. The complex regulation of ferredoxin/thioredoxin-related genes by light and the circadian clock. Planta 209:221-9.
41. Li, Z., Wakao, S., Fischer, B. B. & Niyogi, K. K. 2009. Sensing and responding to excess light. Annu. Rev. Plant Biol. 60:239-60.
42. Maberly, S. C., Courcelle, C., Groben, R. & Gontero, B. 2010. Phylogenetically-based variation in the regulation of the Calvin cycle enzymes, phosphoribulokinase and glyceraldehyde-3-phosphate dehydrogenase, in algae. J. Exp. Bot. 61:735-45.
43. Marri, L., Trost, P., Pupillo, P. & Sparla, F. 2005. Reconstitution and properties of the recombinant glyceraldehyde-3-phosphate dehydrogenase/CP12/phosphoribulokinase supramolecular complex of Arabidopsis. Plant Physiol. 139:1433-43.
44. Marri, L., Zaffagnini, M., Collin, V., Issakidis-Bourguet, E., Lemaire, S., Pupillo, P., Sparla, F., Miginiac-Maslow, M. & Trost, P. 2009. Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAP/CP12/PK supramolecular complex. Mol. Plant 2:259-69.
45. McClung, C. 2001. Circadian rhythms in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:139-62.
46. Michels, A. K., Wedel, N. & Kroth, P. G. 2005. Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway. Plant Physiol. 137:911-20.
47. Millar, A. & Kay, S. 1996. Integration of circadian and phototransduction pathways in the network controlling CB gene transcription in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 93:15491-6.
48. Moustafa, A., Beszteri, B., Maier, U. G., Bowler, C., Valentin, K. & Bhattacharya, D. 2009. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724-6.
49. Mujer, C. V., Andrew, D. L., Manhart, J. R., Pierce, S. K. & Rumpho, M. E. 1996. Chloroplast genes are expressed during the intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc. Natl. Acad. Sci. U. S. A. 93:12333-8.
50. Oelmüller, R., Schneiderbauer, A., Herrmann, R. G. & Kloppstech, K. 1995. The steady-state mRNA levels for thylakoid proteins exhibit coordinate diurnal regulation. Mol. Gen. Genet. 246:478-84.
51. Oesterhelt, C., Klocke, S., Holtgrefe, S., Linke, V., Weber, A. P. M. & Scheibe, R. N. 2007. Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution. Plant Cell Physiol. 48:1359-73.
52. Petersen, J., Teich, R., Brinkmann, H. & Cerff, R. 2006. A "green" phosphoribulokinase in complex algae with red plastids: evidence for a single secondary endosymbiosis leading to haptophytes, cryptophytes, heterokonts and dinoflagellates. J. Mol. Evol. 62:143-57.
53. Pfannschmidt, T., Nilsson, A. & Allen, J. F. 1999. Photosynthetic control of chloroplast gene expression. Nature 397:625-8.
54. Pierce, S. K., Biron, R. W. & Rumpho, M. E. 1996. Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J. Exp. Biol. 199:2323-30.
55. Pierce, S. K., Curtis, N. E., Hanten, J. J., Boerner, S. L. & Schwartz, J. A. 2007. Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 43:57-64.
56. Pierce, S. K., Curtis, N. E. & Schwartz, J. A. 2009. Chlorophyll a synthesis by an animal using transferred algal nuclear genes. Symbiosis 49:121-31.
57. Pierce, S. K., Fang, X., Schwartz, J. A., Jiang, X., Zhao, W., Curtis, N. E., Kocot, K., Yang, B. & Wang, J. 2011. Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol Biol Evol. [Epub ahead of print].
58. Pohlmeyer, K., Papp, B. K., Soll, J. & Wedel, N. 1996. CP12: a small nuclear-encoded chloroplast protein provides novel insights into higher-plant GAPDH evolution. Plant Mol. Biol. 32:969-78.
59. Porter, M. A., Stringer, C. D. & Hartman, F. C. 1988. Characterization of the regulatory thioredoxin site of phosphoribulokinase. J. Biol. Chem. 263:123-9.
60. Puthiyaveetil, S. & Allen, J. 2008. Transients in chloroplast gene transcription. Biochem. Biophys. Res. Commun. 368:871-4.
61. Puthiyaveetil, S. & Allen, J. F. 2009. Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression. Proc. R. Soc. Biol. Sci. Ser. B 276:2133-45.
62. Puthiyaveetil, S., Kavanagh, T. A., Cain, P., Sullivan, J. A., Newell, C. A., Gray, J. C., Robinson, C., van der Glezen, M., Rogers, M. B. & Allen, J. F. 2008. The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 105:10061-6.
63. Rintamaki, E., Martinsuo, P., Pursiheimo, S. & Aro, E. M. 2000. Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferrodoxin-thioredoxin system in chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 97:11644-9.
64. Rochaix, J. D. 2007. Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett. 581:2768-75.
65. Rumpho, M. E., Pochareddy, S., Worful, J. M., Summer, E. J., Bhattacharya, D., Pelletreau, K. N., Tyler, M. S., Lee, J., Manhart, J. R. & 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 2:1384-96.
66. Rumpho, M. E., Summer, E. J., Green, B. J., Fox, T. C. & Manhart, J. R. 2001. Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus? Zoology 104:303-12.
67. Rumpho, M. E., Worful, J. M., Lee, J., Kannan, K., Tyler, M. S., Bhattacharya, D., Moustafa, A. & Manhart, J. R. 2008. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc. Natl. Acad. Sci. U. S. A. 105:17867-71.
68. Scheibe, R. N., Wedel, N., Vetter, S., Emmerlich, V. & Sauermann, S. M. 2002. Co-existence of two regulatory NADP-glyceraldehyde 3-P dehydrogenase complexes in higher plant chloroplasts. Eur. J. Biochem. 269:5617-24.
69. Schwartz, J. A., Curtis, N. E. & Pierce, S. K. 2010. Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evol. Biol. 37:29-37.
70. Stockel, J., Welsh, E., Liberton, M., Kunnvakkam, R., Aurora, R. & Pakrasi, H. 2008. Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. Proc. Natl. Acad. Sci. U. S. A. 105:6156-61.
71. Tamoi, M., Miyazaki, T., Fukamizo, T. & Shigeoka, S. 2005. The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant J. 42:504-13.
72. Tamoi, M., Murakami, A., Takeda, T. & Shigeoka, S. 1998. Lack of light/dark regulation of enzymes involved in the photosynthetic carbon reduction cycle in cyanobacteria, Synechococcus PCC 7942 and Synechocystis PCC 6803. Biosci. Biotechnol. Biochem. 62:374-6.
73. Taylor, W. 1989. Regulatory interactions between nuclear and plastid genomes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:211-33.
74. Wagner, R. & Pfannschmidt, T. 2006. Eukaryotic transcription factors in plastids - bioinformatic assessment and implications for the evolution of gene expression machineries in plants. Gene 381:62-70.
75. Waters, M. T., Wang, P., Korkaric, M., Capper, R. G., Saunders, N. J. & Langdale, J. A. 2009. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21:1109-28.
76. Wedel, N. & Soll, J. 1998. Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/glyceraldehyde-3-phosphate dehydrogenase complex dissociation. Proc. Natl. Acad. Sci. U. S. A. 95:9699-704.
77. Wedel, N., Soll, J. & Paap, B. K. 1997. CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc. Natl. Acad. Sci. U. S. A. 94:10479-84.
78. Wenderoth, I., Scheibe, R. N. & von Schaewen, A. 1997. Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J. Biol. Chem. 272:26985-90.
79. Woodson, J. & Chory, J. 2008. Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. 9:383-95.
80. Young, M. & McKay, S. 2001. Time zones: a comparative genetics of circadian systems. Nat. Rev. Genet. 2:702-15.