Metabolic acclimation to excess light intensity in Chlamydomonas reinhardtii

Plant, Cell and Environment

Volumn 36, Issue 7, 2013, Pages 1391-1405

  Davis, Maria C ^a   Fiehn, Oliver ^b   Durnford, Dion G ^a  

^a UNIVERSITY OF NEW BRUNSWICK   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Light stress; Metabolomics; Photoacclimation; Photorespiration

Indexed keywords

ACCLIMATION; AMINO ACID; ENZYME; GREEN ALGA; GROWTH RATE; LIGHT INTENSITY; MASS SPECTROMETRY; METABOLISM; METABOLITE; NUCLEAR MAGNETIC RESONANCE; PRINCIPAL COMPONENT ANALYSIS;

CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA;

ALCOHOL DEHYDROGENASE; ALGAL PROTEIN; AMINO ACID; GLYCOLIC ACID DEHYDROGENASE; MALATE SYNTHASE; NITROGEN;

ACCLIMATIZATION; CHEMISTRY; CHLAMYDOMONAS REINHARDTII; GENE EXPRESSION REGULATION; GENETICS; LIGHT; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; METABOLISM; METABOLOMICS; MITOCHONDRION; NUCLEAR MAGNETIC RESONANCE; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; RADIATION RESPONSE;

ACCLIMATIZATION; ALCOHOL OXIDOREDUCTASES; ALGAL PROTEINS; AMINO ACIDS; CHLAMYDOMONAS REINHARDTII; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION REGULATION, PLANT; LIGHT; MALATE SYNTHASE; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MITOCHONDRIA; NITROGEN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOTOSYNTHESIS; STRESS, PHYSIOLOGICAL;

EID: 84878655763     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12071     Document Type: Article

References (97)

1. Allen A.E., Dupont C.L., Obornik M., etal. (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473, 203-207.
2. Anderson J.M., Chow W.S. & Park Y.I. (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynthesis Research 46, 129-139.
3. Barker M. & Rayens W. (2003) Partial least squares for discrimination. Journal of Cheometrics 17, 166-173.
4. van den Berg R.A., Hoefsloot H.C.J., Westerhuis J.A., Smilde A.K. & van der Werf M.J. (2006) Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genomics 7, 142-156.
5. Bloom A. (2010) Assimilation of Mineral nutrients. In Plant Physiology (eds L. Taiz & E. Ziger ) 5th edn, pp. 343-368. Sinauer Associates Inc., Publishers, Sunderland, MA, USA.
6. Bölling C. & Fiehn O. (2005) Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiology 139, 1995-2005.
7. Brautigam A., Gagneul D. & Webber A. (2007) High-throughput colorimetric method for the parallel assay of glyoxylic acid and ammonium in a single extract. Analytical Biochemistry 362, 151-153.
8. Brown T.J. & Geen G.H. (1974) The effect of light quality on the carbon metabolism and extracellular release of Chlamydomonas reinhardtii Dangeard. Journal of Phycology 10, 213-220.
9. Brychkova G., Alikulov Z., Fluhr R. & Sagi M. (2008) A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. The Plant Journal 54, 496-509.
10. Codd G.A. & Merrett M.J. (1971) The regulation of glycolate metabolism in division synchronized cultures of Euglena. Plant Physiology 47, 640-643.
11. Coruzzi G. & Last R. (2000) Amino acids. In Biochemistry and Molecular Biology of Plants (eds R.B. Buchanan, W. Gruissem & R. Jones ), pp. 358-410. American Society of Plant Physiology Press, Rockville, MD, USA.
12. Cullimore J.V. & Sims A.P. (1980) An association between photorespiration and protein catabolism: studies with Chlamydomonas. Planta 150, 392-396.
13. Cuperlovic-Culf M., Barnett D.A., Culf A.S. & Chute I. (2010) Cell culture metabolomics: applications and future directions. Drug Discovery Today 15, 610-621.
14. Demming-Adams B. & Adams W.W. (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Science 1, 21-26.
15. 1H NMR metabonomics. Analytical Chemistry 78, 4281-4290.
16. Dietz K.J. & Heber U. (1984) Rate limiting factors in leaf photosynthesis: I. Carbon fluxes in the Calvin cycle. Biochimica et Biophysica Acta 767, 432-443.
17. Doebbe A., Keck M., La Russa M., Mussgnug J.H., Hankamer B., Tekce E., Niehaus K. & Kruse O. (2010) The interplay of proton, electron, and metabolite supply for photosynthetic H-2 production in Chlamydomonas reinhardtii. Journal of Biological Chemistry 285, 30247-30260.
18. Douce R. & Heldt H.W. (2000) Photorespiration. In Advances in Photosynthesis, Photosynthesis: Physiology and Metabolism (eds R.C. Leegood, T.D. Sharkey & S. von Caemmerer ), pp. 115-136. Kluwer Academic Publishers, Dordrecht, Netherlands.
19. 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. Physiologia Plantarum 118, 193-205.
20. Eriksson L., Johansson E., Kettaneh-Wold N., Trygg J., Wikström C. & Wold S. (2006) Multi-and Megavariate Data Analysis 2nd Ed. Part 1 - Basic Principles and Applications. Umetrics AB, Umeå, Sweden.
21. Fernandez E., Llamas A. & Galvan A. (2009) Nitrogen Assimilation and its regulation. In The Chlamydomonas Soucebook 2nd Ed. Volume 2: Organellar and Metabolic Processes (ed. D. Stein ), pp. 69-113. Academic Press, Burlington, MA, USA.
22. Fiehn O. (2003) Metabolic networks of Cucurbita maxima phloem. Phytochemistry 62, 875-886.
23. Fiehn O., Wohlgemuth G. & Scholz M. (2005) Setup and annotation of metabolomic experiments by integrating biological and mass spectrometric metadata. Data Intergration in the Life Sciences: Lecture Notes in Computer Science 3615, 224-239.
24. Finazzi G., Barbagallo R.P., Bergo E., Barbato R. & Forti G. (2001) Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2: damages to the photosynthetic apparatus under linear and cyclic electron flow. Journal of Biological Chemistry 276, 22251-22257.
25. Foyer C.H. & Noctor G. (2002) Photosynthetic nitrogen assimilation: inter-pathway control and signaling. In Advances in Photosynthesis and Respiration Vol. 12: Photosynthetic Nitrogen Assimilation and Associated Carbon and Respiratory Metabolism (eds C.H. Foyer & G. Noctor ), pp. 1-22. Kluwer Academic Publishers, Dordrecht, Netherlands.
26. Foyer C.H., Noctor G. & Hodges M. (2011) Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. Journal of Experimental Botany 62, 1467-1482.
27. Fujita Y., Iwama Y., Ohki K., Murakami A. & Hagiwara N. (1989) Regulation of the size of light-harvesting antennae in response to light intensity in the green alga Chlorella pyrenoidosa. Plant and Cell Physiology 30, 1029-1037.
28. Graham I.A., Denby K.J. & Leaver C.J. (1994) Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. The Plant Cell 6, 761-772.
29. Greenberg B.M., Gaba V., Mattoo A.K. & Edelman M. (1987) Identification of a primary in vivo degradation product of the rapidly turning-over 32kD protein of photosystem II. EMBO Journal 6, 2865-2869.
30. Hare P.D. & Cress W.A. (1997) Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regulation 21, 79-102.
31. Hare P.D., Cress W.A. & Van Staden J. (1998) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535-553.
32. Harris E.H. (2009) Chlamydomonas in the laboratory. In The Chlamydomonas Sourcebook (ed. E.H. Harris ) 2nd edn, Vol. 1, pp. 241-302. Academic Press, Burlington, MA, USA.
33. Heber U., Bligny R., Streb P. & Douce R. (1996) Photorespiration is essential for the protection of the photosynthetic apparatus of C3 plants against photoinactivation under sunlight. Botanica Acta 109, 307-315.
34. Hellebust J.A. (1965) Excretion of some organic compounds by marine phytoplankton. Limnology and Oceanography 10, 192-206.
35. Hoefnagel M.H.N., Atkin O.K. & Wiskich J.T. (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochimica et Biophysica Acta: Bioenergetics 1366, 235-255.
36. Humby P.L. & Durnford D.G. (2006) Photoacclimation: physiological and molecular responses to changes in light environments. In Plant-Environment Interactions (ed. B. Huang ) 3rd edn, pp. 69-99. CRC Press, New York, USA.
37. Humby P.L., Cunningham M.L., Saunders H.L., Price J.A. & Durnford D.G. (2009) Compartmental cross-talk in the regulation of light harvesting complex transcription under short-term light and temperature stress in Chlamydomonas reinhardtii. Botany 87, 375-386.
38. Im C.S. & Grossman A.R. (2001) Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. The Plant Journal 30, 301-313.
39. Jeener J., Meier B.H., Bachmann P. & Ernst R.R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy. Journal of Chemical Physics 71, 4546-4553.
40. Jennings D.H. & Burke R.M. (1990) Compatible solutes-the mycological dimension and their role as physiological buffering agents. New Phytologist 116, 277-283.
41. Kind T., Wohlgemuth G., Lee D.Y., Lu L., Palazoglu M., Shahbaz S. & Fiehn O. (2009) FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Analytical Chemistry 81, 10038-10048.
42. Kozaki A. & Takeba G. (1996) Photorespiration protects C3 plants from photooxidation. Nature 384, 557-560.
43. Ledford H.K., Baroli I., Shin J.W., Fischer B.B., Eggen R.I.L. & Niyogi K.K. (2004) Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas reinhardtii. Molecular Genetics and Genomics 272, 470-479.
44. Lee D.Y. & Fiehn O. (2008) High quality metabolomic data for Chlamydomonas reinhardtii. Plant Methods 4, 7-19.
45. Leegood R.C., Lea P.J., Adcock M.D. & Hausler R.E. (1995) The regulation and control of photorespiration. Journal of Experimental Botany 46, 1397-1414.
46. Lewin R.A. (1956) Extracellular polysaccharides of green algae. Canadian Journal of Microbiology 2, 665-672.
47. Li Z., Wakao S., Fischer B.B. & Niyogi K.K. (2009) Sensing and responding to excess light. Annual Reviews in Plant Biology 60, 239-260.
48. van Lis R. & Atteia A. (2004) Control of mitochondrial function via photosynthetic redox signals. Photosynthesis Research 79, 133-148.
49. Loescher W.H. & Everard J.D. (2000) Regulation of sugar alcohol biosynthesis. In Advances in Photosynthesis, Photosynthesis: Physiology and Metabolism (eds R.C. Leegood, T.D. Sharkey & S. von Caemmerer ), pp. 275-299. Kluwer Academic Publishers, Dordrecht, Netherlands.
50. McKim S. & Durnford D.G. (2006) Translational regulation of light-harvesting complex expression during photoacclimation to high-light in Chlamydomonas reinhardtii. Plant Physiology and Molecular Biology 44, 857-865.
51. Matsuo M. & Obokata J. (2006) Remote control of photosynthetic genes by the mitochondrial respiratory chain. The Plant Journal 47, 873-882.
52. Moroney J.V., Wilson B.J. & Tolbert N.E. (1986) Glycolate metabolism and excretion by Chlamydomonas reinhardtii. Plant Physiology 82, 821-826.
53. Nakamura Y., Kanakagiri S., Van K., He W. & Spalding M.H. (2005) Disruption of the glycolate dehydrogenase gene in the high-CO2-requiring mutant HCR89 of Chlamydomonas reinhardtii. Canadian Journal of Botany 83, 820-832.
54. Nalewajko C. (1966) Photosynthesis and excretion in various plankton algae. Limnology and Oceanography 11, l-10.
55. Nelson E.B. & Tolbert N.E. (1969) The regulations of glycolate metabolism in Chlamydomonas reinhardtii. Biochimica et Biophysica Acta 184, 263-270.
56. Nelson E.B. & Tolbert N.E. (1970) Glycolate dehydrogenase in green algae. Archives of Biochemistry and Biophysics 141, 102-110.
57. Niyogi K.K. (1999) Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50, 333-359.
58. Noctor G., Dutilleul C., De Paepe R. & Foyer C.H. (2004) Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. Journal of Experimental Botany 55, 49-57.
59. Nogales J., Guijo M.I., Quesada A. & Merchan F. (2004) Functional analysis and regulation of malate synthase from Chlamydomonas reinhardtii. Planta 219, 325-331.
60. Novitskaya L., Trevanion S., Driscoll S.D., Foyer C.H. & Noctor G. (2002) How does photorespiration modulate leaf amino acid contents? A dual approach through modeling and metabolite analysis. Plant, Cell & Environment 25, 821-835.
61. Nunes-Nesi A., Fernie A.R. & Stitt M. (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Molecular Plant 3, 973-996.
62. Osmond C.B. & Grace S.C. (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? Journal of Experimental Botany 46, 1351-1362.
63. Parry M.A.J., Madgwick P.J., Carvalho J.F.C. & Andralojc P.J. (2007) Prospects for increasing photosynthesis by overcoming the limitations of Rubisco. Journal of Agricultural Science 145, 31-43.
64. Peterhansel C., Blume C. & Offermann S. (2013) Photorespiratory bypasses: how can they work? Journal of Experimental Botany 64, 709-715.
65. Pfaffl M.W., Horgan G.W. & Dempfle L. (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36.
66. Pineda M., Fernandez E. & Cardenas J. (1984) Urate oxidase of Chlamydomonas reinhardtii. Physiologia Plantarum 62, 453-457.
67. Porra R.J., Thompson W.A. & Kriedemann P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384-394.
68. Post A.F., Dubinsky Z., Wyman K. & Falkowski P.G. (1985) Physiological responses of a marine planktonic diatom to transition in growth irradiance. Marine Ecology Progress Series 25, 141-149.
69. Raghavendra A.S. & Padmasree K. (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends in Plant Science 8, 546-553.
70. 2 in Chlamydomonas reinhardtii. Plant Physiology 154, 187-196.
71. Ruijter J.M., Ramakers C., Hoogaars W.M.H., Karlen Y., Bakker O., van den Hoff M.J.B. & Moorman A.F.M. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45.
72. Schuster G., Timberg R. & Ohad I. (1988) Turnover of photosystem II proteins during photoinhibition of Chlamydomonas reinhardtii. European Journal of Biochemistry 177, 403-410.
73. Shapira M., Lers A., Heifetz P.B., Irihimovitz V., Osmond C.B., Gillham N.W. & Boynton J.E. (1997) Differential regulation of chloroplast gene expression in Chlamydomonas reinhardtii during photoacclimation: light stress transiently suppresses synthesis of the Rubisco LSU protein while enhancing synthesis of the PS II D1 protein. Plant Molecular Biology 33, 1001-1011.
74. Sharp J.H. (1977) Excretion of organic matter by marine phytoplankton: do healthy cells do it? Limnolology and Oceanography 22, 381-399.
75. Smirnoff N. & Cumbes Q.J. (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057-1060.
76. Stitt M., Sulpice R. & Keurentjes J. (2010) Metabolic networks: how to identify key components in the regulation of metabolism and growth. Plant Physiology 152, 428-444.
77. Szabados L. & Savouré A. (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89-97.
78. Takahashi S., Bauwe H. & Badger M. (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair process and not acceleration of damage process in Arabidopsis thaliana. Plant Physiology 144, 487-494.
79. Thomas J.E., Goertzen C.A. & Nakamura K. (1991) Heterogeneity in endogenous amino acid pools of Chlamydomonas reinhardtii and C. eugametos. Canadian Journal of Botany 69, 1194-1198.
80. Thrippleton M.J. & Keeler J. (2003) Elimination of zero-quantum interference in two-dimensional NMR spectra. Angewandte Chemie International Edition 42, 3938-3941.
81. 2 production by sulfur depletion. Journal of Experimental Botany 60, 1691-1702.
82. Tolbert N.E., Harrsion M. & Selph N. (1983) Aminooxyacetate stimulation of glycolate formation and excretion by Chlamydomonas. Plant Physiology 72, 1075-1083.
83. Tural B. & Moroney J.V. (2004) Regulation of the expression of photorespiratory genes in Chlamydomonas reinhardtii. Canadian Journal of Botany 83, 810-819.
84. Urzica E.I., Adler L.N., Page M.D., Linster C.L., Arbing M.A., Casero D., Pellegrini M., Merchant S.S. & Clarke S.G. (2012) Impact of oxidative stress on ascorbate biosynthesis in Chlamydomonas via regulation of the VTC2 gene encoding a GDP-L-galactose phosphorylase. Journal of Biological Chemistry 287, 14234-14245.
85. Vallon O. & Spalding M.H. (2009) Amino acid metabolism. In The Chlamydomonas Soucebook 2nd Ed. Volume 2: Organellar and Metabolic Processes (eds E. Harris & D. Stein ), pp. 115-158. Academic Press, Burlington, MA, USA.
86. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. & Speleman F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, 0034.1-0034.11.
87. Vierling E. & Alberte R.S. (1980) Functional organization and plasticity of the photosynthetic unit of the cyanobacterium Anacystis nidulans. Physiologia Plantarum 50, 93-98.
88. Waring W.S., Convery A., Mishra V., Shenkin A., Webb D.J. & Maxwell S.R.J. (2003) Uric acid reduces exercise-induced oxidative stress in healthy adults. Clinical Science 105, 425-430.
89. Wayner D.D.M., Burton G.W., Ingold K.U., Barclay L.R.C. & Locke S.J. (1987) The relative contributions of vitamin E, urate, ascorbate and proteins to the total peroxyl radical-trapping antioxidant activity of human blood plasma. Biochimica et Biophysica Acta 924, 408-419.
90. Webb M.R. & Melis A. (1995) Chloroplast response to irradiance stress. Plant Physiology 107, 885-893.
91. Wingler A., Lea P.J., Quick W.P. & Leegood R.C. (2000) Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1517-1529.
92. Wollman F.A. (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO Journal 20, 3623-3630.
93. Wood A.M., Everroad R.C. & Wingard L.M. (2005) Measuring growth rates in microalgal cultures. In Algal Culturing Techniques (ed. R.A. Andersen ), pp. 269-286. Elsevier, New York, USA.
94. Wulff-Zottele C., Gatzka N., Kopka J., Orellana A., Hoefgen R., Fisahn J. & Holger H. (2010) Photosynthesis and metabolism interact during acclimation of Arabidopsis thaliana to high irradiance and sulphur depletion. Plant, Cell & Environment 33, 1974-1988.
95. Xia J. & Wishart D.S. (2010) MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics 26, 2342-2344.
96. Xia J., Psychogios N., Young N. & Wishart D.S. (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Research 37, W652-W660.
97. Yang D.H., Webster J., Adam Z., Lindahl M. & Andersson B. (1998) Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiology 118, 827-834.