The regulation of photosynthetic structure and function during nitrogen deprivation in Chlamydomonas reinhardtii

Plant Physiology

Volumn 167, Issue 2, 2015, Pages 558-573

  Juergens, Matthew T ^a   Deshpande, Rahul R ^a   Lucker, Ben F ^a   Park, Jeong Jin ^b   Wang, Hongxia ^c,d   Gargouri, Mahmoud ^b   Omar Holguin, F ^e   Disbrow, Bradley ^a   Schaub, Tanner ^e   Skepper, Jeremy N ^f   Kramer, David M ^a   Gang, David R ^b   Hicks, Leslie M ^c,g   Shachar Hill, Yair ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^d NATIONAL CENTER OF BIOMEDICAL ANALYSIS   (China)

^e NEW MEXICO STATE UNIVERSITY   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; CHLAMYDOMONAS REINHARDTII;

CARBON; CHLOROPHYLL; LIPID; MESSENGER RNA; NITROGEN; OXYGEN; PHOTOSYSTEM I; STARCH; VEGETABLE PROTEIN;

BIOSYNTHESIS; CARBON CYCLE; CHLAMYDOMONAS REINHARDTII; DEFICIENCY; DOWN REGULATION; ENERGY METABOLISM; FLUORESCENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHYSIOLOGY; PROTON MOTIVE FORCE; THYLAKOID; ULTRASTRUCTURE;

CARBON CYCLE; CARBON ISOTOPES; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; DOWN-REGULATION; ENERGY METABOLISM; FLUORESCENCE; GENE EXPRESSION REGULATION, PLANT; LIPIDS; NITROGEN; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PLANT PROTEINS; PROTON-MOTIVE FORCE; RNA, MESSENGER; STARCH; THYLAKOIDS;

EID: 84921959705     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.250530     Document Type: Article

References (122)

1. Allen MM, Smith AJ (1969) Nitrogen chlorosis in blue-green algae. Arch Mikrobiol 69: 114-120
2. Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106: 47-56
3. Alvarez S, Hicks LM, Pandey S (2011) ABA-dependent and -independent G-protein signaling in Arabidopsis roots revealed through an iTRAQ proteomics approach. J Proteome Res 10: 3107-3122
4. Atabani AE, Silitonga AS, Badruddin IA, Mahlia TMI, Masjuki HH, Mekhilef S (2012) A comprehensive review on biodiesel as an alternative energy resource and its characteristics. Renew Sustain Energy Rev 16: 2070-2093
5. Avenson TJ, Cruz JA, Kanazawa A, Kramer DM (2005) Regulating the proton budget of higher plant photosynthesis. Proc Natl Acad Sci USA 102: 9709-9713
6. Bailleul B, Cardol P, Breyton C, Finazzi G (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth Res 106: 179-189
7. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89-113
8. Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30: 1107-1125
9. 2 accumulating mechanism in Chlorella emersonii. J Exp Bot 33: 729-737
10. Beardall J, Roberts S, Millhouse J (1991) Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1,5-bisphosphate carboxylase oxygenase in green microalgae. Canadian Journal of Botany- Revue Canadienne De Botanique 69: 1146-1150
11. Benning C (2010) The anionic chloroplast membrane lipids: phosphatidylglycerol and sulfoquinovosyldiacylglycerol. In CA Rebeiz, C Benning, HJ Bohnert, H Daniell, JK Hoober, HK Lichtenthaler, AR Portis, BC Tripathy, eds, Chloroplast: Basics and Applications, Vol 31. Springer, Dordrecht, The Netherlands, pp 171-183
12. Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110: 689-696
13. Blaby IK, Glaesener AG, Mettler T, Fitz-Gibbon ST, Gallaher SD, Liu B, Boyle NR, Kropat J, Stitt M, Johnson S, et al (2013) Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25: 4305-4323
14. Bölling C, Fiehn O (2005) Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol 139: 1995-2005
15. Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008) The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84: 1359-1370
16. Boudière L, Michaud M, Petroutsos D, Rébeillé F, Falconet D, Bastien O, Roy S, Finazzi G, Rolland N, Jouhet J, et al (2013) Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta 1837: 470-480
17. Britton G, Liaaen-Jensen S, Pfander H (2009) Carotenoids Volume 5. Nutr Health 5: 409-422
18. Cardol P, Bailleul B, Rappaport F, Derelle E, Béal D, Breyton C, Bailey S, Wollman FA, Grossman A, Moreau H, et al (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci USA 105: 7881-7886
19. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25: 294-306
20. Coleman JR, Berry JA, Togasaki RK, Grossman AR (1984) Identification of extracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 76: 472-477
21. Collier JL, Grossman AR (1992) Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacteriol 174: 4718-4726
22. de Vitry C, Olive J, Drapier D, Recouvreur M, Wollman FA (1989) Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii. J Cell Biol 109: 991-1006
23. Dent RM, Han M, Niyogi KK (2001) Functional genomics of plant photosynthesis in the fast lane using Chlamydomonas reinhardtii. Trends Plant Sci 6: 364-371
24. Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575
25. Dong HP, Williams E, Wang DZ, Xie ZX, Hsia RC, Jenck A, Halden R, Li J, Chen F, Place AR (2013) Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol 162: 1110-1126
26. Fan J, Yan C, Andre C, Shanklin J, Schwender J, Xu C (2012) Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol 53: 1380-1390
27. Feng X, Tang KH, Blankenship RE, Tang YJ (2010) Metabolic flux analysis of the mixotrophic metabolisms in the green sulfur bacterium Chlorobaculum tepidum. J Biol Chem 285: 39544-39550
28. Fischer BB, Dayer R, Schwarzenbach Y, Lemaire SD, Behra R, Liedtke A, Eggen RI (2009) Function and regulation of the glutathione peroxidase homologous gene GPXH/GPX5 in Chlamydomonas reinhardtii. Plant Mol Biol 71: 569-583
29. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509
30. Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7: 270-276
31. Geider RJ, Macintyre HL, Graziano LM, McKay RML (1998) Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur J Phycol 33: 315-332
32. Geiger DR, Servaites JC (1994) Diurnal regulation of photosynthetic carbon metabolism in C-3 plants. Annu Rev Plant Physiol Plant Mol Biol 45: 235-256
33. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92
34. Gilmore AM, Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35: 67-78
35. Goodenough U, Blaby I, Casero D, Gallaher SD, Goodson C, Johnson S, Lee JH, Merchant SS, Pellegrini M, Roth R, et al (2014) The path to triacylglyceride obesity in the sta6 strain of Chlamydomonas reinhardtii. Eukaryot Cell 13: 591-613
36. Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 54: 1665-1669
37. Granum E, Kirkvold S, Myklestad SM (2002) Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar Ecol Prog Ser 242: 83-94
38. Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151: 201-224
39. Grossman AR, Gonzalez-Ballester D, Shibagaki N, Pootakham W, Moseley J, Pootakham W (2010) Responses to macronutrient deprivation. In A Pareek, SK Sopory, HJ Bohnert, X Govindjee, eds. Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation. Springer, NY, pp 307-348
40. Hall C, Cruz J, Wood M, Zegara R, De Mars D, Carpenter J, Kanazawa ADK (2011) Photosynthesis: Research for Food, Fuel and Future. 15th International Conference on Photosynthesis. Zhejiang University Press, Beijing, pp 184-188
41. Harris EH, Stern DB, Witman GB, editors (2009) The Chlamydomonas Sourcebook, Vol. 2. Elsevier, Oxford, UK, pp 1-1071
42. He R, Kim MJ, Nelson W, Balbuena TS, Kim R, Kramer R, Crow JA, May GD, Thelen JJ, Soderlund CA, et al (2012) Next-generation sequencingbased transcriptomic and proteomic analysis of the common reed, Phragmites australis (Poaceae), reveals genes involved in invasiveness and rhizome specificity. Am J Bot 99: 232-247
43. Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49: 511-523
44. Hill R, Larkum AWD, Prasil O, Kramer DM, Szabo M, Kumar V, Ralph PJ (2012) Light-induced dissociation of antenna complexes in the symbionts of scleractinian corals correlates with sensitivity to coral bleaching. Coral Reefs 31: 963-975
45. Holguin FO, Schaub T (2013) Characterization of microalgal lipid feedstock by direct-infusion FT-ICR mass spectrometry. Algal Research 2: 43-50
46. Horton P, Ruban AV, Walters RG (1994) Regulation of light harvesting in green plants (indication by nonphotochemical quenching of chlorophyll fluorescence). Plant Physiol 106: 415-420
47. Houille-Vernes L, Rappaport F, Wollman FA, Alric J, Johnson X (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. ProcNatl Acad SciUSA 108: 20820- 20825
48. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54: 621-639
49. Iwai M, Takahashi Y, Minagawa J (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20: 2177-2189
50. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817: 182-193
51. Jamers A, Blust R, De Coen W (2009) Omics in algae: paving the way for a systems biological understanding of algal stress phenomena? Aquat Toxicol 92: 114-121
52. Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuiné S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. ProcNatl Acad Sci USA 105: 20546-20551
53. Jarvis P, Dörmann P, Peto CA, Lutes J, Benning C, Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97: 8175-8179
54. Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 287: 26445-26452
55. Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot Cell 12: 776-793
56. Johnson X, Steinbeck J, Dent RM, Takahashi H, Richaud P, Ozawa S, Houille-Vernes L, Petroutsos D, Rappaport F, Grossman AR, et al (2014) Proton gradient regulation 5-mediated cyclic electron flow under ATP- or redox-limited conditions: a study of ΔATpase pgr5 and ΔrbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol 165: 438-452
57. Jones MR (2007) Lipids in photosynthetic reaction centres: structural roles and functional holes. Prog Lipid Res 46: 56-87
58. Klein U (1987) Intracellular carbon partitioning in Chlamydomonas reinhardtii. Plant Physiol 85: 892-897
59. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of Q(A) redox state and excitation energy fluxes. Photosynth Res 79: 209-218
60. Lee Y, Park JJ, Barupal DK, Fiehn O (2012) System response of metabolic networks in Chlamydomonas reinhardtii to total available ammonium. Mol Cell Proteomics 11: 973-988
61. Leng J, Sakurai I, Wada H, Shen JR (2008) Effects of phospholipase and lipase treatments on photosystem II core dimer from a thermophilic cyanobacterium. Photosynth Res 98: 469-478
62. Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo MH, Benning C (2012) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24: 4670-4686
63. Li Y, Han D, Hu G, Sommerfeld M, Hu Q (2010) Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 107: 258-268
64. Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24: 300-309
65. Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM (2010) An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef) involving the NADPH dehydrogenase complex. Plant Cell 22: 221-233
66. Lohr M (2009) Carotenoids. In D Stern, G Witman, EH Harris, eds, The Chlamydomonas Sourcebook, Ed 2. Academic Press, London, pp 799- 817
67. Longworth J, Noirel J, Pandhal J, Wright PC, Vaidyanathan S (2012) HILIC- and SCX-based quantitative proteomics of Chlamydomonas reinhardtii during nitrogen starvation induced lipid and carbohydrate accumulation. J Proteome Res 11: 5959-5971
68. Lucker B, Kramer DM (2013) Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability. Photosynth Res 117: 449-459
69. Martin NC, Goodenough UW (1975) Gametic differentiation in Chlamydomonas reinhardtii. I. Production of gametes and their fine structure. J Cell Biol 67: 587-605
70. Maruyama S, Tokutsu R, Minagawa J (2014) Transcriptional regulation of the stress-responsive light harvesting complex genes in Chlamydomonas reinhardtii. Plant Cell Physiol 55: 1304-1310
71. Merchant SS, Helmann JD (2012) Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Physiol 60: 91-210
72. Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2012) TAG, you're it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23: 352-363
73. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250
74. Miller R, Wu G, Deshpande RR, Vieler A, Gärtner K, Li X, Moellering ER, Zäuner S, Cornish AJ, Liu B, et al (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154: 1737-1752
75. Mizusawa N, Wada H (2012) The role of lipids in photosystem II. Biochim Biophys Acta 1817: 194-208
76. Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21: 6709-6720
77. Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75: 50-59
78. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558-1566
79. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361-371
80. Murakami A (1997) Quantitative analysis of 77K fluorescence emission spectra in Synechocystis sp. PCC 6714 and Chlamydomonas reinhardtii with variable PS I/PS II stoichiometries. Photosynth Res 53: 141-148
81. Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20: 3148-3162
82. Nguyen HM, Baudet M, Cuiné S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, et al (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11: 4266-4273
83. Niyogi KK, Bjorkman O, Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9: 1369-1380
84. Ohlrogge J, Allen D, Berguson B, Dellapenna D, Shachar-Hill Y, Stymne S (2009) Energy. Driving on biomass. Science 324: 1019-1020
85. Park J, Wang H, Gargouri M, Deshpande R, Skepper J, Holguin FO, Juergens M, Shachar-Hill Y, Hicks L, Gang DR (December 17, 2014) The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis. Plant J http://dx.doi.org/10.1111/tpj.12747
86. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462: 518-521
87. Peltier G, Schmidt GW (1991) Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 88: 4791-4795
88. Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J Biol Chem 284: 32770-32781
89. Pfalz J, Liebers M, Hirth M, Grübler B, Holtzegel U, Schröter Y, Dietzel L, Pfannschmidt T (2012) Environmental control of plant nuclear gene expression by chloroplast redox signals. Front Plant Sci 3: 257
90. Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235: 729-745
91. Plumley FG, Douglas SE, Switzer AB, Schmidt GW (1989) Nitrogendependent biogenesis of chlorophyll-protein complexes. Plant Biology (New York) 8: 311-329
92. Plumley FG, Schmidt GW (1989) Nitrogen-dependent regulation of photosynthetic gene expression. Proc Natl Acad Sci USA 86: 2678-2682
93. Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89: 27-41
94. Rochaix JD (2002) Chlamydomonas, a model system for studying the assembly and dynamics of photosynthetic complexes. FEBS Lett 529: 34-38
95. Rodriguez-Uribe L, Guzman I, Rajapakse W, Richins RD, O’Connell MA (2012) Carotenoid accumulation in orange-pigmented Capsicum annuum fruit, regulated at multiple levels. J Exp Bot 63: 517-526
96. Roessler PG (1990) Environmental control of glycerolipid metabolism in microalgae: commercial implications and future research directions. J Phycol 26: 393-399
97. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30: 1041-1051
98. Sacksteder CA, Jacoby ME, Kramer DM (2001) A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants. Photosynth Res 70: 231-240
99. Schmollinger S, Mühlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Moseley JL, Kropat J, Sommer F, Strenkert D, et al (2014) Nitrogensparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26: 1410-1435
100. 13C metabolic flux analysis of photoautotrophic microorganisms. Phytochemistry 68: 2302-2312
101. Shifrin NS, Chisholm SW (1981) Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles. J Phycol 17: 374-384
102. Shimojima M, Ohta H, Nakamura Y (2010) Biosynthesis and Function of Chloroplast Lipids. In H Wada, N Murata, eds, Lipids in Photosynthesis, Vol 30. Springer, Dordrecht, The Netherlands, pp 35-55
103. Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylidès C, Li-Beisson Y, et al (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11: 7
104. Simionato D, Block MA, La Rocca N, Jouhet J, Maréchal E, Finazzi G, Morosinotto T (2013) The response of Nannochloropsis gaditana to nitrogen starvation includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot Cell 12: 665-676
105. Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9: 1101-1118
106. Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110: 10016-10021
107. Tunçay H, Findinier J, Duchêne T, Cogez V, Cousin C, Peltier G, Ball SG, Dauvillée D (2013) A forward genetic approach in Chlamydomonas reinhardtii as a strategy for exploring starch catabolism. PLoS ONE 8: e74763
108. Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J, Vener AV (2006) Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 5: 1412-1425
109. Urzica EI, Vieler A, Hong-Hermesdorf A, Page MD, Casero D, Gallaher SD, Kropat J, Pellegrini M, Benning C, Merchant SS (2013) Remodeling of membrane lipids in iron-starved Chlamydomonas. J Biol Chem 288: 30246-30258
110. Van K, Spalding MH (1999) Periplasmic carbonic anhydrase structural gene (Cah1) mutant in Chlamydomonas reinhardtii. Plant Physiol 120: 757- 764
111. Wang H, Alvarez S, Hicks LM (2012) Comprehensive comparison of iTRAQ and label-free LC-based quantitative proteomics approaches using two Chlamydomonas reinhardtii strains of interest for biofuels engineering. J Proteome Res 11: 487-501
112. 2 recapture. Photosynth Res 109: 115-122
113. Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8: 1856-1868
114. Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329: 796-799
115. Williams PJL, Laurens LML (2010) Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics. Energy & Environmental Science 3: 554-590
116. Work VH, Radakovits R, Jinkerson RE, Meuser JE, Elliott LG, Vinyard DJ, Laurens LM, Dismukes GC, Posewitz MC (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
117. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117: 129-139
118. Yang ZK, Ma YH, Zheng JW, Yang WD, Liu JS, Li HY (2014) Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum. J Appl Phycol 26: 73-82
119. Yang ZK, Niu YF, Ma YH, Xue J, Zhang MH, Yang WD, Liu JS, Lu SH, Guan Y, Li HY (2013) Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol Biofuels 6: 67
120. Yoshida K, Igarashi E, Mukai M, Hirata K, Miyamoto K (2003) Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii, by abscisic acid. Plant Cell Environ 26: 451-457
121. Young EB, Beardall J (2005) Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron, and light availability. Canadian Journal of Botany-Revue Canadienne De Botanique 83: 917-928
122. 13C flux analysis. Metab Eng 13: 656-665