Systems-Wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism chlamydomonas reinhardtiiw open

Plant Cell

Volumn 26, Issue 11, 2014, Pages 4270-4297

  Hemme, Dorothea ^a,b   Veyel, Daniel ^a,b   Mühlhaus, Timo ^a,b   Sommer, Frederik ^a,b   Jüppner, Jessica ^b   Unger, Ann Katrin ^c   Sandmann, Michael ^d   Fehrle, Ines ^b   Schönfelder, Stephanie ^b   Steup, Martin ^d   Geimer, Stefan ^c   Kopka, Joachim ^b   Giavalisco, Patrick ^b   Schroda, Michael ^b  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c UNIVERSITY OF BAYREUTH   (Germany)

^d UNIVERSITY OF POTSDAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII;

CHAPERONE; LIPID; PROTEOME; VEGETABLE PROTEIN;

ACCLIMATIZATION; CHLAMYDOMONAS REINHARDTII; GENETICS; HEAT; METABOLISM; METABOLOME; PHOTOSYNTHESIS; PHYSIOLOGY; ULTRASTRUCTURE;

ACCLIMATIZATION; CHLAMYDOMONAS REINHARDTII; HOT TEMPERATURE; LIPIDS; METABOLOME; MOLECULAR CHAPERONES; PHOTOSYNTHESIS; PLANT PROTEINS; PROTEOME;

EID: 84919807957     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.130997     Document Type: Article

References (187)

1. Almeida, C.C., Romão, C.V., Lindley, P.F., Teixeira, M., and Saraiva, L.M. (2006). The role of the hybrid cluster protein in oxidative stress defense. J. Biol. Chem. 281: 32445–32450.
2. Anderson, L.E. (1971). Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases. Biochim. Biophys. Acta 235: 237–244.
3. Armbruster, U., et al. (2013). Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell 25: 2661–2678.
4. Armond, P.A., Schreiber, U., and Björkman, O. (1978). Photosynthetic acclimation to temperature in the desert shrub, Larrea divaricata: II. Light-harvesting efficiency and electron transport. Plant Physiol. 61: 411–415.
5. Armond, P.A., Björkman, O., and Staehelin, L.A. (1980). Dissociation of supramolecular complexes in chloroplast membranes. A manifestation of heat damage to the photosynthetic apparatus. Biochim. Biophys. Acta 601: 433–443.
6. Arndt, V., Rogon, C., and Höhfeld, J. (2007). To be, or not to be— molecular chaperones in protein degradation. Cell. Mol. Life Sci. 64: 2525–2541.
7. AsadaII, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141: 391– 396.
8. Austin, J.R., Frost, E., Vidi, P.A., Kessler, F., and Staehelin, L.A. (2006). Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18: 1693–1703.
9. Balogi, Z., Török, Z., Balogh, G., Jósvay, K., Shigapova, N., Vierling, E., Vígh, L., and Horváth, I. (2005). “Heat shock lipid” in cyanobacteria during heat/light-acclimation. Arch. Biochem. Biophys. 436: 346–354.
10. Baudouin-Cornu, P., Surdin-Kerjan, Y., Marlière, P., and Thomas, D. (2001). Molecular evolution of protein atomic composition. Science 293: 297–300.
11. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B Met. 57: 289–300.
12. Berry, J., and Bjorkman, O. (1980). Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. 31: 491–543.
13. Bersuker, K., Hipp, M.S., Calamini, B., Morimoto, R.I., and Kopito, R.R. (2013). Heat shock response activation exacerbates inclusion body formation in a cellular model of Huntington disease. J. Biol. Chem. 288: 23633–23638.
14. Blaby, I.K., et al. (2013). Systems-level analysis of nitrogen starvationinduced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25: 4305–4323.
15. Cakmak, T., Angun, P., Demiray, Y.E., Ozkan, A.D., Elibol, Z., and Tekinay, T. (2012). Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol. Bioeng. 109: 1947–1957.
16. Castruita, M., Casero, D., Karpowicz, S.J., Kropat, J., Vieler, A., Hsieh, S.I., Yan, W., Cokus, S., Loo, J.A., Benning, C., Pellegrini, M., and Merchant, S.S. (2011). Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23: 1273–1292.
17. Cheng, Y., Zhou, W., El Sheery, N.I., Peters, C., Li, M., Wang, X., and Huang, J. (2011). Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation. Plant J. 66: 781–795.
18. Coulson, P.B., and Tyndall, R. (1978). Quantation by flow microfluorometry of total cellular DNA in Acanthamoeba. J. Histochem. Cytochem. 26: 713–718.
19. Coulson, P.B., Bishop, A.O., and Lenarduzzi, R. (1977). Quantitation of cellular deoxyribonucleic acid by flow microfluorometry. J. Histochem. Cytochem. 25: 1147–1153.
20. Craig, R., and Beavis, R.C. (2004). TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20: 1466–1467.
21. Dayer, R., Fischer, B.B., Eggen, R.I., and Lemaire, S.D. (2008). The peroxiredoxin and glutathione peroxidase families in Chlamydomonas reinhardtii. Genetics 179: 41–57.
22. Deryng, D., Conway, D., Ramankutty, N., Price, J., and Warren, R. (2014). Global crop yield response to extreme heat stress under multiple climate change futures. Environ. Res. Lett. 9: 034011.
23. Dieterle, F., Ross, A., Schlotterbeck, G., and Senn, H. (2006). Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Anal. Chem. 78: 4281–4290.
24. Dietz, K.J., Jacob, S., Oelze, M.L., Laxa, M., Tognetti, V., de Miranda, S.M., Baier, M., and Finkemeier, I. (2006). The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57: 1697–1709.
25. Duhaze, C., Gagneul, D., Leport, L., Larher, F.R., and Bouchereau, A. (2003). Uracil as one of the multiple sources of beta-alanine in Limonium latifolium, a halotolerant beta-alanine betaine accumulating Plumbaginaceae. Plant Physiol. Biochem. 41: 993–998.
26. Eilers, P.H.C., and Peeters, J.C.H. (1988). A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol. Modell. 42: 199–215.
27. Elias, J.E., and Gygi, S.P. (2007). Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4: 207–214.
28. Eng, J.K., McCormack, A.L., and Yates, J.R. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5: 976–989.
29. Feller, U., Crafts-Brandner, S.J., and Salvucci, M.E. (1998). Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol. 116: 539–546.
30. Feng, J., Fan, P., Jiang, P., Lv, S., Chen, X., and Li, Y. (2014). Chloroplast-targeted Hsp90 plays essential roles in plastid development and embryogenesis in Arabidopsis possibly linking with VIPP1. Physiol. Plant. 150: 292–307.
31. Ferreira, S., Hjernø, K., Larsen, M., Wingsle, G., Larsen, P., Fey, S., Roepstorff, P., and Salomé Pais, M. (2006). Proteome profiling of Populus euphratica Oliv. upon heat stress. Ann. Bot. (Lond.) 98: 361–377.
32. Garz, A., Sandmann, M., Rading, M., Ramm, S., Menzel, R., and Steup, M. (2012). Cell-to-cell diversity in a synchronized Chlamydomonas culture as revealed by single-cell analyses. Biophys. J. 103: 1078–1086.
33. Geel, C., Versluis, W., and Snel, J.F.H. (1997). Estimation of oxygen evolution by marine phytoplankton from measurement of the efficiency of photosystem II electron flow. Photosynth. Res. 51: 61–70.
34. Geer, L.Y., Markey, S.P., Kowalak, J.A., Wagner, L., Xu, M., Maynard, D.M., Yang, X., Shi, W., and Bryant, S.H. (2004). Open mass spectrometry search algorithm. J. Proteome Res. 3: 958–964.
35. Ghanevati, M., and Jaworski, J.G. (2001). Active-site residues of a plant membrane-bound fatty acid elongase b-ketoacyl-CoA synthase, FAE1 KCS. Biochim. Biophys. Acta 1530: 77–85.
36. Gilbert, M., Wilhelm, C., and Richter, M. (2000). Bio-optical modelling of oxygen evolution using in vivo fluorescence: Comparison of measured and calculated photosynthesis/irradiance (P-I) curves in four representative phytoplankton species. J. Plant Physiol. 157: 307–314.
37. Giroud, C., Gerber, A., and Eichenberger, W. (1988). Lipids of Chlamydomonas reinhardtii: Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol. 29: 587–595.
38. Goloubinoff, P., Mogk, A., Zvi, A.P., Tomoyasu, T., and Bukau, B. (1999). Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. USA 96: 13732–13737.
39. Gounaris, K., Brain, A.R.R., Quinn, P.J., and Williams, W.P. (1984). Structural reorganisation of chloroplast thylakoid membranes in response to heat-stress. Biochim. Biophys. Acta 766: 198–208.
40. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009). Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16: 334–342.
41. Guy, C., Kaplan, F., Kopka, J., Selbig, J., and Hincha, D.K. (2008). Metabolomics of temperature stress. Physiol. Plant. 132: 220–235.
42. Han, D.K., Eng, J., Zhou, H., and Aebersold, R. (2001). Quantitative profiling of differentiation-induced microsomal proteins using isotopecoded affinity tags and mass spectrometry. Nat. Biotechnol. 19: 946–951.
43. Harris, E.H. (2001). Chlamydomonas as a model organism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 363–406.
44. Harris, E.H. (2008). Introduction to Chlamydomonas and its laboratory use. In The Chlamydomonas Sourcebook, 2nd ed, H.H. Elizabeth, B.S. David, and G.B. Witman, eds (San Diego, CA: Elsevier/Academic Press), p. 248.
45. Hatch, M.D., and Stumpf, P.K. (1962). Fat metabolism in higher plants. XVIII. Propionate metabolism by plant tissues. Arch. Biochem. Biophys. 96: 193–198.
46. Hayat, M.A. (1970). Principles and Techniques of Electron Microscopy: Biological Applications. (New York: Van Nostrand Reinhold).
47. Haynes, C.M., Fiorese, C.J., and Lin, Y.F. (2013). Evaluating and responding to mitochondrial dysfunction: the mitochondrial unfoldedprotein response and beyond. Trends Cell Biol. 23: 311–318.
48. Heide, H., Nordhues, A., Drepper, F., Nick, S., Schulz-Raffelt, M., Haehnel, W., and Schroda, M. (2009). Application of quantitative immunoprecipitation combined with knockdown and cross-linking to Chlamydomonas reveals the presence of vesicle-inducing protein in plastids 1 in a common complex with chloroplast HSP90C. Proteomics 9: 3079–3089.
49. Hemschemeier, A., Casero, D., Liu, B., Benning, C., Pellegrini, M., Happe, T., and Merchant, S.S. (2013). Copper response regulator1- dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell 25: 3186–3211.
50. Höhner, R., Barth, J., Magneschi, L., Jaeger, D., Niehues, A., Bald, T., Grossman, A., Fufezan, C., and Hippler, M. (2013). The metabolic status drives acclimation of iron deficiency responses in Chlamydomonas reinhardtii as revealed by proteomics based hierarchical clustering and reverse genetics. Mol. Cell. Proteomics 12: 2774–2790.
51. Houtz, R.L., Magnani, R., Nayak, N.R., and Dirk, L.M. (2008). Coand post-translational modifications in Rubisco: unanswered questions. J. Exp. Bot. 59: 1635–1645.
52. Hsu-Ming, W., Naito, K., Kinoshita, Y., Kobayashi, H., Honjoh, K., Tashiro, K., and Miyamoto, T. (2012). Changes in transcription during recovery from heat injury in Salmonella typhimurium and effects of BCAA on recovery. Amino Acids 42: 2059–2066.
53. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., and Darzins, A. (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 54: 621–639.
54. Hummel, J., Strehmel, N., Selbig, J., Walther, D., and Kopka, J. (2010). Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics 6: 322–333.
55. Hummel, J., Segu, S., Li, Y., Irgang, S., Jueppner, J., and Giavalisco, P. (2011). Ultra performance liquid chromatography and high resolution mass spectrometry for the analysis of plant lipids. Front. Plant Sci. 2: 54.
56. James, G.O., Hocart, C.H., Hillier, W., Price, G.D., and Djordjevic, M.A. (2013). Temperature modulation of fatty acid profiles for biofuel production in nitrogen deprived Chlamydomonas reinhardtii. Bioresour. Technol. 127: 441–447.
57. Janero, D.R., and Barrnett, R. (1981). Cellular and thylakoid-membrane phospholipids of Chlamydomonas reinhardtii 137+. J. Lipid Res. 22: 1126–1130.
58. Jensen, R.G. (2000). Activation of Rubisco regulates photosynthesis at high temperature and CO2. Proc. Natl. Acad. Sci. USA 97: 12937–12938.
59. Jordan, D.B., and Ogren, W.L. (1984). The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase: Dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161: 308–313.
60. Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., and Krauss, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411: 909–917.
61. Jozefczuk, S., Klie, S., Catchpole, G., Szymanski, J., Cuadros-Inostroza, A., Steinhauser, D., Selbig, J., and Willmitzer, L. (2010). Metabolomic and transcriptomic stress response of Escherichia coli. Mol. Syst. Biol. 6: 364.
62. Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y., and Guy, C.L. (2004). Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136: 4159–4168.
63. Karlin, S., and Brendel, V. (1992). Chance and statistical significance in protein and DNA sequence analysis. Science 257: 39–49.
64. Kaup, M.T., Froese, C.D., and Thompson, J.E. (2002). A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol. 129: 1616–1626.
65. Kim, K., and Portis, A.R., Jr. (2004). Oxygen-dependent H2O2 production by Rubisco. FEBS Lett. 571: 124–128.
66. Knothe, G., Bagby, M.O., and Ryan, T.W. (1998). Precombustion of fatty acids and esters of biodiesel. A possible explanation for differing cetane numbers. J. Am. Oil Chem. Soc. 75: 1007–1013.
67. Kobza, J., and Edwards, G.E. (1987). Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol. 83: 69–74.
68. Königshofer, H., Tromballa, H.W., and Löppert, H.G. (2008). Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant Cell Environ. 31: 1771–1780.
69. Kopka, J., et al. (2005). GMD@CSB.DB: The Golm Metabolome Database. Bioinformatics 21: 1635–1638.
70. Krall, L., Huege, J., Catchpole, G., Steinhauser, D., and Willmitzer, L. (2009). Assessment of sampling strategies for gas chromatographymass spectrometry (GC-MS) based metabolomics of cyanobacteria. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 877: 2952–2960.
71. Kühl, N.M., and Rensing, L. (2000). Heat shock effects on cell cycle progression. Cell. Mol. Life Sci. 57: 450–463.
72. Kusano, T., Berberich, T., Tateda, C., and Takahashi, Y. (2008). Polyamines: essential factors for growth and survival. Planta 228: 367–381.
73. Lamosa, P., Turner, D.L., Ventura, R., Maycock, C., and Santos, H. (2003). Protein stabilization by compatible solutes. Effect of diglycerol phosphate on the dynamics of Desulfovibrio gigas rubredoxin studied by NMR. Eur. J. Biochem. 270: 4606–4614.
74. Lamosa, P., Burke, A., Peist, R., Huber, R., Liu, M.Y., Silva, G., Rodrigues-Pousada, C., LeGall, J., Maycock, C., and Santos, H. (2000). Thermostabilization of proteins by diglycerol phosphate, a new compatible solute from the hyperthermophile Archaeoglobus fulgidus. Appl. Environ. Microbiol. 66: 1974–1979.
75. Lee, D.G., Ahsan, N., Lee, S.H., Kang, K.Y., Bahk, J.D., Lee, I.J., and Lee, B.H. (2007). A proteomic approach in analyzing heatresponsive proteins in rice leaves. Proteomics 7: 3369–3383.
76. Li, P.T., Hsiao, W.L., Yu, R.C., and Chou, C.C. (2013). Effect of heat shock on the fatty acid and protein profiles of Cronobacter sakazakii BCRC 13988 as well as its growth and survival in the presence of various carbon, nitrogen sources and disinfectants. Food Microbiol. 36: 142–148.
77. Li, X., Moellering, E.R., Liu, B., Johnny, C., Fedewa, M., Sears, B.B., Kuo, M.H., and Benning, C. (2012). A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24: 4670–4686.
78. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A.R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1: 387–396.
79. Liu, C., Willmund, F., Golecki, J.R., Cacace, S., Hess, B., Markert, C., and Schroda, M. (2007). The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant J. 50: 265–277.
80. Lobell, D.B., Schlenker, W., and Costa-Roberts, J. (2011). Climate trends and global crop production since 1980. Science 333: 616–620.
81. Lohse, M., Nagel, A., Herter, T., May, P., Schroda, M., Zrenner, R., Tohge, T., Fernie, A.R., Stitt, M., and Usadel, B. (2014). Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ. 37: 1250–1258.
82. Lopez, N., Halladay, J., Walter, W., and Craig, E.A. (1999). SSB, encoding a ribosome-associated chaperone, is coordinately regulated with ribosomal protein genes. J. Bacteriol. 181: 3136–3143.
83. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265–275.
84. Luedemann, A., Strassburg, K., Erban, A., and Kopka, J. (2008). TagFinder for the quantitative analysis of gas chromatographymass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 24: 732–737.
85. Mahjoub, M.R., Montpetit, B., Zhao, L., Finst, R.J., Goh, B., Kim, A.C., and Quarmby, L.M. (2002). The FA2 gene of Chlamydomonas encodes a NIMA family kinase with roles in cell cycle progression and microtubule severing during deflagellation. J. Cell Sci. 115: 1759–1768.
86. Majoul, T., Bancel, E., Triboï, E., Ben Hamida, J., and Branlard, G. (2003). Proteomic analysis of the effect of heat stress on hexaploid wheat grain: Characterization of heat-responsive proteins from total endosperm. Proteomics 3: 175–183.
87. Majoul, T., Bancel, E., Triboï, E., Ben Hamida, J., and Branlard, G. (2004). Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from nonprolamins fraction. Proteomics 4: 505–513.
88. Malmendal, A., Overgaard, J., Bundy, J.G., Sørensen, J.G., Nielsen, N.C., Loeschcke, V., and Holmstrup, M. (2006). Metabolomic profiling of heat stress: hardening and recovery of homeostasis in Drosophila. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R205–R212.
89. Marr, A.G., and Ingraham, J.L. (1962). Effect of temperature on the composition of fatty acids in Escherichia coli. J. Bacteriol. 84: 1260–1267.
90. Martin, D.D., Ciulla, R.A., and Roberts, M.F. (1999). Osmoadaptation in archaea. Appl. Environ. Microbiol. 65: 1815–1825.
91. Martins, L.O., Huber, R., Huber, H., Stetter, K.O., Da Costa, M.S., and Santos, H. (1997). Organic solutes in hyperthermophilic archaea. Appl. Environ. Microbiol. 63: 896–902.
92. Marzluff, W.F., and Duronio, R.J. (2002). Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr. Opin. Cell Biol. 14: 692–699.
93. Matos, A.R., and Pham-Thi, A.T. (2009). Lipid deacylating enzymes in plants: old activities, new genes. Plant Physiol. Biochem. 47: 491–503.
94. Mehler, A.H. (1951). Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. Arch. Biochem. Biophys. 34: 339–351.
95. Mejía, R., Gómez-Eichelmann, M.C., and Fernández, M.S. (1995). Membrane fluidity of Escherichia coli during heat-shock. Biochim. Biophys. Acta 1239: 195–200.
96. Merchant, S.S., Kropat, J., Liu, B., Shaw, J., and Warakanont, J. (2012). TAG, you’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr. Opin. Biotechnol. 23: 352–363.
97. Merchant, S.S., et al. (2007). The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250.
98. Mettler, T., et al. (2014). Systems analysis of the response of photosynthesis, metabolism, and growth to an increase in irradiance in the photosynthetic model organism Chlamydomonas reinhardtii. Plant Cell 26: 2310–2350.
99. Miller, R., et al. (2010). Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154: 1737–1752.
100. Mishkind, M., Vermeer, J.E., Darwish, E., and Munnik, T. (2009). Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J. 60: 10–21.
101. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7: 405–410.
102. Mittler, R., Finka, A., and Goloubinoff, P. (2012). How do plants feel the heat? Trends Biochem. Sci. 37: 118–125.
103. Mogk, A., Schlieker, C., Friedrich, K.L., Schönfeld, H.J., Vierling, E., and Bukau, B. (2003). Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J. Biol. Chem. 278: 31033–31042.
104. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rüdiger, S., Röder, D., Langen, H., and Bukau, B. (1999). Identification of thermolabile Escherichia coli proteins: prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18: 6934–6949.
105. Mühlhaus, T.,Weiss, J., Hemme, D., Sommer, F., and Schroda,M. (2011). Quantitative shotgun proteomics using a uniform 15N-labeled standard to monitor proteome dynamics in time course experiments reveals new insights into the heat stress response of Chlamydomonas reinhardtii. Mol. Cell. Proteomics 10, M110 004739.
106. Murakami, Y., Tsuyama, M., Kobayashi, Y., Kodama, H., and Iba, K. (2000). Trienoic fatty acids and plant tolerance of high temperature. Science 287: 476–479.
107. Naumann, B., Stauber, E.J., Busch, A., Sommer, F., and Hippler, M. (2005). N-terminal processing of Lhca3 Is a key step in remodeling of the photosystem I-light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii. J. Biol. Chem. 280: 20431–20441.
108. Nesvizhskii, A.I., Keller, A., Kolker, E., and Aebersold, R. (2003). A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75: 4646–4658.
109. Neuhaus, H., and Stitt, M. (1990). Control analysis of photosynthate partitioning: Impact of reduced activity of ADP-glucose pyrophosphorylase or plastid phosphoglucomutase on the fluxes to starch and sucrose in Arabidopsis thaliana (L.) Heynh. Planta 182: 445–454.
110. Nordhues, A., et al. (2012). Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell 24: 637–659.
111. Nugteren, D.H. (1965). The enzymic chain elongation of fatty acids by rat-liver microsomes. Biochim. Biophys. Acta 106: 280–290.
112. Ohlrogge, J., and Browse, J. (1995). Lipid biosynthesis. Plant Cell 7: 957–970.
113. Ottenhof, H.H., Ashurst, J.L., Whitney, H.M., Saldanha, S.A., Schmitzberger, F., Gweon, H.S., Blundell, T.L., Abell, C., and Smith, A.G. (2004). Organisation of the pantothenate (vitamin B5) biosynthesis pathway in higher plants. Plant J. 37: 61–72.
114. Pace, C.N., Shirley, B.A., McNutt, M., and Gajiwala, K. (1996). Forces contributing to the conformational stability of proteins. FASEB J. 10: 75–83.
115. Page, M.D., Allen, M.D., Kropat, J., Urzica, E.I., Karpowicz, S.J., Hsieh, S.I., Loo, J.A., and Merchant, S.S. (2012). Fe sparing and Fe recycling contribute to increased superoxide dismutase capacity in iron-starved Chlamydomonas reinhardtii. Plant Cell 24: 2649–2665.
116. Palmblad, M., Mills, D.J., and Bindschedler, L.V. (2008). Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. J. Proteome Res. 7: 780–785.
117. Perkins, D.N., Pappin, D.J., Creasy, D.M., and Cottrell, J.S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551–3567.
118. Porra, R.J., Thompson, W.A., and Kriedemann, P.E. (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and chlorophyll b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975: 384–394.
119. Qeli, E., and Ahrens, C.H. (2010). PeptideClassifier for protein inference and targeted quantitative proteomics. Nat. Biotechnol. 28: 647–650.
120. Ramundo, S., et al. (2014). Conditional depletion of the Chlamydomonas chloroplast ClpP protease activates nuclear genes involved in autophagy and plastid protein quality control. Plant Cell 26: 2201–2222.
121. Richter, K., Haslbeck, M., and Buchner, J. (2010). The heat shock response: life on the verge of death. Mol. Cell 40: 253–266.
122. Riekhof, W.R., Sears, B.B., and Benning, C. (2005). Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot. Cell 4: 242–252.
123. Rivals, I., Personnaz, L., Taing, L., and Potier, M.C. (2007). Enrichment or depletion of a GO category within a class of genes: which test? Bioinformatics 23: 401–407.
124. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., and Mittler, R. (2004). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134: 1683–1696.
125. Rosen, R., Büttner, K., Becher, D., Nakahigashi, K., Yura, T., Hecker, M., and Ron, E.Z. (2002). Heat shock proteome of Agrobacterium tumefaciens: evidence for new control systems. J. Bacteriol. 184: 1772–1778.
126. Russell, N.J. (1984). Mechanisms of thermal adaptation in bacteria: Blueprints for survival. Trends Biochem. Sci. 9: 108–112.
127. Rütgers, M., and Schroda, M. (2013). A role of VIPP1 as a dynamic structure within thylakoid centers as sites of photosystem biogenesis? Plant Signal. Behav. 8: e27037. Sage, R.F., Way, D.A., and Kubien, D.S. (2008). Rubisco, Rubisco activase, and global climate change. J. Exp. Bot. 59: 1581–1595.
128. Sagor, G.H., Berberich, T., Takahashi, Y., Niitsu, M., and Kusano, T. (2013). The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shockrelated genes. Transgenic Res. 22: 595–605.
129. Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y.G., Maathuis, F.J., and Goloubinoff, P. (2009). The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21: 2829–2843.
130. Sakurai, I., Shen, J.R., Leng, J., Ohashi, S., Kobayashi, M., and Wada, H. (2006). Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J. Biochem. 140: 201–209.
131. Salvucci, M.E. (2008). Association of Rubisco activase with chaperonin- 60beta: a possible mechanism for protecting photosynthesis during heat stress. J. Exp. Bot. 59: 1923–1933.
132. Sam, O., Ramirez, C., Coronado, M.J., Testillano, P.S., and Risueno, M.C. (2003). Changes in tomato leaves induced by NaCl stress: leaf organization and cell ultrastructure. Biol. Plant. 47: 361–366.
133. Sangwan, V., Orvar, B.L., Beyerly, J., Hirt, H., and Dhindsa, R.S. (2002). Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J. 31: 629–638.
134. Santos, H., and da Costa, M.S. (2002). Compatible solutes of organisms that live in hot saline environments. Environ. Microbiol. 4: 501–509.
135. Scafaro, A.P., Haynes, P.A., and Atwell, B.J. (2010). Physiological and molecular changes in Oryza meridionalis Ng., a heat-tolerant species of wild rice. J. Exp. Bot. 61: 191–202.
136. Schauer, N., Steinhauser, D., Strelkov, S., Schomburg, D., Allison, G., Moritz, T., Lundgren, K., Roessner-Tunali, U., Forbes, M.G., Willmitzer, L., Fernie, A.R., and Kopka, J. (2005). GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett. 579: 1332–1337.
137. Schmollinger, S., Schulz-Raffelt, M., Strenkert, D., Veyel, D., Vallon, O., and Schroda, M. (2013). Dissecting the heat stress response in Chlamydomonas by pharmaceutical and RNAi approaches reveals conserved and novel aspects. Mol. Plant 6: 1795–1813.
138. Schmollinger, S., et al. (2014). Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26: 1410–1435.
139. Schreiber, U., and Neubauer, C. (1990). O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth. Res. 25: 279– 293.
140. 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.
141. Schulz-Raffelt, M., Lodha, M., and Schroda, M. (2007). Heat shock factor 1 is a key regulator of the stress response in Chlamydomonas. Plant J. 52: 286–295.
142. Schuster, G., Even, D., Kloppstech, K., and Ohad, I. (1988). Evidence for protection by heat-shock proteins against photoinhibition during heat-shock. EMBO J. 7: 1–6.
143. Sharkey, T.D. (2005). Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ. 28: 269–277.
144. Sharkey, T.D., and Zhang, R. (2010). High temperature effects on electron and proton circuits of photosynthesis. J. Integr. Plant Biol. 52: 712–722.
145. Sharma, S.K., De Los Rios, P., and Goloubinoff, P. (2011). Probing the different chaperone activities of the bacterial HSP70-HSP40 system using a thermolabile luciferase substrate. Proteins 79: 1991–1998.
146. Sheehan, J., Dunahay, T., Benemann, J., and Roessler, P. (1998). A look back at the U.S. Department of Energy’s Aquatic Species Program: Biodiesel from Algae. National Renewable Energy Laboratory, report number NREL/TP-580-24190.
147. Shigapova, N., Török, Z., Balogh, G., Goloubinoff, P., Vígh, L., and Horváth, I. (2005). Membrane fluidization triggers membrane remodeling which affects the thermotolerance in Escherichia coli. Biochem. Biophys. Res. Commun. 328: 1216–1223.
148. Sinensky, M. (1974). Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 71: 522–525.
149. Singer, M.A., and Lindquist, S. (1998a). Multiple effects of trehalose on protein folding in vitro and in vivo. Mol. Cell 1: 639–648.
150. Singer, M.A., and Lindquist, S. (1998b). Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol. 16: 460–468.
151. Sjögren, L.L., Tanabe, N., Lymperopoulos, P., Khan, N.Z., Rodermel, S.R., Aronsson, H., and Clarke, A.K. (2014). Quantitative analysis of the chloroplast molecular chaperone ClpC/Hsp93 in Arabidopsis reveals new insights into its localization, interaction with the Clp proteolytic core, and functional importance. J. Biol. Chem. 289: 11318–11330.
152. Skylas, D.J., Cordwell, S.J., Hains, P.G., Larsen, M.R., Basseal, D.J., Walsh, B.J., Blumenthal, C., Rathmell, W., Copeland, L., and Wrigley, C.W. (2002). Heat shock of wheat during grain filling: proteins associated with heat tolerance. J. Cereal Sci. 35: 175–188.
153. Sprey, B., and Lichtenthaler, H.K. (1966). Zur frage der beziehungen zwischen plastoglobuli und thylakoidgenese in gerstenkeimlingen. Z. Naturforsch. B 21: 697.
154. Steinhauser, D., and Kopka, J. (2007). Methods, applications and concepts of metabolite profiling: primary metabolism. EXS 97: 171–194.
155. Stenbaek, A., and Jensen, P.E. (2010). Redox regulation of chlorophyll biosynthesis. Phytochemistry 71: 853–859.
156. Strehmel, N., Hummel, J., Erban, A., Strassburg, K., and Kopka, J. (2008). Retention index thresholds for compound matching in GCMS metabolite profiling. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 871: 182–190.
157. Strehmel, N., Praeger, U., Konig, C., Fehrle, I., Erban, A., Geyer, M., Kopka, J., and van Dongen, J.T. (2010). Time course effects on primary metabolism of potato (Solanum tuberosum) tuber tissue after mechanical impact. Postharvest Biol. Technol. 56: 109–116.
158. Süle, A., Vanrobaeys, F., Hajós, G., Van Beeumen, J., and Devreese, B. (2004). Proteomic analysis of small heat shock protein isoforms in barley shoots. Phytochemistry 65: 1853–1863.
159. Suri, S.S., and Dhindsa, R.S. (2008). A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant Cell Environ. 31: 218–226.
160. Tanaka, Y., Nishiyama, Y., and Murata, N. (2000). Acclimation of the photosynthetic machinery to high temperature in Chlamydomonas reinhardtii requires synthesis de novo of proteins encoded by the nuclear and chloroplast genomes. Plant Physiol. 124: 441–449.
161. Terano, S., and Suzuki, Y. (1978). Formation of beta-alanine from spermine and spermidine in maize shoots. Phytochemistry 17: 148–149.
162. Thellier, M., and Lüttge, U. (2013). Plant memory: a tentative model. Plant Biol (Stuttg) 15: 1–12.
163. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L.A., Rhee, S.Y., and Stitt, M. (2004). MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37: 914–939.
164. Tibshirani, R., Walther, G., and Hastie, T. (2001). Estimating the number of clusters in a data set via the gap statistic. J. R. Stat. Soc. Series B Stat. Methodol. 63: 411–423.
165. Trotsenko, IuA., and Khelenina, V.N. (2002). The biology and osmoadaptation of haloalkaliphilic methanotrophs. Mikrobiologiia 71: 149–159.
166. Tsvetkov, S., Ivanova, E., and Djondjurov, L. (1989). The pool of histones in the nucleosol and cytosol of proliferating Friend cells is small, uneven and chasable. Biochem. J. 264: 785–791.
167. Tsvetkova, N.M., Horváth, I., Török, Z., Wolkers, W.F., Balogi, Z., Shigapova, N., Crowe, L.M., Tablin, F., Vierling, E., Crowe, J.H., and Vigh, L. (2002). Small heat-shock proteins regulate membrane lipid polymorphism. Proc. Natl. Acad. Sci. USA 99: 13504–13509.
168. Turrens, J.F. (1997). Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17: 3–8.
169. Valcu, C.M., Lalanne, C., Plomion, C., and Schlink, K. (2008). Heat induced changes in protein expression profiles of Norway spruce (Picea abies) ecotypes from different elevations. Proteomics 8: 4287–4302.
170. Veyel, D., Erban, A., Fehrle, I., Kopka, J., and Schroda, M. (2014a). Rationales and approaches for studying metabolism in eukaryotic microalgae. Metabolites 4: 184–217.
171. Veyel, D., Sommer, F., Muranaka, L.S., Rütgers, M., Lemaire, S.D., and Schroda, M. (2014b). In vitro characterization of bacterial and chloroplast Hsp70 systems reveals an evolutionary optimization of the co-chaperones for their Hsp70 partner. Biochem. J. 460: 13–24.
172. Vila-Sanjurjo, A., Schuwirth, B.S., Hau, C.W., and Cate, J.H. (2004). Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol. 11: 1054–1059.
173. Voellmy, R., and Boellmann, F. (2007). Chaperone regulation of the heat shock protein response. Adv. Exp. Med. Biol. 594: 89–99.
174. Walter, P., and Ron, D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081–1086.
175. Walther, Z., and Hall, J.L. (1995). The uni chromosome of Chlamydomonas: histone genes and nucleosome structure. Nucleic Acids Res. 23: 3756–3763.
176. Wang, Z.T., Ullrich, N., Joo, S., Waffenschmidt, S., and Goodenough, U. (2009). Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot. Cell 8: 1856–1868.
177. Weibezahn, J., Tessarz, P., Schlieker, C., Zahn, R., Maglica, Z., Lee, S., Zentgraf, H., Weber-Ban, E.U., Dougan, D.A., Tsai, F.T., Mogk, A., and Bukau, B. (2004). Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119: 653–665.
178. Weis, E. (1981). Reversible heat-inactivation of the calvin cycle: A possible mechanism of the temperature regulation of photosynthesis. Planta 151: 33–39.
179. Wells, W.W., Xu, D.P., Yang, Y.F., and Rocque, P.A. (1990). Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J. Biol. Chem. 265: 15361–15364.
180. Wu, H.C., Luo, D.L., Vignols, F., and Jinn, T.L. (2012). Heat shockinduced biphasic Ca2+ signature and OsCaM1-1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.). Plant Cell Environ. 35: 1543–1557.
181. Xu, C., and Huang, B. (2008). Root proteomic responses to heat stress in two Agrostis grass species contrasting in heat tolerance. J. Exp. Bot. 59: 4183–4194.
182. Xu, C., and Huang, B. (2010). Differential proteomic response to heat stress in thermal Agrostis scabra and heat-sensitive Agrostis stolonifera. Physiol. Plant. 139: 192–204.
183. Xu, S., Li, J.L., Zhang, X.Q., Wei, H., and Cui, L.J. (2006). Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ. Exp. Bot. 56: 274–285.
184. Yancey, P.H. (2005). Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208: 2819–2830.
185. Yu, H.D., Yang, X.F., Chen, S.T., Wang, Y.T., Li, J.K., Shen, Q., Liu, X.L., and Guo, F.Q. (2012). Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. PLoS Genet. 8: e1002669.
186. Zhang, R., and Sharkey, T.D. (2009). Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth. Res. 100: 29–43.
187. Zhang, R., Wise, R.R., Struck, K.R., and Sharkey, T.D. (2010). Moderate heat stress of Arabidopsis thaliana leaves causes chloroplast swelling and plastoglobule formation. Photosynth. Res. 105: 123–134.