Dynamics of carbon-concentrating mechanism induction and protein relocalization during the dark-to-light transition in synchronized Chlamydomonas reinhardtii

Plant Physiology

Volumn 166, Issue 2, 2014, Pages 1073-1082

  Mitchell, Madeline C ^a   Meyer, Moritz T ^a   Griffiths, Howard ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; VEGETABLE PROTEIN;

BIOSYNTHESIS; CHLAMYDOMONAS REINHARDTII; DARKNESS; GENE EXPRESSION; GENETICS; LIGHT; METABOLISM; PHYSIOLOGY; PLANT GENE;

CARBON; CHLAMYDOMONAS REINHARDTII; DARKNESS; GENE EXPRESSION; GENES, PLANT; LIGHT; PLANT PROTEINS;

EID: 84907790384     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.246918     Document Type: Article

References (47)

1. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophot Int 11: 36-42
2. Arvidsson S, Kwasniewski M, Riaño-Pachón DM, Mueller-Roeber B (2008) QuantPrime: a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 9: 465
3. Badger MR, Kaplan A, Berry JA (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a carbon dioxide-concentrating mechanism. Plant Physiol 66: 407-413
4. Blanco-Rivero A, Shutova T, Román MJ, Villarejo A, Martinez F (2012) Phosphorylation controls the localization and activation of the luminal carbonic anhydrase in Chlamydomonas reinhardtii. PLoS ONE7: e49063
5. Borkhsenious ON, Mason CB, Moroney JV (1998) The intracellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. Plant Physiol 116: 1585-1591
6. Bozzo GG, Colman B (2000) The induction of inorganic carbon transport and external carbonic anhydrase in Chlamydomonas reinhardtii is regulated by external CO2 concentration. Plant Cell Environ 23: 1137-1144
7. Brueggeman AJ, Gangadharaiah DS, Cserhati MF, Casero D, Weeks DP, Ladunga I (2012) Activation of the carbon concentrating mechanism by CO2 deprivation coincides with massive transcriptional restructuring in Chlamydomonas reinhardtii. Plant Cell 24: 1860-1875
8. Colombo SL, Pollock SV, Eger KA, Godfrey AC, Adams JE, Mason CB, Moroney JV (2002) Use of the bleomycin resistance gene to generate tagged insertional mutants of Chlamydomonas reinhardtii that require elevated CO2 for optimal growth. Funct Plant Biol 29: 231-241
9. Dionisio-Sese ML, Fukuzawa H, Miyachi S (1990) Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 94: 1103-1110
10. Duanmu D, Miller AR, Horken KM, Weeks DP, Spalding MH (2009) Knockdown of limiting-CO2-induced gene HLA3 decreases HCO3transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 106: 5990-5995
11. Eriksson M, Villand P, Gardeström P, Samuelsson G (1998) Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 116: 637-641
12. Fang W, Si Y, Douglass S, Casero D, Merchant SS, Pellegrini M, Ladunga I, Liu P, Spalding MH (2012) Transcriptome-wide changes in Chlamydomonas reinhardtii gene expression regulated by carbon dioxide and the CO2concentrating mechanism regulator CIA5/CCM1. Plant Cell 24: 1876-1893
13. Fujiwara S, Ishida N, Tsuzuki M (1996) Circadian expression of the carbonic anhydrase gene, Cah1, in Chlamydomonas reinhardtii. Plant Mol Biol 32: 745-749
14. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131
15. Im CS, Grossman AR (2002) Identification and regulation of high lightinduced genes in Chlamydomonas reinhardtii. Plant J 30: 301-313
16. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 165: 191-194
17. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G (1998) A novel a-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17: 1208-1216
18. Kropat J, Hong-Hermesdorf A, Casero D, Ent P, Castruita M, Pellegrini M, Merchant SS, Malasarn D (2011) A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant J 66: 770-780
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25: 402-408
20. Ma Y, Pollock SV, Xiao Y, Cunnusamy K, Moroney JV (2011) Identification of a novel gene, CIA6, required for normal pyrenoid formation in Chlamydomonas reinhardtii. Plant Physiol 156: 884-896
21. Manuel LJ, Moroney JV (1988) Inorganic carbon accumulation by Chlamydomonas reinhardtii: new proteins are made during adaptation to low CO2. Plant Physiol 88: 491-496
22. Marcus Y, Schuster G, Michaels A, Kaplan A (1986) Adaptation to CO2 levels and changes in the phosphorylation of thylakoid proteins during the cell cycle of Chlamydomonas reinhardtii. Plant Physiol 80: 604-607
23. Meyer MT, Genkov T, Skepper JN, Jouhet J, Mitchell MC, Spreitzer RJ, Griffiths H (2012) Rubisco small-subunit a-helices control pyrenoid formation in Chlamydomonas. Proc Natl Acad Sci USA 109: 19474-19479
24. Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT, et al (2004) Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 135: 1595-1607
25. Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res 109: 133-149
26. Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6: 1251-1259
27. Ohnishi N, Mukherjee B, Tsujikawa T, Yanase M, Nakano H, Moroney JV, Fukuzawa H (2010) Expression of a low CO2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22: 3105-3117
28. Price GD, Badger MR, Woodger FJ, Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441-1461
29. Rawat M, Moroney JV (1995) The regulation of carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase oxygenase activase by light and CO2 in Chlamydomonas reinhardtii. Plant Physiol 109: 937-944
30. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386
31. Schloss JA (1990) A Chlamydomonas gene encodes a G protein b subunit-like polypeptide. Mol Gen Genet 221: 443-452
32. Skepper JN (2000) Immunocytochemical strategies for electron microscopy: choice or compromise. J Microsc 199: 1-36
33. Spalding MH (2008) Microalgal carbon dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters. J Exp Bot 59: 1463-1473
34. Spalding MH, Critchley C, Govindjee, Orgren WL (1984) Influence of carbon dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardii. Photosynth Res 5: 169-176
35. Spalding MH, Ogren WL (1982) Photosynthesis is required for induction of the CO2-concentrating system in Chlamydomonas reinhardii. FEBS Lett 145: 41-44
36. Spalding MH, Spreitzer RJ, Ogren WL (1983) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardii. Plant Physiol 73: 273-276
37. Spreitzer RJ, Mets L (1981) Photosynthesis-deficient mutants of Chlamydomonas reinhardii with associated light-sensitive phenotypes. Plant Physiol 67: 565-569
38. Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449-475
39. Thyssen C, Hermes M, Sültemeyer D (2003) Isolation and characterization of Chlamydomonas reinhardtii mutants with an impaired CO2-concentrating mechanism. Planta 217: 102-112
40. Tirumani S, Kokkanti M, Chaudhari V, Shukla M, Rao BJ (2014) Regulation of CCM genes in Chlamydomonas reinhardtii during conditions of light-dark cycles in synchronous cultures. Plant Mol Biol 85: 277-286
41. Turkina MV, Blanco-Rivero A, Vainonen JP, Vener AV, Villarejo A (2006) CO2 limitation induces specific redox-dependent protein phosphorylation in Chlamydomonas reinhardtii. Proteomics6: 2693-2704
42. Van K, Spalding MH (1999) Periplasmic carbonic anhydrase structural gene (Cah1) mutant in Chlamydomonas reinhardtii. Plant Physiol 120: 757-764
43. Wang Y, Duanmu D, Spalding MH (2011) Carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii: inorganic carbon transport and CO2 recapture. Photosynth Res 109: 115-122
44. Wang Y, Spalding MH (2014) LCIB in the Chlamydomonas CO2-concentrating mechanism. Photosynth Res 121: 185-192
45. Yamano T, Miura K, Fukuzawa H (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 147: 340-354
46. Yamano T, Tsujikawa T, Hatano K, Ozawa S, Takahashi Y, Fukuzawa H (2010) Light and low-CO2-dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol 51: 1453-1468
47. Yoshioka S, Taniguchi F, Miura K, Inoue T, Yamano T, Fukuzawa H (2004) The novel Myb transcription factor LCR1 regulates the CO2responsive gene Cah1, encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Cell 16: 1466-1477