Truncated photosystem chlorophyll antenna size in the green microalga Chlamydomonas reinhardtii upon deletion of the TLA3-CpSRP43 gene

Plant Physiology

Volumn 160, Issue 4, 2012, Pages 2251-2260

  Kirst, Henning ^a   Garcia Cerdan, Jose Gines ^a   Zurbriggen, Andreas ^a   Ruehle, Thilo ^a   Melis, Anastasios ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84870827287     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.206672     Document Type: Article

References (60)

1. Aldridge C, Cain P, Robinson C (2009) Protein transport in organelles: protein transport into and across the thylakoid membrane. FEBS J 276: 1177-1186
2. Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317-326.
3. Amin P, Sy DAC, Pilgrim ML, Parry DH, Nussaume L, Hoffman NE (1999) Arabidopsis mutants lacking the 43- and 54-kilodalton subunits of the chloroplast signal recognition particle have distinct phenotypes. Plant Physiol 121: 61-70.
4. Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1-15.
5. Bals T, Dünschede B, Funke S, Schünemann D (2010) Interplay between the cpSRP pathway components, the substrate LHCP and the translocase Alb3: an in vivo and in vitro study. FEBS Lett 584: 4138-4144.
6. Bellafiore S, Ferris P, Naver H, Göhre V, Rochaix JD (2002) Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell 14: 2303-2314.
7. Dauvillée D, Delhaye S, Gruyer S, Slomianny C, Moretz SE, d'Hulst C, Long CA, Ball SG, Tomavo S (2010) Engineering the chloroplast targeted malarial vaccine antigens in Chlamydomonas starch granules. PLoS ONE 5: e15424.
8. Davies JP, Yildiz FH, Grossman AR (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15: 2150-2159.
9. Debuchy R, Purton S, Rochaix JD (1989) The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J 8: 2803-2809.
10. DeLille J, Peterson EC, Johnson T, Moore M, Kight A, Henry R (2000) A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts. Proc Natl Acad Sci USA 97: 1926-1931.
11. Dent RM, Haglund CM, Chin BL, Kobayashi MC, Niyogi KK (2005) Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol 137: 545-556.
12. Dewez D, Park S, García-Cerdán JG, Lindberg P, Melis A (2009) Mechanism of REP27 protein action in the D1 protein turnover and photosystem II repair from photodamage. Plant Physiol 151: 88-99.
13. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
14. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984.
15. Falk S, Sinning I (2010) cpSRP43 is a novel chaperone specific for lightharvesting chlorophyll a,b-binding proteins. J Biol Chem 285: 21655-21661.
16. Funke S, Knechten T, Ollesch J, Schünemann D (2005) A unique sequence motif in the 54-kDa subunit of the chloroplast signal recognition particle mediates binding to the 43-kDa subunit. J Biol Chem 280: 8912-8917.
17. Goforth RL, Peterson EC, Yuan J, Moore MJ, Kight AD, Lohse MB, Sakon J, Henry RL (2004) Regulation of the GTPase cycle in post-translational signal recognition particle-based protein targeting involves cpSRP43. J Biol Chem 279: 43077-43084.
18. Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 54: 1665-1669.
19. Greenwell HC, Laurens LML, Shields RJ, Lovitt RW, Flynn KJ (2010) Placing microalgae on the biofuels priority list: a review of the technological challenges. J R Soc Interface 7: 703-726.
20. Hankamer B, Lehr F, Rupprecht J, Mussgnug JH, Posten C, Kruse O (2007) Photosynthetic biomass and H2 production by green algae: from bioengineering to bioreactor scale-up. Physiol Plant 131: 10-21.
21. Harris EH (1989) The Chlamydomonas Source Book: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego.
22. 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.
23. Kim JH, Nemson JA, Melis A (1993) Photosystem II reaction center damage and repair in the green alga Dunaliella salina: analysis under physiological and adverse irradiance conditions. Plant Physiol 103: 181-189.
24. Kindle KL (1990) High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 1228-1232.
25. Kirk JTO (1994) Light and Photosynthesis in Aquatic Ecosystems, Ed 2. Cambridge University Press, Cambridge, UK.
26. Kirst H, García-Cerdán JG, Zurbriggen A, Melis A (2012) Assembly of the light-harvesting chlorophyll antenna in the green alga Chlamydomonas reinhardtii requires expression of the TLA2-CpFTSY gene. Plant Physiol 158: 930-945.
27. Klimyuk VI, Persello-Cartieaux F, Havaux M, Contard-David P, Schuenemann D, Meiherhoff K, Gouet P, Jones JD, Hoffman NE, Nussaume L (1999) A chromodomain protein encoded by the Arabidopsis CAO gene is a plant-specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 11: 87-99.
28. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148: 350-382.
29. Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8: 457-463.
30. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 14: 217-232.
31. Mayfield SP, Manuell AL, Chen S, Wu J, Tran M, Siefker D, Muto M, Marin-Navarro J (2007) Chlamydomonas reinhardtii chloroplasts as protein factories. Curr Opin Biotechnol 18: 126-133.
32. Melis A (1989) Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size. Philos Trans R Soc Lond B 323: 397-409.
33. Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058: 87-106.
34. Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226: 1075-1086.
35. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177: 272-280.
36. Melis A (2012) Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production. Energy Environ Sci 5: 5531-5539.
37. Melis A, Brown JS (1980) Stoichiometry of system I and system II reaction centers and of plastoquinone in different photosynthetic membranes. Proc Natl Acad Sci USA 77: 4712-4716.
38. Melis A, Duysens LNM (1979) Biphasic energy conversion kinetics and absorbance difference spectra of PS II of chloroplasts: evidence for two different PS II reaction centers. Photochem Photobiol 29: 373-382.
39. Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23: 343-350.
40. Melis A, Neidhardt J, Benemann JR (1999) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10: 515-525.
41. Melis A, Spangfort M, Andersson B (1987) Light-absorption and electron transport balance between photosystem-II and photosystem-I in spinach chloroplasts. Photochem Photobiol 45: 129-136.
42. Michelet L, Lefebvre-Legendre L, Burr SE, Rochaix JD, Goldschmidt-Clermont M (2011) Enhanced chloroplast transgene expression in a nuclear mutant of Chlamydomonas. Plant Biotechnol J 9: 565-574.
43. Mitra M, Melis A (2008) Optical properties of microalgae for enhanced biofuels production. Opt Express 16: 21807-21820.
44. Moore M, Goforth RL, Mori H, Henry R (2003) Functional interaction of chloroplast SRP/FtsY with the ALB3 translocase in thylakoids: substrate not required. J Cell Biol 162: 1245-1254.
45. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13: 1435-1448.
46. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125: 1558-1566.
47. Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9: 503-510.
48. Nakajima Y, Ueda R (1999) Improvement of microalgal photosynthetic productivity by reducing the content of light harvesting pigments. J Appl Phycol 11: 195-201.
49. Ort DR, Zhu X, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155: 79-85.
50. Pilgrim ML, van Wijk KJ, Parry DH, Sy DA, Hoffman NE (1998) Expression of a dominant negative form of cpSRP54 inhibits chloroplast biogenesis in Arabidopsis. Plant J 13: 177-186.
51. Polle JEW, Benemann JR, Tanaka A, Melis A (2000) Photosynthetic apparatus organization and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii: dependence on carbon source. Planta 211: 335-344.
52. Polle JEW, Kanakagiri S, Jin E, Masuda T, Melis A (2002) Truncated chlorophyll antenna size of the photosystems: a practical method to improve microalgal productivity and hydrogen production in mass culture. Int J Hydrogen Energy 27: 1257-1264.
53. Polle JEW, Kanakagiri SD, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217: 49-59.
54. Sizova IA, Fuhrmann M, Hegemann P (2001) A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene 277: 221-229.
55. Smith BM, Morrissey PJ, Guenther JE, Nemson JA, Harrison MA, Allen JF, Melis A (1990) Response of the photosynthetic apparatus in Dunaliella salina (green algae) to irradiance stress. Plant Physiol 93: 1433-1440.
56. Stengel KF, Holdermann I, Cain P, Robinson C, Wild K, Sinning I (2008) Structural basis for specific substrate recognition by the chloroplast signal recognition particle protein cpSRP43. Science 321: 253-256.
57. Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugière S, Hippler M, Ferro M, Bruley C, Peltier G, et al (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol (in press).
58. Tu CJ, Peterson EC, Henry R, Hoffman NE (2000) The L18 domain of lightharvesting chlorophyll proteins binds to chloroplast signal recognition particle 43. J Biol Chem 275: 13187-13190.
59. Tu CJ, Schuenemann D, Hoffman NE (1999) Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes. J Biol Chem 274: 27219-27224.
60. Tzvetkova-Chevolleau T, Hutin C, Noël LD, Goforth R, Carde JP, Caffarri S, Sinning I, Groves M, Teulon JM, Hoffman NE, et al (2007) Canonical signal recognition particle components can be bypassed for posttranslational protein targeting in chloroplasts. Plant Cell 19: 1635-1648.