Deregulated chlorophyll b synthesis reduces the energy transfer rate between photosynthetic pigments and induces photodamage in arabidopsis thaliana

Plant and Cell Physiology

Volumn 51, Issue 6, 2010, Pages 1055-1065

  Sakuraba, Yasuhito ^a   Yokono, Makio ^b   Akimoto, Seiji ^b   Tanaka, Ryouichi ^a   Tanaka, Ayumi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

Author keywords

Chlorophyll b; Chlorophyllide a oxygenase; Photooxidative damage; Reactive oxygen species (ROS)

Indexed keywords

ANTHOCYANIN; CHLOROPHYLL; CHLOROPHYLL B; HYDROGEN PEROXIDE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; DNA MICROARRAY; ENERGY TRANSFER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; RADIATION EXPOSURE; TRANSGENIC PLANT;

ANTHOCYANINS; ARABIDOPSIS; CHLOROPHYLL; ENERGY TRANSFER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; LIGHT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS, GENETICALLY MODIFIED;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 77953584615     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq050     Document Type: Article

References (39)

1. Akimoto, S., Yokono, M., Ohmae, M., Yamazaki, I., Nagata, N., Tanaka, R., et al. (2005) Excitation energy transfer in the antenna system with divinyl-chlorophylls in the vinyl reductase-expressing Arabidopsis. Chem. Phys. Lett. 409: 167-171.
2. Asada K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141: 391-396.
3. Barber, J., Morris, E. and Buchel, C. (2000) Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim. Biophys. Acta 1459: 239-247.
4. Bellemare, G., Bartlett, S.G. and Chua, N.H. (1982) Biosynthesis of chlorophyll a/b-binding polypeptides in wild type and the chlorina f2 mutant of barley. J. Biol. Chem. 257: 7762-7767.
5. Block, M.A., Tewari, A.K., Albrieux, C., Maréchal, E. and Joyard, J. (2002) The plant S-adenosyl-L-methionine:Mg-protoporphyrin IX methyltransferase is located in both envelope and thylakoid chloroplast membranes. Eur. J. Biochem. 269:
6. Borevitz, J., Xia, Y., Blount, J., Dixon, R.A. and Lamb, C. (2000) Activation tagging identifi es a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2394.
7. Consoli, E., Croce, R., Dunlap, D.D. and Finzi, L. (2005) Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep. 6: 782-786.
8. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K. and Scheible, W.R. (2005) Genome-wide identifi cation and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
9. Elrad, D., Niyogi, K.K. and Grossman, A.R. (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14: 1801-1816.
10. Falbel, T.G., Meehl, J.B. and Staehelin, L, A. (1996) Severity of mutant phenotype in a series of chlorophyll-defi cient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis. Plant Physiol. 112: 821-832.
11. Fryer, M.J., Oxborough, K., Mullineaux, P.M. and Baker, N.R. (2002) Imaging of photo-oxidative stress responses in leaves. J. Exp. Bot. 53: 1249-1254.
12. Green, B.R. and Durnford, D.G. (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 685-714.
13. Grossman, A.R., Bhaya, D., Apt, K.E. and Kehoe, D.M. (1995) Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu. Rev. Genet. 29: 231-288.
14. Harper, A.L., von Gesjen, S.E., Linford, A.S., Peterson, M.P., Faircloth, R.S., Thissen, M.M., et al. (2004) Chlorophyllide a oxygenase mRNA and protein levels correlate with the chlorophyll a/b ratio in Arabidopsis thaliana. Photosynth. Res. 79: 149-159.
15. Hirashima, M., Satoh, S., Tanaka, R. and Tanaka, A. (2006) Pigment shuffl ing in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J. Biol. Chem. 281: 15385-15393.
16. Hirono, Y. and Redei, G.P. (1963) Multiple allelic control of chlorophyll b level in Arabidopsis thaliana. Nature 197: 1324-1325.
17. Kamada-Nobusada,T., Hayashi, M., Fukasawa, M., Sakakibara, H. and Nishimura, M. (2008) A putative peroxisomal polyamine oxidaser, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol. 49: 1272-1282.
18. Koch, E. and Slusarenko, A. (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: 437-445.
19. Koziol, A.G., Borza, T., Ishida, K., Keeling, P., Lee, R.W. and Durnford, D.G. (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143: 1802-1816.
20. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., et al. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428: 287-292.
21. Masuda, T., Tanaka, A. and Melis, A. (2003) Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol. Biol. 51: 757-771.
22. Nakagawara, E., Sakuraba, Y., Yamasato, A., Tanaka, R. and Tanaka, A. (2007) Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J. 49: 800-809.
23. O'Connor, D.V. and Phillips, D. (1984) Time-Correlated Single Photon Counting. Academic Press, London.
24. Pattanayak, G.K., Biswal, A.K., Reddy, V.S. and Tripathy, B.C. (2005) Light-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants. Biochem. Biophys. Res. Commun. 326: 466-471.
25. Sakuraba, Y., Tanaka, R., Yamasato, A. and Tanaka, A. (2009) Determination of a chloroplast degron in the regulatory domain of chlorophyllide a oxygenase. J. Biol. Chem. 284: 36689-36699.
26. Sakuraba, Y., Yamasato, A., Tanaka, R. and Tanaka, A. (2007) Functional analysis of N-terminal domains of Arabidopsis chlorophyllide a oxygenase. Plant Physiol. Biochem. 45: 740-749.
27. Satoh, S., Ikeuchi, M., Mimuro, M. and Tanaka, A. (2001) Chlorophyll b expressed in Cyanobacteria functions as a light-harvesting antenna in photosystem I through fl exibility of the proteins. J. Biol. Chem. 276: 4293-4297.
28. Shimada, Y., Tsuchiya, T., Akimoto, S., Tomo, T., Fukuya, M., Tanaka, K., et al. (2008) Spectral properties of the CP43-deletion mutant of Synechocystis sp. PCC 6803. Photosynth. Res. 98: 303-314.
29. Springob, K., Nakajima, J., Yamazaki, M. and Saito, K. (2003) Recent advances in the biosynthesis and accumulation of anthocyanins. Nat. Prod. Rep. 20: 288-303.
30. Tanaka, A., Ito, H., Tanaka, R., Tanaka, N.K., Yoshida, K. and Okada, K. (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl Acad. Sci. USA 95: 12719-12723.
31. Tanaka, R., Koshino, Y., Sawa, S., Ishiguro, S., Okada, K. and Tanaka, A. (2001) Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J. 26: 365-373.
32. Tanaka, A., Yamamoto, Y. and Tsuji, H. (1991) Formation of chlorophyll-protein complexes during greening. 2. Redistribution of chlorophyll among apoproteins. Plant Cell Physiol. 32: 195-204.
33. Torres, M.A., Dangl, J.L. and Jones, J.D. (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99: 517-522.
34. Vandenabeele, S., Vanderauwera, S., Vuylsteke, M., Rombauts, S., Langebartels, C., Seidlitz, H.K., et al. (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J. 39: 45-58.
35. Vanderauwera, S., Zimmermann, P., Rombauts, S., Vandenabeele, S., Langebartels, C., Gruissem, W., et al. (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol. 139: 806-821.
36. Winkel-Shirley, B. (2002) Biosynthesis of fl avonoids and effects of stress. Curr. Opin. Plant Biol. 5: 218-223.
37. Wu, G. and Spalding, E.P. (2007) Separate functions for nuclear and cytoplasmic cryptochrome 1 during photomorphogenesis of Arabidopsis seedlings. Proc. Natl Acad. Sci. USA 104: 18813-18818.
38. Yamasato, A., Nagata, N., Tanaka, R. and Tanaka, A. (2005) The N-terminal domain of chlorophyllide a oxygenase confers protein instability in response to chlorophyll B accumulation in Arabidopsis. Plant Cell 17: 1585-1597.
39. Yamasato, A., Tanaka, R. and Tanaka, A. (2008) Loss of the N-terminal domain of chlorophyllide a oxygenase induces photodamage during greening of Arabidopsis seedlings. BMC Plant. Biol. 8: 64.