Photosynthesis Research

, Volume 85, Issue 3, pp 327–340 | Cite as

Effects of Chlorophyllide a Oxygenase Overexpression on Light Acclimation inArabidopsis thaliana

  • Ryouichi Tanaka
  • Ayumi Tanaka
Regular paper


Land plants change the compositions of light-harvesting complexes (LHC) and chlorophyll (Chl) a/b ratios in response to the variable light environments which they encounter. In this study, we attempted to determine the mechanism which regulates Chl a/b ratios and whether the changes in Chl a/b ratios are essential in regulation of LHC accumulation during light acclimation. We hypothesized that changes in the mRNA levels for chlorophyll a oxygenase (CAO) involved in Chl b biosynthesis are an essential part of light response of Chl a/b ratios and LHC accumulation. We also examined the light-intensity dependent response of CAO-overexpression and wild-type Arabidopsis thaliana plants. When wild-type plants were acclimated from low-light (LL) to high-light (HL) conditions, CAO mRNA levels decreased and the Chl a/b ratio increased. In transgenic plants overexpressing CAO, the Chl a/b ratio remained low under HL conditions; thereby suggesting that changes in the CAO mRNA levels are necessary for those in Chl a/b ratios upon light acclimation. Under HL conditions, the accumulation of Lhcb1, Lhcb3 and Lhcb6 was enhanced in plants overexpressing CAO. On the contrary, in a CAO-deficient mutant, chlorina 1-1, theaccumulation of Lhcb1, Lhcb2, Lhcb3, Lhcb6 and Lhca4 was reduced. In comparison to wild-type, β-carotene levels were reduced in CAO-overexpressing plants, while they were elevated in chlorina 1-1 mutants. These results imply that the transcriptional control of CAO is a part of the regulatory mechanism for the accumulation of a distinct set of LHC proteins upon light acclimation.


Arabidopsis thaliana, chlorina-1 chlorophyll b chlorophyllide a oxygenase LHCII 



chlorophyllide a oxygenase






chlorophyll pro- tein


light-harvesting protein complex


light-harvesting chlorophyll a/b-protein of PSI


light-harvesting chlorophyll a/b-protein of PSII


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  1. Anderson, J, Chow, W, Goodchild, D 1988Thylakoid membrane organization in Sun/Shade AcclimationAust J Plant Physiol151126Google Scholar
  2. Andersson, J, Walters, R, Horton, P, Jansson, S 2001Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipationPlant Cell1311931204CrossRefPubMedGoogle Scholar
  3. Andersson, J, Wentworth, M, Walters, RG, Howard, CA, Ruban, AV, Horton, P, Jansson, S 2003Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of Photosystem II – effects on photosynthesis, grana stacking and fitnessPlant J35350361CrossRefPubMedGoogle Scholar
  4. Bellemare, G, Bartlett, S, Chua, N-H 1982Biosynthesis of chlorophyll a/b-binding polypeptides in wild type and the chlorina f2 mutant of barleyJ Biol Chem25777627776PubMedGoogle Scholar
  5. Ben-Shem, A, Frolow, F, Nelson, N 2003Crystal structure of plant photosystem INature426630635PubMedGoogle Scholar
  6. Bossmann, B, Knoetzel, J, Jansson, S 1997Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: Absence of specific antenna proteinsPhotosynth Res52127136CrossRefGoogle Scholar
  7. Chow, W, Anderson, J 1987Photosynthetic responses of Pisum sativum to an increase in irradiance during growth II. Thylakoid membrane componentsAust J Plant Physiol14919Google Scholar
  8. Darr, SC, Somerville, SC, Arntzen, CJ 1986Monoclonal antibodies to the light-harvesting chlorophyll a/b protein complex of Photosystem IIJ Cell Biol103733740CrossRefPubMedGoogle Scholar
  9. Elrad, D, Niyogi, KK, Grossman, AR 2002A major light-harvesting polypeptide of Photosystem II functions in thermal dissipationPlant Cell1418011816CrossRefPubMedGoogle Scholar
  10. Flachmann, R 1997Composition of Photosystem II antenna in light-harvesting complex II antisense tobacco plants at varying irradiancesPlant Physiol113787794CrossRefPubMedGoogle Scholar
  11. Flachmann, R, Kühlbrandt, W 1995Accumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobaccoPlant Cell7149160CrossRefPubMedGoogle Scholar
  12. Ganeteg, U, Strand, A, Gustafsson, P, Jansson, S 2001The properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibitionPlant Physiol120150158CrossRefGoogle Scholar
  13. Ghirardi, ML, McCauley, SW, Melis, A 1986Photochemical apparatus organization in the thylakoid membrane of Hordeum vulgare wild type and chlorophyll b-less chlorina-f2 mutantBiochim Biophys Acta851331339Google Scholar
  14. Green, B, Durnford, D 1996The chlorophyll-carotenoid proteins of oxygenic photosynthesisAnnu Rev Plant Physiol Plant Mol Biol47685714CrossRefPubMedGoogle Scholar
  15. Harper, AL, Gesjen, SE, Linford, AS, Peterson, MP, Faircloth, RS, Thissen, MM, Brusslan, JA 2004Chlorophyllide a oxygenase mRNA and protein levels correlate with the chlorophyll a/b ratio in Arabidopsis thalianaPhotosynth Res79149159CrossRefGoogle Scholar
  16. Harrison, MA, Melis, A 1992Organization and Stability of Polypeptides Associated with the Chlorophyll a-b Light-Harvesting Complex of Photosystem IIPlant Cell Physiol33627637Google Scholar
  17. Harrison, MA, Nemson, JA, Melis, A 1993Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutantsPhotosynth Res38141151CrossRefGoogle Scholar
  18. Hoober, J, Eggink, L 2001A potential role of chlorophylls b and c in assembly of light-harvesting complexesFEBS Lett48913CrossRefPubMedGoogle Scholar
  19. Hoober, JK, Eggink, LL 1999Assembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplastsPhotosynth Res61197215CrossRefGoogle Scholar
  20. Jansson, S 1999A guide to the Lhc genes and their relatives in ArabidopsisTrends Plant Sci4236240Google Scholar
  21. Kimura, M, Yamamoto, YY, Seki, M, Sakurai, T, Sato, M, Abe, T, Yoshida, S, Manabe, K, Shinozaki, K, Matsui, M 2003Identification of Arabidopsis genes regulated by high light-stress using cDNA microarrayPhotochem Photobiol77226233CrossRefPubMedGoogle Scholar
  22. Krol, M, Spangfort, MD, Huner, NPA, Oquist, G, Gustafsson, P, Jansson, S 1995Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutantplant physiol107873883PubMedGoogle Scholar
  23. Kuttkat, A, Edhofer, I, Eichacker, L, Paulsen, H 1997Light-harvesting chlorophyll a/b-binding protein stably inserts into etioplast membranes supplemented with Zn-pheophytin a/bJ Biol Chem2722045120455CrossRefPubMedGoogle Scholar
  24. Lee, AI, Thornber, JP 1995Analysis of the pigment stoichiometry of pigment–protein complexes from barley (Hordeum vulgare). the xanthophyll cycle intermediates occur mainly in the light-harvesting complexes of Photosystem I and Photosystem IIPlant Physiol107565574PubMedGoogle Scholar
  25. Lindahl, M, Yang, D-H, Andersson, B 1995Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of Photosystem II by a light-induced membrane-associated enzymic systemEur J Biochem231503509CrossRefPubMedGoogle Scholar
  26. Liu, Z, Yan, H, Wang, K, Kuang, T, Zhang, J, Gui, L, An, X, Chang, W 2004Crystal structure of spinach major light-harvesting complex at 2.72 ANG resolutionNature (London)428287292CrossRefGoogle Scholar
  27. Machold, O 1991Structure of light-harvesting complex II as deduced from its polypeptide composition and stoichiometry I: Studies with Vicia fabaJ Plant Physiol138678684Google Scholar
  28. Masamoto, K, Kinoshita, T, Shimazaki, KI 1993Light-induced de-epoxidation of violaxanthin in guard cell protoplasts of Vicia fabaPlant Cell Physiol34935938Google Scholar
  29. Masuda, T, Polle, J, Melis, A 2002Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stressPlant Physiol128603614CrossRefPubMedGoogle Scholar
  30. Masuda, T, Tanaka, A, Melis, A 2003Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expressionPlant Mol Biol51757771CrossRefPubMedGoogle Scholar
  31. Melis, A 1991Dynamics of photosynthetic membrane composition and functionBiochim Biophys Acta105887106Google Scholar
  32. Melis, A 1996Excitation energy transferDR, OrtCF, Yocum eds. Functional and dynamic aspects of Lhc (cab) proteinsKluwer Academic PublishersDordrecht, The Netherlands523538Google Scholar
  33. Murchie, E, Horton, P 1997Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preferencePlant Cell Environ20438448CrossRefGoogle Scholar
  34. Murchie, E, Horton, P 1998Contrasting patterns of photosynthetic acclimation to the light environment are dependent on the differential expression of the responses to altered irradiance and spectral qualityPlant Cell Environ21139148CrossRefGoogle Scholar
  35. Niyogi, K 1999Photoprotection revised: genetic and molecular approachesAnnu Rev Plant Physiol Plant Mol Biol50333359PubMedGoogle Scholar
  36. Oster, U, Tanaka, R, Tanaka, A, Ruedigger, W 2000Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis CAO from Arabidopsis thalianaPlant J21305310CrossRefPubMedGoogle Scholar
  37. Park, H, Eggink, LL, Roberson, RW, Hoober, JK 1999Transfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (Chlorophyta): a pathway for degradationJ Phycology35528538CrossRefGoogle Scholar
  38. Pattanayak, GK, Biswal, AK, Reddy, VS, Tripathy, BC 2005Light-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plantsBiocheim Biophys Res Commun326466471CrossRefGoogle Scholar
  39. Peter, G, Thornber, J 1991Biochemical composition and organization of higher plant Photosystem II light-harvesting pigment-proteinsJ Biol Chem2661674516754PubMedGoogle Scholar
  40. Pogson, BJ, Niyogi, KK, Bjorkman, O, DellaPenna, D 1998Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutantsProc Natl Acad Sci USA951332413329CrossRefPubMedGoogle Scholar
  41. Porra, R, Thompson, W, Kriedemann, P 1989Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopyBiochim Biophys Acta975384394Google Scholar
  42. Rossel, JB, Wilson, IW, Pogson, BJ 2002Global changes in gene expression in response to high light in ArabidopsisPlant Physiol13011091120CrossRefPubMedGoogle Scholar
  43. Ruban, A, Wentworth, M, Yakushevska, A, Andersson, J, Lee, P, Keegstra, W, Dekker, J, Boekema, E, Jansson, S, Horton, P 2003Plants lacking the main light-harvesting complex retain Photosystem II macro-organizationNature421648652CrossRefPubMedGoogle Scholar
  44. Rupprecht, J, Paulsen, H, Schmid, VHR 2000Protein domains required for formation of stable monomeric Lhca1- and Lhca4-complexesPhotosynth Res63217224CrossRefGoogle Scholar
  45. Scheumann, V, Schoch, S, Rudiger, W 1999Chlorophyll b reduction during senescence of barley seedlingsPlanta209364370CrossRefPubMedGoogle Scholar
  46. Schmid, VHR, Paulsen, H, Rupprecht, J 2002Identification of N- and C-terminal amino acids of Lhca1 and Lhca4 required for formation of the heterodimeric peripheral Photosystem I antenna LHCI-730Biochemistry4191269131PubMedGoogle Scholar
  47. Tanaka, R, Koshino, Y, Sawa, S, Ishiguro, S, Okada, K, Tanaka, A 2001Overexpression of chlorophyllide a oxygenase, (CAO) enlarges the antenna size of Photosystem II in Arabidopsis thalianaPlant J26365373CrossRefPubMedGoogle Scholar
  48. Tanaka, R, Oster, U, Kruse, E, Ruediger, W, Grimm, B 1999Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductasePlant Physiol120695704CrossRefPubMedGoogle Scholar
  49. Tardy, F, Havaux, M 1997Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplastsBiochim Biophys Acta1330179193PubMedGoogle Scholar
  50. Teramoto, H, Nakamori, A, Minagawa, J, Ono, T 2002Light-intensity-dependent expression of Lhc gene family encoding light-harvesting chlorophyll-a/b proteins of Photosystem II in Chlamydomonas reinhardtiiPlant Physiol130325333CrossRefPubMedGoogle Scholar
  51. Tokutsu, R, Teramoto, H, Takahashi, Y, Ono, TA, Minagawa, J 2004The light-harvesting complex of Photosystem I in Chlamydomonas reinhardtii: protein composition, gene structures and phylogenic implicationsPlant Cell Physiol45138145CrossRefPubMedGoogle Scholar
  52. Yakushevska, AE, Jensen, PE, Keegstra, W, RH, , Scheller, HV, Boekema, EJ, Dekker, JP 2001Supermolecular organization of Photosystem II and its associated light-harvesting antenna in Arabidopsis thalianaEur J Biochem26860206028PubMedGoogle Scholar
  53. Yakushevska, AE, Keegstra, W, Boekema, EJ, Dekker, JP, Andersson, J, Jansson, S, Ruban, AV, Horton, P 2003The structure of Photosystem II in Arabidopsis: Localization of the CP26 and CP29 antenna complexesBiochemistry42608613CrossRefPubMedGoogle Scholar
  54. Yang, DH, Paulsen, H, Andersson, B 2000The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysisFEBS Lett466385388CrossRefPubMedGoogle Scholar
  55. Yang, DH, Webster, J, Adam, Z, Lindahl, M, Andersson, B 1998Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of Photosystem II in response to elevated light intensitiesPlant Physiol118827834CrossRefPubMedGoogle Scholar
  56. Zhang, H, Goodman, HM, Jansson, S 1997Antisense inhibition of the Photosystem I antenna protein Lhca4 in Arabidopsis thalianaPlant Physiol11515251531PubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  1. 1.Institute of Low Temperature Science, CRESTHokkaido University,Japan Science and Technology CorporationSapporoJapan

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