Abstract
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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- CAO:
-
chlorophyllide a oxygenase
- ch :
-
chlorina
- Chl:
-
chlorophyll
- CP:
-
chlorophyll pro- tein
- LHC:
-
light-harvesting protein complex
- Lhca:
-
light-harvesting chlorophyll a/b-protein of PSI
- Lhcb:
-
light-harvesting chlorophyll a/b-protein of PSII
References
J Anderson W Chow D Goodchild (1988) ArticleTitleThylakoid membrane organization in Sun/Shade Acclimation Aust J Plant Physiol 15 11–26
J Andersson R Walters P Horton S Jansson (2001) ArticleTitleAntisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation Plant Cell 13 1193–1204 Occurrence Handle10.1105/tpc.13.5.1193 Occurrence Handle11340191
J Andersson M Wentworth RG Walters CA Howard AV Ruban P Horton S Jansson (2003) ArticleTitleAbsence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of Photosystem II – effects on photosynthesis, grana stacking and fitness Plant J 35 350–361 Occurrence Handle10.1046/j.1365-313X.2003.01811.x Occurrence Handle12887586
G Bellemare S Bartlett N-H Chua (1982) ArticleTitleBiosynthesis of chlorophyll a/b-binding polypeptides in wild type and the chlorina f2 mutant of barley J Biol Chem 257 7762–7776 Occurrence Handle7045113
A Ben-Shem F Frolow N Nelson (2003) ArticleTitleCrystal structure of plant photosystem I Nature 426 630–635 Occurrence Handle14668855
B Bossmann J Knoetzel S Jansson (1997) ArticleTitleScreening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: Absence of specific antenna proteins Photosynth Res 52 127–136 Occurrence Handle10.1023/A:1005823711838
W Chow J Anderson (1987) ArticleTitlePhotosynthetic responses of Pisum sativum to an increase in irradiance during growth II. Thylakoid membrane components Aust J Plant Physiol 14 9–19
SC Darr SC Somerville CJ Arntzen (1986) ArticleTitleMonoclonal antibodies to the light-harvesting chlorophyll a/b protein complex of Photosystem II J Cell Biol 103 733–740 Occurrence Handle10.1083/jcb.103.3.733 Occurrence Handle3528171
D Elrad KK Niyogi AR Grossman (2002) ArticleTitleA major light-harvesting polypeptide of Photosystem II functions in thermal dissipation Plant Cell 14 1801–1816 Occurrence Handle10.1105/tpc.002154 Occurrence Handle12172023
R Flachmann (1997) ArticleTitleComposition of Photosystem II antenna in light-harvesting complex II antisense tobacco plants at varying irradiances Plant Physiol 113 787–794 Occurrence Handle10.1104/pp.113.3.787 Occurrence Handle9085572
R Flachmann W Kühlbrandt (1995) ArticleTitleAccumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobacco Plant Cell 7 149–160 Occurrence Handle10.1105/tpc.7.2.149 Occurrence Handle7756826
U Ganeteg A Strand P Gustafsson S Jansson (2001) ArticleTitleThe properties of the chlorophyll a/b-binding proteins Lhca2 and Lhca3 studied in vivo using antisense inhibition Plant Physiol 120 150–158 Occurrence Handle10.1104/pp.127.1.150
ML Ghirardi SW McCauley A Melis (1986) ArticleTitlePhotochemical apparatus organization in the thylakoid membrane of Hordeum vulgare wild type and chlorophyll b-less chlorina-f2 mutant Biochim Biophys Acta 851 331–339
B Green D Durnford (1996) ArticleTitleThe chlorophyll-carotenoid proteins of oxygenic photosynthesis Annu Rev Plant Physiol Plant Mol Biol 47 685–714 Occurrence Handle10.1146/annurev.arplant.47.1.685 Occurrence Handle15012305
AL Harper SE Gesjen Particlevon AS Linford MP Peterson RS Faircloth MM Thissen JA Brusslan (2004) ArticleTitleChlorophyllide a oxygenase mRNA and protein levels correlate with the chlorophyll a/b ratio in Arabidopsis thaliana Photosynth Res 79 149–159 Occurrence Handle10.1023/B:PRES.0000015375.40167.76
MA Harrison A Melis (1992) ArticleTitleOrganization and Stability of Polypeptides Associated with the Chlorophyll a-b Light-Harvesting Complex of Photosystem II Plant Cell Physiol 33 627–637
MA Harrison JA Nemson A Melis (1993) ArticleTitleAssembly 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 mutants Photosynth Res 38 141–151 Occurrence Handle10.1007/BF00146413
J Hoober L Eggink (2001) ArticleTitleA potential role of chlorophylls b and c in assembly of light-harvesting complexes FEBS Lett 489 1–3 Occurrence Handle10.1016/S0014-5793(00)02410-8 Occurrence Handle11231002
JK Hoober LL Eggink (1999) ArticleTitleAssembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplasts Photosynth Res 61 197–215 Occurrence Handle10.1023/A:1006313703640
S Jansson (1999) ArticleTitleA guide to the Lhc genes and their relatives in Arabidopsis Trends Plant Sci 4 236–240
M Kimura YY Yamamoto M Seki T Sakurai M Sato T Abe S Yoshida K Manabe K Shinozaki M Matsui (2003) ArticleTitleIdentification of Arabidopsis genes regulated by high light-stress using cDNA microarray Photochem Photobiol 77 226–233 Occurrence Handle10.1562/0031-8655(2003)077<0226:IOAGRB>2.0.CO;2 Occurrence Handle12785063
M Krol MD Spangfort NPA Huner G Oquist P Gustafsson S Jansson (1995) ArticleTitleChlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant plant physiol 107 873–883 Occurrence Handle7748263
A Kuttkat I Edhofer L Eichacker H Paulsen (1997) ArticleTitleLight-harvesting chlorophyll a/b-binding protein stably inserts into etioplast membranes supplemented with Zn-pheophytin a/b J Biol Chem 272 20451–20455 Occurrence Handle10.1074/jbc.272.33.20451 Occurrence Handle9252354
AI Lee JP Thornber (1995) ArticleTitleAnalysis 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 II Plant Physiol 107 565–574 Occurrence Handle7724673
M Lindahl D-H Yang B Andersson (1995) ArticleTitleRegulatory proteolysis of the major light-harvesting chlorophyll a/b protein of Photosystem II by a light-induced membrane-associated enzymic system Eur J Biochem 231 503–509 Occurrence Handle10.1111/j.1432-1033.1995.tb20725.x Occurrence Handle7635162
Z Liu H Yan K Wang T Kuang J Zhang L Gui X An W Chang (2004) ArticleTitleCrystal structure of spinach major light-harvesting complex at 2.72 ANG resolution Nature (London) 428 287–292 Occurrence Handle10.1038/nature02373
O Machold (1991) ArticleTitleStructure of light-harvesting complex II as deduced from its polypeptide composition and stoichiometry I: Studies with Vicia faba J Plant Physiol 138 678–684
K Masamoto T Kinoshita KI Shimazaki (1993) ArticleTitleLight-induced de-epoxidation of violaxanthin in guard cell protoplasts of Vicia faba Plant Cell Physiol 34 935–938
T Masuda J Polle A Melis (2002) ArticleTitleBiosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress Plant Physiol 128 603–614 Occurrence Handle10.1104/pp.128.2.603 Occurrence Handle11842163
T Masuda A Tanaka A Melis (2003) ArticleTitleChlorophyll 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 Occurrence Handle10.1023/A:1022545118212 Occurrence Handle12678561
A Melis (1991) ArticleTitleDynamics of photosynthetic membrane composition and function Biochim Biophys Acta 1058 87–106
A Melis (1996) Excitation energy transfer Ort DR Yocum CF (Eds) Functional and dynamic aspects of Lhc (cab) proteins Kluwer Academic Publishers Dordrecht, The Netherlands 523–538
E Murchie P Horton (1997) ArticleTitleAcclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference Plant Cell Environ 20 438–448 Occurrence Handle10.1046/j.1365-3040.1997.d01-95.x
E Murchie P Horton (1998) ArticleTitleContrasting patterns of photosynthetic acclimation to the light environment are dependent on the differential expression of the responses to altered irradiance and spectral quality Plant Cell Environ 21 139–148 Occurrence Handle10.1046/j.1365-3040.1998.00262.x
K Niyogi (1999) ArticleTitlePhotoprotection revised: genetic and molecular approaches Annu Rev Plant Physiol Plant Mol Biol 50 333–359 Occurrence Handle15012213
U Oster R Tanaka A Tanaka W Ruedigger (2000) ArticleTitleCloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis CAO from Arabidopsis thaliana Plant J 21 305–310 Occurrence Handle10.1046/j.1365-313x.2000.00672.x Occurrence Handle10758481
H Park LL Eggink RW Roberson JK Hoober (1999) ArticleTitleTransfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (Chlorophyta): a pathway for degradation J Phycology 35 528–538 Occurrence Handle10.1046/j.1529-8817.1999.3530528.x
GK Pattanayak AK Biswal VS Reddy BC Tripathy (2005) ArticleTitleLight-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants Biocheim Biophys Res Commun 326 466–471 Occurrence Handle10.1016/j.bbrc.2004.11.049
G Peter J Thornber (1991) ArticleTitleBiochemical composition and organization of higher plant Photosystem II light-harvesting pigment-proteins J Biol Chem 266 16745–16754 Occurrence Handle1885603
BJ Pogson KK Niyogi O Bjorkman D DellaPenna (1998) ArticleTitleAltered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants Proc Natl Acad Sci USA 95 13324–13329 Occurrence Handle10.1073/pnas.95.22.13324 Occurrence Handle9789087
R Porra W Thompson P Kriedemann (1989) ArticleTitleDetermination 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 spectroscopy Biochim Biophys Acta 975 384–394
JB Rossel IW Wilson BJ Pogson (2002) ArticleTitleGlobal changes in gene expression in response to high light in Arabidopsis Plant Physiol 130 1109–1120 Occurrence Handle10.1104/pp.005595 Occurrence Handle12427978
A Ruban M Wentworth A Yakushevska J Andersson P Lee W Keegstra J Dekker E Boekema S Jansson P Horton (2003) ArticleTitlePlants lacking the main light-harvesting complex retain Photosystem II macro-organization Nature 421 648–652 Occurrence Handle10.1038/nature01344 Occurrence Handle12571599
J Rupprecht H Paulsen VHR Schmid (2000) ArticleTitleProtein domains required for formation of stable monomeric Lhca1- and Lhca4-complexes Photosynth Res 63 217–224 Occurrence Handle10.1023/A:1006499517613
V Scheumann S Schoch W Rudiger (1999) ArticleTitleChlorophyll b reduction during senescence of barley seedlings Planta 209 364–370 Occurrence Handle10.1007/s004250050644 Occurrence Handle10502104
VHR Schmid H Paulsen J Rupprecht (2002) ArticleTitleIdentification of N- and C-terminal amino acids of Lhca1 and Lhca4 required for formation of the heterodimeric peripheral Photosystem I antenna LHCI-730 Biochemistry 41 9126–9131 Occurrence Handle12119027
R Tanaka Y Koshino S Sawa S Ishiguro K Okada A Tanaka (2001) ArticleTitleOverexpression of chlorophyllide a oxygenase, (CAO) enlarges the antenna size of Photosystem II in Arabidopsis thaliana Plant J 26 365–373 Occurrence Handle10.1046/j.1365-313X.2001.2641034.x Occurrence Handle11439124
R Tanaka U Oster E Kruse W Ruediger B Grimm (1999) ArticleTitleReduced 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 reductase Plant Physiol 120 695–704 Occurrence Handle10.1104/pp.120.3.695 Occurrence Handle10398704
F Tardy M Havaux (1997) ArticleTitleThylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts Biochim Biophys Acta 1330 179–193 Occurrence Handle9408171
H Teramoto A Nakamori J Minagawa T Ono (2002) ArticleTitleLight-intensity-dependent expression of Lhc gene family encoding light-harvesting chlorophyll-a/b proteins of Photosystem II in Chlamydomonas reinhardtii Plant Physiol 130 325–333 Occurrence Handle10.1104/pp.004622 Occurrence Handle12226512
R Tokutsu H Teramoto Y Takahashi TA Ono J Minagawa (2004) ArticleTitleThe light-harvesting complex of Photosystem I in Chlamydomonas reinhardtii: protein composition, gene structures and phylogenic implications Plant Cell Physiol 45 138–145 Occurrence Handle10.1093/pcp/pch013 Occurrence Handle14988484
AE Yakushevska PE Jensen W Keegstra RH Particlevan HV Scheller EJ Boekema JP Dekker (2001) ArticleTitleSupermolecular organization of Photosystem II and its associated light-harvesting antenna in Arabidopsis thaliana Eur J Biochem 268 6020–6028 Occurrence Handle11732995
AE Yakushevska W Keegstra EJ Boekema JP Dekker J Andersson S Jansson AV Ruban P Horton (2003) ArticleTitleThe structure of Photosystem II in Arabidopsis: Localization of the CP26 and CP29 antenna complexes Biochemistry 42 608–613 Occurrence Handle10.1021/bi027109z Occurrence Handle12534272
DH Yang H Paulsen B Andersson (2000) ArticleTitleThe N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis FEBS Lett 466 385–388 Occurrence Handle10.1016/S0014-5793(00)01107-8 Occurrence Handle10682866
DH Yang J Webster Z Adam M Lindahl B Andersson (1998) ArticleTitleInduction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of Photosystem II in response to elevated light intensities Plant Physiol 118 827–834 Occurrence Handle10.1104/pp.118.3.827 Occurrence Handle9808726
H Zhang HM Goodman S Jansson (1997) ArticleTitleAntisense inhibition of the Photosystem I antenna protein Lhca4 in Arabidopsis thaliana Plant Physiol 115 1525–1531 Occurrence Handle9414561
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tanaka, R., Tanaka, A. Effects of Chlorophyllide a Oxygenase Overexpression on Light Acclimation inArabidopsis thaliana. Photosynth Res 85, 327–340 (2005). https://doi.org/10.1007/s11120-005-6807-z
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11120-005-6807-z