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Chlorophyllide a Oxygenase mRNA and Protein Levels Correlate with the Chlorophyll a/b Ratio in Arabidopsis thaliana

Photosynthesis Research volume 79, pages 149–159 (2004)Cite this article

Abstract

Plants can change the size of their light harvesting complexes in response to growth at different light intensities. Although these changes are small compared to those observed in algae, their conservation in many plant species suggest they play an important role in photoacclimation. A polyclonal antibody to the C-terminus of the Arabidopsis thaliana chlorophyllide a oxygenase (CAO) protein was used to determine if CAO protein levels change under three conditions which perturb chlorophyll levels. These conditions were: (1) transfer to shaded light intensity; (2) limited chlorophyll synthesis, and (3) during photoinhibition. Transfer of wild-type plants from moderate to shaded light intensity resulted in a slight reduction in the Chl a/b ratio, and increases in both CAO and Lhcb1 mRNA levels as well as CAO protein levels. CAO protein levels were also measured in the cch1 mutant, a P642L missense mutation in the H subunit of Mg-chelatase. This mutant has reduced total Chl levels and an increased Chl a/b ratio when transferred to moderate light intensity. After transfer to moderate light intensity, CAO mRNA levels decreased in the cch1 mutant, and a concomitant decrease in CAO protein levels was also observed. Measurements of tetrapyrrole intermediates suggested that decreased Chl synthesis in the cch1 mutant was not a result of increased feedback inhibition at higher light intensity. When wild-type plants were exposed to photoinhibitory light intensity for 3 h, total Chl levels decreased and both CAO mRNA and CAO protein levels were also reduced. These results indicate that CAO protein levels correlate with CAO mRNA levels, and suggest that changes in Chl b levels in vascular plants, are regulated, in part, at the CAO mRNA level.

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References

  • Adamska I (1997) ELIPs-light-induced stress proteins. Physiol Plant 100: 794–805

    CAS  Article  Google Scholar 

  • Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P and Jansson S (2003) Absence 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

    Google Scholar 

  • Aro E-M, Virgin I and Andersson B (1993) Photoinhibition of Photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134

    PubMed  CAS  Article  Google Scholar 

  • Barber J and Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem 17: 61–66

    CAS  Article  Google Scholar 

  • Barkan A (1998) Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants. Meth Enzymol 297: 38–57

    CAS  Article  Google Scholar 

  • Baroli I, Do AD, Yamane T and Nigyogi K (2003) Zeaxanthin accumulation in the absence of a functional xanthophylls cycle protects Chlamydomonas reinhardtii from photooxidative stress.Plant Cell 15: 992–1008

    PubMed  CAS  Article  Google Scholar 

  • Brusslan JA and Tobin EM (1992) Light-independent developmental regulation of cab gene expression in Arabidopsis thaliana seedlings. Proc Natl Acad Sci USA 89: 7791–7795

    PubMed  CAS  Article  Google Scholar 

  • Cornah JE, Terry MJ and Smith AG (2003) Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 8: 224–230

    PubMed  CAS  Article  Google Scholar 

  • Droppa M, Ghirardi ML, Horvath G and Melis A (1988) Chlorophyll b deficiency in soybean mutants. II. Thylakoid membrane development and differentiation. Biochem Biophys Acta 932: 138–145

    CAS  Article  Google Scholar 

  • Espineda CE, Linford AS, Devine D and Brusslan JA (1999) The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 96: 10507–10511

    PubMed  CAS  Article  Google Scholar 

  • Falbel TG and Staehelin LA (1992) Species-related differences in the electrophoretic behavior of CP 29 and CP 26: an immunochemical analysis. Photosynth Res 34: 249–262

    CAS  Article  Google Scholar 

  • Falbel TG and Staehelin LA (1996) Partial blocks in the early steps of the chlorophyll synthesis pathway: a common feature of chlorophyll b-deficient mutants. Physiol Plant 97: 311–320

    CAS  Article  Google Scholar 

  • Flachmann R and Kühlbrandt W (1995) Accumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobacco. Plant Cell 7: 149–160

    PubMed  CAS  Article  Google Scholar 

  • Greene BA, Allred DR, Morishige DT and Staehelin LA (1988) Hierarchical response of light-harvesting chlorophyll-proteins in a light-sensitive chlorophyll b-deficient mutant of maize. Plant Physiol 87: 357–364

    PubMed  CAS  Google Scholar 

  • Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K and Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100: 4921–4926

    PubMed  CAS  Article  Google Scholar 

  • Kim JH, Glick RE and Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102: 181–190

    PubMed  CAS  Google Scholar 

  • Knoetzel J and Simpson D (1991) Expression and organization of antenna proteins in the light-and temperature-sensitive barley mutant chlorina104. Planta 185: 111–123

    CAS  Article  Google Scholar 

  • Król M, Spangfort MD, Huner NPA, Öquist G, Gustafsson P and Jansson S (1995) Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol 107: 873–883

    PubMed  Article  Google Scholar 

  • Larsson UK, Anderson JM and Andersson B (1987) Variations in the relative content of the peripheral and inner light-harvesting chlorophyll a/b-protein complex (LHCII) subpopulations during thylakoid light adaptation and development. Biochem Biophys Acta 894: 69–75

    CAS  Article  Google Scholar 

  • Leong T-Y and Anderson JM (1984) Adaptation of the thylakoid membranes of the pea chloroplasts to light intensities. I. Study on the distribution of chlorophyll–protein complexes. Photosynth Res 5: 105–115

    CAS  Article  Google Scholar 

  • Masuda T, Polle JEW and Melis A (2002) Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol 128: 603–614

    PubMed  CAS  Article  Google Scholar 

  • 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

    PubMed  CAS  Article  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A and Chory J (2001) Arabidopsis genome uncoupled 5 (gun5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053–2058

    PubMed  CAS  Article  Google Scholar 

  • Montané M-H, Tardy F, Kloppstech K and Havaux M(1998) Differential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of barley leaves to light irradiance.Plant Physiol 118: 227–235

    PubMed  Article  Google Scholar 

  • Murchie EH and Horton P (1997) Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference.Plant Cell Environ 20: 438–448

    Article  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Physiol Plant Mol Biol 50: 333–359

    CAS  Article  Google Scholar 

  • Oster U, Bauer CE and Rüdiger W (1997) Characterization of chlorophyll a and bacteriochlorophyll a synthases by heterologous expression in Escherichia coli. J Biol Chem 272: 9671–9676

    PubMed  CAS  Article  Google Scholar 

  • Oster U, Tanaka R, Tanaka A and Rüdiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana.Plant J 21: 305–310

    PubMed  CAS  Article  Google Scholar 

  • Papenbrock J, Mock HP, Tanaka R, Kruse E and Grimm B (2000) Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol 122: 1161–1169

    PubMed  CAS  Article  Google Scholar 

  • Peter GF and Thornber JP (1991) Biochemical composition and organization of higher plant Photosystem II light-harvesting pigment-proteins. J Biol Chem 266: 16745–16754

    PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA and Kriedmann PA (1989) Determination 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. Biochem Biophys Acta 975: 384–394

    CAS  Google Scholar 

  • Preiss S and Thornber JP (1995) Stability of apoproteins of lightharvesting complex I and II during biogenesis of thylakoids in the chlorophyll b-less barley mutant chlorina f2. Plant Physiol 107: 709–717

    PubMed  CAS  Google Scholar 

  • Rüdiger W(2002) Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynth Res 74: 187–193

    PubMed  Article  Google Scholar 

  • 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 flexibility of the proteins. J Biol Chem 276: 4293–4297

    PubMed  CAS  Article  Google Scholar 

  • Sigrist M and Staehelin LA (1992) Identification of type 1 and type 2 light-harvesting chlorophyll a/b-binding proteins using monospecific antibodies. Biochem Biophys Acta 1098: 191–200

    PubMed  CAS  Google Scholar 

  • Sigrist M and Staehelin LA (1994) Appearance of Type 1, 2, and 3light-harvesting complex II and light-harvesting complex I proteins during light-induced greening of barley (Hordeum vulgare) etioplasts. Plant Physiol 104: 135–145

    PubMed  CAS  Article  Google Scholar 

  • Sukenik A, Bennett J, Mortain-Bertrand A and Falkowski PG (1990) Adaptation of the photosynthetic apparatus to irradiance in Dunaliella tertiolecta. Plant Physiol 92: 891–898

    PubMed  CAS  Article  Google Scholar 

  • Tanaka A, Ito H, Tanaka R, Tanaka NK, 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

    PubMed  CAS  Article  Google Scholar 

  • Tanaka R, Koshino Y, Sawa S, Ishigura 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

    PubMed  CAS  Article  Google Scholar 

  • Teramoto H, Nakamori A, Minagawa J and Ono T-A (2002) Lightintensity-dependent expression of the Lhc gene family encoding light-harvesting chlorophyll-a/b proteins of Photosystem II in Chlamydomonas reinhardtii. Plant Physiol 130: 325–333

    PubMed  CAS  Article  Google Scholar 

  • Thornber JP, Cogdell RJ, Chitnis P, Morishige DT, Peter GF, Gómez SM, Anandan S, Preiss S, Dreyfuss BW, Lee A, Takeuchi T and Kerfield C (1994) Antenna pigment–protein complexes of higher plants and purple bacteria. Adv Mol Cell Biol 10: 55–118

    CAS  Google Scholar 

  • Tomitani A, Okada K, Miyashita H, Matthijs HCP, Ohno T and Tanaka A (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400: 159–162

    PubMed  CAS  Article  Google Scholar 

  • Walters RG and Horton P (1994) Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus. Planta 195: 248–256

    CAS  Article  Google Scholar 

  • Xu H, Vavilin D and Vermaas W (2001) Chlorophyll b can serve as the major pigment in functional Photosystem II complexes of cyanobacterium. Proc Natl Acad Sci USA 98: 14168–14173

    PubMed  CAS  Article  Google Scholar 

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Affiliations

  1. Department of Biological Sciences, California State University, Long Beach, 1250 Bellflower Blvd, Long Beach, CA, 90840-3702, USA

    Andrea L. Harper, Sigrid E. von Gesjen, Alicia S. Linford, Michael P. Peterson, Ruth S. Faircloth, Michelle M. Thissen & Judy A. Brusslan

  2. Department of Biochemistry, University of Washington, 1959 NE Pacific St., Seattle, WA, 98195-7350, USA

    Andrea L. Harper & Alicia S. Linford

  3. Nichols Institute Diagnostics, 1311 Calle Batido, San Clemente, CA, 92673, USA

    Michael P. Peterson

  4. F. Edward Hébert School of Medicine, Uniformed Services University, 4301 Jones Bridge Road, Bethesda, MD, 20814-4799, USA

    Ruth S. Faircloth

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  1. Andrea L. Harper
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  2. Sigrid E. von Gesjen
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Harper, A.L., von Gesjen, S.E., Linford, A.S. et al. Chlorophyllide a Oxygenase mRNA and Protein Levels Correlate with the Chlorophyll a/b Ratio in Arabidopsis thaliana . Photosynthesis Research 79, 149–159 (2004). https://doi.org/10.1023/B:PRES.0000015375.40167.76

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  • DOI: https://doi.org/10.1023/B:PRES.0000015375.40167.76

  • CAO
  • chlorophyll b
  • chlorophyllide
  • a oxygenase
  • Elip
  • Lhcb
  • photoacclimation
  • photoinhibition
  • protochlorophyllide