Advertisement

Plant Molecular Biology

, Volume 42, Issue 2, pp 303–316 | Cite as

Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii

  • Christian Richard
  • Hugues Ouellet
  • Michel Guertin
Article

Abstract

The LI818 gene from Chlamydomonas encodes a polypeptide that is related to the chlorophyll a/b-binding proteins (CAB) of higher plants and green algae. However, despite this relatedness, LI818 gene expression is not coordinated with that of cab genes and is regulated differently by light, suggesting a different role for LI818 polypeptide. We show here that, in contrast to CAB polypeptides, LI818 polypeptide is not tightly embedded into the thylakoid membranes and is localized in stroma-exposed regions. Moreover, during chloroplast development, LI818 polypeptide accumulates before CAB polypeptides. We also show that the LI818 polypeptide forms with certain chlorophyll a/c-binding proteins (CAC) from the haptophyte Isochrysis galbana and the diatom Cyclotella cryptica a natural group that is distinct from those constituted by CAB, CAC and the chlorophyll a/a-binding proteins (CAA). Such an association suggests a very ancient origin for this group of polypeptides, which predates the division of the early photosynthetic eukaryotes into green (chlorophyte), red (rhodophyte) and brown (chromophyte) algae. Possible roles for the LI818 polypeptide are discussed.

chlorophyll a/b-binding protein green alga greening light-regulated expression phylogeny thylakoid 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adir, N., Shochat, S. and Ohad, I. 1990. Light-dependent D1 protein synthesis and translocation is regulated by reaction center II. Reaction center II serves as an acceptor for the D1 precursor. J. Biol. Chem. 265: 12563–12568.Google Scholar
  2. Allen, K.D. and Staehelin, L.A. 1994. Polypeptide composition, assembly and phosphorylation patterns of the photosystem II antenna system of Chlamydomonas reinhardtii. Planta 194: 42–54.Google Scholar
  3. Anandan, S., Morishige, D.T. and Thornber, J.P. 1993. Lightinduced biogenesis of light-harvesting complex I (LHC I) during chloroplast development in barley (Hordeum vulgare). Studies using cDNA clones of the 21-and 20-kilodalton LHC I apoproteins. Plant Physiol. 101: 227–236.Google Scholar
  4. Apt, K.E., Clendennen, S.K., Powers, D.A. and Grossman, A.R. 1995. The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera. Mol. Gen. Genet. 246: 455–464.Google Scholar
  5. Bassi, R. and Wollman, F.A. 1991. The chlorophyll a/b proteins of photosystem II in Chlamydomonas reinhardtii: isolation, characterization and immunological cross-reactivity to higher-plant polypeptides. Planta 183: 423–433.Google Scholar
  6. Bassi, R., Soen, S.Y., Frank, G., Zuber, H. and Rochaix, J.D. 1992. Characterization of chlorophyll a/b proteins of photosystem I from Chlamydomonas reinhardtii. J. Biol. Chem. 267: 25714–25721.Google Scholar
  7. Breyton, C., de Vitry, C. and Popot, J.L. 1994. Membrane association of cytochrome b6f subunits. The Rieske iron-sulfur protein from Chlamydomonas reinhardtii is an extrinsic protein. J. Biol. Chem. 269: 7597–7602.Google Scholar
  8. Caron, L., Douady, D., Quinetszely, M., Degoer, S. and Berkaloff, C. 1996. Gene structure of a chlorophyll a/c-binding protein from a brown alga: presence of an intron and phylogenetic implications. J. Mol. Evol. 43: 270–280.Google Scholar
  9. Chua, N.H. and Bennoun, P. 1975. Thylakoid membrane polypeptides of Chlamydomonas reinhardtii wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl. Acad. Sci. USA 72: 2175–2179.Google Scholar
  10. Couture, M. and Guertin, M. 1996. Purification and spectroscopic characterization of a recombinant chloroplastic hemoglobin from the green unicellular alga Chlamydomonas eugametos. Eur. J. Biochem. 242: 779–787.Google Scholar
  11. Durnford, D.G., Aebersold, R. and Green, B.R. 1996. The fucoxanthin-chlorophyll proteins from a chromophyte alga are part of a large multigene family: structural and evolutionary relationships to other light harvesting antennae. Mol. Gen. Genet. 253: 377–386.Google Scholar
  12. Durnford, D.G., Deane, J.A., Tan, S., McFadden, G.L., Gantt, E. and Green, B.R. 1999. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 48: 59–68.Google Scholar
  13. Eppard, M. and Rhiel, E. 1998. The genes encoding light-harvesting subunits of Cyclotella cryptica (Bacillariophyceae) constitute a complex and heterogeneous family. Mol. Gen. Genet. 260: 335–345.Google Scholar
  14. Gagne, G. and Guertin, M. 1992. The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol. Biol. 18: 429–445.Google Scholar
  15. Green, B.R. and Kuhlbrandt, W. 1995. Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosyn. Res. 44: 139–148.Google Scholar
  16. Herrin, D.L., Plumley, F.G., Ikeuchi, M., Michaels, A.S. and Schmidt, G.W. 1987. Chlorophyll antenna proteins of photosystem I: topology, synthesis and regulation of the 20-kDa subunit of Chlamydomonas light-harvesting complex of photosystem I. Arch. Biochem. Biophys. 254: 397–408.Google Scholar
  17. Hiller, R.G., Wrench, P.M. and Sharples, F.P. 1995. The lightharvesting chlorophyll a-c-binding protein of dinoflagellates: a putative polyprotein. FEBS Lett 363: 175–178.Google Scholar
  18. Hoober, J.K., Marks, D.B., Keller, B.J. and Margulies, M.M. 1982. Regulation of accumulation of the major thylakoid polypeptides in Chlamydomonas reinhardtii y-1 at 25 º C and 38 º C. J. Cell Biol. 95: 552–558.Google Scholar
  19. Kroth-Pancic, P.G. 1995. Nucleotide sequence of two cDNAs encoding fucoxanthin chlorophyll a/c proteins in the diatom Odontella sinensis. Plant Mol. Biol. 27: 825–828.Google Scholar
  20. Kuhlbrandt, W., Wang, D.N. and Fujiyoshi, Y. 1994. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621.Google Scholar
  21. LaRoche, J., Henry, D., Wyman, K., Sukenik, A. and Falkowski, P. 1994. Cloning and nucleotide sequence of a cDNA encoding a major fucoxanthin-, chlorophyll a/c-containing protein from the chrysophyte Isochrysis galbana: implications for evolution of the cab gene family. Plant Mol. Biol. 25: 355–368.Google Scholar
  22. Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193: 265–275.Google Scholar
  23. Malnoe, P., Mayfield, S.P., Rochaix, J.D. 1988. Comparative analysis of the biogenesis of photosystem II in the wild-type and Y-1 mutant of Chlamydomonas reinhardtii. J. Cell. Biol. 106: 609–616.Google Scholar
  24. Melis, A., Murakami, A., Nemson, J.A., Aizawa, K., Ohki, K. and Fujita, Y. 1996. Chromatic regulation in Chlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosyn. Res. 47: 253–265.Google Scholar
  25. Morrissey, P.J., McCauley, S.W. and Melis, A. 1986. Differential detergent solubilization of integral thylakoid membrane complexes in spinach chloroplasts. Localization of photosystem II, cytochrome b6-f complex and photosystem I. Eur. J. Biochem. 160: 389–393.Google Scholar
  26. Ohad, I., Siekevitz, P. and Palade, G.E. 1967a. Biogenesis of chloroplast membranes. I. Plastid dedifferentiation in a dark-grown algal mutant (Chlamydomonas reinhardtii). J. Cell. Biol. 35: 521–552.Google Scholar
  27. Ohad, I., Siekevitz, P. and Palade, G.E. 1967b. Biogenesis of chloroplast membranes. II. Plastid differentiation during greening of a dark-grown algal mutant (Chlamydomonas reinhardtii). J. Cell. Biol. 35: 553–584.Google Scholar
  28. Porra, R., Thompson, W. and Kriedemann, P. 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. Biochim. Biophys. Acta 975: 384–394.Google Scholar
  29. Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.Google Scholar
  30. Savard, F., Richard, C. and Guertin, M. 1996. The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI/II genes that is regulated during the cell cycle and in response to illumination. Plant Mol. Biol. 32: 461–473.Google Scholar
  31. Swofford, D.L. 1991. PAUP: Phylogenetic Analysis Using Parsimony, Champaign, IL.Google Scholar
  32. Tan, S., Ducret, A., Aebersold, R. and Gantt, E. 1997. Red algal LHC I genes have similarities with both Chl a/b-and a/c-binding proteins: a 21 kDa polypeptide encoded by LhcaR2 is one of the six LHC I polypeptides. Photosyn. Res. 53: 129–140.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Christian Richard
    • 1
  • Hugues Ouellet
    • 1
  • Michel Guertin
    • 1
  1. 1.Department of Biochemistry, Faculty of Sciences and EngineeringLaval UniversityCanada

Personalised recommendations