Skip to main content
Log in

Effects of pigment-deficient mutants on the accumulation of photosynthetic proteins in maize

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have monitored the accumulation of photosynthetic proteins in developing pigment-deficient mutants of Zea mays. The proteins examined are the CO2-fixing enzymes, phoshoenolpyruvate carboxylase (E.C. 4.1.1.31) and ribulose-1,5-bisphosphate carboxylase (E.C.4.1.1.39), and three thylakoid membrane proteins, the light-harvesting chlorophyll a/b binding protein (LHCP) of photosystem II, the 65 kilodalton chlorophyll a binding protein of photosystem I and the alpha subunit polypeptide of coupling factor I. Using a sensitive protein-blot technique, we have compared the relative quantities of each protein in mutants and their normal siblings. Carboxylase accumulation was found to be independent of chlorophyll content, while the amounts of the thylakoid proteins increase at about the same time as chlorophyll in delayed-greening mutants. The relative quantity of LHCP is closely correlated with the relative quantity of chlorophyll at all stages of development in all mutants. Because pigment-deficient mutants are arrested at early stages in chloroplast development, these findings suggest that the processes of chloroplast development, chlorophyll synthesis and thylakoid protein accumulation are coordinated during leaf development but that carboxylase accumulation is controlled by different regulatory mechanisms. A white leaf mutant was found to contain low levels of LHCP mRNA, demonstrating that the accumulation of LHCP mRNA is not controlled exclusively by phytochrome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Anderson, JM, Woo, KC, Boardman, NK: Photochemical studies in mesophyll and bundle sheath chloroplasts of C4 plants. Biochim Biophys Acta 245: 398–408, 1971.

    Google Scholar 

  2. Anderson, JM, Levine, RP. The relationship between chlorophyll-protein complexes and chloroplast membrane polypeptides. Biochim Biophys Acta 357: 118–128, 1974.

    Google Scholar 

  3. Apel, K, Kloppstech, K: The plastid membranes of barley (Hordeum vulgare). Light-induced appearance of mRNA coding for the apoprotein of the light-harvesting chlorophyll a/b protein. Eur J Biochem 85: 581–588 1978.

    Google Scholar 

  4. Apel, K: Phytochrome-induced appearance of mRNA activity for the apoprotein of the light-harvesting chlorophyll a/b protein of barley (Hordeum vulgare). Eur J Biochem 97: 183–188, 1979.

    Google Scholar 

  5. Apel, K, Kloppstech, K: The effect of light on the biosynthesis of the light-harvesting chlorophyll a/b protein. Planta 150: 426–430, 1980.

    Google Scholar 

  6. Arnon, D: Copper enzymes in isolated chloroplasts: polyphenyl-oxidases in Beta vulgaris. Plant Physiol 24: 1–15, 1949.

    Google Scholar 

  7. Aviv, H, Leder, P: Purification of biologically active messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci USA 69: 1408–1412, 1972.

    Google Scholar 

  8. Bennett, J. Biosynthesis of the light-harvesting chlorophyll a/b protein: polypeptide turnover in darkness. Eur J Biochem 118: 61–70, 1981.

    Google Scholar 

  9. Bensadoun, A, Weinstein, D: Assay of proteins in the presence of interfering materials. Anal Biochem 70: 241–250, 1976.

    Google Scholar 

  10. Bjorkman, O, Troughton, J, Nobs, M: Photosynthesis in relation to leaf structure. In: Basic Mechanisms in Plant Morphogenesis. Brookhaven Symp in Biol, vol. XXV, U.S. Dept. of Commerce Springfield, Virginia, 1974, pp. 206–217.

    Google Scholar 

  11. Bogorad, L: Control mechanisms in plastid development. In: Locke, M (ed) Control Mechanisms in Developmental Processes. Suppl. 1. Academic Press, New York, 1967, pp. 1–31.

    Google Scholar 

  12. Bradbeer, JW: Development of photosynthetic function during chloroplast biogenesis. In: Stumpf, PK, Conn, EE (eds) Biochemistry of Plants. Vol. 8, Academic Press, New York, 1981, pp. 424–472.

    Google Scholar 

  13. Cashmore, AR, Broadhurst, MK, Gray, RE: Cell-free synthesis of leaf protein: identification of an apparent precursor of the small subunit of ribulose 1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 75: 655–659, 1978.

    Google Scholar 

  14. Chollet, R, Ogren, WL. Greening in a virescent mutant of maize. II. Enzyme studies. Z Pflanzenphysiol 68: 45–54, 1972.

    Google Scholar 

  15. Chua, N-H, Blomberg, F: Immunological studies of thylakoid membrane polypeptides from spinach and Chlamydomonas reinhardii. J Biol Chem 254: 215–233, 1979.

    Google Scholar 

  16. Chua, N-H, Schmidt, GW. Transprrt of proteins into mitochondria and chloroplasts. J Cell Biol 81: 461–483, 1979.

    Google Scholar 

  17. Chua, N-H: Electrophoretic analysis of chloroplast proteins. Methods Enzymol 69: 434–446, 1980.

    Google Scholar 

  18. Coe, EH, Neuffer, MG: The genetics of corn. In: Sprague, GF (ed) Corn and Corn Improvement. American Society of Agronomy, Madison, Wisconsin (USA), 1977, pp. 111–223.

    Google Scholar 

  19. Coen, DM, Bedbrook, JR, Bogorad, L, Rich, A. Maize chloroplast DNA fragment encoding the large subunit of ribulose bisphosphate carboxylase. Proc Natl Acad Sci USA 74: 5487–5491, 1977.

    Google Scholar 

  20. Cuming, AC, Bennett, J: Biosynthesis of the light-harvesting chlorophyll a/b protein: control of messenger RNA activity by light. Eur J Biochem 118: 71–80, 1981.

    Google Scholar 

  21. Denhardt, DT: A membrane filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23: 641–646, 1966.

    Google Scholar 

  22. Eyster, WH: Plastid studies in genetic types of maize: argentia chlorophyll. Plant Physiol 8: 105–122, 1933.

    Google Scholar 

  23. Forger, JMIII, Bogorad, L. Steps in the acquisition of photosynthetic competence by plastids of maize. Plant Physiol 52: 491–497, 1973.

    Google Scholar 

  24. Fork, DC, Heber, HW: Studies in electron transport reactions of photosynthesis in plastome mutants of Oenothera. Plant Physiol 43: 606–612, 1968.

    Google Scholar 

  25. Goldberg, DA: Isolation and partial characterization of the Drosophila alcohol dehydrogenase gene. Proc Natl Acad Sci USA 77: 5794, 1980.

    Google Scholar 

  26. Hachtel, W: In vitro synthesis of membrane proteins by isolated chloroplasts of Vicia faba. Ber Dtsch Bot Ges Bd 89: 185–192, 1976.

    Google Scholar 

  27. Hague, DR, Sims, TL: Evidence for the light-stimulated synthesis of phosphoenolpyruvate carboxylase in leaves of maize. Plant Physiol 66: 505–509, 1980.

    Google Scholar 

  28. Hayakawa, S, Matsunaga, K, Sugiyama, T: Light induction of phosphoenolpyruvate carboxylase in etiolated maize leaf tissue. Plant Physiol 67: 133–138, 1981.

    Google Scholar 

  29. Highland, PE, Ellis, RJ: Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271: 420–424, 1978.

    Google Scholar 

  30. Huber, SC, Hall, TC, Edward, GE: Differential location of fraction I protein between chloroplast types. Plant Physiol 57: 730–733, 1976.

    Google Scholar 

  31. Kamienietzky, A, Nelson, N: Preparation and properties of chloroplast coupling factor 1 by sodium bromide treatment. Plant Physiol 55: 282–287, 1975.

    Google Scholar 

  32. Kawashima, N, Wildman, SG: Studies on fraction I protein. IV. Mode of inheritance of primary structure in relation to whether chloroplast or nuclear DNA contains the code for a chloroplast protein. Biochim Biophys Acta 262: 42–49, 1972.

    Google Scholar 

  33. Kirchanski, SJ, Park, RB. Comparative studies of the thylakoid proteins of mesophyll and bundle sheath plastids of Zea mays. Plant Physiol 58: 45–49, 1976.

    Google Scholar 

  34. Kirk, JTO, Tilney-Basset, RAE: The Plastids: Their Chemistry Structure, Growth and Inheritance. Elsevier/North Holland Biomedica, Amsterdam, The Netherlands, 1978.

    Google Scholar 

  35. Kobayashi, H, Asami, S, Akazawa, T: Development of enzymes involved in photosynthetic carbon assimilation in greening seedlings of Zea mays Plant Physiol 65: 198–203, 1980.

    Google Scholar 

  36. Kung, SD: Tobacco fraction I protein: a unique genetic marker. Science 191: 429–434, 1976.

    Google Scholar 

  37. Laetsch, WM: The C-4 syndrome; a structural analysis. Ann Rev Plant Physiol 25: 27–52, 1974.

    Google Scholar 

  38. Lehrach, H, Diamond, D, Wozney, JM, Boedtker, H: RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical evaluation. Biochem 16: 4743–4751, 1977.

    Google Scholar 

  39. Link, G, Coen, DM, Bogorad, L: Differential expression of the gene for the large subunt of ribulose bisphosphate carboxylase in maize leaf cells. Cell 15: 725–731, 1978.

    Google Scholar 

  40. Lowry, OH, Rosebrough, NJ, Farr, DL, Randall, RJ: Protein measurement with the folin phenol reagent. J Biol Chem 193: 265–275, 1951.

    Google Scholar 

  41. Mascia, PN, Robertson, DS: Studies in chloroplast development in four maize mutants defective in chlorophyll biosynthesis. Planta 143: 207–211, 1978.

    Google Scholar 

  42. Mascia, PN, Robertson, DS: Genetic studies of the chlorophyll biosynthesis mutants of maize. J Heredity 71: 19–24, 1980.

    Google Scholar 

  43. Mendiola-Morgenthaler, LR, Morgenthaler, JJ Price, CA: Synthesis of coupling factor CF1 protein by isolated spinach chloroplasts. FEBS Letts 62: 96–100, 1976.

    Google Scholar 

  44. Miles, D: The use of mutations to probe photosynthesis in higher plants. In: Edelman, M, Hallick, RB, Chua, N-H (eds) Methods in Chloroplast Molecular Biology. Elsevier Biomedical Press. Amsterdam, 1982, pp. 75–107.

    Google Scholar 

  45. Nelson T, Harpster MH, Mayfield SP, Taylor WC: Lightregulated gene expression during maize leaf development. J Cell Biol: 1984, in press.

  46. Neuffer, MG, Coe, EH: Paraffin oil technique for treating corn pollen with chemical mutagens. Maydica 13: 21–28, 1978.

    Google Scholar 

  47. Nyari, LJ, Tan, YH, Ehrlich, HA: Production and characterization of monoclonal antibodies to human fibroblasts (beta) interferon. In: DeMaeyer, E, Galasso, G, Schellekenes, H (eds) The Biology of the Interferons. Elsevier/North Holland, New York, 1981, pp. 67–73.

    Google Scholar 

  48. Perchorowicz, JT, Gibbs, M: Carbon dioxide fixation and related properties in sections of the developing green maize leaf. Plant Physiol 65: 802–809, 1980.

    Google Scholar 

  49. Perrot-Rechenmann, C, Vidal, J, Brulfert, J, Burlet, A, Gadal, P: A comparative immunocytochemical localization study of phosphoenolpyruvate carboxylase in leaves of higher plants. Planta 155: 24–30, 1982.

    Google Scholar 

  50. Rigby, PW, Dieckman, M, Rhodes, C, Berg, P: Labelling deoxyribonucleic acids to high specific activity in vitro by nick-translation with DNA polymerase I. J Mol Biol 113: 237–251, 1977.

    Google Scholar 

  51. Schmidt, GW, Bartlett, S, Grossman, AR, Cashmore, AR, Chua, N-H: In vitro synthesis, transport and assembly of the constituent polypeptides of the light-harvesting chlorophyll a/b protein complex. In: Leaver, CJ (ed) Genome Organization and Expression in Plants. Plenum Press, New York, 1980, pp.337–352.

    Google Scholar 

  52. Schmidt, GW, Bartlett, SG, Grossman, AR. Chua, N-H: Biosynthetic pathways of two polypeptide subunits of the light-harvesting chlorophyll a/b protein complex. J Cell Biol 91:468–478, 1981.

    Google Scholar 

  53. Schwarz, HP, Kloppstech, K: Effects of nuclear mutations on the structure and function of plastids in pea. Planta 155: 116–123 1982.

    Google Scholar 

  54. Sharman, BC: Developmental anatomy of the shoot of Zea mays L. Ann Bot 6:245–282 1942.

    Google Scholar 

  55. Siemenroth, A, Borner, T, Metzger, U: Biochemical studies on the iojap mutant of maize. Plant Physiol 65:108–110, 1980.

    Google Scholar 

  56. Simpson, DG, Hoyer-Hansen, Chua, N-H, vonWectstein, D: The use of gene mutants in barley to correlate thylakoid polypeptide composition with structures of the photosynthetic membrane. In: Hall, DO, Coombs, J, Goodwin, JW (eds) Proc 4th Int Congr Photosynthesis. The Biochemical Society, London, 1977, pp.527–548.

    Google Scholar 

  57. Simpson, E: Biochemical and genetic studies of the synthesis and degradation of RUBP carboxylase. In: Siegelman, HW, Hind, G (eds) Basic Life Sciences. Vol II. Photosynthetic Carbon Assimilation. Plenum Press. New York, 1978, pp.113–124.

    Google Scholar 

  58. Slovin, JP, Tobin, EM: Synthesis and turnover of the light-harvesting chlorophyll a/b protein in Lemna gibba grown with intermittent red light: possible translation control. Planta 154:465–472, 1982.

    Google Scholar 

  59. Smillie, RM, Nielson, NC, Henningsen, KW, vonWettstein, D: Development of photochemical activity in chloroplast membranes. I. Studies with mutants of barley grown under a single environment. Aust J Plant Physiol 4:415–438, 1977.

    Google Scholar 

  60. Smith, JHC, Durham, L, Weinstein, CF. Formation and bleaching of chlorophyll in albino corn seedlings. Plant Physiol 150:41–45, 1959.

    Google Scholar 

  61. Smith, SM, Ellis, RJ: Processing of small subunit precursor of ribulose bisphosphate carboxylase and its assembly into whole enzyme are stromal events. Nature 278:662–664, 1979.

    Google Scholar 

  62. Stamp, P: Der Chlorophyllgehalt, die PEP-und-RuDP-Car-boxylase Aktivitäten während der Blattentwicklung einet ergrünenden Chlorophyll mutants und eine normalen Linie von Zea mays L. Z Pflanzenphysiol 86:395–404, 1978.

    Google Scholar 

  63. Thomas, PS: Hybridization of denatured RNA and small DNA fragments to nitrocellulose. Proc Natl Acad Sci USA 77:5201–5205, 1980.

    Google Scholar 

  64. Tobin, EM, Suttie, JL: Light effects on the synthesis of ribulose 1,5-bisphosphate carboxylase in Lemna gibba L. (G-3). Plant Physiol 65:641–647, 1980.

    Google Scholar 

  65. Tobin, EM: White light effects on the mRNA for the light-harvesting chlorophyll a/b-protein in Lemna gibba L. (G-3). Plant Physiol 67:1078–1083, 1981a.

    Google Scholar 

  66. Tobin, EM: Phytochrome-mediated regulation of mRNAs for the small subunit of ribulose 1,5-bisphosphate carboxylase and the light-harvesting chlorophyll a/b-protein in Lemna gibba. Plant Molec Biol 1:35–51, 1981b.

    Google Scholar 

  67. Viro, M, Kloppstech, K: Expression of genes for plastid membrane proteins in barley under intermittent light conditions. Planta 154:18–23, 1982.

    Google Scholar 

  68. Weidner, M, Steinbiss, H, Kremer, BP: Correlations between photosynthetic enzymes, CO2-fixation and plastid structure in an albino mutant of Zea mays L. Planta 131:262–270, 1976.

    Google Scholar 

  69. Wettstein, Dvon Hennigsen, KW, Boynton, JE, Kannagara, GF, Nielsen, OF: The genetic control of chloroplast development in barley. In: Boardman, NK, Linane, AW, Smillie, RM (eds) Autonomy and Biogenesis of Mitochondria and Chloroplasts. North Holland, Amsterdam, 1971, pp.205–223.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harpster, M.H., Mayfield, S.P. & Taylor, W.C. Effects of pigment-deficient mutants on the accumulation of photosynthetic proteins in maize. Plant Mol Biol 3, 59–71 (1984). https://doi.org/10.1007/BF00040030

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00040030

Key words

Navigation