Plant Molecular Biology

, Volume 8, Issue 3, pp 227–238 | Cite as

Regulation of levels of nuclear transcripts for C4 photosynthesis in bundle sheath and mesophyll cells of maize leaves

  • Jenq-Yunn Sheen
  • Lawrence Bogorad
Article
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Abstract

In vitro translation of polyA+ mRNAs isolated from purified maize bundle sheath and mesophyll cells results in the production of distinctive, cell-specific polypeptides. Immunoprecipitation experiments show that translatable polyA+ mRNAs for phosphoenolpyruvate carboxylase (PEPC), pyruvate orthophosphate dikinase (PPDK) and NADP-malate dehydrogenase (MDH) are prominent in mesophyll but not bundle sheath cells. On the contrary, those for sedoheptulose-1,7-bisphosphatase (SBP), fructose-1,6-bisphosphatase (FBP), NADP-malic enzyme (ME) and the small subunit of ribulose-1,5-bisphosphate carboxylase (RuBPC SS) are present only in bundle sheath cells. Moreover, polyA+ mRNAs encoding the 33 kD, 23 kD and 16 kD polypeptides of the oxygen-evolving complex (OE33, OE23 and OE16) and the light-harvesting chlorophyll a/b binding protein of photosystem II (LHCP II) are much more abundant in mesophyll than in bundle sheath cells. Northern blot analyses with cDNA clones of PEPC, PPDK, ME, RuBPC SS, OE33, OE23, OE16 and LHCP II are consistent with the conclusion that the cell-specific expression of these genes is regulated at the RNA level. The RNA level differences are especially dramatic in dark-grown maize seedlings after illumination for 24 h.

Key words

bundle sheath cells C4 photosynthesis immunoprecipitation mesophyll cells Northern blot polyA+ mRNA-in vitro translation 
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References

  1. 1.
    Aoyagi K, Nakamoto H: Pyruvate, Pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves. Plant Physiol 78:661–664, 1985.Google Scholar
  2. 2.
    Bassi R: Spectral properties and polypeptide composition of the chlorophyll-proteins from thylakoids of granal and agranal chloroplasts of maize. Carlsberg Res Commun 50:127–143, 1985.Google Scholar
  3. 3.
    Bassi R, Peruffo AB, Barbato R, Ghisi R: Differences in chlorophyll-protein complexes and composition of polypeptides between thylakoids from bundle sheath and mesophyll cells in maize. Eur J Biochem 146:589–595, 1985.Google Scholar
  4. 4.
    Black CC: Photosynthetic carbon function in relation to net CO2 uptake. Ann Rev Plant Physiol 24:253–286, 1973.Google Scholar
  5. 5.
    Broglie R, Coruzzi G, Keith B, Chua N-H: Molecular biology of C4 photosynthesis in Zea mays: differential localization of proteins and mRNAs in the two leaf cell types. Plant Mol Biol 3:431–444, 1984.Google Scholar
  6. 6.
    Chapman KSR, Berry JA, Hatch MD: Photosynthetic metabolism in bundle sheath cells of the C4 species Zea mays: sources of ATP and NADPH and the contribution of photosystem II. Arch Biochem Biophys 202:330–341, 1980.Google Scholar
  7. 7.
    Collins PD, Hague DR: Light-stimulated synthesis of NADP malic enzyme in leaves of maize. J Biol Chem 258:4012–4018, 1983.Google Scholar
  8. 8.
    Crossland LD, Rodermel SR, Bogorad L: Single gene for the large subunit of ribulosebisphosphate carboxylase in maize yields two differentially regulated mRNAs. Proc Natl Acad Sci USA 81:4060–4060, 1984.Google Scholar
  9. 9.
    Edwards GE, Black CC: Photosynthesis in mesophyll cells and bundle sheath cells isolated from Digitaria sanguinalis (L) leaves. In: Hatch MD, Osmond CD, Slatyer RO (eds) Photosynthesis and Photorespiration, Wiley-Interscience, New York, 1971, pp 153–168.Google Scholar
  10. 10.
    Edwards GE, Huber SC: The C4 pathway. In: Hatch MD, Boardman NK (eds) The Biochemistry of Plants, Vol 8, Photosynthesis. Academic Press, New York, 1981, pp 238–281.Google Scholar
  11. 11.
    Franssen H, Goldbach R, Broekhuijsen M, Moerman M, Kammen A: Expression of middle-component RNA of Cowpea mosaic virus: in vitro generation of a precursor to both capsid proteins by a bottom-component RNA-encoded protease from injected cells. J Virology 41:8–17, 1982.Google Scholar
  12. 12.
    Gubler U, Hoffman BJ: A simple and very efficient method for generating cDNA libraries. Gene 25:263–269, 1983.Google Scholar
  13. 13.
    Hague DR, Sims TL: Evidence for light-stimulated synthesis of phosphoenolpyruvate carboxylase in leaves of maize. Plant Physiol 66:505–509, 1980.Google Scholar
  14. 14.
    Hague DR, Uhler M, Collins PD: Cloning of cDNA for pyruvate, Pi dikinase from maize leaves. Nucl Acids Res 11:4853–4865, 1983.Google Scholar
  15. 15.
    Harrison PA, Black CC: Two-dimensional electrophoretic mapping of proteins of bundle sheath and mesophyll cells of the C4 grass Digitaria sanguinalis. Plant Physiol 70:1359–1366, 1982.Google Scholar
  16. 16.
    Hatch MD: Photosynthesis: the path of carbon. In: Bonner J, Varner JE (eds) Plant Biochemistry, 3rd edn. Academic Press, New York, 1976, pp 797–844.Google Scholar
  17. 17.
    Hatch MD: Regulation of enzymes in C4 photosynthesis. In: Horecker BL, Stadtman ER (eds) Current Topics in Cellular Regulation, Vol 14. Academic Press, New York, 1978, pp 1–27.Google Scholar
  18. 18.
    Hatch MD, Slack CR: Photosynthetic CO2-fixation pathways. Ann Rev Plant Physiol 21:141–162, 1970.Google Scholar
  19. 19.
    Jacquot JP, Buchanan BB, Martin F, Vidal J: Enzyme regulation in C4 photosynthesis, purification and properties of thioredoxin-linked NADP-malate dehydrogenase from corn leaves. Plant Physiol 68:300–304, 1981.Google Scholar
  20. 20.
    Kanai R, Edwards GE: Separation of mesophyll protoplasts and bundle sheath cells from maize leaves for photosynthetic studies. Plant Physiol 51:1133–1137, 1973.Google Scholar
  21. 21.
    Kirchanski SJ, Park RB: Comparative studies of the thylakoid proteins of mesophyll and bundle sheath plastids of Zea mays. Plant Physiol 58:345–349, 1976.Google Scholar
  22. 22.
    Ku SB, Gutierrez M, Kanai R, Edwards GE: Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants, II. Chlorophyll and Hill reaction studies. Z Pflanzenphysiol 72:320–337, 1974.Google Scholar
  23. 23.
    Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277:680–685, 1970.Google Scholar
  24. 24.
    Link G, Coen DM, Bogorad L: Differential expression of the gene for the large subunit of ribulose bisphosphate carboxylase in maize leaf cell types. Cell 15:725–731, 1978.Google Scholar
  25. 25.
    Maas R: An improved colony hybridization method with significantly increased sensitivity for detection of single genes. Plasmid 10:296–298, 1983.Google Scholar
  26. 26.
    Maniatis T, Fritsch EF, Sambrook J: Molecular cloning. Cold Spring Harbor Laboratory, New York, 1982.Google Scholar
  27. 27.
    Martineau B, Taylor WC: Photosynthetic gene expression and cellular differentiation in developing maize leaves. Plant Physiol 78:399–404, 1985.Google Scholar
  28. 28.
    Mayfield SP, Taylor WC: The appearance of photosynthetic proteins in developing maize leaves. Planta 161:481–486, 1984.Google Scholar
  29. 29.
    Nelson T, Harpster MH, Mayfield P, Taylor WC: Light-regulated gene expression during maize leaf development. J Cell Biol 98:558–564, 1984.Google Scholar
  30. 30.
    Nishizawa AN, Buchanan BB: Enzyme regulation in C4 photosynthesis, purification and properties of thioredoxin-linked fructose bisphosphatase and sedoheptulose bisphosphatase from corn leaves. J Biol Chem 256:6119–6126, 1981.Google Scholar
  31. 31.
    Osmond CB: Photorespiration and photoinhibition, some implications for the energetics of photosynthesis. Biochim Biophys Acta 639:77–98, 1981.Google Scholar
  32. 32.
    Parnes JR, Velan B, Felsenfeld A, Ramanthan L, Ferrini U, Appella E, Seidman JG: Mouse β2-microglobulin cDNA clones: a screeding procedure for cDNA clones corresponding to rare mRNAs. Proc Natl Acad Sci USA 78:2253–2257, 1981.Google Scholar
  33. 33.
    Perrot-Rechenmann C, Jacquot JP, Gadal P, Weeden NF, Cseke C, Buchanan BB: Localization of NADP-malate dehydrogenase of corn leaves by immunological methods. Plant Sci Lett 30:219–226, 1983.Google Scholar
  34. 34.
    Perrot-Rechenmann C, Vidal J, Brulfet 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
  35. 35.
    Potter JW, Black CC: Differential protein composition and gene expression in leaf mesophyll cells and bundle sheath cells of the C4 plant Digitaria sanguinalis. Plant Physiol 70:590–597, 1982.Google Scholar
  36. 36.
    Rodermel SR, Bogorad L: Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development. J Cell Biol 100:463–476, 1985.Google Scholar
  37. 37.
    Schuster G, Ohad I, Martineau B, Taylor WC: Differentiation and development of bundle sheath and mesophyll thylakoids in maize. J Biol Chem 260:11866–11873, 1985.Google Scholar
  38. 38.
    Sheen J, Bogorad L: Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells of developing maize leaves is influenced by light. Plant Physiol 79:1072–1076, 1985.Google Scholar
  39. 39.
    Sims TL, Hague DR: Light-stimulated increase of translatable mRNA for phosphoenolpyruvate carboxylase in leaves of maize. J Biol Chem 256:8252–8255, 1981.Google Scholar
  40. 40.
    Slack CR, Hatch MD, Goodchild DJ: Distribution of enzymes in mesophyll and parenchyma-sheath chloroplasts of maize leaves in relation to the C4-dicarboxylic acid pathway of photosynthesis. Biochem J 114:489–498, 1969.Google Scholar

Copyright information

© Martinus Nijhoff Publishers 1987

Authors and Affiliations

  • Jenq-Yunn Sheen
    • 1
  • Lawrence Bogorad
    • 1
  1. 1.The Department of Cellular and Developmental Biology, Biological LaboratoriesHarvard UniversityCambridgeUSA

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