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Post-transcriptional control of cell type-specific gene expression in bundle sheath and mesophyll chloroplasts of Amaranthus hypochondriacus

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Abstract

Plants that utilize the highly efficient C4 photosynthetic pathway possess two types of specialized leaf cells, the mesophyll and bundle sheath. In mature leaves of amaranth, a dicotyledonous C4 plant, ribulose 1,5-bisphosphate carboxylase (Rubisco) is localized specifically to the chloroplasts of bundle sheath cells, and is not present in the chloroplasts of mesophyll cells. The cell type-specific expression of the chloroplast-encoded Rubisco large subunit (rbcL) gene, and other representative chloroplastic genes, was investigated by using separated bundle sheath and mesophyll chloroplasts prepared from mature amaranth leaves. One-dimensional SDS-polyacrylamide gel electrophoresis revealed several differences in the polypeptide compositions of the two chloroplast types. Western analysis demonstrated that, as in the intact leaves, the Rubisco LSU polypeptide was present only in chloroplast preparations from bundle sheath cells. Pyruvate orthophosphate dikinase (PPdK), a nuclear-encoded chloroplastic enzyme, was found only in the mesophyll chloroplast preparations. rbcL mRNA was present only in the bundle sheath chloroplast preparations, whereas transcripts for the chloroplast-encoded psbA, psaA-B, and rpl2 genes were present in both chloroplast types. Although the rbcL message accumulated only in bundle sheath chloroplasts, run-on transcription analysis indicated that the rbcL gene was transcribed in both bundle sheath and mesophyll chloroplast preparations. Therefore, differential rbcL gene expression in the isolated C4 chloroplasts is regulated, at least in part, at the post-transcriptional level. Possibly this control is mediated by differential processing or stabilization of the rbcL transcript.

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References

  1. Berry JO, Nickolau BJ, Carr JP, Klessig DF: Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol 5: 2238–2246 (1985).

    PubMed  Google Scholar 

  2. Berry JO, Carr JP, Klessig DF: mRNAs encoding ribulose-1,5-bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc Natl Acad Sci USA 85: 4190–4194 (1988).

    Google Scholar 

  3. Berry JO, Breiding DE, Klessig DF: Light-mediated control of translational initiation of ribulose-1,5-bisphosphate carboxylase in amaranth cotyledons. Plant Cell 2: 795–803 (1990).

    Article  PubMed  Google Scholar 

  4. Bookjans G, Stummann BM, Henningsen KW: Preparation of chloroplast DNA from pea plastids isolated in a medium of high ionic strength. Anal Biochem 141: 244–247 (1984).

    PubMed  Google Scholar 

  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. Delepelarie P, Chua N-H: Eletrophoretic purification of chlorophyll a/b-protein complexes from Chlamydomonas reinhardtii and spinach and analysis of their polypeptide composition. J Biol Chem 256: 9300–9307 (1981).

    PubMed  Google Scholar 

  7. Deng X-W, Gruissem W: Control of plastid gene expression during development: Limited role of transcriptional regulation. Cell 49: 379–387 (1987).

    Article  PubMed  Google Scholar 

  8. Deng X-W, Gruissem W: Constitutive transcription and regulation of gene expression in non-photosynthetic plastids of higher plants. EMBO J 7: 3301–3308 (1988).

    Google Scholar 

  9. Deng X-W, Tonkyn JC, Peter GF, Thornber JP, Gruissem W: Post-transcriptional control of plastid mRNA accumulation during adaptation of chloroplasts to different light quality environments. Plant Cell 1: 645–654 (1989).

    Article  PubMed  Google Scholar 

  10. Edwards GE, Lilley RM, Craig S, Hatch MD: Isolation of intact and functional chloroplasts from mesophyll and bundle sheath protoplasts of the C4 plant Panicum miiliaceum. Plant Physiol 63: 821–827 (1979).

    Google Scholar 

  11. Edwards GE, Huber SC: The C4 pathway. In: Hatch MD, Boardman NK (eds) The Biochemistry of Plants: A Comprehensive Treatise, vol. 8, pp. 237–281. Academic Press, New York (1981).

    Google Scholar 

  12. Green C, Hollingsworth M: Expression of the large ATP synthase gene cluster in spinach plastids during light-induced development. Plant Physiol 100: 1164–1170 (1992).

    Google Scholar 

  13. Gruissem W: Chloroplast gene expression: How Plants turn their plastids on. Cell 56: 161–170 (1989).

    Article  PubMed  Google Scholar 

  14. Gutierrez M, Gracen VE, Edwards GE: Biochemical and cytological relationships in C4 plants. Planta 119: 279–300 (1974).

    Google Scholar 

  15. Hatch MD, Slack CR: The C4-carboxylic acid pathway of photosynthesis. In: Reinhold L, Liwschitz Y (eds) Progress in Phytochemistry, pp. 35–106. Wiley-Interscience, London (1970).

    Google Scholar 

  16. Hatch MD, Tsuzuki M, Edwards GE: Determination of NAD malic enzyme in leaves of C4 plants. Plant Physiol 69: 483–491 (1982).

    Google Scholar 

  17. Hoober JK: Chloroplasts. Cellular organelles series. Plenum Press, New York (1984).

    Google Scholar 

  18. Klaff P, Gruissem W: Changes in chloroplast mRNA stability during leaf development. Plant Cell 3: 517–529 (1991).

    Article  PubMed  Google Scholar 

  19. Klein RR, Mullet JE: Light-induced transcription of chloroplast genes. psbA transcription is differentially enhanced in illuminated barley. J Biol Chem 265: 1–8 (1990).

    PubMed  Google Scholar 

  20. Klein RR: Regulation of light-induced chloroplast transcription and translation in eight-day-old dark-grown barley seedlings. Plant Physiol 97: 335–342 (1991).

    Google Scholar 

  21. Langdale JA, Taylor WC, Nelson T: Cell-specific accumulation of maize phosphoenolpyruvate carboxylase is correlated with demethylation at a specific site > 3 kb upstream of the gene. Mol Gen Genet 225: 49–55 (1991).

    Article  PubMed  Google Scholar 

  22. Laetsch WM: Chloroplast specialization in dicotyledons possessing the C4-dicarboxylic acid pathway of photosynthetic CO2 fixation. Am J Bot 55: 875–883 (1968).

    Google Scholar 

  23. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1982).

    Google Scholar 

  24. Michalowski CB, Bohnert HJ, Klessig DF, Berry JO: Nucleotide sequence of rbcL from Amaranthus hypochondriacus chloroplasts. Nucl Acids Res 18: 2187 (1990).

    PubMed  Google Scholar 

  25. Moore BD, Ku MSB, Edwards EE: Isolation of leaf bundle sheath protoplasts from C4 dicot species and intracellular localization of selected enzymes. Plant Sci Lett 35: 127–138 (1984).

    Article  Google Scholar 

  26. Moore BD, Monson RK, Ku MSB, Edwards GE: Activities of principal photosynthetic and Photorespiratory enzymes in leaf mesophyll and bundle sheath protoplasts from the C3–C4 intermediate Flaveria ramosissima. Plant Cell Physiol 29: 999–1006 (1988).

    Google Scholar 

  27. Mullet JE: Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39: 475–502 (1988).

    Article  Google Scholar 

  28. Mullet JE, Klein RR: Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J 6: 1571–1579 (1987).

    Google Scholar 

  29. Ngernprasirtsir J, Chollet R, Kobayashi H, Sugiyama T, Akazawa T: DNA methylation and the differential expression of C4 photosynthesis genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 264: 8241–8248 (1989).

    PubMed  Google Scholar 

  30. Orozco EM, Mullet JE, Hanley-Bowdoin L, Chua N-H: In vitro transcription of chloroplasts protein genes. Meth Enzymol 118: 232–253 (1986).

    PubMed  Google Scholar 

  31. Sammons DW, Adams LD, Nishizawa EE: Ultrasensitive silver-based color staining of polypeptides in polyacrylamide gels. Electrophoresis 2: 135–141 (1981).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  33. 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).

    PubMed  Google Scholar 

  34. Schuster G, Gruissem W: Chloroplast mRNA 3′ end processing requires a nuclear-encoded RNA-binding protein. EMBO J 10: 1493–1502 (1991).

    PubMed  Google Scholar 

  35. Sexton TB, Christopher DA, Mullet JE: Light-induced switch in barley psbD-psbC promoter utilization: a novel mechanism regulating chloroplast gene expression. EMBO J 9: 4485–4494 (1990).

    PubMed  Google Scholar 

  36. Sheen J: Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038 (1990).

    Article  PubMed  Google Scholar 

  37. Shirley BW, Ham DP, Senecoff JF, Berry-Lowe SL, Zurfluh LL, Shah DM, Meagher RB: Comparison of the expression of two highly homologous members of the soybean ribulose-1,5-bisphosphate carboxylase small subunit gene family. Plant Mol Biol 14: 909–925 (1990).

    PubMed  Google Scholar 

  38. Silverthorne J, Tobin EM: Post-transcriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. Plant Cell 2: 1181–1190 (1990).

    Article  PubMed  Google Scholar 

  39. Stern DB, Gruissem W: Control of plastid gene expression: 3′ inverted repeats act as mRNA processing signals and stabilizing elements, but do not terminate transcription. Cell 51: 1145–1157 (1987).

    Article  PubMed  Google Scholar 

  40. Stern DB, Jones H, Gruissem W: Function of plastid mRNA 3′ inverted repeats: RNA stabilization and gene specific protein binding. J Biol Chem 264: 18742–18750 (1989).

    PubMed  Google Scholar 

  41. Stern DB, Radwanski ER, Kindle KL: A 3′ stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell 3: 285–297 (1991).

    Article  PubMed  Google Scholar 

  42. Wang JL, Klessig DF, Berry JO: Regulation of C4 gene expression in developing amaranth leaves. Plant Cell 4: 173–184 (1992).

    Article  PubMed  Google Scholar 

  43. Woo KC, Anderson JM, Boardman NK, Downton WJS, Osmond CB, Thorne SW: Deficient photosystem II in agranal bundle sheath chloroplasts of C4 plants. Proc Natl Acad Sci USA 67: 18–25 (1970).

    Google Scholar 

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  1. Jing-Liang Wang

    Present address: Department of Biological Sciences, State University of New York, 14260, Buffalo, NY, USA

Authors and Affiliations

  1. Department of Biological Sciences, State University of New York, 14260, Buffalo, NY, USA

    Joseph J. Boinski, Ping Xu, Tracy Hotchkiss & James O. Berry

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  5. James O. Berry
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Boinski, J.J., Wang, JL., Xu, P. et al. Post-transcriptional control of cell type-specific gene expression in bundle sheath and mesophyll chloroplasts of Amaranthus hypochondriacus . Plant Mol Biol 22, 397–410 (1993). https://doi.org/10.1007/BF00015971

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  • DOI: https://doi.org/10.1007/BF00015971

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