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. 1997 Jul;114(3):801–815. doi: 10.1104/pp.114.3.801

C4 Gene Expression in Photosynthetic and Nonphotosynthetic Leaf Regions of Amaranthus tricolor.

D McCormac 1, J J Boinski 1, V C Ramsperger 1, J O Berry 1
PMCID: PMC158366  PMID: 12223743

Abstract

Throughout most of its growth and development, Amaranthus tricolor produces fully green leaves. However, near the onset of flowering, unique leaves emerge that consist of three distinct color regions: green apices, yellow middle regions, and red basal regions. The green apices are identical to fully green leaves in terms of pigment composition, photosynthetic function, and C4 gene expression. The yellow and red regions possess greatly reduced levels of chlorophyll and they lack photosynthetic activity. The absence of photosynthetic capacity in the nongreen leaf regions was associated with three distinct alterations in C4 gene expression. First, there was a reduction in the translation of C4 polypeptides, and in the yellow regions synthesis of the ribulose-1,5-bisphosphate carboxylase small subunit occurred in the absence of large subunit synthesis. Second, there was a reduction in the relative transcription rates of two plastid-encoded photosynthetic genes, rbcL and psbA. Third, there was a loss of bundle-sheath cell-specific accumulation of the rbcL and RbcS mRNAs (but not the polypeptides, which remained bundle-sheath-specific). This study indicates that alterations in photosynthetic activity or developmental processes responsible for the loss of activity can influence C4 gene expression at multiple regulatory levels.

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Selected References

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  1. Berry J. O., Breiding D. E., Klessig D. F. Light-mediated control of translational initiation of ribulose-1, 5-bisphosphate carboxylase in amaranth cotyledons. Plant Cell. 1990 Aug;2(8):795–803. doi: 10.1105/tpc.2.8.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985 Sep;5(9):2238–2246. doi: 10.1128/mcb.5.9.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bookjans G., Stummann B. M., Henningsen K. W. Preparation of chloroplast DNA from pea plastids isolated in a medium of high ionic strength. Anal Biochem. 1984 Aug 15;141(1):244–247. doi: 10.1016/0003-2697(84)90452-4. [DOI] [PubMed] [Google Scholar]
  4. Fluhr R., Kuhlemeier C., Nagy F., Chua N. H. Organ-specific and light-induced expression of plant genes. Science. 1986 May 30;232(4754):1106–1112. doi: 10.1126/science.232.4754.1106. [DOI] [PubMed] [Google Scholar]
  5. Furbank R. T., Taylor W. C. Regulation of Photosynthesis in C3 and C4 Plants: A Molecular Approach. Plant Cell. 1995 Jul;7(7):797–807. doi: 10.1105/tpc.7.7.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gilmartin P. M., Sarokin L., Memelink J., Chua N. H. Molecular light switches for plant genes. Plant Cell. 1990 May;2(5):369–378. doi: 10.1105/tpc.2.5.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Green C. D., Hollingsworth M. J. Expression of the Large ATP Synthase Gene Cluster in Spinach Plastids during Light-Induced Development. Plant Physiol. 1992 Nov;100(3):1164–1170. doi: 10.1104/pp.100.3.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Green C. D., Hollingsworth M. J. Tissue-specific expression of the large ATP synthase gene cluster in spinach plastids. Plant Mol Biol. 1994 Jun;25(3):369–376. doi: 10.1007/BF00043866. [DOI] [PubMed] [Google Scholar]
  9. Gruissem W. Chloroplast gene expression: how plants turn their plastids on. Cell. 1989 Jan 27;56(2):161–170. doi: 10.1016/0092-8674(89)90889-1. [DOI] [PubMed] [Google Scholar]
  10. Hensel L. L., Grbić V., Baumgarten D. A., Bleecker A. B. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell. 1993 May;5(5):553–564. doi: 10.1105/tpc.5.5.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Long J. J., Wang J. L., Berry J. O. Cloning and analysis of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. J Biol Chem. 1994 Jan 28;269(4):2827–2833. [PubMed] [Google Scholar]
  12. Mayfield S. P., Taylor W. C. Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur J Biochem. 1984 Oct 1;144(1):79–84. doi: 10.1111/j.1432-1033.1984.tb08433.x. [DOI] [PubMed] [Google Scholar]
  13. Ramsperger V. C., Summers R. G., Berry J. O. Photosynthetic Gene Expression in Meristems and during Initial Leaf Development in a C4 Dicotyledonous Plant. Plant Physiol. 1996 Aug;111(4):999–1010. doi: 10.1104/pp.111.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Schmidt G. W., Mishkind M. L. Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci U S A. 1983 May;80(9):2632–2636. doi: 10.1073/pnas.80.9.2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schäffner A. R., Sheen J. Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. Plant Cell. 1991 Sep;3(9):997–1012. doi: 10.1105/tpc.3.9.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sheen J. Metabolic repression of transcription in higher plants. Plant Cell. 1990 Oct;2(10):1027–1038. doi: 10.1105/tpc.2.10.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Shirley B. W., Ham D. P., Senecoff J. F., Berry-Lowe S. L., Zurfluh L. L., Shah D. M., Meagher R. B. Comparison of the expression of two highly homologous members of the soybean ribulose-1,5-bisphosphate carboxylase small subunit gene family. Plant Mol Biol. 1990 Jun;14(6):909–925. doi: 10.1007/BF00019389. [DOI] [PubMed] [Google Scholar]
  18. Silverthorne J., Tobin E. M. Post-transcriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. Plant Cell. 1990 Dec;2(12):1181–1190. doi: 10.1105/tpc.2.12.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sonnewald U., Willmitzer L. Molecular approaches to sink-source interactions. Plant Physiol. 1992 Aug;99(4):1267–1270. doi: 10.1104/pp.99.4.1267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wang J. L., Klessig D. F., Berry J. O. Regulation of C4 Gene Expression in Developing Amaranth Leaves. Plant Cell. 1992 Feb;4(2):173–184. doi: 10.1105/tpc.4.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wanner L. A., Gruissem W. Expression dynamics of the tomato rbcS gene family during development. Plant Cell. 1991 Dec;3(12):1289–1303. doi: 10.1105/tpc.3.12.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]

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