Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Jan 29;358(1429):135–145. doi: 10.1098/rstb.2002.1180

Coordination of plastid and nuclear gene expression.

John C Gray 1, James A Sullivan 1, Jun-Hui Wang 1, Cheryl A Jerome 1, Daniel MacLean 1
PMCID: PMC1693108  PMID: 12594922

Abstract

The coordinated expression of genes distributed between the nuclear and plastid genomes is essential for the assembly of functional chloroplasts. Although the nucleus has a pre-eminent role in controlling chloroplast biogenesis, there is considerable evidence that the expression of nuclear genes encoding photosynthesis-related proteins is regulated by signals from plastids. Perturbation of several plastid-located processes, by inhibitors or in mutants, leads to decreased transcription of a set of nuclear photosynthesis-related genes. Characterization of arabidopsis gun (genomes uncoupled) mutants, which express nuclear genes in the presence of norflurazon or lincomycin, has provided evidence for two separate signalling pathways, one involving tetrapyrrole biosynthesis intermediates and the other requiring plastid protein synthesis. In addition, perturbation of photosynthetic electron transfer produces at least two different redox signals, as part of the acclimation to altered light conditions. The recognition of multiple plastid signals requires a reconsideration of the mechanisms of regulation of transcription of nuclear genes encoding photosynthesis-related proteins.

Full Text

The Full Text of this article is available as a PDF (245.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abdallah F., Salamini F., Leister D. A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci. 2000 Apr;5(4):141–142. doi: 10.1016/s1360-1385(00)01574-0. [DOI] [PubMed] [Google Scholar]
  2. Adamska I. Regulation of Early Light-Inducible Protein Gene Expression by Blue and Red Light in Etiolated Seedlings Involves Nuclear and Plastid Factors. Plant Physiol. 1995 Apr;107(4):1167–1175. doi: 10.1104/pp.107.4.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allison L. A., Simon L. D., Maliga P. Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J. 1996 Jun 3;15(11):2802–2809. [PMC free article] [PubMed] [Google Scholar]
  4. Barak S., Nejidat A., Heimer Y., Volokita M. Transcriptional and posttranscriptional regulation of the glycolate oxidase gene in tobacco seedlings. Plant Mol Biol. 2001 Mar;45(4):399–407. doi: 10.1023/a:1010688804719. [DOI] [PubMed] [Google Scholar]
  5. Batschauer A., Mösinger E., Kreuz K., Dörr I., Apel K. The implication of a plastid-derived factor in the transcriptional control of nuclear genes encoding the light-harvesting chlorophyll a/b protein. Eur J Biochem. 1986 Feb 3;154(3):625–634. doi: 10.1111/j.1432-1033.1986.tb09444.x. [DOI] [PubMed] [Google Scholar]
  6. Bolle C., Sopory S., Lubberstedt T., Klosgen R. B., Herrmann R. G., Oelmuller R. The Role of Plastids in the Expression of Nuclear Genes for Thylakoid Proteins Studied with Chimeric [beta]-Glucuronidase Gene Fusions. Plant Physiol. 1994 Aug;105(4):1355–1364. doi: 10.1104/pp.105.4.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brusslan Judy A., Peterson Michael P. Tetrapyrrole regulation of nuclear gene expression. Photosynth Res. 2002;71(3):185–194. doi: 10.1023/A:1015539109209. [DOI] [PubMed] [Google Scholar]
  8. Chekounova E., Voronetskaya V., Papenbrock J., Grimm B., Beck C. F. Characterization of Chlamydomonas mutants defective in the H subunit of Mg-chelatase. Mol Genet Genomics. 2001 Nov;266(3):363–373. doi: 10.1007/s004380100574. [DOI] [PubMed] [Google Scholar]
  9. Dickey L. F., Gallo-Meagher M., Thompson W. F. Light regulatory sequences are located within the 5' portion of the Fed-1 message sequence. EMBO J. 1992 Jun;11(6):2311–2317. doi: 10.1002/j.1460-2075.1992.tb05290.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ernst D., Schefbeck K. Photooxidation of Plastids Inhibits Transcription of Nuclear Encoded Genes in Rye (Secale cereale). Plant Physiol. 1988 Oct;88(2):255–258. doi: 10.1104/pp.88.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Giuliano G., Scolnik P. A. Transcription of Two Photosynthesis-Associated Nuclear Gene Families Correlates with the Presence of Chloroplasts in Leaves of the Variegated Tomato ghost Mutant. Plant Physiol. 1988 Jan;86(1):7–9. doi: 10.1104/pp.86.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hahn D., Kück U. Identification of DNA sequences controlling light- and chloroplast-dependent expression of the lhcb1 gene from Chlamydomonas reinhardtii. Curr Genet. 1999 Jan;34(6):459–466. doi: 10.1007/s002940050420. [DOI] [PubMed] [Google Scholar]
  13. Hajdukiewicz P. T., Allison L. A., Maliga P. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 1997 Jul 1;16(13):4041–4048. doi: 10.1093/emboj/16.13.4041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Helliwell C. A., Webster C. I., Gray J. C. Light-regulated expression of the pea plastocyanin gene is mediated by elements within the transcribed region of the gene. Plant J. 1997 Sep;12(3):499–506. doi: 10.1046/j.1365-313x.1997.00499.x. [DOI] [PubMed] [Google Scholar]
  15. Jasper F., Quednau B., Kortenjann M., Johanningmeier U. Control of cab gene expression in synchronized Chlamydomonas reinhardtii cells. J Photochem Photobiol B. 1991 Nov;11(2):139–150. doi: 10.1016/1011-1344(91)80256-h. [DOI] [PubMed] [Google Scholar]
  16. Johanningmeier U. Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur J Biochem. 1988 Nov 1;177(2):417–424. doi: 10.1111/j.1432-1033.1988.tb14391.x. [DOI] [PubMed] [Google Scholar]
  17. Kapoor S., Suzuki J. Y., Sugiura M. Identification and functional significance of a new class of non-consensus-type plastid promoters. Plant J. 1997 Feb;11(2):327–337. doi: 10.1046/j.1365-313x.1997.11020327.x. [DOI] [PubMed] [Google Scholar]
  18. Kohchi T., Mukougawa K., Frankenberg N., Masuda M., Yokota A., Lagarias J. C. The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell. 2001 Feb;13(2):425–436. doi: 10.1105/tpc.13.2.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Krause K., Maier R. M., Kofer W., Krupinska K., Herrmann R. G. Disruption of plastid-encoded RNA polymerase genes in tobacco: expression of only a distinct set of genes is not based on selective transcription of the plastid chromosome. Mol Gen Genet. 2000 Jul;263(6):1022–1030. doi: 10.1007/pl00008690. [DOI] [PubMed] [Google Scholar]
  20. Kropat J., Oster U., Rüdiger W., Beck C. F. Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J. 2000 Nov;24(4):523–531. doi: 10.1046/j.1365-313x.2000.00898.x. [DOI] [PubMed] [Google Scholar]
  21. Kumar M. A., Chaturvedi S., Söll D. Selective inhibition of HEMA gene expression by photooxidation in Arabidopsis thaliana. Phytochemistry. 1999 Aug;51(7):847–851. doi: 10.1016/s0031-9422(99)00114-4. [DOI] [PubMed] [Google Scholar]
  22. Kusnetsov V., Bolle C., Lübberstedt T., Sopory S., Herrmann R. G., Oelmüller R. Evidence that the plastid signal and light operate via the same cis-acting elements in the promoters of nuclear genes for plastid proteins. Mol Gen Genet. 1996 Oct 28;252(6):631–639. doi: 10.1007/BF02173968. [DOI] [PubMed] [Google Scholar]
  23. La Rocca N., Rascio N., Oster U., Rüdiger W. Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta. 2001 May;213(1):101–108. doi: 10.1007/s004250000477. [DOI] [PubMed] [Google Scholar]
  24. Lübberstedt T., Oelmüller R., Wanner G., Herrmann R. G. Interacting cis elements in the plastocyanin promoter from spinach ensure regulated high-level expression. Mol Gen Genet. 1994 Mar;242(5):602–613. doi: 10.1007/BF00285284. [DOI] [PubMed] [Google Scholar]
  25. Martínez-Hernández Aída, López-Ochoa Luisa, Argüello-Astorga Gerardo, Herrera-Estrella Luis. Functional properties and regulatory complexity of a minimal RBCS light-responsive unit activated by phytochrome, cryptochrome, and plastid signals. Plant Physiol. 2002 Apr;128(4):1223–1233. doi: 10.1104/pp.010678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mathews D. E., Durbin R. D. Tagetitoxin inhibits RNA synthesis directed by RNA polymerases from chloroplasts and Escherichia coli. J Biol Chem. 1990 Jan 5;265(1):493–498. [PubMed] [Google Scholar]
  27. Maxwell D. P., Laudenbach D. E., Huner NPA. Redox Regulation of Light-Harvesting Complex II and cab mRNA Abundance in Dunaliella salina. Plant Physiol. 1995 Nov;109(3):787–795. doi: 10.1104/pp.109.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. McCormac A. C., Fischer A., Kumar A. M., Söll D., Terry M. J. Regulation of HEMA1 expression by phytochrome and a plastid signal during de-etiolation in Arabidopsis thaliana. Plant J. 2001 Mar;25(5):549–561. doi: 10.1046/j.1365-313x.2001.00986.x. [DOI] [PubMed] [Google Scholar]
  30. Mochizuki N., Brusslan J. A., Larkin R., Nagatani A., Chory J. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):2053–2058. doi: 10.1073/pnas.98.4.2053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mullineaux Philip, Karpinski Stanislaw. Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol. 2002 Feb;5(1):43–48. doi: 10.1016/s1369-5266(01)00226-6. [DOI] [PubMed] [Google Scholar]
  32. Muramoto T., Kohchi T., Yokota A., Hwang I., Goodman H. M. The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell. 1999 Mar;11(3):335–348. doi: 10.1105/tpc.11.3.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Møller S. G., Kunkel T., Chua N. H. A plastidic ABC protein involved in intercompartmental communication of light signaling. Genes Dev. 2001 Jan 1;15(1):90–103. doi: 10.1101/gad.850101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Oelmüller R., Briggs W. R. Intact plastids are required for nitrate- and light-induced accumulation of nitrate reductase activity and mRNA in squash cotyledons. Plant Physiol. 1990 Feb;92(2):434–439. doi: 10.1104/pp.92.2.434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Oswald O., Martin T., Dominy P. J., Graham I. A. Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci U S A. 2001 Jan 30;98(4):2047–2052. doi: 10.1073/pnas.021449998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Papenbrock J., Pfündel E., Mock H. P., Grimm B. Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J. 2000 Apr;22(2):155–164. doi: 10.1046/j.1365-313x.2000.00724.x. [DOI] [PubMed] [Google Scholar]
  37. Petracek M. E., Dickey L. F., Huber S. C., Thompson W. F. Light-regulated changes in abundance and polyribosome association of ferredoxin mRNA are dependent on photosynthesis. Plant Cell. 1997 Dec;9(12):2291–2300. doi: 10.1105/tpc.9.12.2291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Petracek M. E., Dickey L. F., Nguyen T. T., Gatz C., Sowinski D. A., Allen G. C., Thompson W. F. Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):9009–9013. doi: 10.1073/pnas.95.15.9009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Puente P., Wei N., Deng X. W. Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 1996 Jul 15;15(14):3732–3743. [PMC free article] [PubMed] [Google Scholar]
  40. Rapp J. C., Mullet J. E. Chloroplast transcription is required to express the nuclear genes rbcS and cab. Plastid DNA copy number is regulated independently. Plant Mol Biol. 1991 Oct;17(4):813–823. doi: 10.1007/BF00037063. [DOI] [PubMed] [Google Scholar]
  41. Rujan T., Martin W. How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trends Genet. 2001 Mar;17(3):113–120. doi: 10.1016/s0168-9525(00)02209-5. [DOI] [PubMed] [Google Scholar]
  42. Sagar A. D., Briggs W. R. Effects of High Light Stress on Carotenoid-Deficient Chloroplasts in Pisum sativum. Plant Physiol. 1990 Dec;94(4):1663–1670. doi: 10.1104/pp.94.4.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sagar A. D., Horwitz B. A., Elliott R. C., Thompson W. F., Briggs W. R. Light effects on several chloroplast components in norflurazon-treated pea seedlings. Plant Physiol. 1988 Oct;88(2):340–347. doi: 10.1104/pp.88.2.340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schwartz B. W., Daniel S. G., Becker W. M. Photooxidative Destruction of Chloroplasts Leads to Reduced Expression of Peroxisomal NADH-Dependent Hydroxypyruvate Reductase in Developing Cucumber Cotyledons. Plant Physiol. 1992 Jun;99(2):681–685. doi: 10.1104/pp.99.2.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Simpson J., VAN Montagu M., Herrera-Estrella L. Photosynthesis-associated gene families: differences in response to tissue-specific and environmental factors. Science. 1986 Jul 4;233(4759):34–38. doi: 10.1126/science.233.4759.34. [DOI] [PubMed] [Google Scholar]
  46. Stockhaus J., Eckes P., Blau A., Schell J., Willmitzer L. Organ-specific and dosage-dependent expression of a leaf/stem specific gene from potato after tagging and transfer into potato and tobacco plants. Nucleic Acids Res. 1987 Apr 24;15(8):3479–3491. doi: 10.1093/nar/15.8.3479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sullivan JA, Gray JC. Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant . Plant Cell. 1999 May;11(5):901–910. doi: 10.1105/tpc.11.5.901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sullivan James A., Gray John C. Multiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. Plant J. 2002 Dec;32(5):763–774. doi: 10.1046/j.1365-313x.2002.01464.x. [DOI] [PubMed] [Google Scholar]
  49. Susek R. E., Ausubel F. M., Chory J. Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell. 1993 Sep 10;74(5):787–799. doi: 10.1016/0092-8674(93)90459-4. [DOI] [PubMed] [Google Scholar]
  50. Tonkyn J. C., Deng X. W., Gruissem W. Regulation of Plastid Gene Expression during Photooxidative Stress. Plant Physiol. 1992 Aug;99(4):1406–1415. doi: 10.1104/pp.99.4.1406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ulrich A., Pühler A. The new class II transposon Tn163 is plasmid-borne in two unrelated Rhizobium leguminosarum biovar viciae strains. Mol Gen Genet. 1994 Mar;242(5):505–516. doi: 10.1007/BF00285274. [DOI] [PubMed] [Google Scholar]
  52. Vinti G., Hills A., Campbell S., Bowyer J. R., Mochizuki N., Chory J., López-Juez E. Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signalling. Plant J. 2000 Dec;24(6):883–894. doi: 10.1046/j.1365-313x.2000.00936.x. [DOI] [PubMed] [Google Scholar]
  53. Wilson R. J. M. Iain, Rangachari K., Saldanha J. W., Rickman L., Buxton R. S., Eccleston J. F. Parasite plastids: maintenance and functions. Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):155–164. doi: 10.1098/rstb.2002.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES