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. 1999 May;11(5):901–910. doi: 10.1105/tpc.11.5.901

Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant

JA Sullivan 1, JC Gray 1
PMCID: PMC144231  PMID: 10330474

Abstract

The expression of nuclear photosynthesis genes in pea seedlings requires both light and a postulated signal produced by developing plastids. The requirement for the plastid signal for the accumulation of transcripts of Lhcb1, RbcS, PetE, and AtpC genes was investigated in the pea mutant lip1, which shows light-independent photomorphogenic development. Lincomycin and erythromycin, inhibitors of plastid translation, decreased the accumulation of transcripts of nuclear photosynthesis genes in shoots of light-grown wild-type and lip1 seedlings, indicating that the plastid signal is required in the lip1 mutant. Treatment with lincomycin or erythromycin also reduced the accumulation of transcripts in shoots of dark-grown lip1 seedlings, indicating that light is not an obligate requirement for the synthesis or activity of the plastid signal. Lincomycin had a similar effect on the accumulation of Lhcb1 transcripts in dark-grown cop1-4 seedlings of Arabidopsis. Accumulation of transcripts of nuclear photosynthesis genes was also observed in roots of light-grown lip1 seedlings, and this accumulation, which was associated with the development of chloroplasts, was again dependent on plastid translation. The plastid signal therefore regulates the expression of nuclear photosynthesis genes in the dark and in roots of the lip1 mutant.

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Selected References

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  1. Anderson S., Smith S. M. Synthesis of the small subunit of ribulose-bisphosphate carboxylase from genes cloned into plasmids containing the SP6 promoter. Biochem J. 1986 Dec 15;240(3):709–715. doi: 10.1042/bj2400709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arguello-Astorga Gerardo, Herrera-Estrella Luis. EVOLUTION OF LIGHT-REGULATED PLANT PROMOTERS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):525–555. doi: 10.1146/annurev.arplant.49.1.525. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Chory J., Nagpal P., Peto C. A. Phenotypic and Genetic Analysis of det2, a New Mutant That Affects Light-Regulated Seedling Development in Arabidopsis. Plant Cell. 1991 May;3(5):445–459. doi: 10.1105/tpc.3.5.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chory J., Peto C. A. Mutations in the DET1 gene affect cell-type-specific expression of light-regulated genes and chloroplast development in Arabidopsis. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8776–8780. doi: 10.1073/pnas.87.22.8776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cline K., Fulsom D. R., Viitanen P. V. An imported thylakoid protein accumulates in the stroma when insertion into thylakoids is inhibited. J Biol Chem. 1989 Aug 25;264(24):14225–14232. [PubMed] [Google Scholar]
  7. Deng X. W., Caspar T., Quail P. H. cop1: a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 1991 Jul;5(7):1172–1182. doi: 10.1101/gad.5.7.1172. [DOI] [PubMed] [Google Scholar]
  8. Ellis R. J., Hartley M. R. Sites of synthesis of chloroplast proteins. Nature. 1971 Oct 13;233(5320):193–196. [PubMed] [Google Scholar]
  9. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  10. Frances S., Thompson W. F. The dark-adaptation response of the de-etiolated pea mutant lip1 is modulated by external signals and endogenous programs. Plant Physiol. 1997 Sep;115(1):23–28. doi: 10.1104/pp.115.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Frances S., White M. J., Edgerton M. D., Jones A. M., Elliott R. C., Thompson W. F. Initial characterization of a pea mutant with light-independent photomorphogenesis. Plant Cell. 1992 Dec;4(12):1519–1530. doi: 10.1105/tpc.4.12.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Hou Y., Von Arnim A. G., Deng X. W. A New Class of Arabidopsis Constitutive Photomorphogenic Genes Involved in Regulating Cotyledon Development. Plant Cell. 1993 Mar;5(3):329–339. doi: 10.1105/tpc.5.3.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Leon P., Arroyo A., Mackenzie S. NUCLEAR CONTROL OF PLASTID AND MITOCHONDRIAL DEVELOPMENT IN HIGHER PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):453–480. doi: 10.1146/annurev.arplant.49.1.453. [DOI] [PubMed] [Google Scholar]
  16. Leutwiler L. S., Meyerowitz E. M., Tobin E. M. Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res. 1986 May 27;14(10):4051–4064. doi: 10.1093/nar/14.10.4051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. McNellis T. W., Deng X. W. Light control of seedling morphogenetic pattern. Plant Cell. 1995 Nov;7(11):1749–1761. doi: 10.1105/tpc.7.11.1749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mochizuki N., Susek R., Chory J. An intracellular signal transduction pathway between the chloroplast and nucleus is involved in de-etiolation. Plant Physiol. 1996 Dec;112(4):1465–1469. doi: 10.1104/pp.112.4.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Napier J. A., Höglund A. S., Plant A. L., Gray J. C. Chloroplast import of the precursor of the gamma subunit of pea chloroplast ATP synthase. Plant Mol Biol. 1992 Nov;20(4):737–741. doi: 10.1007/BF00046458. [DOI] [PubMed] [Google Scholar]
  21. Navaratnam V., Jacques T. S., Skepper J. N. Ultrastructural and cytochemical study of neurones in the rat dorsal motor nucleus of the vagus after axon crush. Microsc Res Tech. 1998 Sep 1;42(5):334–344. doi: 10.1002/(SICI)1097-0029(19980901)42:5<334::AID-JEMT4>3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  22. Peracchia C., Mittler B. S. Fixation by means of glutaraldehyde-hydrogen peroxide reaction products. J Cell Biol. 1972 Apr;53(1):234–238. doi: 10.1083/jcb.53.1.234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Pwee K. H., Gray J. C. The pea plastocyanin promoter directs cell-specific but not full light-regulated expression in transgenic tobacco plants. Plant J. 1993 Mar;3(3):437–449. doi: 10.1046/j.1365-313x.1993.t01-26-00999.x. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Sponsel V. M., Ross J. J., Reynolds M. R., Symons G. M., Reid J. B. The Gibberellin Status of lip1, a Mutant of Pea That Exhibits Light-Independent Photomorphogenesis. Plant Physiol. 1996 Sep;112(1):61–66. doi: 10.1104/pp.112.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Staub J. M., Deng X. W. Light signal transduction in plants. Photochem Photobiol. 1996 Dec;64(6):897–905. doi: 10.1111/j.1751-1097.1996.tb01853.x. [DOI] [PubMed] [Google Scholar]
  28. Watts F. Z., Moore A. L. Nucleotide sequence of a full length cDNA clone encoding a polyubiquitin gene from Pisum sativum. Nucleic Acids Res. 1989 Dec 11;17(23):10100–10100. doi: 10.1093/nar/17.23.10100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Webster C. I., Packman L. C., Pwee K. H., Gray J. C. High mobility group proteins HMG-1 and HMG-I/Y bind to a positive regulatory region of the pea plastocyanin gene promoter. Plant J. 1997 Apr;11(4):703–715. doi: 10.1046/j.1365-313x.1997.11040703.x. [DOI] [PubMed] [Google Scholar]
  30. Wei N., Deng X. W. The role of the COP/DET/FUS genes in light control of arabidopsis seedling development. Plant Physiol. 1996 Nov;112(3):871–878. doi: 10.1104/pp.112.3.871. [DOI] [PMC free article] [PubMed] [Google Scholar]

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