Home LiteratureArticle Details
PMID: 12324602 Published · ppublish English Journal Article

Changes in Chloroplast mRNA Stability during Leaf Development.

The Plant cell ·Vol. 3 ·No. 5 ·1991-05-00 ·Pages 517-529

Klaff P, Gruissem W

Abstract

During spinach leaf development, chloroplast-encoded mRNAs accumulate to different steady-state levels. Their relative transcription rates alone, however, cannot account for the changes in mRNA amount. In this study, we examined the importance of mRNA stability for the regulation of plastid mRNA accumulation using an in vivo system to measure mRNA decay in intact leaves by inhibiting transcription with actinomycin D. Decay of psbA and rbcL mRNAs was assayed in young and mature leaves. The psbA mRNA half-life was increased more than twofold in mature leaves compared with young leaves, whereas rbcL mRNA decayed with a similar relative half-life at both leaf developmental stages. The direct in vivo measurements demonstrated that differential mRNA stability in higher plant plastids can account for differences in mRNA accumulation during leaf development. The role of polysome association in mRNA decay was also investigated. Using organelle-specific translation inhibitors that force mRNAs into a polysome-bound state or deplete mRNAs of ribosomes, we measured mRNA decay in vivo in either state. The results showed that rbcL and psbA mRNAs are less stable when bound to polysomes relative to the polysome-depleted mRNAs and that their stabilities are differentially affected by binding to polysomes. The results suggested that ribosome binding and/or translation of the psbA and rbcL mRNAs may function to modulate the rate of their decay in chloroplasts.

Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Klaff P.
Department of Plant Biology, University of California, Berkeley, California 94720.
Gruissem W.
References (29)
29 references, click to expand
  1. The maize plastid psbB-psbF-petB-petD gene cluster: spliced and unspliced petB and petD RNAs encode alternative products.
    Curr Genet. 1987;12(1):69-77 PMID: 2835175
  2. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 May;10(5):2269-84 PMID: 2183028
  3. The structure of the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase from spinach chloroplast DNA.
    Nucleic Acids Res. 1981 Jul 24;9(14):3251-70 PMID: 6269077
  4. Control of mRNA stability in chloroplasts by 3' inverted repeats: effects of stem and loop mutations on degradation of psbA mRNA in vitro.
    Nucleic Acids Res. 1990 Oct 25;18(20):6003-10 PMID: 2235482
  5. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals.
    Mol Gen Genet. 1989 Jun;217(2-3):185-94 PMID: 2770692
  6. Transcriptional and post-transcriptional control of plastid mRNA levels in higher plants.
    Trends Genet. 1988 Sep;4(9):258-63 PMID: 3070872
  7. Translation and mRNA decay.
    Mol Gen Genet. 1978 Apr 6;160(2):121-9 PMID: 349350
  8. Growth-rate dependent regulation of mRNA stability in Escherichia coli.
    Nature. 1984 Nov 1-7;312(5989):75-7 PMID: 6387508
  9. Influence of Ionic Strength, pH, and Chelation of Divalent Metals on Isolation of Polyribosomes from Tobacco Leaves.
    Plant Physiol. 1976 Jan;57(1):5-10 PMID: 16659423
  10. Plastid run-on transcription. Application to determine the transcriptional regulation of spinach plastid genes.
    J Biol Chem. 1987 Jul 15;262(20):9641-8 PMID: 3597430
  11. Light-regulated translation of chloroplast proteins. I. Transcripts of psaA-psaB, psbA, and rbcL are associated with polysomes in dark-grown and illuminated barley seedlings.
    J Cell Biol. 1988 Feb;106(2):289-301 PMID: 3339092
  12. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation.
    Cell. 1983 Aug;34(1):207-14 PMID: 6192932
  13. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation.
    Cell. 1989 Sep 8;58(5):857-67 PMID: 2673535
  14. Tissue-dependent plastid RNA splicing in maize: transcripts from four plastid genes are predominantly unspliced in leaf meristems and roots.
    Plant Cell. 1989 Apr;1(4):437-45 PMID: 2562564
  15. Extreme instability of myc mRNA in normal and transformed human cells.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):7046-50 PMID: 6594679
  16. Chloroplast gene expression: how plants turn their plastids on.
    Cell. 1989 Jan 27;56(2):161-70 PMID: 2643471
  17. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression.
    EMBO J. 1986 Sep;5(9):2043-2049 PMID: 16453699
  18. Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II.
    Cell. 1989 Sep 8;58(5):869-76 PMID: 2673536
  19. Nuclease activity associated with mammalian mRNA in its native state: possible basis for selectivity in mRNA decay.
    Mol Cell Biol. 1990 May;10(5):2060-9 PMID: 2325645
  20. Complex RNA maturation in chloroplasts. The psbB operon from spinach.
    Eur J Biochem. 1988 Feb 1;171(3):551-64 PMID: 2831053
  21. Rapid splicing and stepwise processing of a transcript from the psbB operon in tobacco chloroplasts: determination of the intron sites in petB and petD.
    Mol Gen Genet. 1987 Oct;209(3):427-31 PMID: 17193705
  22. Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development.
    J Cell Biol. 1985 Feb;100(2):463-76 PMID: 2981888
  23. Function of plastid mRNA 3' inverted repeats. RNA stabilization and gene-specific protein binding.
    J Biol Chem. 1989 Nov 5;264(31):18742-50 PMID: 2478550
  24. Effect of premature termination of translation on mRNA stability depends on the site of ribosome release.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4890-4 PMID: 2440033
  25. Control of plastid gene expression during development: the limited role of transcriptional regulation.
    Cell. 1987 May 8;49(3):379-87 PMID: 3568130
  26. Control of plastid gene expression: 3' inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription.
    Cell. 1987 Dec 24;51(6):1145-57 PMID: 3690662
  27. Constitutive transcription and regulation of gene expression in non-photosynthetic plastids of higher plants.
    EMBO J. 1988 Nov;7(11):3301-8 PMID: 16453858
  28. General occurrence and structural similarity of the rapidly synthesized, 32,000-dalton protein of the chloroplast membrane.
    J Biol Chem. 1982 Apr 25;257(8):4583-7 PMID: 7068652
  29. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro.
    Mol Cell Biol. 1989 Feb;9(2):659-70 PMID: 2565532
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
1991-05-00
Pages
517-529
Language
English
Region
England
NLM ID
9208688
PMCID
PMC160019
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]