Upstream sequences other than AAUAAA are required for efficient messenger RNA 3'-end formation in plants (original) (raw)

Abstract

We have characterized the upstream nucleotide sequences involved in mRNA 3'-end formation in the 3' regions of the cauliflower mosaic virus (CaMV) 19S/35S transcription unit and a pea gene encoding ribulose-1,5-bisphosphate carboxylase small subunit (rbcS). Sequences between 57 bases and 181 bases upstream from the CaMV polyadenylation site were required for efficient polyadenylation at this site. In addition, an AAUAAA sequence located 13 bases to 18 bases upstream from this site was also important for efficient mRNA 3'-end formation. An element located between 60 bases and 137 bases upstream from the poly(A) addition sites in a pea rbcS gene was needed for functioning of these sites. The CaMV -181/-57 and rbcS -137/-60 elements were different in location and sequence composition from upstream sequences needed for polyadenylation in mammalian genes, but resembled the signals that direct mRNA 3'-end formation in yeast. However, the role of the AAUAAA motif in 3'-end formation in the CaMV 3' region was reminiscent of mRNA polyadenylation in animals. We suggest that multiple elements are involved in mRNA 3'-end formation in plants, and that interactions of different components of the plant polyadenylation apparatus with their respective sequence elements and with each other are needed for efficient mRNA 3'-end formation.

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Selected References

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  1. An G., Mitra A., Choi H. K., Costa M. A., An K., Thornburg R. W., Ryan C. A. Functional analysis of the 3' control region of the potato wound-inducible proteinase inhibitor II gene. Plant Cell. 1989 Jan;1(1):115–122. doi: 10.1105/tpc.1.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  3. Butler J. S., Sadhale P. P., Platt T. RNA processing in vitro produces mature 3' ends of a variety of Saccharomyces cerevisiae mRNAs. Mol Cell Biol. 1990 Jun;10(6):2599–2605. doi: 10.1128/mcb.10.6.2599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Christofori G., Keller W. 3' cleavage and polyadenylation of mRNA precursors in vitro requires a poly(A) polymerase, a cleavage factor, and a snRNP. Cell. 1988 Sep 9;54(6):875–889. doi: 10.1016/s0092-8674(88)91263-9. [DOI] [PubMed] [Google Scholar]
  5. Connelly S., Manley J. L. A functional mRNA polyadenylation signal is required for transcription termination by RNA polymerase II. Genes Dev. 1988 Apr;2(4):440–452. doi: 10.1101/gad.2.4.440. [DOI] [PubMed] [Google Scholar]
  6. Coruzzi G., Broglie R., Edwards C., Chua N. H. Tissue-specific and light-regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J. 1984 Aug;3(8):1671–1679. doi: 10.1002/j.1460-2075.1984.tb02031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dean C., Tamaki S., Dunsmuir P., Favreau M., Katayama C., Dooner H., Bedbrook J. mRNA transcripts of several plant genes are polyadenylated at multiple sites in vivo. Nucleic Acids Res. 1986 Mar 11;14(5):2229–2240. doi: 10.1093/nar/14.5.2229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dunsmuir P., Smith S. M., Bedbrook J. The major chlorophyll a/b binding protein of petunia is composed of several polypeptides encoded by a number of distinct nuclear genes. J Mol Appl Genet. 1983;2(3):285–300. [PubMed] [Google Scholar]
  9. Gil A., Proudfoot N. J. Position-dependent sequence elements downstream of AAUAAA are required for efficient rabbit beta-globin mRNA 3' end formation. Cell. 1987 May 8;49(3):399–406. doi: 10.1016/0092-8674(87)90292-3. [DOI] [PubMed] [Google Scholar]
  10. Gilmartin G. M., McDevitt M. A., Nevins J. R. Multiple factors are required for specific RNA cleavage at a poly(A) addition site. Genes Dev. 1988 May;2(5):578–587. doi: 10.1101/gad.2.5.578. [DOI] [PubMed] [Google Scholar]
  11. Guilley H., Dudley R. K., Jonard G., Balàzs E., Richards K. E. Transcription of Cauliflower mosaic virus DNA: detection of promoter sequences, and characterization of transcripts. Cell. 1982 Oct;30(3):763–773. doi: 10.1016/0092-8674(82)90281-1. [DOI] [PubMed] [Google Scholar]
  12. Hunt A. G. Identification and characterization of cryptic polyadenylation sites in the 3' region of a pea ribulose-1,5-bisphosphate carboxylase small subunit gene. DNA. 1988 Jun;7(5):329–336. doi: 10.1089/dna.1.1988.7.329. [DOI] [PubMed] [Google Scholar]
  13. Hunt A. G., MacDonald M. H. Deletion analysis of the polyadenylation signal of a pea ribulose-1,5-bisphosphate carboxylase small-subunit gene. Plant Mol Biol. 1989 Aug;13(2):125–138. doi: 10.1007/BF00016132. [DOI] [PubMed] [Google Scholar]
  14. Ingelbrecht I. L., Herman L. M., Dekeyser R. A., Van Montagu M. C., Depicker A. G. Different 3' end regions strongly influence the level of gene expression in plant cells. Plant Cell. 1989 Jul;1(7):671–680. doi: 10.1105/tpc.1.7.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Joshi C. P. Putative polyadenylation signals in nuclear genes of higher plants: a compilation and analysis. Nucleic Acids Res. 1987 Dec 10;15(23):9627–9640. doi: 10.1093/nar/15.23.9627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kay R., Chan A., Daly M., McPherson J. Duplication of CaMV 35S Promoter Sequences Creates a Strong Enhancer for Plant Genes. Science. 1987 Jun 5;236(4806):1299–1302. doi: 10.1126/science.236.4806.1299. [DOI] [PubMed] [Google Scholar]
  17. Logan J., Falck-Pedersen E., Darnell J. E., Jr, Shenk T. A poly(A) addition site and a downstream termination region are required for efficient cessation of transcription by RNA polymerase II in the mouse beta maj-globin gene. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8306–8310. doi: 10.1073/pnas.84.23.8306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McDevitt M. A., Gilmartin G. M., Reeves W. H., Nevins J. R. Multiple factors are required for poly(A) addition to a mRNA 3' end. Genes Dev. 1988 May;2(5):588–597. doi: 10.1101/gad.2.5.588. [DOI] [PubMed] [Google Scholar]
  19. McDevitt M. A., Imperiale M. J., Ali H., Nevins J. R. Requirement of a downstream sequence for generation of a poly(A) addition site. Cell. 1984 Jul;37(3):993–999. doi: 10.1016/0092-8674(84)90433-1. [DOI] [PubMed] [Google Scholar]
  20. Nagy F., Morelli G., Fraley R. T., Rogers S. G., Chua N. H. Photoregulated expression of a pea rbcS gene in leaves of transgenic plants. EMBO J. 1985 Dec 1;4(12):3063–3068. doi: 10.1002/j.1460-2075.1985.tb04046.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Platt T. Transcription termination and the regulation of gene expression. Annu Rev Biochem. 1986;55:339–372. doi: 10.1146/annurev.bi.55.070186.002011. [DOI] [PubMed] [Google Scholar]
  22. Russo P., Sherman F. Transcription terminates near the poly(A) site in the CYC1 gene of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8348–8352. doi: 10.1073/pnas.86.21.8348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sanfaçon H., Hohn T. Proximity to the promoter inhibits recognition of cauliflower mosaic virus polyadenylation signal. Nature. 1990 Jul 5;346(6279):81–84. doi: 10.1038/346081a0. [DOI] [PubMed] [Google Scholar]
  24. Schardl C. L., Byrd A. D., Benzion G., Altschuler M. A., Hildebrand D. F., Hunt A. G. Design and construction of a versatile system for the expression of foreign genes in plants. Gene. 1987;61(1):1–11. doi: 10.1016/0378-1119(87)90359-3. [DOI] [PubMed] [Google Scholar]
  25. Sisodia S. S., Sollner-Webb B., Cleveland D. W. Specificity of RNA maturation pathways: RNAs transcribed by RNA polymerase III are not substrates for splicing or polyadenylation. Mol Cell Biol. 1987 Oct;7(10):3602–3612. doi: 10.1128/mcb.7.10.3602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Takagaki Y., Ryner L. C., Manley J. L. Separation and characterization of a poly(A) polymerase and a cleavage/specificity factor required for pre-mRNA polyadenylation. Cell. 1988 Mar 11;52(5):731–742. doi: 10.1016/0092-8674(88)90411-4. [DOI] [PubMed] [Google Scholar]
  27. Whitelaw E., Proudfoot N. Alpha-thalassaemia caused by a poly(A) site mutation reveals that transcriptional termination is linked to 3' end processing in the human alpha 2 globin gene. EMBO J. 1986 Nov;5(11):2915–2922. doi: 10.1002/j.1460-2075.1986.tb04587.x. [DOI] [PMC free article] [PubMed] [Google Scholar]