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Plant Molecular Biology

, Volume 36, Issue 4, pp 573–583 | Cite as

U-richness is a defining feature of plant introns and may function as an intron recognition signal in maize

  • Christopher H. Ko
  • Volker Brendel
  • Rebecca D. Taylor
  • Virginia Walbot
Article

Abstract

Using a large set of plant gene sequences we compared individual introns to their flanking exons. Both Zea mays and Arabidopsis thaliana introns are U-rich but display no apparent bias for A. We identified fifteen 11-mer U-rich motifs as frequent elements of maize introns, and these are virtually absent from exons. By mutagenesis, we show that the single U-rich motif in the Bronze2 intron of maize plays a key role in intron processing in vivo.

intron processing base composition U-rich motif Zea mays 

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References

  1. 1.
    Ausubel F, Brent R, Kingston R, Moore D, Seidman J, Smith J, Struhl K, (eds) Current Protocols in Molecular Biology, pp. 13.13.1–13.13.9. John Wiley, New York (1987).Google Scholar
  2. 2.
    Baynton CE, Potthoff SJ, McCullough AJ, Schuler MA: U-rich tracts enhance 3′splice site recognition in plant nuclei. Plant J 10: 703–711 (1996).PubMedGoogle Scholar
  3. 3.
    Brendel V: PROSET a fast procedure to create non-redundant sets of protein sequences. Math Comput Mod 16 (6/7): 37–43 (1992).Google Scholar
  4. 4.
    Brendel V, Carle-Urioste JC, Walbot V: Intron recognition in plants. In: Bailey-Serres J, Gallie DR (eds) A Look Beyond Transcription: Mechanisms Determining mRNA Stability and Translation in Plants. American Society for Plant Physiology, Rockville, MD, in press (1997).Google Scholar
  5. 5.
    Brown JWS: A catalogue of splice junction and putative branch point sequences from plant introns. Nucl Acids Res 14: 9549–9559 (1986).PubMedGoogle Scholar
  6. 6.
    Carle-Urioste JC, Ko CH, Benito M-I, W albot V: In vivo analysis of intron processing using splicing-dependent reporter gene assays. Plant Mol Biol 26: 1785–1795 (1994).PubMedGoogle Scholar
  7. 7.
    Carle-Urioste JC, Brendel V, Walbot V: A combinatorial role for exon, intron and splice site sequences in splicing in maize. Plant J 11: 1253–1263 (1997).PubMedGoogle Scholar
  8. 8.
    Csank C, Taylor FM, Martindale DW: Nuclear pre-mRNA introns: analysis and comparison of intron sequences from Tetrahymena thermophila and other eukaryotes. Nucl Acids Res 18: 5133–5141 (1990).PubMedGoogle Scholar
  9. 9.
    Egeland DB, Sturtevant AP, Schuler MA: Molecular analysis of dicot and monocot small nuclear RNA populations. Plant Cell 1: 633–643 (1989).PubMedGoogle Scholar
  10. 10.
    Filipowicz W, Gniadkowski M, Klahre U, Liu H-X: Pre-mRNA splicing in plants. In: Lamond A (ed) Pre-mRNA Processing, pp. 65–77. Landes Company, Austin, TX (1995).Google Scholar
  11. 11.
    Foster R, Gasch A, Kay S: Analysis of protein, DNA interactions. In: Koncz C, Chua N-H, Schell J (eds) Methods in Arabidopsis Research, pp. 378–392. World Scientific, Singapore (1993).Google Scholar
  12. 12.
    Gniadkowski M, Hemmings-Mieszczak M, Klahre U, Liu HX, Filipowicz W: Characterization of intronic uridine-rich sequence elements acting as possible targets for nuclear proteins during pre-mRNA splicing in Nicotiana plumbaginifolia. Nucl Acids Res 24: 619–627 (1996).PubMedGoogle Scholar
  13. 13.
    Goodall GJ, Filipowicz W: The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 58: 473–483 (1989).CrossRefPubMedGoogle Scholar
  14. 14.
    Goodall GJ, Filipowicz W: Different effects of intron nucleotide composition and secondary structure on pre-mRNA splicing in monocot and dicot plants. EMBO J 10: 2635–2644 (1991).PubMedGoogle Scholar
  15. 15.
    Guthrie C: Messenger RNA splicing in yeast: clues to why the spliceosome is a ribonucleoprotein. Science 253: 157–163 (1991).PubMedGoogle Scholar
  16. 16.
    Hanley BA, Schuler MA: Plant intron sequences: evidence for distinct groups of introns. Nucl Acids Res 16: 7159–7176 (1988).PubMedGoogle Scholar
  17. 17.
    Harris NL, Senapathy P: Distribution and consensus of branch point signals in eukaryotic genes: a computerized statistical analysis. Nucl Acids Res 18: 3015–3019 (1990).PubMedGoogle Scholar
  18. 18.
    Hodges PE, Jackson SP, Brown JD, Beggs JD: Extraordinary sequence conservation of the PRP8 splicing factor. Yeast 11: 337–342 (1995).PubMedGoogle Scholar
  19. 19.
    Karlin S, Brendel V: Chance and statistical significance in protein and DNA sequence analysis. Science 257: 39–49 (1992).PubMedGoogle Scholar
  20. 20.
    Karlin S, Brendel V: Patchiness and correlations in DNA sequences. Science 259: 677–68 (1993).PubMedGoogle Scholar
  21. 21.
    Keith B, Chua N-H: Monocot and dicot pre-mRNAs are processed with different efficiencies in transgenic tobacco. EMBO J 5: 2419–2425 (1986).Google Scholar
  22. 22.
    Kulesza H, Simpson GG, Waugh R, Beggs JD, Brown JWS: Detection of a plant protein analogous to the yeast spliceosomal protein, PRP8. FEBS Lett 318: 4–6 (1993).PubMedGoogle Scholar
  23. 23.
    Lazar G, Schaal T, Maniatis T, Goodman HM: Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Proc Natl Acad Sci USA 92: 7672–7676 (1996).Google Scholar
  24. 24.
    Liu H-X, Filipowicz W: Mapping of branch point nucleotides in mutant pre-mRNAs expressed in plant cells. Plant J 9: 381–389 (1996).PubMedGoogle Scholar
  25. 25.
    Lopato S, Mayeda A, Krainer AR, Barta A: Pre-mRNAsplicing in plants: characterization of SR splicing factors. Proc Natl Acad Sci USA 93: 3074–3079 (1996).PubMedGoogle Scholar
  26. 26.
    Lopato S, Waigmann E, Barta A: Characterization of a novel Arginine/Serine-rich splicing factor in Arabidopsis. Plant Cell 8: 2255–2264 (1996).PubMedGoogle Scholar
  27. 27.
    Lou H, McCullough AJ, Schuler MA: 30 splice site selection in dicot plant nuclei is position dependent. Mol Cell Biol 13: 4485–4493 (1993).PubMedGoogle Scholar
  28. 28.
    Lou H, McCullough AJ, Schuler MA: Expression of maize Adh1 intron mutants in tobacco nuclei. Plant J 3: 393–403 (1993).CrossRefPubMedGoogle Scholar
  29. 29.
    Luehrsen KR, de Wet JR, Walbot V: Transient expression analysis in plants using firefly luciferase reporter gene. Meth Enzymol 216: 397–414 (1992).PubMedGoogle Scholar
  30. 30.
    Luehrsen KR, Taha S, Walbot V: Nuclear pre-mRNA splicing in higher plants. Prog Nucl Acids Res Mol Biol 47: 149–193 (1994).Google Scholar
  31. 31.
    Luehrsen KR, Walbot V: Addition of A-and U-rich sequence increases the splicing efficiency of a deleted form of a maize intron. Plant Mol Biol 24: 449–463 (1994).CrossRefPubMedGoogle Scholar
  32. 32.
    Luehrsen KR, Walbot V: Intron creation and polyadenylation in maize are directed by AU-rich RNA. Genes Devel 8: 1117–1130 (1994).PubMedGoogle Scholar
  33. 33.
    Nash J: Bronze-2 gene of maize: analysis of transcription and splicing patterns. Ph. D. Thesis, Stanford University, Stanford, CA (1992).Google Scholar
  34. 34.
    Schbath S, Prum B, Turckheim E de: Exceptional motifs in different Markov chain models for a statistical analysis ofDNA sequences. J Comp Biol 2: 417–437 (1995).Google Scholar
  35. 35.
    Simpson GG, Clark CP, Rothnie HM, Boelens W, van Venrooij W, Brown JWS: Molecular characterization of the spliceosomal proteins U1A and U2B00 from higher plants. EMBO J 14: 4540–4550 (1995).PubMedGoogle Scholar
  36. 36.
    Simpson CG, Clark G, Davidson D, Smith P, Brown JWS: Mutation of putative branch point consensus sequence in plant introns reduces splicing efficiency. Plant J 9: 369–380 (1996).PubMedGoogle Scholar
  37. 37.
    Simpson GG, Filipowicz W: Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery. Plant Mol Biol 32: 1–41 (1996).PubMedGoogle Scholar
  38. 38.
    Singh R, Valcárcel J, Green MR: Distinct binding specificities and functions of higher eukaryotic polypyrimidine tractbinding proteins. Science 268: 1173–1176 (1995).PubMedGoogle Scholar
  39. 39.
    Solymosy F, Pollák T: Uridylate-rich small nuclear RNAs (UsnRNAs), their genes and pseudogenes, and UsnRNPs in plants: structure and function. A comparative approach. Crit Rev Plant Sci 12: 275–369 (1993).Google Scholar
  40. 40.
    Umen JG, Guthrie C: A novel role for a U5 snRNP protein in 3′splice the selection. Genes Devel 9: 855–868 (1995).PubMedGoogle Scholar
  41. 41.
    van Santen SV, Spritz RA: Splicing of plant pre-mRNAs in animal systems and vice versa. Gene 56: 253–265 (1987).CrossRefPubMedGoogle Scholar
  42. 42.
    White O, Soderlund C, Shanmugan P, Fields C: Information contents and dinuclotide compositions of plant intron sequences vary with evolutionary origin. Plant Mol Biol 9: 1057–1064 (1992).Google Scholar
  43. 43.
    Wiebauer K, Herrero J-J, Filipowicz W: Nuclear pre-mRNA processing in plants: Distinct modes of 30-splice site selection in plants and animals. Mol Cell Biol 8: 2042–2051 (1988).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Christopher H. Ko
    • 1
  • Volker Brendel
    • 2
  • Rebecca D. Taylor
    • 1
  • Virginia Walbot
    • 1
  1. 1.Department of Biological SciencesUSA
  2. 2.Department of MathematicsStanford UniversityStanfordUSA

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