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. 1988 Jul 25;16(14B):7159–7176. doi: 10.1093/nar/16.14.7159

Plant intron sequences: evidence for distinct groups of introns.

B A Hanley 1, M A Schuler 1
PMCID: PMC338358  PMID: 3405760

Abstract

In vivo and in vitro RNA splicing experiments have demonstrated that the intron splicing machineries are not interchangeable in all organisms. These differences have prevented the efficient in vivo expression of monocot genes containing introns in dicot plants and the in vitro excision of some plant introns in HeLa cell in vitro splicing extracts. We have analyzed plant introns for sequence differences which potentially account for the functional splicing differences. Three classes of plant introns can be differentiated by the purine or pyrimidine-richness of sequences upstream from the 3' splice site. The frequency of these three types of introns in monocots and dicots varies significantly. The degree of variability in the 5' and 3' intron boundaries is evaluated for each of these classes in monocots and dicots. The 5' splice site consensus sequences developed for the monocot and dicot introns differ in their ability to base pair with conserved nucleotides present at the 5' end of many U1 snRNAs.

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Selected References

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  1. Berry-Lowe S. L., Mc Knight T. D., Shah D. M., Meagher R. B. The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J Mol Appl Genet. 1982;1(6):483–498. [PubMed] [Google Scholar]
  2. Bevan M., Barker R., Goldsbrough A., Jarvis M., Kavanagh T., Iturriaga G. The structure and transcription start site of a major potato tuber protein gene. Nucleic Acids Res. 1986 Jun 11;14(11):4625–4638. doi: 10.1093/nar/14.11.4625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Black D. L., Chabot B., Steitz J. A. U2 as well as U1 small nuclear ribonucleoproteins are involved in premessenger RNA splicing. Cell. 1985 Oct;42(3):737–750. doi: 10.1016/0092-8674(85)90270-3. [DOI] [PubMed] [Google Scholar]
  4. Boutry M., Chua N. H. A nuclear gene encoding the beta subunit of the mitochondrial ATP synthase in Nicotiana plumbaginifolia. EMBO J. 1985 Sep;4(9):2159–2165. doi: 10.1002/j.1460-2075.1985.tb03910.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bown D., Levasseur M., Croy R. R., Boulter D., Gatehouse J. A. Sequence of a pseudogene in the legumin gene family of pea (Pisum sativum L.). Nucleic Acids Res. 1985 Jun 25;13(12):4527–4538. doi: 10.1093/nar/13.12.4527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Breathnach R., Benoist C., O'Hare K., Gannon F., Chambon P. Ovalbumin gene: evidence for a leader sequence in mRNA and DNA sequences at the exon-intron boundaries. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4853–4857. doi: 10.1073/pnas.75.10.4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown D. T., Morris G. F., Chodchoy N., Sprecher C., Marzluff W. F. Structure of the sea urchin U1 RNA repeat. Nucleic Acids Res. 1985 Jan 25;13(2):537–556. doi: 10.1093/nar/13.2.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown J. W. A catalogue of splice junction and putative branch point sequences from plant introns. Nucleic Acids Res. 1986 Dec 22;14(24):9549–9559. doi: 10.1093/nar/14.24.9549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown J. W., Feix G., Frendewey D. Accurate in vitro splicing of two pre-mRNA plant introns in a HeLa cell nuclear extract. EMBO J. 1986 Nov;5(11):2749–2758. doi: 10.1002/j.1460-2075.1986.tb04563.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bäumlein H., Wobus U., Pustell J., Kafatos F. C. The legumin gene family: structure of a B type gene of Vicia faba and a possible legumin gene specific regulatory element. Nucleic Acids Res. 1986 Mar 25;14(6):2707–2720. doi: 10.1093/nar/14.6.2707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chen J., Varner J. E. An extracellular matrix protein in plants: characterization of a genomic clone for carrot extensin. EMBO J. 1985 Sep;4(9):2145–2151. doi: 10.1002/j.1460-2075.1985.tb03908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Cramer J. H., Lea K., Slightom J. L. Expression of phaseolin cDNA genes in yeast under control of natural plant DNA sequences. Proc Natl Acad Sci U S A. 1985 Jan;82(2):334–338. doi: 10.1073/pnas.82.2.334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dennis E. S., Gerlach W. L., Pryor A. J., Bennetzen J. L., Inglis A., Llewellyn D., Sachs M. M., Ferl R. J., Peacock W. J. Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res. 1984 May 11;12(9):3983–4000. doi: 10.1093/nar/12.9.3983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fluhr Robert, Moses Phyllis, Morelli Giorgio, Coruzzi Gloria, Chua Nam-Hai. Expression dynamics of the pea rbcS multigene family and organ distribution of the transcripts. EMBO J. 1986 Sep;5(9):2063–2071. doi: 10.1002/j.1460-2075.1986.tb04467.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Frendewey D., Keller W. Stepwise assembly of a pre-mRNA splicing complex requires U-snRNPs and specific intron sequences. Cell. 1985 Aug;42(1):355–367. doi: 10.1016/s0092-8674(85)80131-8. [DOI] [PubMed] [Google Scholar]
  17. Gerke V., Steitz J. A. A protein associated with small nuclear ribonucleoprotein particles recognizes the 3' splice site of premessenger RNA. Cell. 1986 Dec 26;47(6):973–984. doi: 10.1016/0092-8674(86)90812-3. [DOI] [PubMed] [Google Scholar]
  18. Hartmuth K., Barta A. In vitro processing of a plant pre-mRNA in a HeLa cell nuclear extract. Nucleic Acids Res. 1986 Oct 10;14(19):7513–7528. doi: 10.1093/nar/14.19.7513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hernandez N., Keller W. Splicing of in vitro synthesized messenger RNA precursors in HeLa cell extracts. Cell. 1983 Nov;35(1):89–99. doi: 10.1016/0092-8674(83)90211-8. [DOI] [PubMed] [Google Scholar]
  20. Hyldig-Nielsen J. J., Jensen E. O., Paludan K., Wiborg O., Garrett R., Jørgensen P., Marcker K. A. The primary structures of two leghemoglobin genes from soybean. Nucleic Acids Res. 1982 Jan 22;10(2):689–701. doi: 10.1093/nar/10.2.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnson R. A., Jakobs K. H., Schultz G. Extraction of the adenylate cyclase-activating factor of bovine sperm and its identification as a trypsin-like protease. J Biol Chem. 1985 Jan 10;260(1):114–121. [PubMed] [Google Scholar]
  22. Katinakis P., Verma D. P. Nodulin-24 gene of soybean codes for a peptide of the peribacteroid membrane and was generated by tandem duplication of a sequence resembling an insertion element. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4157–4161. doi: 10.1073/pnas.82.12.4157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Keith B., Chua N. H. Monocot and dicot pre-mRNAs are processed with different efficiencies in transgenic tobacco. EMBO J. 1986 Oct;5(10):2419–2425. doi: 10.1002/j.1460-2075.1986.tb04516.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Keller E. B., Noon W. A. Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs. Nucleic Acids Res. 1985 Jul 11;13(13):4971–4981. doi: 10.1093/nar/13.13.4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Keller E. B., Noon W. A. Intron splicing: a conserved internal signal in introns of animal pre-mRNAs. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7417–7420. doi: 10.1073/pnas.81.23.7417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Krämer A., Keller W., Appel B., Lührmann R. The 5' terminus of the RNA moiety of U1 small nuclear ribonucleoprotein particles is required for the splicing of messenger RNA precursors. Cell. 1984 Aug;38(1):299–307. doi: 10.1016/0092-8674(84)90551-8. [DOI] [PubMed] [Google Scholar]
  27. Lamppa G., Nagy F., Chua N. H. Light-regulated and organ-specific expression of a wheat Cab gene in transgenic tobacco. Nature. 1985 Aug 22;316(6030):750–752. doi: 10.1038/316750a0. [DOI] [PubMed] [Google Scholar]
  28. Langford C. J., Gallwitz D. Evidence for an intron-contained sequence required for the splicing of yeast RNA polymerase II transcripts. Cell. 1983 Jun;33(2):519–527. doi: 10.1016/0092-8674(83)90433-6. [DOI] [PubMed] [Google Scholar]
  29. Langford C., Nellen W., Niessing J., Gallwitz D. Yeast is unable to excise foreign intervening sequences from hybrid gene transcripts. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1496–1500. doi: 10.1073/pnas.80.6.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lee J. S., Verma D. P. Structure and chromosomal arrangement of leghemoglobin genes in kidney bean suggest divergence in soybean leghemoglobin gene loci following tetraploidization. EMBO J. 1984 Dec 1;3(12):2745–2752. doi: 10.1002/j.1460-2075.1984.tb02205.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lycett G. W., Croy R. R., Shirsat A. H., Boulter D. The complete nucleotide sequence of a legumin gene from pea (Pisum sativum L.). Nucleic Acids Res. 1984 Jun 11;12(11):4493–4506. doi: 10.1093/nar/12.11.4493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Maniatis T., Reed R. The role of small nuclear ribonucleoprotein particles in pre-mRNA splicing. Nature. 1987 Feb 19;325(6106):673–678. doi: 10.1038/325673a0. [DOI] [PubMed] [Google Scholar]
  33. Marchionni M., Gilbert W. The triosephosphate isomerase gene from maize: introns antedate the plant-animal divergence. Cell. 1986 Jul 4;46(1):133–141. doi: 10.1016/0092-8674(86)90867-6. [DOI] [PubMed] [Google Scholar]
  34. Marco Y. A., Thanh V. H., Tumer N. E., Scallon B. J., Nielsen N. C. Cloning and structural analysis of DNA encoding an A2B1a subunit of glycinin. J Biol Chem. 1984 Nov 10;259(21):13436–13441. [PubMed] [Google Scholar]
  35. Matzke M. A., Susani M., Binns A. N., Lewis E. D., Rubenstein I., Matzke A. J. Transcription of a zein gene introduced into sunflower using a Ti plasmid vector. EMBO J. 1984 Jul;3(7):1525–1531. doi: 10.1002/j.1460-2075.1984.tb02006.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mazur B. J., Chui C. F. Sequence of a genomic DNA clone for the small subunit of ribulose bis-phosphate carboxylase-oxygenase from tobacco. Nucleic Acids Res. 1985 Apr 11;13(7):2373–2386. doi: 10.1093/nar/13.7.2373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mount S. M., Pettersson I., Hinterberger M., Karmas A., Steitz J. A. The U1 small nuclear RNA-protein complex selectively binds a 5' splice site in vitro. Cell. 1983 Jun;33(2):509–518. doi: 10.1016/0092-8674(83)90432-4. [DOI] [PubMed] [Google Scholar]
  39. Newman A. J., Lin R. J., Cheng S. C., Abelson J. Molecular consequences of specific intron mutations on yeast mRNA splicing in vivo and in vitro. Cell. 1985 Aug;42(1):335–344. doi: 10.1016/s0092-8674(85)80129-x. [DOI] [PubMed] [Google Scholar]
  40. Nguyen T., Zelechowska M., Foster V., Bergmann H., Verma D. P. Primary structure of the soybean nodulin-35 gene encoding uricase II localized in the peroxisomes of uninfected cells of nodules. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5040–5044. doi: 10.1073/pnas.82.15.5040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Padgett R. A., Grabowski P. J., Konarska M. M., Seiler S., Sharp P. A. Splicing of messenger RNA precursors. Annu Rev Biochem. 1986;55:1119–1150. doi: 10.1146/annurev.bi.55.070186.005351. [DOI] [PubMed] [Google Scholar]
  42. Padgett R. A., Hardy S. F., Sharp P. A. Splicing of adenovirus RNA in a cell-free transcription system. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5230–5234. doi: 10.1073/pnas.80.17.5230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Pikaard C. S., Mignery G. A., Ma D. P., Stark V. J., Park W. D. Sequence of two apparent pseudogenes of the major potato tuber protein, patatin. Nucleic Acids Res. 1986 Jul 11;14(13):5564–5566. doi: 10.1093/nar/14.13.5564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pikielny C. W., Teem J. L., Rosbash M. Evidence for the biochemical role of an internal sequence in yeast nuclear mRNA introns: implications for U1 RNA and metazoan mRNA splicing. Cell. 1983 Sep;34(2):395–403. doi: 10.1016/0092-8674(83)90373-2. [DOI] [PubMed] [Google Scholar]
  45. Reddy R. Compilation of small RNA sequences. Nucleic Acids Res. 1985;13 (Suppl):r155–r163. doi: 10.1093/nar/13.suppl.r155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Reed R., Maniatis T. Intron sequences involved in lariat formation during pre-mRNA splicing. Cell. 1985 May;41(1):95–105. doi: 10.1016/0092-8674(85)90064-9. [DOI] [PubMed] [Google Scholar]
  47. Ruskin B., Green M. R. Specific and stable intron-factor interactions are established early during in vitro pre-mRNA splicing. Cell. 1985 Nov;43(1):131–142. doi: 10.1016/0092-8674(85)90018-2. [DOI] [PubMed] [Google Scholar]
  48. Ruskin B., Krainer A. R., Maniatis T., Green M. R. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell. 1984 Aug;38(1):317–331. doi: 10.1016/0092-8674(84)90553-1. [DOI] [PubMed] [Google Scholar]
  49. Ruskin B., Pikielny C. W., Rosbash M., Green M. R. Alternative branch points are selected during splicing of a yeast pre-mRNA in mammalian and yeast extracts. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2022–2026. doi: 10.1073/pnas.83.7.2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Rymond B. C., Rosbash M. Cleavage of 5' splice site and lariat formation are independent of 3' splice site in yeast mRNA splicing. Nature. 1985 Oct 24;317(6039):735–737. doi: 10.1038/317735a0. [DOI] [PubMed] [Google Scholar]
  51. Schuler M. A., Schmitt E. S., Beachy R. N. Closely related families of genes code for the alpha and alpha' subunits of the soybean 7S storage protein complex. Nucleic Acids Res. 1982 Dec 20;10(24):8225–8244. doi: 10.1093/nar/10.24.8225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Shah D. M., Hightower R. C., Meagher R. B. Complete nucleotide sequence of a soybean actin gene. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1022–1026. doi: 10.1073/pnas.79.4.1022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Shah D. M., Hightower R. C., Meagher R. B. Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not. J Mol Appl Genet. 1983;2(1):111–126. [PubMed] [Google Scholar]
  54. Slightom J. L., Sun S. M., Hall T. C. Complete nucleotide sequence of a French bean storage protein gene: Phaseolin. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1897–1901. doi: 10.1073/pnas.80.7.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tazi J., Alibert C., Temsamani J., Reveillaud I., Cathala G., Brunel C., Jeanteur P. A protein that specifically recognizes the 3' splice site of mammalian pre-mRNA introns is associated with a small nuclear ribonucleoprotein. Cell. 1986 Dec 5;47(5):755–766. doi: 10.1016/0092-8674(86)90518-0. [DOI] [PubMed] [Google Scholar]
  56. Tollervey D. High level of complexity of small nuclear RNAs in fungi and plants. J Mol Biol. 1987 Jul 20;196(2):355–361. doi: 10.1016/0022-2836(87)90696-6. [DOI] [PubMed] [Google Scholar]
  57. Tumer N. E., Clark W. G., Tabor G. J., Hironaka C. M., Fraley R. T., Shah D. M. The genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase are expressed differentially in petunia leaves. Nucleic Acids Res. 1986 Apr 25;14(8):3325–3342. doi: 10.1093/nar/14.8.3325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Watts F., Castle C., Beggs J. Aberrant splicing of Drosophila alcohol dehydrogenase transcripts in Saccharomyces cerevisiae. EMBO J. 1983;2(11):2085–2091. doi: 10.1002/j.1460-2075.1983.tb01704.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Werr W., Frommer W. B., Maas C., Starlinger P. Structure of the sucrose synthase gene on chromosome 9 of Zea mays L. EMBO J. 1985 Jun;4(6):1373–1380. doi: 10.1002/j.1460-2075.1985.tb03789.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Wiborg O., Hyldig-Nielsen J. J., Jensen E. O., Paludan K., Marcker K. A. The nucleotide sequences of two leghemoglobin genes from soybean. Nucleic Acids Res. 1982 Jun 11;10(11):3487–3494. doi: 10.1093/nar/10.11.3487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Wiborg O., Hyldig-Nielsen J. J., Jensen E. O., Paludan K., Marcker K. A. The structure of an unusual leghemoglobin gene from soybean. EMBO J. 1983;2(3):449–452. doi: 10.1002/j.1460-2075.1983.tb01443.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Zhuang Y., Weiner A. M. A compensatory base change in U1 snRNA suppresses a 5' splice site mutation. Cell. 1986 Sep 12;46(6):827–835. doi: 10.1016/0092-8674(86)90064-4. [DOI] [PubMed] [Google Scholar]
  63. van Santen V. L., Spritz R. A. Nucleotide sequence of a bean (Phaseolus vulgaris) U1 small nuclear RNA gene: implications for plant pre-mRNA splicing. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9094–9098. doi: 10.1073/pnas.84.24.9094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. van Santen V. L., Spritz R. A. Splicing of plant pre-mRNAs in animal systems and vice versa. Gene. 1987;56(2-3):253–265. doi: 10.1016/0378-1119(87)90142-9. [DOI] [PubMed] [Google Scholar]

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