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. 1997 Jun;9(6):967–978. doi: 10.1105/tpc.9.6.967

Retrotransposon insertion into the maize waxy gene results in tissue-specific RNA processing.

S Marillonnet 1, S R Wessler 1
PMCID: PMC156971  PMID: 9212470

Abstract

We previously reported that three alleles of the maize waxy (wx) gene were alternatively spliced as a result of the insertion of retrotransposons into intronic sequences. In addition, inefficient splicing of element sequences with the surrounding intron produced wild-type transcripts that presumably were responsible for the observed residual gene expression in the endosperm. In this study, we report that one of these alleles, wxG, has a tissue-specific phenotype with 30-fold more WX enzymatic activity in pollen than in the endosperm. Quantification of wxG-encoded transcripts in pollen and the endosperm demonstrates that this difference can be accounted for by tissue-specific differences in RNA processing. Specifically, there is approximately 30-fold more correctly spliced RNA in pollen than in the endosperm. Based on an analogy to similar examples of tissue-specific alternative splicing in animal systems, we hypothesize that the tissue-specific phenotype of the wxG allele may reflect differences in the concentration of splicing factors in these tissues.

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Selected References

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  1. Barkan A., Martienssen R. A. Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3502–3506. doi: 10.1073/pnas.88.8.3502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belgrader P., Maquat L. E. Nonsense but not missense mutations can decrease the abundance of nuclear mRNA for the mouse major urinary protein, while both types of mutations can facilitate exon skipping. Mol Cell Biol. 1994 Sep;14(9):6326–6336. doi: 10.1128/mcb.14.9.6326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bureau T. E., Wessler S. R. Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. Plant Cell. 1994 Jun;6(6):907–916. doi: 10.1105/tpc.6.6.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bureau T. E., Wessler S. R. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell. 1992 Oct;4(10):1283–1294. doi: 10.1105/tpc.4.10.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coen E. S., Carpenter R., Martin C. Transposable elements generate novel spatial patterns of gene expression in Antirrhinum majus. Cell. 1986 Oct 24;47(2):285–296. doi: 10.1016/0092-8674(86)90451-4. [DOI] [PubMed] [Google Scholar]
  6. Dawe R. K., Lachmansingh A. R., Freeling M. Transposon-mediated mutations in the untranslated leader of maize Adh1 that increase and decrease pollen-specific gene expression. Plant Cell. 1993 Mar;5(3):311–319. doi: 10.1105/tpc.5.3.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fedoroff N., Mauvais J., Chaleff D. Molecular studies on mutations at the Shrunken locus in maize caused by the controlling element Ds. J Mol Appl Genet. 1983;2(1):11–29. [PubMed] [Google Scholar]
  8. Görlach J., Raesecke H. R., Abel G., Wehrli R., Amrhein N., Schmid J. Organ-specific differences in the ratio of alternatively spliced chorismate synthase (LeCS2) transcripts in tomato. Plant J. 1995 Sep;8(3):451–456. doi: 10.1046/j.1365-313x.1995.08030451.x. [DOI] [PubMed] [Google Scholar]
  9. Hirochika H., Sugimoto K., Otsuki Y., Tsugawa H., Kanda M. Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7783–7788. doi: 10.1073/pnas.93.15.7783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Johns M. A., Mottinger J., Freeling M. A low copy number, copia-like transposon in maize. EMBO J. 1985 May;4(5):1093–1101. doi: 10.1002/j.1460-2075.1985.tb03745.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kim H. Y., Schiefelbein J. W., Raboy V., Furtek D. B., Nelson O. E., Jr RNA splicing permits expression of a maize gene with a defective Suppressor-mutator transposable element insertion in an exon. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5863–5867. doi: 10.1073/pnas.84.16.5863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kloeckener-Gruissem B., Freeling M. Transposon-induced promoter scrambling: a mechanism for the evolution of new alleles. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):1836–1840. doi: 10.1073/pnas.92.6.1836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kopriva S., Cossu R., Bauwe H. Alternative splicing results in two different transcripts for H-protein of the glycine cleavage system in the C4 species Flaveria trinervia. Plant J. 1995 Sep;8(3):435–441. doi: 10.1046/j.1365-313x.1995.08030435.x. [DOI] [PubMed] [Google Scholar]
  14. Lazar G., Schaal T., Maniatis T., Goodman H. M. Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7672–7676. doi: 10.1073/pnas.92.17.7672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Liu Y., Alleman M., Wessler S. R. A Ds insertion alters the nuclear localization of the maize transcriptional activator R. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7816–7820. doi: 10.1073/pnas.93.15.7816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Luehrsen K. R., Taha S., Walbot V. Nuclear pre-mRNA processing in higher plants. Prog Nucleic Acid Res Mol Biol. 1994;47:149–193. doi: 10.1016/s0079-6603(08)60252-4. [DOI] [PubMed] [Google Scholar]
  17. Masson P., Surosky R., Kingsbury J. A., Fedoroff N. V. Genetic and molecular analysis of the Spm-dependent a-m2 alleles of the maize a locus. Genetics. 1987 Sep;117(1):117–137. doi: 10.1093/genetics/117.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mayeda A., Krainer A. R. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell. 1992 Jan 24;68(2):365–375. doi: 10.1016/0092-8674(92)90477-t. [DOI] [PubMed] [Google Scholar]
  19. Niwa M., Berget S. M. Mutation of the AAUAAA polyadenylation signal depresses in vitro splicing of proximal but not distal introns. Genes Dev. 1991 Nov;5(11):2086–2095. doi: 10.1101/gad.5.11.2086. [DOI] [PubMed] [Google Scholar]
  20. Niwa M., Rose S. D., Berget S. M. In vitro polyadenylation is stimulated by the presence of an upstream intron. Genes Dev. 1990 Sep;4(9):1552–1559. doi: 10.1101/gad.4.9.1552. [DOI] [PubMed] [Google Scholar]
  21. Ortiz D. F., Strommer J. N. The Mu1 maize transposable element induces tissue-specific aberrant splicing and polyadenylation in two Adh1 mutants. Mol Cell Biol. 1990 May;10(5):2090–2095. doi: 10.1128/mcb.10.5.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Parkhurst S. M., Corces V. G. Forked, gypsys, and suppressors in Drosophila. Cell. 1985 Jun;41(2):429–437. doi: 10.1016/s0092-8674(85)80016-7. [DOI] [PubMed] [Google Scholar]
  23. Pulak R., Anderson P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 1993 Oct;7(10):1885–1897. doi: 10.1101/gad.7.10.1885. [DOI] [PubMed] [Google Scholar]
  24. SanMiguel P., Tikhonov A., Jin Y. K., Motchoulskaia N., Zakharov D., Melake-Berhan A., Springer P. S., Edwards K. J., Lee M., Avramova Z. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. doi: 10.1126/science.274.5288.765. [DOI] [PubMed] [Google Scholar]
  25. Seperack P. K., Mercer J. A., Strobel M. C., Copeland N. G., Jenkins N. A. Retroviral sequences located within an intron of the dilute gene alter dilute expression in a tissue-specific manner. EMBO J. 1995 May 15;14(10):2326–2332. doi: 10.1002/j.1460-2075.1995.tb07227.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shen J., Zu K., Cass C. L., Beyer A. L., Hirsh J. Exon skipping by overexpression of a Drosophila heterogeneous nuclear ribonucleoprotein in vivo. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):1822–1825. doi: 10.1073/pnas.92.6.1822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shure M., Wessler S., Fedoroff N. Molecular identification and isolation of the Waxy locus in maize. Cell. 1983 Nov;35(1):225–233. doi: 10.1016/0092-8674(83)90225-8. [DOI] [PubMed] [Google Scholar]
  28. Springer P. S., Edwards K. J., Bennetzen J. L. DNA class organization on maize Adh1 yeast artificial chromosomes. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):863–867. doi: 10.1073/pnas.91.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Varagona M. J., Purugganan M., Wessler S. R. Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell. 1992 Jul;4(7):811–820. doi: 10.1105/tpc.4.7.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vignols F., Rigau J., Torres M. A., Capellades M., Puigdomènech P. The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell. 1995 Apr;7(4):407–416. doi: 10.1105/tpc.7.4.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wessler S. R., Baran G., Varagona M. The maize transposable element Ds is spliced from RNA. Science. 1987 Aug 21;237(4817):916–918. doi: 10.1126/science.3039661. [DOI] [PubMed] [Google Scholar]
  32. Wessler S. R., Bureau T. E., White S. E. LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev. 1995 Dec;5(6):814–821. doi: 10.1016/0959-437x(95)80016-x. [DOI] [PubMed] [Google Scholar]
  33. Wessler S. R., Varagona M. J. Molecular basis of mutations at the waxy locus of maize: correlation with the fine structure genetic map. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4177–4181. doi: 10.1073/pnas.82.12.4177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. White S. E., Habera L. F., Wessler S. R. Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11792–11796. doi: 10.1073/pnas.91.25.11792. [DOI] [PMC free article] [PubMed] [Google Scholar]

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