Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1994 Jun;6(6):907–916. doi: 10.1105/tpc.6.6.907

Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants.

T E Bureau 1, S R Wessler 1
PMCID: PMC160488  PMID: 8061524

Abstract

Members of a new inverted repeat element family, named Stowaway, have been found in close association with more than 40 monocotyledonous and dicotyledonous plant genes listed in the GenBank and EMBL nucleic acid data bases. Stowaway elements are characterized by a conserved terminal inverted repeat, small size, target site specificity (TA), and potential form stable DNA secondary structures. Some elements are located at the extreme 3' ends of sequenced cDNAs and supply polyadenylation signals to their host genes. Other elements are in the 5' upstream regions of several genes and appear to contain previously identified cis-acting regulatory domains. Although the Stowaway elements share many structural features with the recently discovered Tourist elements, the two families share no significant sequence similarity. Together, the Stowaway and Tourist families serve to define an important new class of short inverted repeat elements found in possibly all flowering plant genomes.

Full Text

The Full Text of this article is available as a PDF (958.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albert H. A., Martin T., Sun S. S. Structure and expression of a sugarcane gene encoding a housekeeping phosphoenolpyruvate carboxylase. Plant Mol Biol. 1992 Nov;20(4):663–671. doi: 10.1007/BF00046451. [DOI] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Athma P., Grotewold E., Peterson T. Insertional mutagenesis of the maize P gene by intragenic transposition of Ac. Genetics. 1992 May;131(1):199–209. doi: 10.1093/genetics/131.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Banville D., Boie Y. Retroviral long terminal repeat is the promoter of the gene encoding the tumor-associated calcium-binding protein oncomodulin in the rat. J Mol Biol. 1989 Jun 5;207(3):481–490. doi: 10.1016/0022-2836(89)90458-0. [DOI] [PubMed] [Google Scholar]
  5. Batschauer A., Ehmann B., Schäfer E. Cloning and characterization of a chalcone synthase gene from mustard and its light-dependent expression. Plant Mol Biol. 1991 Feb;16(2):175–185. doi: 10.1007/BF00020550. [DOI] [PubMed] [Google Scholar]
  6. Baumruker T., Gehe C., Horak I. Insertion of a retrotransposon within the 3' end of a mouse gene provides a new functional polyadenylation signal. Nucleic Acids Res. 1988 Aug 11;16(15):7241–7251. doi: 10.1093/nar/16.15.7241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benfey P. N., Takatsuji H., Ren L., Shah D. M., Chua N. H. Sequence Requirements of the 5-Enolpyruvylshikimate-3-phosphate Synthase 5[prime]-Upstream Region for Tissue-Specific Expression in Flowers and Seedlings. Plant Cell. 1990 Sep;2(9):849–856. doi: 10.1105/tpc.2.9.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Breslauer K. J., Frank R., Blöcker H., Marky L. A. Predicting DNA duplex stability from the base sequence. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3746–3750. doi: 10.1073/pnas.83.11.3746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bureau T. E., Wessler S. R. Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1411–1415. doi: 10.1073/pnas.91.4.1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Chang-Yeh A., Mold D. E., Huang R. C. Identification of a novel murine IAP-promoted placenta-expressed gene. Nucleic Acids Res. 1991 Jul 11;19(13):3667–3672. doi: 10.1093/nar/19.13.3667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clemens M. J. A potential role for RNA transcribed from B2 repeats in the regulation of mRNA stability. Cell. 1987 Apr 24;49(2):157–158. doi: 10.1016/0092-8674(87)90553-8. [DOI] [PubMed] [Google Scholar]
  13. Das O. P., Ward K., Ray S., Messing J. Sequence variation between alleles reveals two types of copy correction at the 27-kDa zein locus of maize. Genomics. 1991 Dec;11(4):849–856. doi: 10.1016/0888-7543(91)90007-2. [DOI] [PubMed] [Google Scholar]
  14. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Doak T. G., Doerder F. P., Jahn C. L., Herrick G. A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common "D35E" motif. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):942–946. doi: 10.1073/pnas.91.3.942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Drouin G., Dover G. A. Independent gene evolution in the potato actin gene family demonstrated by phylogenetic procedures for resolving gene conversions and the phylogeny of angiosperm actin genes. J Mol Evol. 1990 Aug;31(2):132–150. doi: 10.1007/BF02109482. [DOI] [PubMed] [Google Scholar]
  17. Flavell R. B. Repetitive DNA and chromosome evolution in plants. Philos Trans R Soc Lond B Biol Sci. 1986 Jan 29;312(1154):227–242. doi: 10.1098/rstb.1986.0004. [DOI] [PubMed] [Google Scholar]
  18. Franz G., Hatzopoulos P., Jones T. J., Krauss M., Sung Z. R. Molecular and genetic analysis of an embryonic gene, DC 8, from Daucus carota L. Mol Gen Genet. 1989 Jul;218(1):143–151. doi: 10.1007/BF00330577. [DOI] [PubMed] [Google Scholar]
  19. Fuchs T., Beier D., Beier H. The tRNA(Tyr) multigene family of Nicotiana rustica: genome organization, sequence analyses and expression in vitro. Plant Mol Biol. 1992 Dec;20(5):869–878. doi: 10.1007/BF00027158. [DOI] [PubMed] [Google Scholar]
  20. Fukuda Y., Ohme M., Shinshi H. Gene structure and expression of a tobacco endochitinase gene in suspension-cultured tobacco cells. Plant Mol Biol. 1991 Jan;16(1):1–10. doi: 10.1007/BF00017912. [DOI] [PubMed] [Google Scholar]
  21. Gasser C. S., Klee H. J. A Brassica napus gene encoding 5-enolpyruvylshikimate-3-phosphate synthase. Nucleic Acids Res. 1990 May 11;18(9):2821–2821. doi: 10.1093/nar/18.9.2821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Goodchild N. L., Wilkinson D. A., Mager D. L. A human endogenous long terminal repeat provides a polyadenylation signal to a novel, alternatively spliced transcript in normal placenta. Gene. 1992 Nov 16;121(2):287–294. doi: 10.1016/0378-1119(92)90133-a. [DOI] [PubMed] [Google Scholar]
  23. Grandbastien M. A. Retroelements in higher plants. Trends Genet. 1992 Mar;8(3):103–108. doi: 10.1016/0168-9525(92)90198-d. [DOI] [PubMed] [Google Scholar]
  24. Halford N. G., Vicente-Carbajosa J., Sabelli P. A., Shewry P. R., Hannappel U., Kreis M. Molecular analyses of a barley multigene family homologous to the yeast protein kinase gene SNF1. Plant J. 1992 Sep;2(5):791–797. [PubMed] [Google Scholar]
  25. Hatzopoulos P., Franz G., Choy L., Sung R. Z. Interaction of nuclear factors with upstream sequences of a lipid body membrane protein gene from carrot. Plant Cell. 1990 May;2(5):457–467. doi: 10.1105/tpc.2.5.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Huttly A. K., Phillips A. L., Tregear J. W. Localisation of cis elements in the promoter of a wheat alpha-Amy2 gene. Plant Mol Biol. 1992 Sep;19(6):903–911. doi: 10.1007/BF00040523. [DOI] [PubMed] [Google Scholar]
  27. Kersanach R., Brinkmann H., Liaud M. F., Zhang D. X., Martin W., Cerff R. Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature. 1994 Jan 27;367(6461):387–389. doi: 10.1038/367387a0. [DOI] [PubMed] [Google Scholar]
  28. Kim J. K., Wu R. Nucleotide sequence of a high-pI rice (Oryza sativa) -amylase gene. Plant Mol Biol. 1992 Jan;18(2):399–402. doi: 10.1007/BF00034966. [DOI] [PubMed] [Google Scholar]
  29. Kirihara J. A., Petri J. B., Messing J. Isolation and sequence of a gene encoding a methionine-rich 10-kDa zein protein from maize. Gene. 1988 Nov 30;71(2):359–370. doi: 10.1016/0378-1119(88)90053-4. [DOI] [PubMed] [Google Scholar]
  30. Koes R. E., Spelt C. E., van den Elzen P. J., Mol J. N. Cloning and molecular characterization of the chalcone synthase multigene family of Petunia hybrida. Gene. 1989 Sep 30;81(2):245–257. doi: 10.1016/0378-1119(89)90185-6. [DOI] [PubMed] [Google Scholar]
  31. Lepiniec L., Keryer E., Philippe H., Gadal P., Crétin C. Sorghum phosphoenolpyruvate carboxylase gene family: structure, function and molecular evolution. Plant Mol Biol. 1993 Feb;21(3):487–502. doi: 10.1007/BF00028806. [DOI] [PubMed] [Google Scholar]
  32. Maichele A. J., Farwell N. J., Chamberlain J. S. A B2 repeat insertion generates alternate structures of the mouse muscle gamma-phosphorylase kinase gene. Genomics. 1993 Apr;16(1):139–149. doi: 10.1006/geno.1993.1151. [DOI] [PubMed] [Google Scholar]
  33. Mandaci S., Dobres M. S. Sequence of a vegetative homolog of the pea seed lectin gene. Plant Physiol. 1993 Oct;103(2):663–664. doi: 10.1104/pp.103.2.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Manzara T., Carrasco P., Gruissem W. Developmental and organ-specific changes in DNA-protein interactions in the tomato rbcS1, rbcS2 and rbcS3A promoter regions. Plant Mol Biol. 1993 Jan;21(1):69–88. doi: 10.1007/BF00039619. [DOI] [PubMed] [Google Scholar]
  35. Paulson K. E., Matera A. G., Deka N., Schmid C. W. Transcription of a human transposon-like sequence is usually directed by other promoters. Nucleic Acids Res. 1987 Jul 10;15(13):5199–5215. doi: 10.1093/nar/15.13.5199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Perez C., Michelet B., Ferrant V., Bogaerts P., Boutry M. Differential expression within a three-gene subfamily encoding a plasma membrane H(+)-ATPase in Nicotiana plumbaginifolia. J Biol Chem. 1992 Jan 15;267(2):1204–1211. [PubMed] [Google Scholar]
  37. 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]
  38. Stanford A. C., Northcote D. H., Bevan M. W. Spatial and temporal patterns of transcription of a wound-induced gene in potato. EMBO J. 1990 Mar;9(3):593–603. doi: 10.1002/j.1460-2075.1990.tb08151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stanford A., Bevan M., Northcote D. Differential expression within a family of novel wound-induced genes in potato. Mol Gen Genet. 1989 Jan;215(2):200–208. doi: 10.1007/BF00339718. [DOI] [PubMed] [Google Scholar]
  40. Stavenhagen J. B., Robins D. M. An ancient provirus has imposed androgen regulation on the adjacent mouse sex-limited protein gene. Cell. 1988 Oct 21;55(2):247–254. doi: 10.1016/0092-8674(88)90047-5. [DOI] [PubMed] [Google Scholar]
  41. Sutliff T. D., Huang N., Litts J. C., Rodriguez R. L. Characterization of an alpha-amylase multigene cluster in rice. Plant Mol Biol. 1991 Apr;16(4):579–591. doi: 10.1007/BF00023423. [DOI] [PubMed] [Google Scholar]
  42. Suzuka I., Hata S., Matsuoka M., Kosugi S., Hashimoto J. Highly conserved structure of proliferating cell nuclear antigen (DNA polymerase delta auxiliary protein) gene in plants. Eur J Biochem. 1991 Jan 30;195(2):571–575. doi: 10.1111/j.1432-1033.1991.tb15739.x. [DOI] [PubMed] [Google Scholar]
  43. Thompson G. A., Siemieniak D. R., Sieu L. C., Slightom J. L., Larkins B. A. Sequence analysis of linked maize 22 kDa alpha-zein genes. Plant Mol Biol. 1992 Feb;18(4):827–833. doi: 10.1007/BF00020030. [DOI] [PubMed] [Google Scholar]
  44. Twell D., Yamaguchi J., Wing R. A., Ushiba J., McCormick S. Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev. 1991 Mar;5(3):496–507. doi: 10.1101/gad.5.3.496. [DOI] [PubMed] [Google Scholar]
  45. Umeda M., Ohtsubo H., Ohtsubo E. Diversification of the rice Waxy gene by insertion of mobile DNA elements into introns. Jpn J Genet. 1991 Oct;66(5):569–586. doi: 10.1266/jjg.66.569. [DOI] [PubMed] [Google Scholar]
  46. Wang Z. Y., Wu Z. L., Xing Y. Y., Zheng F. G., Guo X. L., Zhang W. G., Hong M. M. Nucleotide sequence of rice waxy gene. Nucleic Acids Res. 1990 Oct 11;18(19):5898–5898. doi: 10.1093/nar/18.19.5898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wimmers L. E., Ewing N. N., Bennett A. B. Higher plant Ca(2+)-ATPase: primary structure and regulation of mRNA abundance by salt. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9205–9209. doi: 10.1073/pnas.89.19.9205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wolf N. Complete Nucleotide Sequence of a Hordeum vulgare Gene Encoding (1-->3, 1-->4)-beta-Glucanase Isoenzyme II. Plant Physiol. 1991 Aug;96(4):1382–1384. doi: 10.1104/pp.96.4.1382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. van de Löcht U., Meier I., Hahlbrock K., Somssich I. E. A 125 bp promoter fragment is sufficient for strong elicitor-mediated gene activation in parsley. EMBO J. 1990 Sep;9(9):2945–2950. doi: 10.1002/j.1460-2075.1990.tb07486.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES