Skip to main content
Log in

A retrotransposon-like sequence linked to the S-locus ofNicotiana alata is expressed in styles in response to touch

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

We have identified a family of repetitive sequences in the genome ofNicotiana alata namedTnal (Transposon ofN. alata). The first element we characterised was on a genomic clone for theN. alata S6-ribonuclease (S6-RNase), a gene required for self-incompatibility in this species. The DNA sequence of this element resembles the integrase domain of retro-transposons of thegypsy class and is most similar to a retrotransposon fromLilium henryi. A transcript present inN. alata styles (self-incompatibility genotype S6S6) hybridized toTnal and accumulated in the style following either pollination or touching. This transcript was cloned from a cDNA library and was encoded by a second, partialTnal element. Neither the transcribed sequence nor the originalTnal element contain an open reading frame or is likely to be able to transpose. The second element was mapped using a population ofN. alata plants segregating for alleles of the self-incompatibility locus and is closely linked to the S6-allele. TheTnal element is present in a number ofNicotiana species and appears to have been active at least twice during the evolution of this genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson MA, McFadden GI, Bernatzky R, Atkinson A, Orpin T, Dedman H, Tregear G, Fernley R, Clarke AE (1989) Sequence variability of three alleles of the self-incompatibility gene ofNicotiana alata. Plant Cell 1:483–491

    Article  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1987) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434

    Article  PubMed  Google Scholar 

  • Braam J, Davies RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes inArabidopsis. Cell 60:357–364

    Article  PubMed  Google Scholar 

  • Dobinson KF, Harris RE, Hamer JE (1993)Grasshopper, a long terminal repeat (LTR) retroelement in the phytopathogenic fungusMagnaporthe grisea. Mol Plant-Microbe Interact 6:114–126

    PubMed  Google Scholar 

  • Dodds PN, Bönig I, Du H, Rödin J, Anderson MA, Newbigin E, Clarke AE (1993) S-R Nase gene ofNicotiana alata is expressed in developing pollen. Plant Cell 5:1771–1782

    Article  PubMed  Google Scholar 

  • Doolittle RF, Feng DF, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Quart Rev Biol 64:1–29

    Article  PubMed  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radio-labelling DNA restriction fragments to high specific activity. Anal Biochem 132:6–13

    Article  PubMed  Google Scholar 

  • Flavell AJ (1992)Tyl-copia group retrotransposons and the evolution of retroelements in the eukaryotes. Genetics 86:203–214

    Article  Google Scholar 

  • Goodspeed TH (1954) The genusNicotiana. Chronica Botanica, Waltham, Mass.

    Google Scholar 

  • Grandbastein M-A (1992) Retroelements in higher plants. Trends Genet 8:103–108

    PubMed  Google Scholar 

  • Grandbastein M-A, Spielmann A, Caboche M (1989)Tntl, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376–380

    Google Scholar 

  • Harberd NP, Flavell RB, Thompson RD (1987) Identification of a transposon-like insertion in aGlu-1 allele of wheat. Mol Gen Genet 209:326–332

    Article  Google Scholar 

  • Hansen LJ, Chalker DL, Sandmeyer SB (1988)Ty3, a yeast retro-transposon associated with tRNA genes has homology to animal retroviruses. Mol Cell Biol 8:5245–5256

    PubMed  Google Scholar 

  • Hazuda DJ, Wolfe AL, Hastings JC, Robbins HL, Graham PL, LaFemina RL, Emini EA (1994) Viral long terminal repeat substrate binding characteristics of the human immunodeficiency virus type 1 integrase. J Biol Chem 269:3999–4004

    PubMed  Google Scholar 

  • Hoekstra FA, Weges R (1986) Effects of interspecific pollination on stylar ethylene production and flower longevity inPetunia hybrida. Acta Hortic 181:105–112

    Google Scholar 

  • Johns JL, Mottinger J, Freeling M (1985) A low copy number,copia-like transposon in maize. EMBO J 4:1093–1102

    PubMed  Google Scholar 

  • Johnson MS, McClure MA, Feng D-F, Gray J, Doolittle RF (1986) Computer analysis of retroviralpol genes: assignment of enzymatic functions to specific sequences and homologies with non-viral enzymes. Proc Natl Acad Sci USA 83:7648–7652

    PubMed  Google Scholar 

  • Khan E, Mack JPG, Katz RA, Kulkosky J, Skalka AM (1991) Retroviral integrase domains: DNA binding and the recognition of LTR sequences. Nucleic Acids Res 19:851–860

    PubMed  Google Scholar 

  • Kim A, Terzian C, Santamaria P, Pelisson A, Purd'homme N, Bucheton A (1994) Retroviruses in invertebrates: thegypsy retro-transposon is apparently an infectious retrovirus ofDrosophila melanogaster. Proc Natl Acad Sci USA 91:1285–1289

    PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  Google Scholar 

  • Leeton PRJ, Smyth DR (1993) An abundant LINE-like element amplified in the genome ofLilium speciosum. Mol Gen Genet 237:97–104

    Article  PubMed  Google Scholar 

  • Levin HL, Weaver DC, Boeke JD (1990) Two related families of retrotransposons fromSchizosaccharomyces pombe. Mol Cell Biol 10:6791–6798

    PubMed  Google Scholar 

  • Matton DP, Mau S-L, Okamoto S, Clarke AE, Newbigin E (1995) The S-locus ofNicotiana alata: genomic organization and sequence analysis of two S-RNase alleles. Plant Mol Biol 28:847–858

    Article  PubMed  Google Scholar 

  • McClure BA, Gray JE, Anderson M, Clarke AE (1990) Self-incompatibility inNicotiana alata involves degradation of pollen rRNA. Nature 347:757–760

    Article  Google Scholar 

  • McClure MA, Johnson MS, Feng D-F, Doolittle RF (1988) Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci USA 85:2469–2473

    PubMed  Google Scholar 

  • McHale MT, Roberts IN, Noble SM, Beaumont Ch, Whitehead MP, Seth D, Oliver RP (1992) Cft-I: an LTR-retrotransposon inCladosporium fulvum, a fungal pathogen of tomato. Mol Gen Genet 233:337–347

    PubMed  Google Scholar 

  • Narayan RKJ (1987) Nuclear DNA changes, genome differentiation, and evolution inNicotiana (Solanaceae). Pl Syst Evol 157:161–180

    Article  Google Scholar 

  • Nielsen KK, Bojsen K, Collinge DB, Mikkelsen JD (1994) Induced resistance in sugar beet againstCercospora beticola: induction by dichloroisonicotinic acid is independent of chitinase and β-1,3-glucanase transcript accumulation. Physiol Mol Plant Pathol 45:849–899

    Article  Google Scholar 

  • O'Neill SD, Nadeau JA, Zhang XS, Bui AQ, Halevy AH (1993) Interorgan regulation of ethylene biosynthetic genes by pollination. Plant Cell 5:419–432

    Article  PubMed  Google Scholar 

  • Pouteau S, Huttner E, Grandbastien M-A, Caboche M (1991) Specific expression of the tobaccoTntl retrotransposon in protoplasts. EMBO J 10:1911–1918

    PubMed  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barely: Mendelian inheritance chromosomal location and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sentry JW, Smyth DR (1989) An element with long terminal repeats and its variant arrangements in the genome ofLilium henryi. Mol Gen Genet 215:349–354

    Article  PubMed  Google Scholar 

  • Singh A, Evensen KB, Kao T-h (1992) Ethylene synthesis and floral senescence following compatible and incompatible pollinations inPetunia inflata. Plant Physiol 99:38–45

    Google Scholar 

  • Skalka AM (1993) Retroviral DNA integration: lessons for transposon shuffling. Gene 135:175–182

    Article  PubMed  Google Scholar 

  • Smyth DR (1993) Plant retrotransposons. In: Verma DPS (ed) Control of Plant Gene Expression. CRC Press, Boca Raton, pp 1–15

    Google Scholar 

  • Smyth DR, Kalitsis P, Joseph JL, Sentry JW (1989) Plant retrotransposon fromLilium henryi is related toTy3 of yeast and thegypsy group ofDrosophila. Proc Natl Acad Sci USA 86:5015–5019

    PubMed  Google Scholar 

  • Turcich MP, Mascarenhas JP (1994) PREM-1, a putative maize retroelement has LTR (long terminal repeat) sequences that are preferentially transcribed in pollen. Sex Plant Reprod 7:2–11

    Google Scholar 

  • Voytas DF, Ausubel FM (1988) A copia-like transposable element family inArabidopsis thaliana. Nature 336:242–244

    PubMed  Google Scholar 

  • Voytas DF, Cummings MP, Konieczny A, Ausubel F, Rodermel SD (1992)copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89:7124–7128

    PubMed  Google Scholar 

  • Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retrotransposons: genes, pseudogenes and transposable elements generated by the reverse flow of information. Annu Rev Biochem 55:631–661

    Article  PubMed  Google Scholar 

  • Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by H. Saedler

Rights and permissions

Reprints and permissions

About this article

Cite this article

Royo, J., Nass, N., Matton, D.P. et al. A retrotransposon-like sequence linked to the S-locus ofNicotiana alata is expressed in styles in response to touch. Molec. Gen. Genet. 250, 180–188 (1996). https://doi.org/10.1007/BF02174177

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02174177

Key words

Navigation