Skip to main content
SpringerLink
Log in

Interspecies compatibility of the anther specific cell wall invertase promoters from Arabidopsis and tobacco for generating male sterile plants

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Histochemical GUS-staining and fluorometric analyses revealed strong tissue specific activities of the cell wall invertase promoters Nin88 from Nicotiana tabacum and AtcwINV2 from Arabidopsis thaliana that are restricted tightly to anthers and pollen, respectively. Both in A. thaliana and N. tabacum repression of invertase activity by anther specific RNA-interference turned out to be an efficient method to circumvent carbohydrate supply of the symplastically isolated pollen with subsequent strong decrease of pollen germination ability and seed setting. In the case of tobacco, comparable results were also obtained by expressing a proteinaceous invertase inhibitor, whereas this approach was less efficient in Arabidopis. The present study revealed that anther specific interference with invertase-activity in order to generate male sterile plants can be applied to members of the two different plant families Solanaceae (N. tabacum) and Brassicaceae (A. thalaina) and the strategy seems to be a general tool for practical application in hybrid breeding or as biological safety precautions. To elucidate the compatibility of the isolated promoters beyond plant families, we transferred the regulatory sequences into the respectively heterologous systems, i.e. the Nin88 promoter into Arabidopsis and the AtcwINV2 promoter into tobacco. The specificities of both promoters are maintained in the heterologous backgrounds, but their activities are strongly reduced as GUS-stainings of flowers and pollen revealed and fluorometrical quantification confirmed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bannerot H, Boulidard L, Chupeau Y (1977) Unexpected difficulties met with radish cytoplasm in Brassica oleracea. Eucarp Cruc Newsl 2:16

    Google Scholar 

  • Bäumlein H, Boerjan W, Nagy I, Bassüner R, van Montagu M, Inzé D, Wobus U (1991) A novfel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Mol Gen Genet 225:459–467

    PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Brewbaker JL (1964) Agricultural genetics. Englewood Cliffs, Prentice-Hall

    Google Scholar 

  • Clément C, Burrus M, Audran JC (1996) Floral organ growth and carbohydrate content during pollen development in Lilium. Am J Bot 83:459–469

    Article  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Delourme R, Foisset N, Horvais R, Barret P, Champagne G, Cheung WY, Landry BS, Renard M (1998) Characterisation of the radish introgression carrying the Rfo restorer gene for the Ogu-INRA cytoplasmic male sterility in rapeseed (Brassica napus L.). Theor Appl Genet 97:129–134

    Article  CAS  Google Scholar 

  • Dickson MH (1970) A temperature sensitive male sterile gene in Broccoli, Brassica oleracea L var. italica. J Am Soc Hortic Sci 95:13–14

    Google Scholar 

  • Dong NV, Subudhi PK, Luong PN, Quang VD, Quy TD, Zheng HG, Wang B, Nguyen HT (2000) Molecular mapping of a rice gene conditioning thermosensitive genic male sterility using AFLP, RFLP and SSR techniques. Theor Appl Genet 100:727–734

    Article  CAS  Google Scholar 

  • Dorion S, Lalonde S, Saini HS (1996) Induction of male sterility in wheat by meiotic-stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111:137–145

    PubMed  CAS  Google Scholar 

  • Engelke T, Terefe D, Tatlioglu T (2003) A PCR-based markersystem monitoring CMS-(S), CMS-(T) and (N)-cytoplasm in the onion (Allium cepa L.). Theor Appl Genet 107:162–167

    PubMed  CAS  Google Scholar 

  • Engelke T, Gera G, Tatlioglu T (2004a) Determination of the frequencies of restorer- and maintainer- alleles involved in CMS1 and CMS2 in German chive varieties. Plant Breed 123:51–59

    Article  CAS  Google Scholar 

  • Engelke T, Agbicodo E, Tatlioglu T (2004b) Mitochondrial genome variation in Allium ampeloprasum and its wild relatives. Euphytica 137:181–191

    Article  CAS  Google Scholar 

  • Feistritzer WR, Kelly AF (1987) Hybrid seed production of selected cereal oil and vegetable crops. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Gallusci P, Salamini F, Thompson RD (1994) Differences in cell type-specific expression of the gene Opaque 2 in maize and transgenic tobacco. Mol Gen Genet 244:391–400

    Article  PubMed  CAS  Google Scholar 

  • Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115:273–282

    Article  PubMed  CAS  Google Scholar 

  • Goetz M, Godt DE, Guivarc’h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98:6522–6527

    Article  PubMed  CAS  Google Scholar 

  • Greiner S, Krausgrill S, Rausch T (1998) Cloning of a tobacco apoplasmic invertase inhibitor. Plant Physiol 116:733–742

    Article  PubMed  CAS  Google Scholar 

  • Hamilton DA, Roy M, Rueda J, Sindhu RK, Sandford J, Mascarenhas JP (1992) Dissection of a pollen-specific promoter from maize by transient transformation assays. Plant Mol Biol 18:211–218

    Article  PubMed  CAS  Google Scholar 

  • He YQ, Yang J, Xu CG, Zhang ZG, Zhang Q (1999) Genetic bases of instability of male sterility and fertility reversibility in photoperiod-sensitive genic male-sterile rice. Theor Appl Genet 99:683–693

    Article  CAS  Google Scholar 

  • Henikoff S (1990) Position-effect variegation after 60 years. Trends Genet 6:422–426

    Article  PubMed  CAS  Google Scholar 

  • Horsch RB, Fry JB, Hoffmann NL, Wallroth M, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  • Hülskamp M, Kopczak S, Horejsi TF, Kihl BK, Pruitt RE (1995) Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J 8:703–714

    Article  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Latha R, Thiyagarajan K, Senthilvel S (2004) Genetics, fertility behaviour and molecular marker analysis of a new TGMS line, TS6, in rice. Plant Breed 123:235–240

    Article  CAS  Google Scholar 

  • Link M, Rausch T, Greiner S (2004) In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specifities and expression profiles. FEBS Lett 573:105–109

    Article  PubMed  CAS  Google Scholar 

  • Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McComble R, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    Article  PubMed  CAS  Google Scholar 

  • Maddison AL, Hedley PE, Meyer RC, Aziz N, Davidson D, Machray GC (1999) Expression of tandem invertase genes associated with sexual and vegetative growth cycles in potato. Plant Mol Biol 41:741–751

    Article  PubMed  CAS  Google Scholar 

  • Menczel L, Morgan A, Brown S, Maliga P (1987) Fusion-mediated combination of Ogura-type cytoplasmic male sterility with Brassica napus plastids using X-irradiated CMS protoplasts. Plant Cell Rep 6:98–101

    Google Scholar 

  • Pacini E, Franchi GG (1991) Diversification and evolution of the tapetum. In microspores: evolution and ontogeny. Academic Press, San Diego

    Google Scholar 

  • Pauls PK, Kunert K, Huttner E, Grandbastien MA (1994) Expression of the tobacco Tnt1 retrotransposon promoter in heterologous species. Plant Mol Biol 26:393–402

    Article  PubMed  CAS  Google Scholar 

  • Peach C, Velten J (1991) Transgene expression variability (position effect) of CAT and GUS reporter genes driven by linked divergent T-DNA promoters. Plant Mol Biol 17:49–60

    Article  PubMed  CAS  Google Scholar 

  • Rai M, Datta K, Parkhi V, Tan J, Oliva N, Chawla HS, Datta SK (2007) Variable T-DNA linkage configuration affects inheritance of carotenogenic transgenes and carotenoid accumulation in transgenic indica rice. Plant Cell Rep 26:1221–1231

    Article  PubMed  CAS  Google Scholar 

  • Ranwala AP, Miller WB (1998) Sucrose cleaving enzymes and carbohydrate pools in Lilium longiflorum floral organs. Physiol Plant 103:541–550

    Article  CAS  Google Scholar 

  • Roitsch T, Engelke T (2006) Cytoplasmic, genic and transgen induced male sterility. In Jaime A. Teixeira da Silva (edts.): floriculture, ornamental and plant biotechnology. Global Science Books, Ltd, London

    Google Scholar 

  • Ruiz ON, Daniell H (2005) Engineering cytoplasmic male sterility via the chloroplast genome by expression of β-ketothiolase. Plant Phys 138:1232–1246

    Article  CAS  Google Scholar 

  • Sato T, Thorsness MK, Kandasamy MK, Nishio T, Hirai M, Nasrallah JB, Nasrallah ME (1991) Activity of an S locus gene promoter in pistils and anthers of transgenic Brassica. Plant Cell 3:867–876

    Article  PubMed  CAS  Google Scholar 

  • Schubert D, Lechtenberg B, Forsbach A, Gills M, Bahadur S, Schmidt R (2004) Silencing in Arabidopsis T-DNA transformants: the predominant role of a gene-specific RNA sensing mechanism versus position effects. Plant Cell 16:2561–2572

    Article  PubMed  CAS  Google Scholar 

  • Shivanna KR, Sawhney VK (1995) Polyethylene glycol improves the in vitro growth of Brassica pollen tubes without loss in germination. J Exp Bot 46:1771–1774

    Article  CAS  Google Scholar 

  • Springer NM, Napoli CA, Selinger DA, Pandey R, Cone KC, Chandler VL, Kaeppler HF, Kaeppler SM (2003) Comparative analysis of SET domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132:907–925

    Article  PubMed  CAS  Google Scholar 

  • Stålberg K, Ellerström M, Sjödahl S, Ezcurra I, Wycliffe P, Rask L (1998) Heterologous and homologous trangenic expression directed by a 2S seed storage promoter of Brassica napus. Transgenic Res 7:165–172

    Article  Google Scholar 

  • Subudhi K, Borkakati RP, Virmani SS, Huang N (1997) Molecular mapping of a thermosensitive genetic male sterility gene in rice using bulked segregant analysis. Genome 40:188–194

    Article  PubMed  CAS  Google Scholar 

  • Takaiwa F, Oono K, Kato A (1991) Analysis of the 5′ flanking region responsible for the endosperm-specific expression of a rice glutelin chimeric gene in transgenic tobacco. Plant Mol Biol 16:49–58

    Article  PubMed  CAS  Google Scholar 

  • Tsuchiya T, Toriyama K, Ejiri SI, Hinata K (1994) Molecular characterization of rice genes specifically expressed in the anther tapetum. Plant Mol Biol 26:1737–1746

    Article  PubMed  CAS  Google Scholar 

  • Weil M, Krausgrill S, Schuster A, Rausch T (1994) A 17-kDa Nicotiana tabacum cell-wall peptide acts as an in-vitro inhibitor of the cell-wall isoforms of acid invertase. Planta 193:438–445

    PubMed  CAS  Google Scholar 

  • Weising K, Schell J, Kahl G (1988) Foreign genes in plants: transfer, structure, expression, and applications. Ann Rev Genet 22:421–477

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Davies SP, Kwan BYH, O’Brien AP, Singh M, Knox RB (1993) Haploid and diploid expression of a Brassica campestris anther-specific gene promoter in Arabidopsis and tobacco. Mol Gen Genet 239:58–65

    PubMed  CAS  Google Scholar 

  • Yamada S, Nelson DE, Ley E, Marquez S, Bohnert HJ (1997) The expression of an aquaporin promoter from Mesembryanthemum crystallinum in tobacco. Plant Cell Physiol 38:1326–1332

    PubMed  CAS  Google Scholar 

  • Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using Genevestigator. TIPS 10:407–409

    CAS  Google Scholar 

Download references

Acknowledgments

The skillful technical assistance of Christine Hampp, Jenifer Rech, Doris Waffler and Lisa Schneider and financial support by the Bundesministerium für Bildung und Forschung, Bayerisches Staatsministerium für Umwelt, Gesundheit und Verbraucherschutz and DFG-Graduiertenkolleg-1342 is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Lehrstuhl für Pharmazeutische Biologie, Julius von Sachs Institut, Universität Würzburg, Julius von Sachs Platz 2, 97082, Würzburg, Germany

    J. Hirsche, T. Engelke, D. Völler, M. Götz & T. Roitsch

Authors
  1. J. Hirsche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Engelke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Völler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Götz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Roitsch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Engelke.

Additional information

Communicated by Y. Xue.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hirsche, J., Engelke, T., Völler, D. et al. Interspecies compatibility of the anther specific cell wall invertase promoters from Arabidopsis and tobacco for generating male sterile plants. Theor Appl Genet 118, 235–245 (2009). https://doi.org/10.1007/s00122-008-0892-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-008-0892-2

Keywords

Search

Navigation