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The expression profile of Arabidopsis thaliana β-1,3-glucanase promoter in tobacco

  • Genomics. Transcriptomics
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Abstract

Well characterized promoters with specific activity only during male gametophyte development of transgenic organism are widely utilized in strategies aimed at the elimination of unwanted transgene escape from the transgenic to the non-transgenic plant population. Since the specificity and timing of the applied promoter in the original and transgenic organism don’t have to be consistent, here we have tested by promoter-GUS fusion analysis the APRS promoter isolated from Arabidopsis thaliana in transgenic tobacco plants. Unlike of A. thaliana transcriptomic microarray data that identified gene expression from this promoter in late stages of pollen development, in tobacco plants the APRS promoter was active in the developing microspores during a short period of time before the microspores are released from the tetrads. Despite these discrepancies, the APRS promoter remains strictly pollen specific in tobacco plants. However, verification of its specificity in other important crops should precede the use of the APRS promoter in the engineered male sterility or in production of transgene-free pollen via site-specific recombination systems.

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References

  1. Moon H.S., Li Y., Stewart C.N. 2010. Keeping the genie in the bottle: Transgene biocontainment by excision in pollen. Trends Biotechnol. 28, 3–8.

    Article  CAS  PubMed  Google Scholar 

  2. Mariani C., Debeuckeleer M., Truettner J., Leemans J., Goldberg R.B. 1990. Induction of male sterility in plants by a chimeric ribonuclease gene. Nature. 347, 737–741.

    Article  CAS  Google Scholar 

  3. Mlynarova L., Conner A.J., Nap J.P. 2006. Directed microspore-specific recombination of transgenic alleles to prevent pollen-mediated transmission of transgenes. Plant Biotechnol. J. 4, 445–452.

    Article  CAS  PubMed  Google Scholar 

  4. Custers J.B.M., Oldenhof M.T., Schrauwen J.A.M., Cordewener J.H.G., Wullems G.J., Campagne M.M.V. 1997. Analysis of microspore-specific promoters in transgenic tobacco. Plant Mol. Biol. 35, 689–699.

    Article  CAS  PubMed  Google Scholar 

  5. Koltunow A.M., Truettner J., Cox K.H., Wallroth M., Goldberg R.B. 1990. Different temporal and spatial gene expression patterns occur during anther development. Plant Cell. 2, 1201–1224.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Twell D., Yamaguchi J., Mc Cormick S. 1990. Pollenspecific gene-expression in transgenic plants—coordinate regulation of 2 different tomato gene promoters during microsporogenesis. Development. 109, 705–713.

    CAS  PubMed  Google Scholar 

  7. Twell D., Yamaguchi J., Wing R.A., Ushiba J., Mc Cormick S. 1991. Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Gen. Dev. 5, 496–507.

    Article  CAS  Google Scholar 

  8. Hamilton D.A., Schwarz Y.H., Mascarenhas J.P. 1998. A monocot pollen-specific promoter contains separable pollen-specific and quantitative elements. Plant Mol. Biol. 38, 663–669.

    Article  CAS  PubMed  Google Scholar 

  9. Weterings K., Schrauwen J., Wullems G., Twell D. 1995. Functional dissection of the promoter of the pollen-specific gene NPT303 reveals a novel pollen-specific, and conserved cis-regulatory element. Plant J. 8, 55–63.

    Article  CAS  PubMed  Google Scholar 

  10. Gupta R., Ting J.T.L., Sokolov L.N., Johnson S.A., Luan S. 2002. A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell. 14, 2495–2507.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Truernit E., Stadler R., Baier K., Sauer N. 1999. A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J. 17, 191–201.

    Article  CAS  PubMed  Google Scholar 

  12. Li Y.B., Suen D.F., Huang C.Y., Kung S.Y., Huang A.H.C. 2012. The maize tapetum employs diverse mechanisms to synthesize and store proteins and flavonoids and transfer them to the pollen surface. Plant Physiol. 158, 1548–1561.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Bucciaglia P.A., Smith A.G. 1994. Cloning and characterization of Tag1, a tobacco anther beta-1,3-glucanase expressed during tetrad dissolution. Plant Mol. Biol. 24, 903–914.

    Article  CAS  PubMed  Google Scholar 

  14. Rhee S.Y., Somerville C.R. 1998. Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J. 15, 79–88.

    Article  CAS  PubMed  Google Scholar 

  15. Jakobsen M.K., Poulsen L.R., Schulz A., Fleurat Lessard P., Moller A., Husted S., Schiott M., Amtmann A., Palmgren M.G. 2005. Pollen development and fertilization in Arabidopsis is dependent on the male gametogenesis impaired anthers gene encoding a type VP-type ATPase. Gen. Dev. 19, 2757–2769.

    Article  CAS  Google Scholar 

  16. Bucciaglia P.A., Zimmermann E., Smith A.G. 2003. Functional analysis of a beta-1,3-glucanase gene (Tag1) with anther-specific RNA and protein accumulation using antisense RNA inhibition. J. Plant Physiol. 160, 1367–1373.

    Article  CAS  PubMed  Google Scholar 

  17. Zimmermann P., Hirsch-Hoffmann M., Hennig L., Gruissem W. 2004. Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621–2632.

    Article  CAS  PubMed  Google Scholar 

  18. Doxey A.C., Yaish M.W.F., Moffatt B.A., Griffith M., Mc Conkey B.J. 2007. Functional divergence in the Arabidopsis beta-1,3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol. Biol. Evol. 24, 1045–1055.

    Article  CAS  PubMed  Google Scholar 

  19. Hird D.L., Worrall D., Hodge R., Smartt S., Paul W., Scott R. 1993. The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6 gene displays similarity to beta-1,3-glucanases. Plant J. 4, 1023–1033.

    Article  CAS  PubMed  Google Scholar 

  20. Pirselova B., Matusikova I. 2013. Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiol. Plant. 35, 635–644.

    Article  CAS  Google Scholar 

  21. Balasubramanian V., Vashisht D., Cletus J., Sakthivel N. 2012. Plant beta-1,3-glucanases: Their biological functions and transgenic expression against phytopathogenic fungi. Biotechnol. Lett. 34, 1983–1990.

    Article  CAS  PubMed  Google Scholar 

  22. Delp G., Palva E.T. 1999. A novel flower-specific Arabidopsis gene related to both pathogen-induced and developmentally regulated plant beta-1,3-glucanase genes. Plant Mol. Biol. 39, 565–575.

    Article  CAS  PubMed  Google Scholar 

  23. Roberts C.S., Rajagopal S., Smith L.A., Nguyen T.A., Yang W., Nugroho S., Ravi K.S., Vijayachandra K., Harcourt K.L., Dransfield L., Desamero N., Hajdukiewicz P., Svab Z., Maliga P., Mayer J.E., Keese P., Kilian K., Jefferson R.A. 2002. A comprehensive set of modular vectors for advanced manipulations and efficient transformation of plants by both Agrobacterium and direct DNA uptake methods. CAMBIA, Canberra, Australia. http://www.cambia.org.

    Google Scholar 

  24. Jopcik M., Bauer M., Moravcikova J., Boszoradova E., Matusikova I., Libantova J. 2013. Plant tissue-specific promoters can drive gene expression in Escherichia coli. Plant Cell Tiss. Organ. 113, 387–396.

    Article  CAS  Google Scholar 

  25. Jopcik M., Moravcikova J., Matusikova I., Libantova J. 2014. Spacer length-dependent protection of specific activity of pollen and/or embryo promoters from influence of CaMV 35S promoter/enhancer in transgenic plants. Plant Cell Tiss. Organ. doi 10.1007/s11240-0140503-7

    Google Scholar 

  26. Höfgen R., Willmitzer L. 1988. Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 16, 9877–9877.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Horsch R.B., Fry J.E., Hoffmann N.L., Eichholtz D., Rogers S.G., Fraley R.T. 1985. A simple and general method for transferring genes into plants. Science. 227, 1229–1231.

    Article  CAS  Google Scholar 

  28. Jefferson R.A., Kavanagh T.A., Bevan M.W. 1987. Gus fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907.

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Brewbaker J.L., Kwack B.H. 1963. The essential role of calcium ion in pollen germination and pollen tube growth. J. Exp. Bot. 50, 859–865.

    Article  CAS  Google Scholar 

  30. Honys D., Twell D. 2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5 (11), R85.

    Article  PubMed Central  PubMed  Google Scholar 

  31. Qin Y., Leydon A.R., Manziello A., Pandey R., Mount D., Denic S., Vasic B., Johnson M.A., Palanivelu R. 2009. Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLOS Genet. 5, (8) e1000621.

    Article  PubMed Central  PubMed  Google Scholar 

  32. Wilson Z.A., Zhang D.B. 2009. From Arabidopsis to rice: Pathways in pollen development. J. Exp. Bot. 60, 1479–1492.

    Article  CAS  PubMed  Google Scholar 

  33. Futamura N., Mori H., Kouchi H., Shinohara, K. 2000. Male flower-specific expression of genes for polygalacturonase, pectin methylesterase and beta-1,3glucanase in a dioecious willow (Salix gilgiana Seemen). Plant Cell Physiol. 41, 16–26.

    Article  CAS  PubMed  Google Scholar 

  34. Higo K., Ugawa Y., Iwamoto M., Korenaga T. 1999. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27, 297–300.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Bate N., Twell D. 1998. Functional architecture of a late pollen promoter: Pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol. Biol. 37, 859–869.

    Article  CAS  PubMed  Google Scholar 

  36. Filichkin S.A., Leonard J.M., Monteros A., Liu P.P., Nonogaki H. 2004. A novel endo-beta-mannanase associated with anther and gene in tomato LeMAN5 is pollen development. Plant Physiol. 134, 1080–1087.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. David-Schwartz R., Weintraub L., Vidavski R., Zemach H., Murakhovsky L., Swartzberg D., Granot D. 2013. The SlFRK4 promoter is active only during late stages of pollen and anther development. Plant Sci. 199, 61–70.

    Article  PubMed  Google Scholar 

  38. Rogers H.J., Bate N., Combe J., Sullivan J., Sweetman J., Swan C., Lonsdale D.M., Twell D. 2001. Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol. Biol. 45, 577–585.

    Article  CAS  PubMed  Google Scholar 

  39. Zhou P., Yang F., Yu J.J., Ao G.M., Zhao Q. 2010. Several cis-elements including a palindrome involved in pollen-specific activity of SBgLR promoter. Plant Cell Rep. 29, 503–511.

    Article  CAS  PubMed  Google Scholar 

  40. Honys D., Oh S.A., Renak D., Donders M., Solcova B., Johnson J.A., Boudova R., Twell D. 2006. Identification of microspore-active promoters that allow targeted manipulation of gene expression at early stages of microgametogenesis in Arabidopsis. BMC Plant Biol. 6, 31.

    Article  PubMed Central  PubMed  Google Scholar 

  41. Xie X.J., Huang J.J., Gao H.H., Guo G.Q. 2011. Expression patterns of two Arabidopsis endo-beta-1,4glucanase genes (At3g43860, At4g39000) in reproductive development. Mol. Biol. (Moscow). 45, 458–465.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Plant Genetics and Biotechnology, Slovak Academy of Sciences, Akademicka 2, P.O. Box 39A, 950 07, Nitra, Slovak Republic

    M. Jopcik, I. Matusikova, J. Moravcikova, D. Durechova & J. Libantova

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  1. M. Jopcik
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  2. I. Matusikova
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  3. J. Moravcikova
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  4. D. Durechova
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  5. J. Libantova
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Correspondence to J. Libantova.

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The article is published in the original.

Published in Russian in Molekulyarnaya Biologiya, 2015, Vol. 49, No. 4, pp. 610–616.

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Jopcik, M., Matusikova, I., Moravcikova, J. et al. The expression profile of Arabidopsis thaliana β-1,3-glucanase promoter in tobacco. Mol Biol 49, 543–549 (2015). https://doi.org/10.1134/S0026893315040068

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  • DOI: https://doi.org/10.1134/S0026893315040068

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