Skip to main content
SpringerLink
Log in

The transmitting tissue of Nicotiana tabacum is not essential to pollen tube growth, and its ablation can reverse prezygotic interspecific barriers

  • Original Article
  • Published:
Plant Reproduction Aims and scope Submit manuscript

Abstract

The Nicotiana tabacum transmitting tissue is a highly specialized file of metabolically active cells that is the pathway for pollen tubes from the stigma to the ovules where fertilization occurs. It is thought to be essential to pollen tube growth because of the nutrients and guidance it provides to the pollen tubes. It also regulates gametophytic self-incompatibility in the style. To test the function of the transmitting tissue in pollen tube growth and to determine its role in regulating prezygotic interspecific incompatibility, genetic ablation was used to eliminate the mature transmitting tissue, producing a hollow style. Despite the absence of the mature transmitting tissue and greatly reduced transmitting-tissue-specific gene expression, self-pollen tubes had growth to the end of the style. Pollen tubes grew at a slower rate in the transmitting-tissue-ablated line during the first 24 h post-pollination. However, pollen tubes grew to a similar length 40 h post-pollination with and without a transmitting tissue. Ablation of the N. tabacum transmitting tissue significantly altered interspecific pollen tube growth. These results implicate the N. tabacum transmitting tissue in facilitating or inhibiting interspecific pollen tube growth in a species-dependent manner and in controlling prezygotic reproductive barriers.

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

Similar content being viewed by others

References

  • Ascher PD (1976) Self incompatibility systems in floriculture crops. Acta Hortic 63:205–215

    Google Scholar 

  • Bedinger PA, Chetelat RT, McClure B, Moyle LC, Rose JKC, Stack SM, van der Knaap E, Baek YS, Lopez-Casado G, Covey PA, Kumar A, Li W, Nunez R, Cruz-Garcia F, Royer S (2011) Interspecific reproductive barriers in the tomato clade: opportunities to decipher mechanisms of reproductive isolation. Sex Plant Reprod 24:171–187

    Article  PubMed  Google Scholar 

  • Bell L, Hicks G (1976) Transmitting tissue in the pistil of tobacco: light and electron microscopic Observations. Planta 131:187–200

    Article  Google Scholar 

  • Bosch M, Derksen J, Mariani C (2003) A functional study of stylar hydroxyproline-rich glycoproteins during pollen tube growth. Sex Plant Reprod 16:87–98

    Article  CAS  Google Scholar 

  • Cheung AY, May B, Gu Q, Wu H-M (1993) Characterization of cDNAs for stylar transmitting tissue-specific proline-rich proteins in tobacco. Plant J 3:151–160

    Article  PubMed  CAS  Google Scholar 

  • Cheung AY, Wang H, Wu H-M (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393

    Article  PubMed  CAS  Google Scholar 

  • Cheung AY, Wu H-M, Di Stilio V, Glaven R, Chen C, Wong E, Ogdahl J, Estavillo A (2000) Pollen-pistil interactions in Nicotiana tabacum. Ann Bot 85:29–37

    Article  CAS  Google Scholar 

  • Covey P, Parsons RL, Ryan CA, Lay F, Anderson M, Pearce G, Bedinger PA (2010) PRALF, a peptide regulator of pollen tube growth in S. lycopersicum. Plant Physiol 153:703–715

    Article  PubMed  CAS  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Crawford BCW, Ditta G, Yanofsky MF (2007) The NTT gene is required for transmitting-tissue development in carpels of Arabidopsis thaliana. Curr Biol 17:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Cruz-Garcia F, Hancock CN, Kim D, McClure B (2005) Stylar glycoproteins bind to S-RNase in vitro. Plant J 42:295–304

    Article  PubMed  CAS  Google Scholar 

  • de Graaf BHJ, Derksen JWM, Mariani C (2001) Pollen and pistil in the progamic phase. Sex Plant Reprod 14:41–55

    Article  Google Scholar 

  • de Graaf BHJ, Knuiman BA, Derksen J, Mariani C (2003) Characterization and localization of the transmitting tissue-specific PELPIII proteins of Nicotiana tabacum. J Exp Biol 54:55–63

    CAS  Google Scholar 

  • de Graaf BHJ, Knuiman BA, Weerden GM, Feron R, Derksen J, Mariani C (2004) The PELPIII glycoproteins in Solanaceae: stylar expression and transfer into pollen tube walls. Sex Plant Reprod 16:245–252

    Article  CAS  Google Scholar 

  • de Nettancourt D (1977) Incompatibility in angiosperms. Springer, New York

    Book  Google Scholar 

  • de Nettancourt D (2010) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin

    Google Scholar 

  • Eberle CA, Clasen BM, Anderson NO, Smith AG (2012) A novel pollen tube growth assay utilizing a transmitting tract-ablated Nicotiana tabacum style. Sex Plant Reprod 25:27–37

    Article  PubMed  Google Scholar 

  • Eberle CA, Anderson NO, Clasen BM, Hegeman AD, Smith AG (2013) PELPIII: the Class III Pistil-Specific Extensin-Like Nicotiana tabacum proteins are essential for interspecific incompatibility. Plant J. doi:10.1111/tpj.12163

    PubMed  Google Scholar 

  • Gardner N, Felsheim R, Smith AG (2009) Production of male- and female-sterile plants through reproductive tissue ablation. J Plant Physiol 166:871–881

    Article  PubMed  CAS  Google Scholar 

  • Gasser CS, Robinson-Beers K (1993) Pistil development. Plant Cell 5:1231–1239

    PubMed  Google Scholar 

  • Goldberg RB (1988) Plants: novel developmental processes. Science 240:1460–1467

    Article  PubMed  CAS  Google Scholar 

  • Goldraij A, Katsuhiko K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805–810

    Article  PubMed  CAS  Google Scholar 

  • Golz JF, Clarke AE, Newbigin E, Anderson M (1998) A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. Plant J 16:591–599

    Article  PubMed  CAS  Google Scholar 

  • Hancock CN, Kondo K, Beecher B, McClure B (2003) The S-locus and unilateral incompatibility. Philos Trans R Soc B Biol 358:1133–1140

    Article  CAS  Google Scholar 

  • Hancock CN, Kent L, McClure B (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723

    Article  PubMed  CAS  Google Scholar 

  • Higashiyama T (2002) The synergid cell: attractor and acceptor of the pollen tube for double fertilization. J Plant Res 115:149–160

    Article  PubMed  Google Scholar 

  • Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S (2001) Pollen tube attraction by the synergid cell. Science 293:1480–1483

    Article  PubMed  CAS  Google Scholar 

  • Hogenboom NG (1984) Incongruity: non-function of intercellular and intracellular partner relationships through non-matching information. In: Linskens HF, Heslop-Harrison J, (eds) Encycl Plant Physiol 17:641–654

  • Iwano M, Takayama S (2012) Self/non-self discrimination in angiosperm self-incompatibility. Curr Opin Plant Biol 15:78–83

    Article  PubMed  Google Scholar 

  • Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73–82

    Article  Google Scholar 

  • Knox RB (1984) Pollen–pistil interactions. Encycl Plant Physiol 17:506–608

    Google Scholar 

  • Kroh M, Miki-Hirosige H, Rosen W, Loewus F (1970a) Distribution and utilization of label from myoinositol-U 14C and -2-3H by detached flowers and pistils of Lilium longiflorum. Plant Physiol 45:86–91

    Article  PubMed  CAS  Google Scholar 

  • Kroh M, Miki-Hirosige H, Rosen W, Loewus F (1970b) Incorporation of label into pollen tube walls from myoinositol-labeled Lilium longiflorum pistils. Plant Physiol 45:92–94

    Article  PubMed  CAS  Google Scholar 

  • Kuboyama T, Chung CS, Takeda G (1994) The diversity of interspecific pollen–pistil incongruity in Nicotiana. Sex Plant Reprod 7:250–258

    Article  Google Scholar 

  • Labarca C, Kroh M, Loewus F (1970) Composition of stigmatic exudate from Lilium longiflorum: labeling studies with Myo-inositol, d-Glucose, and l-Proline. Plant Physiol 46:150–156

    Article  PubMed  CAS  Google Scholar 

  • Lee CB, Page LE, McClure BA, Holtsford TP (2008) Post-pollination hybridization barriers in Nicotiana section Alatae. Sex Plant Reprod 21:183–195

    Article  Google Scholar 

  • Li W, Chetelat RT (2010) A pollen factor linking inter- and intraspecific pollen rejection in tomato. Science 330:1827–1830

    Article  PubMed  CAS  Google Scholar 

  • Lord EM (2003) Adhesion and guidance in compatible pollination. J Exp Bot 54:47–54

    Article  PubMed  CAS  Google Scholar 

  • Lord EM, Sanders LC (1992) Roles for the extracellular matrix in plant development and pollination: a special case of cell movement in plants. Dev Biol 153:16–28

    Article  PubMed  CAS  Google Scholar 

  • Lush WM, Spurck T, Joosten R (2000) Pollen tube guidance by the pistil of a Solanaceous plant. Ann Bot 85(Suppl A):39–47

    Google Scholar 

  • McClure BA, Cruz-Garcia F, Beecher BS, Sulaman W (2000) Factors affecting inter- and intra-specific pollen rejection in Nicotiana. Ann Bot 85:113–123

    Article  Google Scholar 

  • McClure BA, Cruz-García F, Romero C (2011) Compatibility and incompatibility in S-RNase-based systems. Ann Bot 108:647–658

    Article  PubMed  CAS  Google Scholar 

  • Murfett JM, Strabala TJ, Zurek DM, Mou B, Beecher B, McClure BA (1996) S-RNase and interspecific pollen rejection in the genus Nicotiana: multiple pollen rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8:943–958

    PubMed  CAS  Google Scholar 

  • Ori N, Sessa G, Lotan T, Himmelhoch S, Fluhr R (1990) A major stylar polypeptide (Sp41 is a member of the pathogenesis-related proteins superclass. EMBO J 9:3429–3436

    PubMed  CAS  Google Scholar 

  • Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59

    Article  PubMed  CAS  Google Scholar 

  • Pandey KK (1969) Elements of the S-gene complex V. Interspecific cross-compatibility relationships and theory of the evolution of the S complex. Genetica 40:447–474

    Article  Google Scholar 

  • Pandey KK (1979) The genus Nicotiana: evolution of incompatibility in flowering plants. In: Hawkes HG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Academic Press, London, pp 421–434

    Google Scholar 

  • Pandey KK (1981) Evolution of unilateral incompatibility in flowering plants: further evidence in favor of twin specificities controlling intra- and interspecific incompatibility. New Phytol 89:705–728

    Article  Google Scholar 

  • Quiapim AC, Brito MS, Bernardes LA, Dasilva I, Malavazi I, DePaoli HC, Molfetta-Machado JB, Giuliatti S, Goldman GH, Goldman MH (2009) Analysis of the Nicotiana tabacum stigma/style transcriptome reveals gene expression differences between wet and dry stigma species. Plant Physiol 149:1211–1230

    Article  PubMed  CAS  Google Scholar 

  • Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C (2004) Pistil factors controlling pollination. Plant Cell 16:S98–S106

    Article  PubMed  CAS  Google Scholar 

  • Sessa G, Fluhr R (1995) The expression of an abundant transmitting tract-specific endoglucanase (Sp41) is promoter-dependent and not essential for the reproductive physiology of tobacco. Plant Mol Biol 29:969–982

    Article  PubMed  CAS  Google Scholar 

  • Stephenson AG, Travers SE, Mena-Ali J, Winsor JA (2003) Pollen performance before and during the autotrophic-heterotrophic growth transition. Philos Trans R Soc B Biol 358:1009–1018

    Article  Google Scholar 

  • Tezuka T (2012) Hybrid lethality in the genus Nicotiana, Botany, Dr. John Mworia (ed) In Tech. ISBN: 978-953-51-0355-4. doi:10.5772/33544. Available from: http://www.intechopen.com/books/botany/hybrid-lethality-in-the-genus-nicotiana

  • Tung C, Dwyer KG, Nasrallah ME, Nasrallah JB (2005) Genome-wide identification of genes expressed in Arabidopsis pistils specifically along the path of pollen tube growth. Plant Physiol 138:977–989

    Article  PubMed  CAS  Google Scholar 

  • van Cauwenberghe OR, Makhmoudova A, McLean MD, Clark SM, Shelp BJ (2002) Plant pyruvate-dependent gamma-aminobutyrate transaminase: identification of an Arabidopsis cDNA and its expression in Escherichia coli. Can J Bot 80:933–941

    Article  Google Scholar 

  • Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen tube growth. Nature 392:818–821

    Article  PubMed  CAS  Google Scholar 

  • Wu H-M, Wang H, Cheung AY (1995) A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82:395–403

    Article  PubMed  CAS  Google Scholar 

  • Wu H-M, Wong E, Ogdahl J, Cheung AY (2000) A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco TTS protein. Plant J 22:165–176

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank B. McClure, Department of Biochemistry, University of Missouri, for generously supplying antibodies for TTS, PELPIII, and 120-kDa proteins. This material is based upon work supported by the National Science Foundation under Grant No. 0920114 and the Minnesota Agricultural Experiment Station.

Author information

Author notes

  1. Benjamin M. Clasen

    Present address: Cellectis Plant Sciences, 600 West County Road D, New Brighton, MN, 55112, USA

Authors and Affiliations

  1. Department of Horticultural Science, University of Minnesota, Saint Paul, MN, 55108, USA

    Alan G. Smith, Carrie A. Eberle, Nicole G. Moss, Neil O. Anderson & Adrian D. Hegeman

Authors
  1. Alan G. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carrie A. Eberle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicole G. Moss
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Neil O. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Benjamin M. Clasen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adrian D. Hegeman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alan G. Smith.

Additional information

Communicated by Teh-hui Kao.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, A.G., Eberle, C.A., Moss, N.G. et al. The transmitting tissue of Nicotiana tabacum is not essential to pollen tube growth, and its ablation can reverse prezygotic interspecific barriers. Plant Reprod 26, 339–350 (2013). https://doi.org/10.1007/s00497-013-0233-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-013-0233-8

Keywords

Search

Navigation