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Sexual Plant Reproduction

, Volume 16, Issue 5, pp 245–252 | Cite as

The PELPIII glycoproteins in Solanaceae: stylar expression and transfer into pollen tube walls

  • B. H. J. de Graaf
  • B. A. Knuiman
  • G. M. van der Weerden
  • R. Feron
  • J. DerksenEmail author
  • C. Mariani
Original Article

Abstract

The class III pistil-specific extensin-like proteins (PELPIII) of Nicotiana tabacum accumulate in the intercellular matrix (IM) of the style transmitting tissue (TT). After pollination, the 110–140 kDa PELPIII is translocated from the IM into the pollen tube walls. PELPIII-like sequences have been found in several solanaceous species. These sequences are expressed in mature non-pollinated styles at both RNA and protein level. Of the genus Nicotiana, the species N. alata, N. x sanderae and N. sylvestris (section Alatae), and N. tomentosiformis and N. otophora (section Tomentosae) showed an expression level of PELPIII homologues similar to that in mature styles of N. tabacum. PELPIII genes were absent in the most ancient species studied, namely N. trigonophylla (section Trigonophyllae). To study the species dependence of the translocation of PELPIII into the pollen tube wall in tobacco, interspecific pollinations on N. tabacum pistils were carried out with pollen from the incongruous species N. rustica, N. trigonophylla and Petunia hybrida, where PELPIII homologues are absent in the style. Immunocytological tests showed that the N. tabacum PELPIII is translocated into the pollen tube walls of all three species. Thus, the pollen tube walls of these species do not form a barrier for IM compounds such as the 110–140 kDa PELPIII and the absence of any possible effect of PELPIII on pollen tube growth cannot be due to failure of PELPIII transport through the wall. The importance of these findings is discussed with respect to the evolutionary origin of PELPIII, the pollen pistil interaction, the function of style TT-specific proteins and the physical properties of pollen tube walls.

Keywords

Transmitting tissue PELPIII Pollen tube Interspecific crosses Nicotiana tabacum 

References

  1. Bellartz S (1956) Das Pollenschlauchwachstum nach Arteigener und Artfremder Bestäubung einiger Solanaceen und die Inhaltstoffe ihres Pollens und ihrer Griffel. Planta 47:588–612Google Scholar
  2. Bosch M, Knudsen JS, Derksen J, Mariani C (2001) Class III pistil-specific extensin-like proteins from tobacco have characteristics of arabinogalactan proteins. Plant Physiol 125:2180–2188PubMedGoogle Scholar
  3. Bosch M, Derksen J, Mariani C (2003) A functional study of stylar HRGPs during pollen tube growth. Sex Plant Reprod 16:87–98CrossRefGoogle Scholar
  4. Chen C-G, Cornish EC, Clarke AE (1992) Specific expression of an extensin-like gene in the style of Nicotiana alata. Plant Cell 4:1053–1062CrossRefPubMedGoogle Scholar
  5. Cheung AY, Wu H-M (1999) Arabinogalactan proteins in plant sexual reproduction. Protoplasma 208:87–98Google Scholar
  6. Cheung AY, Wang H, Wu H-M (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393PubMedGoogle Scholar
  7. D’Arcy WG (1991) The Solanaceae since 1976, with a review of its biogeography. In: Hawkes JG, Lester RN, Nee M, Estrada N (eds) Solanaceae III: taxonomy, chemistry, evolution. The Royal Botanic Gardens Kew/Linnean Society of London, Richmond, pp 75–137Google Scholar
  8. Eldik GJ van, Wingens M, Ruiter RK, van Herpen MMA, Schrauwen JAM, Wullems GJ (1996) Molecular analysis of a pistil-specific gene expressed in the stigma and stylar cortex of Solanum tuberosum. Plant Mol Biol 30:171–176PubMedGoogle Scholar
  9. Frankis R, Mascarenhas JP (1980) Messenger RNA in the ungerminated pollen grain: a direct demonstration of its presence. Ann Bot 45:595–599Google Scholar
  10. Goldberg RB, Hoshek G, Tam SH, Ditta GS, Breidenbach RW (1981) Abundance, diversity and regulation of mRNA sequence sets in soybean embryogenesis. Dev Biol 83:201–217PubMedGoogle Scholar
  11. Goldman MH de S, Pezzotti M, Seurinck J, Mariani C (1992) Developmental expression of tobacco pistil-specific genes encoding novel extensin-like proteins. Plant Cell 4:1041–1051PubMedGoogle Scholar
  12. Goldman MH de S, Goldberg RB, Mariani C (1994) Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J 13:2976–2984PubMedGoogle Scholar
  13. Goodrum LJ, Patel A, Leykam JF, Kieliszewski MJ (2000) Gum arabic glycoprotein contains glycomodules of both extensin and arabinogalactan-glycoproteins. Phytochemistry 54:99–106CrossRefPubMedGoogle Scholar
  14. Goodspeed TH (1954) The genus Nicotiana: origins, relationships and evolution of its species in light of their distribution, morphology and cytogenetics. Chronica Botanica, Waltham, Mass.Google Scholar
  15. Graaf BHJ de, Derksen JWM, Mariani C (2001) Pollen and pistil in the progamic phase. Sex Plant Reprod 14:41–55CrossRefGoogle Scholar
  16. Graaf BHJ de, Knuiman BA, Derksen J, Mariani C (2003) Characterisation and localisation of the transmitting tissue-specific PELPIII proteins of Nicotiana tabacum. J Exp Bot 54:55–63CrossRefPubMedGoogle Scholar
  17. Harikrishna K, Jampates-Beale R, Milligan SB, Gasser CS (1996) An endochitinase expressed at high levels in the stylar transmitting tissue of tomatoes. Plant Mol Biol 30:899–911PubMedGoogle Scholar
  18. Hoggart RM, Clarke AE (1984) Porosity of Gladiolus stigmatic papillae and pollen tube walls. Ann Bot 53:271–277Google Scholar
  19. Hunziker AT (1979) South American Solanaceae: a synoptic survey. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Linnean Society Symposium series, no 7, Linnean Society of London, Academic Press, London, pp 49–86Google Scholar
  20. Kieliszewski MJ, Shpak E (2001) Synthetic genes for the elucidation of glycosylation codes for arabinogalactan-proteins and other hydroxyproline-rich glycoproteins. Cell Mol Life Sci 58:1386–1398PubMedGoogle Scholar
  21. Kuboyama T (1998) A novel thaumatin-like protein gene of tobacco is specifically expressed in the transmitting tissue of stigma and style. Sex Plant Reprod 11:251–256CrossRefGoogle Scholar
  22. Kuboyama T, Chung CS, Takeda G (1994) The diversity of interspecific pollen-pistil incongruity in Nicotiana. Sex Plant Reprod 7:250–258Google Scholar
  23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedGoogle Scholar
  24. Li YQ, Faleri C, Thompson RD, Tiezzi A, Eijlander R, Cresti M (1994) Cytochemical immunolocalization of the abundant pistil protein Sk2 in potato (Solanum tuberosum). Sex Plant Reprod 7:164–168Google Scholar
  25. Lind JL, Bacic A, Clarke AE, Anderson MA (1994) A style-specific hydroxyproline-rich glycoprotein with properties of both extensins and arabinogalactan proteins. Plant J 6:491–502CrossRefPubMedGoogle Scholar
  26. Lord EM (2000) Adhesion and cell movement during pollination: cherchez la femme. Trends Plant Sci 5:368–373CrossRefPubMedGoogle Scholar
  27. Lord EM, Russell SD (2002) The mechanisms of pollination and fertilisation in plants. Annu Rev Cell Dev Biol 18:81–105Google Scholar
  28. Narayan RKJ (1987) Nuclear DNA changes, genome differentiation and evolution in Nicotiana (Solanaceae). Plant Syst Evol 157:161–180Google Scholar
  29. O’Driscoll D, Hann C, Read SM, Steer MW (1993) Endocytotic uptake of fluorescent dextrans by pollen tubes grown in vitro. Protoplasma 175:126–130Google Scholar
  30. Pierson ES, de Graaf BHJ, Derksen J (1999) Immunofluorescence localization of glycoproteins using tissue printing: detection of pistil extensin-like proteins in tobacco. Biotechniques 26:450–453PubMedGoogle Scholar
  31. Schultz CJ, Hauser K, Lind JL, Atkinson AH, Pu ZY, Anderson MA, Clarke AE (1997) Molecular characterisation of a cDNA sequence encoding the backbone of a style-specific 120 kDa glycoprotein which has features of both extensins and arabinogalactan proteins. Plant Mol Biol 35:833–845CrossRefPubMedGoogle Scholar
  32. Sommer-Knudsen J, Clarke AE, Bacic A (1996) A galactose-rich, cell-wall glycoprotein from styles of Nicotiana alata. Plant J 9:71–83CrossRefPubMedGoogle Scholar
  33. Sommer-Knudsen J, Clarke AE, Bacic A (1997) Proline- and hydroxyproline-rich gene products in the sexual tissues of flowers. Sex Plant Reprod 10:253–260CrossRefGoogle Scholar
  34. 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 82:393–403Google Scholar
  35. 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 22:165–176CrossRefPubMedGoogle Scholar
  36. Wu H, de Graaf B, Mariani C, Cheung AY (2001) Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell Mol Life Sci. 58:1418–1429Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • B. H. J. de Graaf
    • 1
    • 3
  • B. A. Knuiman
    • 1
  • G. M. van der Weerden
    • 2
  • R. Feron
    • 1
  • J. Derksen
    • 1
    Email author
  • C. Mariani
    • 1
  1. 1.Department of Experimental Botany, Laboratory of Plant Cell Biology, Graduate School of Experimental Plant ScienceUniversity of Nijmegen NijmegenThe Netherlands
  2. 2.Botanical GardenUniversity of NijmegenNijmegenThe Netherlands
  3. 3.School of BiosciencesUniversity of BirminghamBirminghamUK

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