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. 1996 Apr 30;93(9):3853–3858. doi: 10.1073/pnas.93.9.3853

Organ-specific and Agamous-regulated expression and glycosylation of a pollen tube growth-promoting protein.

A Y Cheung 1, X Y Zhan 1, H Wang 1, H M Wu 1
PMCID: PMC39448  PMID: 8632979

Abstract

Transmitting tissue-specific (TTS) protein is a pollen tube growth-promoting and attracting glycoprotein located in the stylar transmitting tissue extracellular matrix of the pistil of tobacco. The TTS protein backbones have a deduced molecular mass of about 28 kDa, whereas the glycosylated stylar TTS proteins have apparent molecular masses ranging between 50 and 100 kDa. TTS mRNAs and proteins are ectopically produced in transgenic tobacco plants that express either a cauliflower mosaic virus (CaMV) 35S promoter-TTS2 transgene or a CaMV 35S-promoter-NAG1 (NAG1 = Nicotiana tabacum Agamous gene) transgene. However, the patterns of TTS mRNA and protein accumulation and the quality of the TTS proteins produced are different in these two types of transgenic plants. In 35S-TTS transgenic plants, TTS mRNAs and proteins accumulate constitutively in vegetative and floral tissues. However, the ectopically expressed TTS proteins in these transgenic plants accumulate as underglycosylated protein species with apparent molecular masses between 30 and 50 kDa. This indicates that the capacity to produce highly glycosylated TTS proteins is restricted to the stylar transmitting tissue. In 35S-NAG transgenic plants, NAG1 mRNAs accumulate constitutively in vegetative and floral tissues, and TTS mRNAs are induced in the sepals of these plants. Moreover, highly glycosylated TTS proteins in the 50- to 100-kDa molecular mass range accumulate in the sepals of these transgenic, 35S-NAG plants. These results show that the tobacco NAGI gene, together with other yet unidentified regulatory factors, control the expression of TTS genes and the cellular capacity to glycosylate TTS proteins, which are normally expressed very late in the pistil developmental pathway and function in the final stage of floral development. The sepals in the transgenic 35S-NAG plants also support efficient pollen germination and tube growth, similar to what normally occurs in the pistil, and this ability correlates with the accumulation of the highest levels of the 50- to 100-kDa glycosylated TTS proteins.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atkinson A. H., Heath R. L., Simpson R. J., Clarke A. E., Anderson M. A. Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell. 1993 Feb;5(2):203–213. doi: 10.1105/tpc.5.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bradley D., Carpenter R., Sommer H., Hartley N., Coen E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell. 1993 Jan 15;72(1):85–95. doi: 10.1016/0092-8674(93)90052-r. [DOI] [PubMed] [Google Scholar]
  3. Chen C. G., Cornish E. C., Clarke A. E. Specific expression of an extensin-like gene in the style of Nicotiana alata. Plant Cell. 1992 Sep;4(9):1053–1062. doi: 10.1105/tpc.4.9.1053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen C. G., Pu Z. Y., Moritz R. L., Simpson R. J., Bacic A., Clarke A. E., Mau S. L. Molecular cloning of a gene encoding an arabinogalactan-protein from pear (Pyrus communis) cell suspension culture. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10305–10309. doi: 10.1073/pnas.91.22.10305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheung A. Y., May B., Kawata E. E., Gu Q., Wu H. M. Characterization of cDNAs for stylar transmitting tissue-specific proline-rich proteins in tobacco. Plant J. 1993 Jan;3(1):151–160. [PubMed] [Google Scholar]
  6. Cheung A. Y. Pollen-pistil interactions in compatible pollination. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3077–3080. doi: 10.1073/pnas.92.8.3077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheung A. Y., Wang H., Wu H. M. A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell. 1995 Aug 11;82(3):383–393. doi: 10.1016/0092-8674(95)90427-1. [DOI] [PubMed] [Google Scholar]
  8. Chu F. K. Requirements of cleavage of high mannose oligosaccharides in glycoproteins by peptide N-glycosidase F. J Biol Chem. 1986 Jan 5;261(1):172–177. [PubMed] [Google Scholar]
  9. Coen E. S., Meyerowitz E. M. The war of the whorls: genetic interactions controlling flower development. Nature. 1991 Sep 5;353(6339):31–37. doi: 10.1038/353031a0. [DOI] [PubMed] [Google Scholar]
  10. Du H., Simpson R. J., Moritz R. L., Clarke A. E., Bacic A. Isolation of the protein backbone of an arabinogalactan-protein from the styles of Nicotiana alata and characterization of a corresponding cDNA. Plant Cell. 1994 Nov;6(11):1643–1653. doi: 10.1105/tpc.6.11.1643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldman M. H., Goldberg R. B., Mariani C. Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J. 1994 Jul 1;13(13):2976–2984. doi: 10.1002/j.1460-2075.1994.tb06596.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldman M. H., Pezzotti M., Seurinck J., Mariani C. Developmental expression of tobacco pistil-specific genes encoding novel extensin-like proteins. Plant Cell. 1992 Sep;4(9):1041–1051. doi: 10.1105/tpc.4.9.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kang H. G., Noh Y. S., Chung Y. Y., Costa M. A., An K., An G. Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol Biol. 1995 Oct;29(1):1–10. doi: 10.1007/BF00019114. [DOI] [PubMed] [Google Scholar]
  14. Kempin S. A., Mandel M. A., Yanofsky M. F. Conversion of perianth into reproductive organs by ectopic expression of the tobacco floral homeotic gene NAG1. Plant Physiol. 1993 Dec;103(4):1041–1046. doi: 10.1104/pp.103.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kieliszewski M. J., Lamport D. T. Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 1994 Feb;5(2):157–172. doi: 10.1046/j.1365-313x.1994.05020157.x. [DOI] [PubMed] [Google Scholar]
  16. Lind J. L., Bacic A., Clarke A. E., Anderson M. A. A style-specific hydroxyproline-rich glycoprotein with properties of both extensins and arabinogalactan proteins. Plant J. 1994 Oct;6(4):491–502. doi: 10.1046/j.1365-313x.1994.6040491.x. [DOI] [PubMed] [Google Scholar]
  17. Lolle S. J., Cheung A. Y. Promiscuous germination and growth of wildtype pollen from Arabidopsis and related species on the shoot of the Arabidopsis mutant, fiddlehead. Dev Biol. 1993 Jan;155(1):250–258. doi: 10.1006/dbio.1993.1022. [DOI] [PubMed] [Google Scholar]
  18. Lolle S. J., Cheung A. Y., Sussex I. M. Fiddlehead: an Arabidopsis mutant constitutively expressing an organ fusion program that involves interactions between epidermal cells. Dev Biol. 1992 Aug;152(2):383–392. doi: 10.1016/0012-1606(92)90145-7. [DOI] [PubMed] [Google Scholar]
  19. Lynch M. A., Staehelin L. A. Domain-specific and cell type-specific localization of two types of cell wall matrix polysaccharides in the clover root tip. J Cell Biol. 1992 Jul;118(2):467–479. doi: 10.1083/jcb.118.2.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mandel M. A., Bowman J. L., Kempin S. A., Ma H., Meyerowitz E. M., Yanofsky M. F. Manipulation of flower structure in transgenic tobacco. Cell. 1992 Oct 2;71(1):133–143. doi: 10.1016/0092-8674(92)90272-e. [DOI] [PubMed] [Google Scholar]
  21. Mau S. L., Chen C. G., Pu Z. Y., Moritz R. L., Simpson R. J., Bacic A., Clarke A. E. Molecular cloning of cDNAs encoding the protein backbones of arabinogalactan-proteins from the filtrate of suspension-cultured cells of Pyrus communis and Nicotiana alata. Plant J. 1995 Aug;8(2):269–281. doi: 10.1046/j.1365-313x.1995.08020269.x. [DOI] [PubMed] [Google Scholar]
  22. Meyerowitz E. M. Flower development and evolution: new answers and new questions. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5735–5737. doi: 10.1073/pnas.91.13.5735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mizukami Y., Ma H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell. 1992 Oct 2;71(1):119–131. doi: 10.1016/0092-8674(92)90271-d. [DOI] [PubMed] [Google Scholar]
  24. Mort A. J., Lamport D. T. Anhydrous hydrogen fluoride deglycosylates glycoproteins. Anal Biochem. 1977 Oct;82(2):289–309. doi: 10.1016/0003-2697(77)90165-8. [DOI] [PubMed] [Google Scholar]
  25. Ori N., Sessa G., Lotan T., Himmelhoch S., Fluhr R. A major stylar matrix polypeptide (sp41) is a member of the pathogenesis-related proteins superclass. EMBO J. 1990 Nov;9(11):3429–3436. doi: 10.1002/j.1460-2075.1990.tb07550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pennell R. I., Janniche L., Kjellbom P., Scofield G. N., Peart J. M., Roberts K. Developmental Regulation of a Plasma Membrane Arabinogalactan Protein Epitope in Oilseed Rape Flowers. Plant Cell. 1991 Dec;3(12):1317–1326. doi: 10.1105/tpc.3.12.1317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pnueli L., Hareven D., Rounsley S. D., Yanofsky M. F., Lifschitz E. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell. 1994 Feb;6(2):163–173. doi: 10.1105/tpc.6.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Roberts P. L., Martin F. M., Schoetz D. J., Jr, Murray J. J., Coller J. A., Veidenheimer M. C. Bleeding stomal varices. The role of local treatment. Dis Colon Rectum. 1990 Jul;33(7):547–549. doi: 10.1007/BF02052204. [DOI] [PubMed] [Google Scholar]
  29. Savidge B., Rounsley S. D., Yanofsky M. F. Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell. 1995 Jun;7(6):721–733. doi: 10.1105/tpc.7.6.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schmidt R. J., Veit B., Mandel M. A., Mena M., Hake S., Yanofsky M. F. Identification and molecular characterization of ZAG1, the maize homolog of the Arabidopsis floral homeotic gene AGAMOUS. Plant Cell. 1993 Jul;5(7):729–737. doi: 10.1105/tpc.5.7.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Showalter A. M. Structure and function of plant cell wall proteins. Plant Cell. 1993 Jan;5(1):9–23. doi: 10.1105/tpc.5.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Staehelin L. A., Giddings T. H., Jr, Kiss J. Z., Sack F. D. Macromolecular differentiation of Golgi stacks in root tips of Arabidopsis and Nicotiana seedlings as visualized in high pressure frozen and freeze-substituted samples. Protoplasma. 1990;157(1-3):75–91. doi: 10.1007/BF01322640. [DOI] [PubMed] [Google Scholar]
  33. Tarentino A. L., Gómez C. M., Plummer T. H., Jr Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry. 1985 Aug 13;24(17):4665–4671. doi: 10.1021/bi00338a028. [DOI] [PubMed] [Google Scholar]
  34. Tsuchimoto S., van der Krol A. R., Chua N. H. Ectopic expression of pMADS3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell. 1993 Aug;5(8):843–853. doi: 10.1105/tpc.5.8.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wang H., Wu H. M., Cheung A. Y. Development and Pollination Regulated Accumulation and Glycosylation of a Stylar Transmitting Tissue-Specific Proline-Rich Protein. Plant Cell. 1993 Nov;5(11):1639–1650. doi: 10.1105/tpc.5.11.1639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wu H. M., Wang H., Cheung A. Y. A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell. 1995 Aug 11;82(3):395–403. doi: 10.1016/0092-8674(95)90428-x. [DOI] [PubMed] [Google Scholar]
  37. Yanofsky M. F., Ma H., Bowman J. L., Drews G. N., Feldmann K. A., Meyerowitz E. M. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990 Jul 5;346(6279):35–39. doi: 10.1038/346035a0. [DOI] [PubMed] [Google Scholar]
  38. van Holst G. J., Varner J. E. Reinforced Polyproline II Conformation in a Hydroxyproline-Rich Cell Wall Glycoprotein from Carrot Root. Plant Physiol. 1984 Feb;74(2):247–251. doi: 10.1104/pp.74.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]

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