Abstract
We screened for pollen-specific kinase genes, which are potential signal transduction components of pollen-pistil interactions, and isolated two structurally related receptor-like kinases (RLKs) from tomato, LePRK1 and LePRK2. These kinases are similar to a pollen-expressed RLK from petunia, but they are expressed later during pollen development than is the petunia RLK. The abundance of LePRK2 increases when pollen germinates, but LePRK1 remains constant. Both LePRK1 and LePRK2 are localized to the plasma membrane/cell wall of growing pollen tubes. Both kinase domains have kinase activity when expressed in Escherichia coli. In phosphorylation assays with pollen membrane preparations, LePRK2, but not LePRK1, is phosphorylated, and the addition of tomato style, but not leaf, extracts to these membrane preparations results at least partially in specific dephosphorylation of LePRK2. Taken together, these results suggest that LePRK1 and LePRK2 play different roles in postpollination events and that at least LePRK2 may mediate some pistil response.
Full Text
The Full Text of this article is available as a PDF (276.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Braun D. M., Walker J. C. Plant transmembrane receptors: new pieces in the signaling puzzle. Trends Biochem Sci. 1996 Feb;21(2):70–73. [PubMed] [Google Scholar]
- Chang C., Schaller G. E., Patterson S. E., Kwok S. F., Meyerowitz E. M., Bleecker A. B. The TMK1 gene from Arabidopsis codes for a protein with structural and biochemical characteristics of a receptor protein kinase. Plant Cell. 1992 Oct;4(10):1263–1271. doi: 10.1105/tpc.4.10.1263. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark E. A., Brugge J. S. Integrins and signal transduction pathways: the road taken. Science. 1995 Apr 14;268(5208):233–239. doi: 10.1126/science.7716514. [DOI] [PubMed] [Google Scholar]
- Dixon M. S., Jones D. A., Keddie J. S., Thomas C. M., Harrison K., Jones J. D. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996 Feb 9;84(3):451–459. doi: 10.1016/s0092-8674(00)81290-8. [DOI] [PubMed] [Google Scholar]
- Dodds P. N., Clarke A. E., Newbigin E. A molecular perspective on pollination in flowering plants. Cell. 1996 Apr 19;85(2):141–144. doi: 10.1016/s0092-8674(00)81090-9. [DOI] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
- Goring D. R., Rothstein S. J. The S-locus receptor kinase gene in a self-incompatible Brassica napus line encodes a functional serine/threonine kinase. Plant Cell. 1992 Oct;4(10):1273–1281. doi: 10.1105/tpc.4.10.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman S. W., Banasiak D., Fairley C., McCormick S. A 610 kb YAC clone harbors 7 cM of tomato (Lycopersicon esculentum) DNA that includes the male sterile 14 gene and a hotspot for recombination. Mol Gen Genet. 1996 Apr 24;251(1):52–59. doi: 10.1007/BF02174344. [DOI] [PubMed] [Google Scholar]
- Hanks S. K., Hunter T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 1995 May;9(8):576–596. [PubMed] [Google Scholar]
- Hashimoto C., Hudson K. L., Anderson K. V. The Toll gene of Drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell. 1988 Jan 29;52(2):269–279. doi: 10.1016/0092-8674(88)90516-8. [DOI] [PubMed] [Google Scholar]
- Higgins D. G., Sharp P. M. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. doi: 10.1093/bioinformatics/5.2.151. [DOI] [PubMed] [Google Scholar]
- Hiscock S. J., Doughty J., Willis A. C., Dickinson H. G. A 7-kDa pollen coating-borne peptide from Brassica napus interacts with S-locus glycoprotein and S-locus-related glycoprotein. Planta. 1995;196(2):367–374. doi: 10.1007/BF00201397. [DOI] [PubMed] [Google Scholar]
- Jones D. A., Thomas C. M., Hammond-Kosack K. E., Balint-Kurti P. J., Jones J. D. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994 Nov 4;266(5186):789–793. doi: 10.1126/science.7973631. [DOI] [PubMed] [Google Scholar]
- Kao T. H., McCubbin A. G. How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12059–12065. doi: 10.1073/pnas.93.22.12059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kobe B., Deisenhofer J. The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci. 1994 Oct;19(10):415–421. doi: 10.1016/0968-0004(94)90090-6. [DOI] [PubMed] [Google Scholar]
- Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
- Lin Y., Wang Y., Zhu J. K., Yang Z. Localization of a Rho GTPase Implies a Role in Tip Growth and Movement of the Generative Cell in Pollen Tubes. Plant Cell. 1996 Feb;8(2):293–303. doi: 10.1105/tpc.8.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Logemann J., Schell J., Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. doi: 10.1016/0003-2697(87)90086-8. [DOI] [PubMed] [Google Scholar]
- Lopez J. A., Chung D. W., Fujikawa K., Hagen F. S., Papayannopoulou T., Roth G. J. Cloning of the alpha chain of human platelet glycoprotein Ib: a transmembrane protein with homology to leucine-rich alpha 2-glycoprotein. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5615–5619. doi: 10.1073/pnas.84.16.5615. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lord E. M., Sanders L. C. Roles for the extracellular matrix in plant development and pollination: a special case of cell movement in plants. Dev Biol. 1992 Sep;153(1):16–28. doi: 10.1016/0012-1606(92)90088-x. [DOI] [PubMed] [Google Scholar]
- Manly K. F. A Macintosh program for storage and analysis of experimental genetic mapping data. Mamm Genome. 1993;4(6):303–313. doi: 10.1007/BF00357089. [DOI] [PubMed] [Google Scholar]
- Morisato D., Anderson K. V. Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu Rev Genet. 1995;29:371–399. doi: 10.1146/annurev.ge.29.120195.002103. [DOI] [PubMed] [Google Scholar]
- Mu J. H., Lee H. S., Kao T. H. Characterization of a pollen-expressed receptor-like kinase gene of Petunia inflata and the activity of its encoded kinase. Plant Cell. 1994 May;6(5):709–721. doi: 10.1105/tpc.6.5.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muschietti J., Dircks L., Vancanneyt G., McCormick S. LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 1994 Sep;6(3):321–338. doi: 10.1046/j.1365-313x.1994.06030321.x. [DOI] [PubMed] [Google Scholar]
- Nick P., Lambert A. M., Vantard M. A microtubule-associated protein in maize is expressed during phytochrome-induced cell elongation. Plant J. 1995 Dec;8(6):835–844. doi: 10.1046/j.1365-313x.1995.8060835.x. [DOI] [PubMed] [Google Scholar]
- Pang Q., Hays J. B., Rajagopal I. A plant cDNA that partially complements Escherichia coli recA mutations predicts a polypeptide not strongly homologous to RecA proteins. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8073–8077. doi: 10.1073/pnas.89.17.8073. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierson E. S., Miller D. D., Callaham D. A., Shipley A. M., Rivers B. A., Cresti M., Hepler P. K. Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell. 1994 Dec;6(12):1815–1828. doi: 10.1105/tpc.6.12.1815. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pokalsky A. R., Hiatt W. R., Ridge N., Rasmussen R., Houck C. M., Shewmaker C. K. Structure and expression of elongation factor 1 alpha in tomato. Nucleic Acids Res. 1989 Jun 26;17(12):4661–4673. doi: 10.1093/nar/17.12.4661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rubinstein A. L., Broadwater A. H., Lowrey K. B., Bedinger P. A. Pex1, a pollen-specific gene with an extensin-like domain. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3086–3090. doi: 10.1073/pnas.92.8.3086. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rudd J. J., Franklin FCH., Lord J. M., Franklin-Tong V. E. Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas. Plant Cell. 1996 Apr;8(4):713–724. doi: 10.1105/tpc.8.4.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaller M. D., Parsons J. T. Focal adhesion kinase and associated proteins. Curr Opin Cell Biol. 1994 Oct;6(5):705–710. doi: 10.1016/0955-0674(94)90097-3. [DOI] [PubMed] [Google Scholar]
- Schweitzer R., Howes R., Smith R., Shilo B. Z., Freeman M. Inhibition of Drosophila EGF receptor activation by the secreted protein Argos. Nature. 1995 Aug 24;376(6542):699–702. doi: 10.1038/376699a0. [DOI] [PubMed] [Google Scholar]
- Song W. Y., Wang G. L., Chen L. L., Kim H. S., Pi L. Y., Holsten T., Gardner J., Wang B., Zhai W. X., Zhu L. H. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995 Dec 15;270(5243):1804–1806. doi: 10.1126/science.270.5243.1804. [DOI] [PubMed] [Google Scholar]
- Stein J. C., Howlett B., Boyes D. C., Nasrallah M. E., Nasrallah J. B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8816–8820. doi: 10.1073/pnas.88.19.8816. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stein J. C., Nasrallah J. B. A plant receptor-like gene, the S-locus receptor kinase of Brassica oleracea L., encodes a functional serine/threonine kinase. Plant Physiol. 1993 Mar;101(3):1103–1106. doi: 10.1104/pp.101.3.1103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stotz H. U., Contos J. J., Powell A. L., Bennett A. B., Labavitch J. M. Structure and expression of an inhibitor of fungal polygalacturonases from tomato. Plant Mol Biol. 1994 Jul;25(4):607–617. doi: 10.1007/BF00029600. [DOI] [PubMed] [Google Scholar]
- Tanksley S. D., Ganal M. W., Prince J. P., de Vicente M. C., Bonierbale M. W., Broun P., Fulton T. M., Giovannoni J. J., Grandillo S., Martin G. B. High density molecular linkage maps of the tomato and potato genomes. Genetics. 1992 Dec;132(4):1141–1160. doi: 10.1093/genetics/132.4.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Titani K., Takio K., Handa M., Ruggeri Z. M. Amino acid sequence of the von Willebrand factor-binding domain of platelet membrane glycoprotein Ib. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5610–5614. doi: 10.1073/pnas.84.16.5610. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Twell D., Yamaguchi J., McCormick S. Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development. 1990 Jul;109(3):705–713. doi: 10.1242/dev.109.3.705. [DOI] [PubMed] [Google Scholar]
- Valon C., Smalle J., Goodman H. M., Giraudat J. Characterization of an Arabidopsis thaliana gene (TMKL1) encoding a putative transmembrane protein with an unusual kinase-like domain. Plant Mol Biol. 1993 Oct;23(2):415–421. doi: 10.1007/BF00029017. [DOI] [PubMed] [Google Scholar]
- Walker J. C. Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J. 1993 Mar;3(3):451–456. doi: 10.1111/j.1365-313x.1993.tb00164.x. [DOI] [PubMed] [Google Scholar]
- Weinstein J. N., Blumenthal R., van Renswoude J., Kempf C., Klausner R. D. Charge clusters and the orientation of membrane proteins. J Membr Biol. 1982;66(3):203–212. doi: 10.1007/BF01868495. [DOI] [PubMed] [Google Scholar]
- 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]
- von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]