Alternative splicing modulation by a LAMMER kinase impinges on developmental and transcriptome expression

Plant Cell

Volumn 15, Issue 4, 2003, Pages 926-938

  Savaldi Goldstein, Sigal ^a   Aviv, Dvora ^a   Davydov, Olga ^a   Fluhr, Robert ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GENES; PLANTS (BOTANY); RNA;

GENE EXPRESSION;

CELLS;

ARABIDOPSIS; NICOTIANA TABACUM;

EID: 0037394416     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.011056     Document Type: Article

References (62)

1. Allemand, E., Gattoni, R., Bourbon, H.M., Stevenin, J., Caceres, J.F., Soret, J., and Tazi, J. (2001), Distinctive features of Drosophila alternative splicing factor RS domain: Implication for specific phosphorylation, shuttling, and splicing activation. Mol. Cell. Biol. 21, 1345-1359.
2. Auboeuf, D., Honig, A., Berget, S.M., and O'Malley, B.W. (2002). Coordinate regulation of transcription and splicing by steroid receptor coregulators. Science 298, 416-419.
3. Ben David, Y., Letwin, K., Tannock, L., Bernstein, A., and Pawson, T. (1991). A mammalian protein kinase with potential for serine/threonine and tyrosine phosphorylation is related to cell cycle regulators. EMBO J. 10, 317-325.
4. Beven, A.F., Simpson, G.G., Brown, J.W.S., and Shaw, P.J. (1995). The organization of spliceosomal components in the nuclei of higher plants. J. Cell Sci. 108, 509-518.
5. Bohmann, K., Ferreira, J.A., and Lamond, A.I. (1995). Mutational analysis of P80 coilin indicates a functional interaction between coiled bodies and the nucleolus. J. Cell Biol. 131, 817-831.
6. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Carmofonseca, M., Pepperkok, R., Carvalho, M.T., and Lamond, A.I. (1992). Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J. Cell Biol. 117, 1-14.
8. Chung, B.C., Lee, S.Y., Oh, S.A., Rhew, T.H., Nam, H.G., and Lee, C.H. (1997). The promoter activity of sen1, a senescence-associated gene of Arabidopsis, is repressed by sugars. J. Plant Physiol. 151, 339-345.
9. Clark, T.A., Sugnet, C.W., and Ares, M., Jr. (2002). Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296, 907-910.
10. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
11. Colwill, K., Feng, L.L., Yeakley, J.M., Gish, G.D., Caceres, J.F., Pawson, T., and Fu, X.D. (1996a). SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol. Chem, 271, 24569-24575.
12. Colwill, K., Pawson, T., Andrews, B., Prasad, J., Manley, J.L., Bell, J.C., and Duncan, P.I. (1996b). The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15, 265-275.
13. Dinesh-Kumar, S.P., and Baker, B.J. (2000). Alternatively spliced N resistance gene transcripts: Their possible role in tobacco mosaic virus resistance. Proc. Natl. Acad. Sci. USA 97, 1908-1913.
14. Du, C., McGuffin, M.E., Dauwalder, B., Rabinow, L., and Mattox, W. (1998). Protein phosphorylation plays an essential role in the regulation of alternative splicing and sex determination in Drosophila. Mol. Cell 2, 741-750.
15. Duncan, P.I., Stojdl, D.F., Marius, R.M., and Bell, J.C. (1997). In vivo regulation of alternative pre-mRNA splicing by the Cik1 protein kinase. Mol. Cell. Biol. 17, 5996-6001.
16. Fu, X.D. (1995). The superfamily of arginine/serine-rich splicing factors. RNA 1, 663-680.
17. Golovkin, M., and Reddy, A.S.N. (1996). Structure and expression of a plant U1 snRNP 70K gene: Alternative splicing of U1 snRNP 70K pre-mRNAs produces two different transcripts. Plant Cell 8, 1421-1435.
18. Golovkin, M., and Reddy, A.S.N. (1999). An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1-70K protein. J. Biol. Chem. 274, 36428-36438.
19. Graveley, B.R. (2000). Sorting out the complexity of SR protein functions. RNA 6, 1197-1211.
20. Graveley, B.R. (2001). Alternative splicing: Increasing diversity in the proteomic world. Trends Genet. 17, 100-107.
21. Gui, J.F., Tronchere, H., Chandler, S.D., and Fu, X.D. (1994). Purification and characterization of a kinase specific for the serine- and arginine-rich pre-mRNA splicing factors. Prec. Natl. Acad. Sci. USA 91, 10824-10828.
22. Guzman, P., and Ecker, J.R. (1990). Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523.
23. Howel, B.W., Afar, D.E.H., Lew, J., Douville, E.M.J., Icely, P.L.E., Gray, D.A., and Bell, J.C. (1991). Tyrosine-phosphorylating enzyme with sequence homology to serine/threonine kinases. Mol. Cell. Biol. 11, 568-572.
24. Kramer, A. (1996). The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65, 367-409.
25. Kuroyanagi, N., Onogi, H., Wakabayashi, T., and Hagiwara, M. (1998). Novel SR-protein-specific kinase, SRPK2, disassembles nuclear speckles. Biochem. Biophys. Res. Commun. 242, 357-364.
26. Lam, H.M., Peng, S.S.Y., and Coruzzi, G.M. (1994). Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol. 106, 1347-1357.
27. Lambermon, M.H.L., Simpson, G.G., Kirk, D.A.W., Hemmings-Mieszczak, M., Klahre, U., and Filipowicz, W. (2000). UBP1, a novel hnRNP-like protein that functions at multiple steps of higher plant nuclear pre-mRNA maturation. EMBO J. 19, 1638-1649.
28. Lazar, G., and Goodman, H.M. (2000). The Arabidopsis splicing factor SR1 is regulated by alternative splicing. Plant Mol. Biol. 42, 571-581.
29. Lazar, G., Schaal, T., Maniatis, T., and Goodman, H.M. (1995). Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor Sf2/Asf. Proc. Natl. Acad. Sci. USA 92, 7672-7676.
30. Lee, K., Du, C., Horn, M., and Rabinow, L. (1996). Activity and autophosphorylation of LAMMER protein kinases. J. Biol. Chem. 271, 27299-27303.
31. Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J.L., and Lafyatis, R. (2002). Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: A novel function for SR proteins. Genes Dev. 16, 594-607.
32. Lopato, S., Kalyna, M., Dorner, S., Kobayashi, R., Krainer, A.R., and Barta, A. (1999). atSRp30, one of two SF2/ASF-like proteins from Arabidopsis thaliana, regulates splicing of specific plant genes. Genes Dev. 13, 987-1001.
33. Lopato, S., Mayeda, A., Krainer, A.R., and Barta, A. (1996). Pre-mRNA splicing in plants: Characterization of Ser/Arg splicing factors. Proc. Natl. Acad. Sci. USA 93, 3074-3079.
34. Lopez, A.J. (1998), Alternative splicing of pre-mRNA: Developmental consequences and mechanisms of regulation. Annu. Rev. Genet. 32, 279-305.
35. Lorkovic, Z.J., and Barta, A. (2002). Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30, 623-635.
36. Lorkovic, Z.J., Kirk, D.A.W., Klahre, U., Hemmings-Mieszczak, M., and Filipowicz, W. (2000a). RBP45 and RBP47, two oligouridylate-specific hnRNP-like proteins interacting with poly(A)(+) RNA in nuclei of plant cells. RNA 6, 1610-1624.
37. Lorkovic, Z.J., Kirk, D.A.W., Lambermon, M.H.L., and Filipowicz, W. (2000b). Pre-mRNA splicing in higher plants. Trends Plant Sci. 5, 160-167.
38. Ma, L., Li, J., Qu, L., Hager, J., Chen, Z., Zhao, H., and Deng, X.W. (2001). Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13, 2589-2607.
39. Menegay, H., Moeslein, F., and Landreth, G. (1999). The dual specificity protein kinase CLK3 is abundantly expressed in mature mouse spermatozoa. Exp. Cell Res. 253, 463-473.
40. Mintz, P.J., and Spector, D.L. (2000). Compartmentalization of RNA processing factors within nuclear speckles. J. Struct. Biol. 129, 241-251.
41. Modrek, B., and Lee, C. (2002). A genomic view of alternative splicing. Nat. Genet. 30, 13-19.
42. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473-497.
43. Nishihama, R., Banno, H., Kawahara, E., Irie, K., and Machida, Y. (1997). Possible involvement of differential splicing in regulation of the activity of Arabidopsis ANP1 that is related to mitogen-activated protein kinase kinase kinases (MAPKKKs). Plant J. 12, 39-48.
44. Nitsch, J.P. (1969). Experimental androgenesis in Nicotiana. Phytomorphology 19, 389-404.
45. Okamoto, Y., Onogi, H., Honda, R., Yasuda, H., Wakabayashi, T., Nimura, Y., and Hagiwara, M. (1998). cdc2 kinase-mediated phosphorylation of splicing factor SF2/ASF. Biochem. Biophys. Res. Commun. 249, 872-878.
46. Oswald, O., Martin, T., Dominy, P.J., and Graham, I.A. (2001). Plastid redox state and sugars: Interactive regulators of nuclear-encoded photosynthetic gene expression. Proc. Natl. Acad. Sci. USA 98, 2047-2052.
47. Proudfoot, N.J., Furger, A., and Dye, M.J. (2002). Integrating mRNA processing with transcription. Cell 108, 510-512.
48. Queitsch, C., Sangster, T.A., and Lindquist, S. (2002). Hsp90 as a capacitor of phenotypic variation. Nature 417, 618-624.
49. Reddy, A.S.N. (2001). Nuclear pre-mRNA splicing in plants. Crit. Rev. Plant Sci. 20, 523-571.
50. Rossi, F., Labourier, E., Forne, T., Divita, G., Derancourt, J., Riou, J.F., Antoine, E., Cathala, G., Brunel, C., and Tazi, J. (1996). Specific phosphorylation of SR proteins by mammalian DNA topoisomerase I. Nature 381, 80-82.
51. Sacco-Bubulya, P., and Spector, D.L. (2002). Disassembly of interchromatin granule clusters alters the coordination of transcription and pre-mRNA splicing. J. Cell Biol. 156, 425-436.
52. Savaldi-Goldstein, S., Sessa, G., and Fluhr, R. (2000). The ethylene-inducible PK12 kinase mediates the phosphorylation of SR splicing factors. Plant J. 21, 91-96.
53. Sessa, G., Raz, V., Savaldi, S., and Fluhr, R. (1996). PK12, a plant dual-specificity protein kinase of the LAMMER family, is regulated by the hormone ethylene. Plant Cell 8, 2223-2234.
54. Smalle, J., Haegman, M., Kurepa, J., Van Montagu, M., and Straeten, D.V. (1997). Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc. Natl. Acad. Sci. USA 94, 2756-2761.
55. Smetana, K., Busch, R., Chan, P.K., and Busch, H. (2001). Immunocytochemical localization of nucleophosmin and RH-II/Gu protein in nucleoli of HeLa cells after treatment with actinomycin D. Acta Histochem. 103, 325-333.
56. Solano, R., Stepanova, A., Chao, Q.M., and Ecker, J.R. (1998). Nuclear events in ethylene signaling: A transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703-3714.
57. Wilson, K., Long, D., Swinburne, J., and Coupland, G. (1996). A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8, 659-671.
58. Xiao, S.H., and Manley, J.L. (1997). Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev. 11, 334-344.
59. Yun, B., Farkas, R., Lee, K., and Rabinow, L. (1994). The Doa locus encodes a member of a new protein kinase family and is essential for eye and embryonic development in Drosophila melanogaster. Genes Dev. 8, 1160-1173.
60. Yun, B., Lee, K., Farkas, R., Hitte, C., and Rabinow, L. (2000). The LAMMER protein kinase encoded by the Doa locus of Drosophila is required in both somatic and germline cells and is expressed as both nuclear and cytoplasmic isoforms throughout development. Genetics 156, 749-761.
61. Zahler, A.M., Lane, W.S., Stolk, J.A., and Roth, M.B. (1992). SR proteins: A conserved family of pre-messenger RNA splicing factors. Genes Dev. 6, 837-847.
62. Zik, M., and Irish, V.F. (2003). Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15, 207-222.