CYCLIN-DEPENDENT KINASE G1 is associated with the spliceosome to regulate CALLOSE SYNTHASE5 splicing and pollen wall formation in Arabidopsis

Plant Cell

Volumn 25, Issue 2, 2013, Pages 637-648

  Huang, Xue Yong ^a   Niu, Jin ^a   Sun, Ming Xi ^a   Zhu, Jun ^a   Gao, Ju Fang ^a   Yang, Jun ^a   Zhou, Que ^a   Yang, Zhong Nan ^a  

^a SHANGHAI NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 84875512967     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.107896     Document Type: Article

References (61)

1. Alexander, M.P. (1969). Differential staining of aborted and nonaborted pollen. Stain Technol. 44: 117-122.
2. Ariizumi, T., Hatakeyama, K., Hinata, K., Inatsugi, R., Nishida, I., Sato, S., Kato, T., Tabata, S., and Toriyama, K. (2004). Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J. 39: 170-181.
3. Ariizumi, T., and Toriyama, K. (2011). Genetic regulation of sporopollenin synthesis and pollen exine development. Annu. Rev. Plant Biol. 62: 437-460.
4. Barrôco, R.M., De Veylder, L., Magyar, Z., Engler, G., Inzé, D., and Mironov, V. (2003). Novel complexes of cyclin-dependent kinases and a cyclin-like protein from Arabidopsis thaliana with a function unrelated to cell division. Cell. Mol. Life Sci. 60: 401-412.
5. Bentley, D. (1999). Coupling RNA polymerase II transcription with premRNA processing. Curr. Opin. Cell Biol. 11: 347-351.
6. Black, D.L. (2003). Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72: 291-336.
7. Boudolf, V., Vlieghe, K., Beemster, G.T., Magyar, Z., Torres Acosta, J.A., Maes, S., Van Der Schueren, E., Inzé, D., and De Veylder, L. (2004). The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16: 2683-2692.
8. Chang, H.S., Zhang, C., Chang, Y.H., Zhu, J., Xu, X.F., Shi, Z.H., Zhang, X.L., Xu, L., Huang, H., Zhang, S., and Yang, Z.N. (2012). No primexine and plasma membrane undulation is essential for primexine deposition and plasma membrane undulation during microsporogenesis in Arabidopsis. Plant Physiol. 158: 264-272.
9. Chen, H.H., Wang, Y.C., and Fann, M.J. (2006). Identification and characterization of the CDK12/cyclin L1 complex involved in alternative splicing regulation. Mol. Cell. Biol. 26: 2736-2745.
10. Chen, H.H., Wong, Y.H., Geneviere, A.M., and Fann, M.J. (2007). CDK13/CDC2L5 interacts with L-type cyclins and regulates alternative splicing. Biochem. Biophys. Res. Commun. 354: 735-740.
11. Cho, S., Hoang, A., Sinha, R., Zhong, X.Y., Fu, X.D., Krainer, A.R., and Ghosh, G. (2011). Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1-70K snRNP protein determines early spliceosome assembly. Proc. Natl. Acad. Sci. USA 108: 8233-8238.
12. 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.
13. Cokol, M., Nair, R., and Rost, B. (2000). Finding nuclear localization signals. EMBO Rep. 1: 411-415.
14. Cui, X., Fan, B., Scholz, J., and Chen, Z. (2007). Roles of Arabidopsis cyclin-dependent kinase C complexes in cauliflower mosaic virus infection, plant growth, and development. Plant Cell 19: 1388-1402.
15. Culbertson, M.R., and Leeds, P.F. (2003). Looking at mRNA decay pathways through the window of molecular evolution. Curr. Opin. Genet. Dev. 13: 207-214.
16. Dong, X., Hong, Z., Sivaramakrishnan, M., Mahfouz, M., and Verma, D.P. (2005). Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J. 42: 315-328.
17. Doonan, J.H., and Kitsios, G. (2009). Functional evolution of cyclindependent kinases. Mol. Biotechnol. 42: 14-29.
18. Even, Y., Durieux, S., Escande, M.L., Lozano, J.C., Peaucellier, G., Weil, D., and Genevière, A.M. (2006). CDC2L5, a Cdk-like kinase with RS domain, interacts with the ASF/SF2-associated protein p32 and affects splicing in vivo. J. Cell. Biochem. 99: 890-904.
19. Fang, Y., Hearn, S., and Spector, D.L. (2004). Tissue-specific expression and dynamic organization of SR splicing factors in Arabidopsis. Mol. Biol. Cell 15: 2664-2673.
20. Fill, B.K., Qiu, J.L., Petersen, K., Petersen, M., and Mundy, J. (2008). Coimmunoprecipitation (co-IP) of nuclear proteins and chromatin immunoprecipitation (ChIP) from Arabidopsis. CSH Protoc. 2008: 5049
21. Gao, Z.P., Yu, Q.B., Zhao, T.T., Ma, Q., Chen, G.X., and Yang, Z.N. (2011). A functional component of the transcriptionally active chromosome complex, Arabidopsis pTAC14, interacts with pTAC12/ HEMERA and regulates plastid gene expression. Plant Physiol. 157: 1733-1745.
22. Golovkin, M., and Reddy, A.S. (1998). The plant U1 small nuclear ribonucleoprotein particle 70K protein interacts with two novel serine/arginine-rich proteins. Plant Cell 10: 1637-1648.
23. Golovkin, M., and Reddy, A.S. (1999). An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1-70K protein. J. Biol. Chem. 274: 36428-36438.
24. Guan, Y.F., Huang, X.Y., Zhu, J., Gao, J.F., Zhang, H.X., and Yang, Z.N. (2008). RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol. 147: 852-863.
25. Hajheidari, M., Farrona, S., Huettel, B., Koncz, Z., and Koncz, C. (2012). CDKF;1 and CDKD protein kinases regulate phosphorylation of serine residues in the C-terminal domain of Arabidopsis RNA polymerase II. Plant Cell 24: 1626-1642.
26. Heslop-Harrison, J. (1968). Pollen wall development. The succession of events in the growth of intricately patterned pollen walls is described and discussed. Science 161: 230-237.
27. Heslop-Harrison, J., and Mackenzie, A. (1967). Autoradiography of soluble [2-14-C]thymidine derivatives during meiosis and microsporogenesis in Lilium anthers. J. Cell Sci. 2: 387-400.
28. Hu, C.D., Chinenov, Y., and Kerppola, T.K. (2002). Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9: 789-798.
29. Hu, D., Mayeda, A., Trembley, J.H., Lahti, J.M., and Kidd, V.J. (2003). CDK11 complexes promote pre-mRNA splicing. J. Biol. Chem. 278: 8623-8629.
30. Isken, O., and Maquat, L.E. (2007). Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21: 1833-1856.
31. Iwakawa, H., Shinmyo, A., and Sekine, M. (2006). Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J. 45: 819-831.
32. Kaldis, P. (1999). The cdk-activating kinase (CAK): From yeast to mammals. Cell. Mol. Life Sci. 55: 284-296.
33. Kitsios, G., Alexiou, K.G., Bush, M., Shaw, P., and Doonan, J.H. (2008). A cyclin-dependent protein kinase, CDKC2, colocalizes with and modulates the distribution of spliceosomal components in Arabidopsis. Plant J. 54: 220-235.
34. Ko, T.K., Kelly, E., and Pines, J. (2001). CrkRS: A novel conserved Cdc2-related protein kinase that colocalises with SC35 speckles. J. Cell Sci. 114: 2591-2603.
35. Kozar, K., Ciemerych, M.A., Rebel, V.I., Shigematsu, H., Zagozdzon, A., Sicinska, E., Geng, Y., Yu, Q., Bhattacharya, S., Bronson, R.T., Akashi, K., and Sicinski, P. (2004). Mouse development and cell proliferation in the absence of D-cyclins. Cell 118: 477-491.
36. Kralovicova, J., Hwang, G., Asplund, A.C., Churbanov, A., Smith, C.I., and Vorechovsky, I. (2011). Compensatory signals associated with the activation of human GC 59 splice sites. Nucleic Acids Res. 39: 7077-7091.
37. Krämer, A. (1996). The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65: 367-409.
38. Lopato, S., Forstner, C., Kalyna, M., Hilscher, J., Langhammer, U., Indrapichate, K., Lorkovic, Z.J., and Barta, A. (2002). Network of interactions of a novel plant-specific Arg/Ser-rich protein, atRSZ33, with atSC35-like splicing factors. J. Biol. Chem. 277: 39989-39998.
39. Menges, M., de Jager, S.M., Gruissem, W., and Murray, J.A. (2005). Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J. 41: 546-566.
40. Meuter-Gerhards, A., Riegart, S., and Wiermann, R. (1999). Studies on sporopollenin biosynthesis in Curcurbita maxima (DUCH)-II: the involvement of aliphatic metabolism. J. Plant Physiol. 154: 431-436.
41. Moore, J.D., Kirk, J.A., and Hunt, T. (2003). Unmasking the S-phasepromoting potential of cyclin B1. Science 300: 987-990.
42. Morgan, D.O. (1997). Cyclin-dependent kinases: Engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13: 261-291.
43. Nishikawa, S., Zinkl, G.M., Swanson, R.J., Maruyama, D., and Preuss, D. (2005). Callose (β-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol. 5: 22.
44. Paxson-Sowders, D.M., Dodrill, C.H., Owen, H.A., and Makaroff, C.A. (2001). DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol. 127: 1739-1749.
45. Pinhero, R., Liaw, P., Bertens, K., and Yankulov, K. (2004). Three cyclin-dependent kinases preferentially phosphorylate different parts of the C-terminal domain of the large subunit of RNA polymerase II. Eur. J. Biochem. 271: 1004-1014.
46. Rane, S.G., Dubus, P., Mettus, R.V., Galbreath, E.J., Boden, G., Reddy, E.P., and Barbacid, M. (1999). Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat. Genet. 22: 44-52.
47. Reddy, A.S. (2004). Plant serine/arginine-rich proteins and their role in pre-mRNA splicing. Trends Plant Sci. 9: 541-547.
48. Ross, K.J., Fransz, P., and Jones, G.H. (1996). A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4: 507-516.
49. Sanders, P.M., Anhthu, Q.B., Weterings, K., McIntire, K.N., Hsu, Y., Lee, P.Y., Troung, M.T., Beals, T.P., and Goldberg, R.B. (1999). Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11: 297-322.
50. Schwartz, S.H., Silva, J., Burstein, D., Pupko, T., Eyras, E., and Ast, G. (2008). Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res. 18: 88-103.
51. Shepard, P.J., and Hertel, K.J. (2009). The SR protein family. Genome Biol. 10: 242.
52. Shimotohno, A., Umeda-Hara, C., Bisova, K., Uchimiya, H., and Umeda, M. (2004). The plant-specific kinase CDKF;1 is involved in activating phosphorylation of cyclin-dependent kinase-activating kinases in Arabidopsis. Plant Cell 16: 2954-2966.
53. Sun, M.X., Huang, X.Y., Yang, J., Guan, Y.F., and Yang, Z.N. (2013). Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Plant Reprod. doi:10.1007/s00497-012-0208-1
54. Terzi, L.C., and Simpson, G.G. (2009). Arabidopsis RNA immunoprecipitation. Plant J. 59: 163-168.
55. Umeda, M., Shimotohno, A., and Yamaguchi, M. (2005). Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants. Plant Cell Physiol. 46: 1437-1442.
56. Valadkhan, S., and Jaladat, Y. (2010). The spliceosomal proteome: At the heart of the largest cellular ribonucleoprotein machine. Proteomics 10: 4128-4141.
57. Wang, W., and Chen, X. (2004). HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis. Development 131: 3147-3156.
58. Wang, Y.H. (2008). How effective is T-DNA insertional mutagenesis in Arabidopsis? J. Biochem. Tech. 1: 11-20.
59. Wu, J.Y., and Maniatis, T. (1993). Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75: 1061-1070.
60. Zhang, Z.B., Zhu, J., Gao, J.F., Wang, C., Li, H., Zhang, H.Q., Zhang, S., Wang, D.M., Wang, Q.X., Huang, H., Xia, H.J., and Yang, Z.N. (2007). Transcription factor AtMYB103 is required for anther development by regulating microspore release from tetrads and exine formation in Arabidopsis. Plant J. 52: 528-538.
61. Zhu, J., and Krainer, A.R. (2000). Pre-mRNA splicing in the absence of an SR protein RS domain. Genes Dev. 14: 3166-3178.