Tissue-specific Expression and Dynamic Organization of SR Splicing Factors in Arabidopsis

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2004 Mar 23

PMID 15034145

Citations 43

Authors

Yuda Fang

Stephen Hearn

David L Spector

Affiliations

Soon will be listed here.

Abstract

The organization of the pre-mRNA splicing machinery has been extensively studied in mammalian and yeast cells and far less is known in living plant cells and different cell types of an intact organism. Here, we report on the expression, organization, and dynamics of pre-mRNA splicing factors (SR33, SR1/atSRp34, and atSRp30) under control of their endogenous promoters in Arabidopsis. Distinct tissue-specific expression patterns were observed, and differences in the distribution of these proteins within nuclei of different cell types were identified. These factors localized in a cell type-dependent speckled pattern as well as being diffusely distributed throughout the nucleoplasm. Electron microscopic analysis has revealed that these speckles correspond to interchromatin granule clusters. Time-lapse microscopy revealed that speckles move within a constrained nuclear space, and their organization is altered during the cell cycle. Fluorescence recovery after photobleaching analysis revealed a rapid exchange rate of splicing factors in nuclear speckles. The dynamic organization of plant speckles is closely related to the transcriptional activity of the cells. The organization and dynamic behavior of speckles in Arabidopsis cell nuclei provides significant insight into understanding the functional compartmentalization of the nucleus and its relationship to chromatin organization within various cell types of a single organism.

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References

Turner B, Franchi L . Identification of protein antigens associated with the nuclear matrix and with clusters of interchromatin granules in both interphase and mitotic cells. J Cell Sci. 1987; 87 ( Pt 2):269-82. DOI: 10.1242/jcs.87.2.269. View

Caceres J, Stamm S, Helfman D, Krainer A . Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science. 1994; 265(5179):1706-9. DOI: 10.1126/science.8085156. View

Lopato S, Gattoni R, Fabini G, Stevenin J, Barta A . A novel family of plant splicing factors with a Zn knuckle motif: examination of RNA binding and splicing activities. Plant Mol Biol. 1999; 39(4):761-73. DOI: 10.1023/a:1006129615846. View

Lopato S, Waigmann E, Barta A . Characterization of a novel arginine/serine-rich splicing factor in Arabidopsis. Plant Cell. 1996; 8(12):2255-64. PMC: 161350. DOI: 10.1105/tpc.8.12.2255. View

Melaragno J, Mehrotra B, Coleman A . Relationship between Endopolyploidy and Cell Size in Epidermal Tissue of Arabidopsis. Plant Cell. 1993; 5(11):1661-1668. PMC: 160394. DOI: 10.1105/tpc.5.11.1661. View

Lazar G, Schaal T, Maniatis T, Goodman H . Identification of a plant serine-arginine-rich protein similar to the mammalian splicing factor SF2/ASF. Proc Natl Acad Sci U S A. 1995; 92(17):7672-6. PMC: 41207. DOI: 10.1073/pnas.92.17.7672. View

Smith C, Valcarcel J . Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem Sci. 2000; 25(8):381-8. DOI: 10.1016/s0968-0004(00)01604-2. View

Kruhlak M, Lever M, Fischle W, Verdin E, Bazett-Jones D, Hendzel M . Reduced mobility of the alternate splicing factor (ASF) through the nucleoplasm and steady state speckle compartments. J Cell Biol. 2000; 150(1):41-51. PMC: 2185567. DOI: 10.1083/jcb.150.1.41. View

Yamaguchi Y, Wada T, Handa H . Interplay between positive and negative elongation factors: drawing a new view of DRB. Genes Cells. 1998; 3(1):9-15. DOI: 10.1046/j.1365-2443.1998.00162.x. View

10.

Cui P, Moreno Diaz de la Espina S . Sm and U2B" proteins redistribute to different nuclear domains in dormant and proliferating onion cells. Planta. 2003; 217(1):21-31. DOI: 10.1007/s00425-002-0966-3. View

11.

Shopland L, Johnson C, Byron M, McNeil J, Lawrence J . Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. J Cell Biol. 2003; 162(6):981-90. PMC: 2172856. DOI: 10.1083/jcb.200303131. View

12.

Golovkin M, Reddy A . The plant U1 small nuclear ribonucleoprotein particle 70K protein interacts with two novel serine/arginine-rich proteins. Plant Cell. 1998; 10(10):1637-48. PMC: 143944. DOI: 10.1105/tpc.10.10.1637. View

13.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

14.

Graveley B . Sorting out the complexity of SR protein functions. RNA. 2000; 6(9):1197-211. PMC: 1369994. DOI: 10.1017/s1355838200000960. View

15.

Kato N, Lam E . Chromatin of endoreduplicated pavement cells has greater range of movement than that of diploid guard cells in Arabidopsis thaliana. J Cell Sci. 2003; 116(Pt 11):2195-201. DOI: 10.1242/jcs.00437. View

16.

Golovkin M, Reddy A . An SC35-like protein and a novel serine/arginine-rich protein interact with Arabidopsis U1-70K protein. J Biol Chem. 1999; 274(51):36428-38. DOI: 10.1074/jbc.274.51.36428. View

17.

Thiry M . The interchromatin granules. Histol Histopathol. 1995; 10(4):1035-45. View

18.

Kato N, Pontier D, Lam E . Spectral profiling for the simultaneous observation of four distinct fluorescent proteins and detection of protein-protein interaction via fluorescence resonance energy transfer in tobacco leaf nuclei. Plant Physiol. 2002; 129(3):931-42. PMC: 1540237. DOI: 10.1104/pp.005496. View

19.

Boudonck K, Dolan L, Shaw P . Coiled body numbers in the Arabidopsis root epidermis are regulated by cell type, developmental stage and cell cycle parameters. J Cell Sci. 1998; 111 ( Pt 24):3687-94. DOI: 10.1242/jcs.111.24.3687. View

20.

Fakan S, PUVION E . The ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int Rev Cytol. 1980; 65:255-99. DOI: 10.1016/s0074-7696(08)61962-2. View