The Integral Spliceosomal Component CWC15 is Required for Development in Arabidopsis

Overview

Journal Sci Rep

Specialty Science

Date 2020 Aug 10

PMID 32770129

Citations 5

Authors

Daniel Slane

Cameron H Lee

Martina Kolb

Craig Dent

Yingjing Miao

Mirita Franz-Wachtel

Steffen Lau

Boris Macek

Sureshkumar Balasubramanian

Martin Bayer

Gerd Jurgens

Affiliations

Soon will be listed here.

Abstract

Efficient mRNA splicing is a prerequisite for protein biosynthesis and the eukaryotic splicing machinery is evolutionarily conserved among species of various phyla. At its catalytic core resides the activated splicing complex Bact consisting of the three small nuclear ribonucleoprotein complexes (snRNPs) U2, U5 and U6 and the so-called NineTeen complex (NTC) which is important for spliceosomal activation. CWC15 is an integral part of the NTC in humans and it is associated with the NTC in other species. Here we show the ubiquitous expression and developmental importance of the Arabidopsis ortholog of yeast CWC15. CWC15 associates with core components of the Arabidopsis NTC and its loss leads to inefficient splicing. Consistent with the central role of CWC15 in RNA splicing, cwc15 mutants are embryo lethal and additionally display strong defects in the female haploid phase. Interestingly, the haploid male gametophyte or pollen in Arabidopsis, on the other hand, can cope without functional CWC15, suggesting that developing pollen might be more tolerant to CWC15-mediated defects in splicing than either embryo or female gametophyte.

Citing Articles

Alternative splicing of a potato disease resistance gene maintains homeostasis between growth and immunity.

Sun B, Huang J, Kong L, Gao C, Zhao F, Shen J Plant Cell. 2024; 36(9):3729-3750.

PMID: 38941447 PMC: 11371151. DOI: 10.1093/plcell/koae189.

The Prp19C/NTC subunit Syf2 and the Prp19C/NTC-associated protein Cwc15 function in TREX occupancy and transcription elongation.

Henke-Schulz L, Minocha R, Maier N, Strasser K RNA. 2024; 30(7):854-865.

PMID: 38627018 PMC: 11182008. DOI: 10.1261/rna.079944.124.

The spliceosome-associated protein CWC15 promotes miRNA biogenesis in Arabidopsis.

Zhou B, Yu H, Xue Y, Li M, Zhang C, Yu B Nat Commun. 2024; 15(1):2399.

PMID: 38493158 PMC: 10944506. DOI: 10.1038/s41467-024-46676-z.

Ubiquitination and Ubiquitin-Like Modifications as Mediators of Alternative Pre-mRNA Splicing in .

Lan W, Qiu Y, Xu Y, Liu Y, Miao Y Front Plant Sci. 2022; 13:869870.

PMID: 35646014 PMC: 9134077. DOI: 10.3389/fpls.2022.869870.

Long-Term High-Temperature Stress Impacts on Embryo and Seed Development in .

Macova K, Prabhullachandran U, Stefkova M, Spyroglou I, Pencik A, Endlova L Front Plant Sci. 2022; 13:844292.

PMID: 35528932 PMC: 9075611. DOI: 10.3389/fpls.2022.844292.

References

Liao Y, Smyth G, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013; 30(7):923-30. DOI: 10.1093/bioinformatics/btt656. View

Steinborn K, Maulbetsch C, Priester B, Trautmann S, Pacher T, Geiges B . The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev. 2002; 16(8):959-71. PMC: 152350. DOI: 10.1101/gad.221702. View

Fang Y, Hearn S, Spector D . Tissue-specific expression and dynamic organization of SR splicing factors in Arabidopsis. Mol Biol Cell. 2004; 15(6):2664-73. PMC: 420091. DOI: 10.1091/mbc.e04-02-0100. View

Lee Y, Rio D . Mechanisms and Regulation of Alternative Pre-mRNA Splicing. Annu Rev Biochem. 2015; 84:291-323. PMC: 4526142. DOI: 10.1146/annurev-biochem-060614-034316. View

Lukowitz W, Mayer U, Jurgens G . Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell. 1996; 84(1):61-71. DOI: 10.1016/s0092-8674(00)80993-9. View

Bai R, Yan C, Wan R, Lei J, Shi Y . Structure of the Post-catalytic Spliceosome from Saccharomyces cerevisiae. Cell. 2017; 171(7):1589-1598.e8. DOI: 10.1016/j.cell.2017.10.038. View

Tian T, Liu Y, Yan H, You Q, Yi X, Du Z . agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017; 45(W1):W122-W129. PMC: 5793732. DOI: 10.1093/nar/gkx382. View

Liu M, Yuan L, Liu N, Shi D, Liu J, Yang W . GAMETOPHYTIC FACTOR 1, involved in pre-mRNA splicing, is essential for megagametogenesis and embryogenesis in Arabidopsis. J Integr Plant Biol. 2009; 51(3):261-71. DOI: 10.1111/j.1744-7909.2008.00783.x. View

Dresselhaus T, Sprunck S, Wessel G . Fertilization Mechanisms in Flowering Plants. Curr Biol. 2016; 26(3):R125-39. PMC: 4934421. DOI: 10.1016/j.cub.2015.12.032. View

10.

Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher E . MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature. 2010; 464(7290):913-6. DOI: 10.1038/nature08836. View

11.

Weijers D, Geldner N, Offringa R, Jurgens G . Seed development: Early paternal gene activity in Arabidopsis. Nature. 2001; 414(6865):709-10. DOI: 10.1038/414709a. View

12.

Speth C, Szabo E, Martinho C, Collani S, Zur Oven-Krockhaus S, Richter S . Arabidopsis RNA processing factor SERRATE regulates the transcription of intronless genes. Elife. 2018; 7. PMC: 6135607. DOI: 10.7554/eLife.37078. View

13.

Kornblihtt A, Schor I, Allo M, Dujardin G, Petrillo E, Munoz M . Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol. 2013; 14(3):153-65. DOI: 10.1038/nrm3525. View

14.

Nodine M, Bartel D . MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 2010; 24(23):2678-92. PMC: 2994041. DOI: 10.1101/gad.1986710. View

15.

Haselbach D, Komarov I, Agafonov D, Hartmuth K, Graf B, Dybkov O . Structure and Conformational Dynamics of the Human Spliceosomal B Complex. Cell. 2018; 172(3):454-464.e11. DOI: 10.1016/j.cell.2018.01.010. View

16.

Lau S, Slane D, Herud O, Kong J, Jurgens G . Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol. 2012; 63:483-506. DOI: 10.1146/annurev-arplant-042811-105507. View

17.

Nesic D, Kramer A . Domains in human splicing factors SF3a60 and SF3a66 required for binding to SF3a120, assembly of the 17S U2 snRNP, and prespliceosome formation. Mol Cell Biol. 2001; 21(19):6406-17. PMC: 99788. DOI: 10.1128/MCB.21.19.6406-6417.2001. View

18.

Hamann T, Mayer U, Jurgens G . The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development. 1999; 126(7):1387-95. DOI: 10.1242/dev.126.7.1387. View

19.

Nguyen T, Galej W, Fica S, Lin P, Newman A, Nagai K . CryoEM structures of two spliceosomal complexes: starter and dessert at the spliceosome feast. Curr Opin Struct Biol. 2016; 36:48-57. PMC: 4830896. DOI: 10.1016/j.sbi.2015.12.005. View

20.

Hartmann L, Drewe-Boss P, Wiessner T, Wagner G, Geue S, Lee H . Alternative Splicing Substantially Diversifies the Transcriptome during Early Photomorphogenesis and Correlates with the Energy Availability in Arabidopsis. Plant Cell. 2016; 28(11):2715-2734. PMC: 5155347. DOI: 10.1105/tpc.16.00508. View