A KH-Domain RNA-Binding Protein Interacts with FIERY2/CTD Phosphatase-Like 1 and Splicing Factors and Is Important for Pre-mRNA Splicing in Arabidopsis

被引:83
作者
Chen, Tao [1 ]
Cui, Peng [1 ]
Chen, Hao [1 ]
Ali, Shahjahan [1 ]
Zhang, Shoudong [1 ]
Xiong, Liming [1 ]
机构
[1] KAUST, Div Biol & Environm Sci & Engn, Thuwal, Saudi Arabia
关键词
FLOWERING-LOCUS-C; FRAGILE-X GENE; POLYMERASE-II; SR PROTEINS; PROCESSING FACTORS; ONE MOTIF; IN-VIVO; STRESS; TRANSCRIPTION; EXPRESSION;
D O I
10.1371/journal.pgen.1003875
中图分类号
Q3 [遗传学];
学科分类号
071007 ; 090102 ;
摘要
Eukaryotic genomes encode hundreds of RNA-binding proteins, yet the functions of most of these proteins are unknown. In a genetic study of stress signal transduction in Arabidopsis, we identified a K homology (KH)-domain RNA-binding protein, HOS5 (High Osmotic Stress Gene Expression 5), as required for stress gene regulation and stress tolerance. HOS5 was found to interact with FIERY2/RNA polymerase II (RNAP II) carboxyl terminal domain (CTD) phosphatase-like 1 (FRY2/CPL1) both in vitro and in vivo. This interaction is mediated by the first double-stranded RNA-binding domain of FRY2/CPL1 and the KH domains of HOS5. Interestingly, both HOS5 and FRY2/CPL1 also interact with two novel serine-arginine (SR)-rich splicing factors, RS40 and RS41, in nuclear speckles. Importantly, FRY2/CPL1 is required for the recruitment of HOS5. In fry2 mutants, HOS5 failed to be localized in nuclear speckles but was found mainly in the nucleoplasm. hos5 mutants were impaired in mRNA export and accumulated a significant amount of mRNA in the nuclei, particularly under salt stress conditions. Arabidopsis mutants of all these genes exhibit similar stress-sensitive phenotypes. RNA-seq analyses of these mutants detected significant intron retention in many stress-related genes under salt stress but not under normal conditions. Our study not only identified several novel regulators of pre-mRNA processing as important for plant stress response but also suggested that, in addition to RNAP II CTD that is a well-recognized platform for the recruitment of mRNA processing factors, FRY2/CPL1 may also recruit specific factors to regulate the co-transcriptional processing of certain transcripts to deal with environmental challenges.
引用
收藏
页数:14
相关论文
共 63 条
[1]   Phosphorylation of serine 2 within the RNA polymerase IIC-terminal domain couples transcription and 3′ end processing [J].
Ahn, SH ;
Kim, M ;
Buratowski, S .
MOLECULAR CELL, 2004, 13 (01) :67-76
[2]   Genome-wide analyses of alternative splicing in plants: Opportunities and challenges [J].
Barbazuk, W. Brad ;
Fu, Yan ;
McGinnis, Karen M. .
GENOME RESEARCH, 2008, 18 (09) :1381-1392
[3]   Implementing a Rational and Consistent Nomenclature for Serine/Arginine-Rich Protein Splicing Factors (SR Proteins) in Plants [J].
Barta, Andrea ;
Kalyna, Maria ;
Reddy, Anireddy S. N. .
PLANT CELL, 2010, 22 (09) :2926-2929
[4]   Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors [J].
Bentley, DL .
CURRENT OPINION IN CELL BIOLOGY, 2005, 17 (03) :251-256
[5]   Progression through the RNA Polymerase II CTD Cycle [J].
Buratowski, Stephen .
MOLECULAR CELL, 2009, 36 (04) :541-546
[6]   The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters [J].
Cheng, NH ;
Pittman, JK ;
Barkla, BJ ;
Shigaki, T ;
Hirschi, KD .
PLANT CELL, 2003, 15 (02) :347-364
[7]   Two RNA binding proteins, HEN4 and HUM, act in the processing of AGAMOUS Pre-mRNA in Arabidopsis thaliana [J].
Cheng, YL ;
Kato, N ;
Wang, WM ;
Li, JJ ;
Chen, XM .
DEVELOPMENTAL CELL, 2003, 4 (01) :53-66
[8]   DOUBLE-STRANDED-RNA-DEPENDENT PROTEIN-KINASE AND TAR RNA-BINDING PROTEIN FORM HOMODIMERS AND HETERODIMERS IN-VIVO [J].
COSENTINO, GP ;
VENKATESAN, S ;
SERLUCA, FC ;
GREEN, SR ;
MATHEWS, MB ;
SONENBERG, N .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1995, 92 (21) :9445-9449
[9]  
Currie JR, 1999, AM J MED GENET, V84, P272, DOI 10.1002/(SICI)1096-8628(19990528)84:3<272::AID-AJMG21>3.3.CO
[10]  
2-4