RNA Binding Proteins RZ-1B and RZ-1C Play Critical Roles in Regulating Pre-mRNA Splicing and Gene Expression during Development in Arabidopsis

Wu, Zhe; Zhu, Danling; Lin, Xiaoya; Miao, Junwei; Gu, Lianfeng; Deng, Xian; Yang, Qian; Sun, Kangtai; Zhu, Danmeng; Cao, Xiaofeng; Tsuge, Tomohiko; Dean, Caroline; Aoyama, Takashi; Gu, Hongya; Liu, Qu

doi:10.1105/tpc.15.00949

Cited by 77 publications

(82 citation statements)

References 64 publications

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“…It was known that the RRM domain(s) of SR proteins have the ability to bind to the target pre-mRNA, and preferentially to specific RNA sequences [87,89–91]. We found that SCL30 binds to the AGAAGA motif, in comparison to previous studies showed that the GAAG repeats function as the splicing enhancers [92–94] in animals, and RZ-1C and SR45 proteins bind to the AG-riched motif in plant [66,95], suggesting that the AG-rich sequence might play conservative and important role in splicing both in plant and animals. It was known that most exons are bound by at least one SR protein [87,91,96,97], we thought SR45 and SC35/SCL proteins may bind to specific motifs to play redundant and cooperative roles in splicing.…”

Section: Discussionmentioning

confidence: 60%

Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes

Yan

Xia

Sun³

et al. 2017

PLoS Genet

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Serine/arginine-rich (SR) proteins are important splicing factors which play significant roles in spliceosome assembly and splicing regulation. However, little is known regarding their biological functions in plants. Here, we analyzed the phenotypes of mutants upon depleting different subfamilies of Arabidopsis SR proteins. We found that loss of the functions of SC35 and SC35-like (SCL) proteins cause pleiotropic changes in plant morphology and development, including serrated leaves, late flowering, shorter roots and abnormal silique phyllotaxy. Using RNA-seq, we found that SC35 and SCL proteins play roles in the pre-mRNA splicing. Motif analysis revealed that SC35 and SCL proteins preferentially bind to a specific RNA sequence containing the AGAAGA motif. In addition, the transcriptions of a subset of genes are affected by the deletion of SC35 and SCL proteins which interact with NRPB4, a specific subunit of RNA polymerase II. The splicing of FLOWERING LOCUS C (FLC) intron1 and transcription of FLC were significantly regulated by SC35 and SCL proteins to control Arabidopsis flowering. Therefore, our findings provide mechanistic insight into the functions of plant SC35 and SCL proteins in the regulation of splicing and transcription in a direct or indirect manner to maintain the proper expression of genes and development.

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Section: Discussionmentioning

confidence: 60%

Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes

Yan

Xia

Sun³

et al. 2017

PLoS Genet

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“…Similarly, other examples of mutations of RBPs resulted in global changes to the transcriptome. This includes a 14-day old mutant in two RNA recognition motif proteins, RZ-1B and RZ-1C, that had 3,176 DEGs (difference > 1.5-fold, P < 0.01) compared to wild-type (Wu et al, 2016). By contrast, much smaller changes to the alba456 transcriptome were observed; only 1.6% of the alba456 transcriptome were DEGs at the 2-fold change cutoff (or 0.05% at the 5-fold change cutoff) and there were very few DSGs (Figure S7).…”

Section: Discussionmentioning

confidence: 99%

The ALBA RNA-binding proteins function redundantly to promote growth and flowering in Arabidopsis

Wang

Jalajakumari

Miller

et al. 2019

Preprint

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26RNA-binding proteins (RBPs) are critical regulators of gene expression, but have 27 been poorly studied relative to other classes of gene regulators. Recently, 28 mRNA-interactome capture identified many Arabidopsis RBPs of unknown function, 29including a family of ALBA domain containing proteins. Arabidopsis has three 30 short-form ALBA homologues (ALBA1-3) and three long-form ALBA homologues 31 (ALBA4-6), both of which are conserved throughout the plant kingdom. Despite this 32 ancient origin, ALBA-GUS translational fusions of ALBA1, ALBA2, ALBA4, and 33 ALBA5 had indistinguishable expression patterns, all being preferentially expressed in 34 young, rapidly dividing tissues. Likewise, all four ALBA proteins had 35indistinguishable ALBA-GFP subcellular localizations in roots, all being preferentially 36 located to the cytoplasm, consistent with being mRNA-binding. Genetic analysis 37 demonstrated redundancy within the long-form ALBA family members; in contrast to 38 single alba mutants that all appeared wild-type, a triple alba456 mutant had slower 39 rosette growth and a strong delay in flowering-time. RNA-sequencing found most 40 differentially expressed genes in alba456 were related to metabolism, not 41 development. Additionally, changes to the alba456 transcriptome were subtle, 42 suggesting ALBA4-6 participates in a process that does not strongly affect 43 transcriptome composition. Together, our findings demonstrate that ALBA protein 44 function is highly redundant, and is essential for proper growth and flowering in 45 Arabidopsis. 46

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“…Studies in Arabidopsis demonstrate widespread AS regulatory functions for the hnRNP proteins GLY-RICH PROTEIN7 (GRP7) and GRP8 (Streitner et al, 2012), POLYPYRIMIDINE TRACT BINDING PROTEIN1 (PTB1) and PTB2 , RZ-1B/RZ-1C (Wu et al, 2016), and the SR-like protein SR45 (Carvalho et al, 2016). Furthermore, binding motifs required for AS control by SR45 (Day et al, 2012) and the SC35-LIKE33 (SCL33; Thomas et al, 2012) have been identified in single target premRNAs.…”

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confidence: 99%

Subcellular Compartmentation of Alternatively Spliced Transcripts Defines SERINE/ARGININE-RICH PROTEIN30 Expression

2018

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Alternative splicing (AS) is prevalent in higher eukaryotes, and generation of different AS variants is tightly regulated. Widespread AS occurs in response to altered light conditions and plays a critical role in seedling photomorphogenesis, but despite its frequency and effect on plant development, the functional role of AS remains unknown for most splicing variants. Here, we characterized the light-dependent AS variants of the gene encoding the splicing regulator Ser/Arg-rich protein SR30 in Arabidopsis (Arabidopsis thaliana). We demonstrated that the splicing variant SR30.2, which is predominantly produced in darkness, is enriched within the nucleus and strongly depleted from ribosomes. Light-induced AS from a downstream 39 splice site gives rise to SR30.1, which is exported to the cytosol and translated, coinciding with SR30 protein accumulation upon seedling illumination. Constitutive expression of SR30.1 and SR30.2 fused to fluorescent proteins revealed their identical subcellular localization in the nucleoplasm and nuclear speckles. Furthermore, expression of either variant shifted splicing of a genomic SR30 reporter toward SR30.2, suggesting that an autoregulatory feedback loop affects SR30 splicing. We provide evidence that SR30.2 can be further spliced and, unlike SR30.2, the resulting cassette exon variant SR30.3 is sensitive to nonsense-mediated decay. Our work delivers insight into the complex and compartmentalized RNA processing mechanisms that control the expression of the splicing regulator SR30 in a light-dependent manner.Maturation of eukaryotic mRNAs involves intricate co-and posttranscriptional RNA processing, which has critical functions in regulating gene expression and diversifying the transcriptome. Among several mechanisms, alternative precursor mRNA splicing (AS) in particular generates many transcript variants by removing distinct intronic regions and joining the resulting exons. Deep analysis of transcriptomes via high-throughput RNA sequencing (RNA-seq) has revealed that a major fraction of all intron-containing genes from higher eukaryotes generates AS variants. In humans, more than 95% of multiexon genes display AS (Pan et al., 2008). The prevalence of AS has also been demonstrated for other eukaryotes including plants (Reddy et al., 2013;Staiger and Brown, 2013), with current estimates of ;61% and ;42% of intron-containing genes giving rise to AS variants in the model plants Arabidopsis (Arabidopsis thaliana;Marquez et al., 2012) and Brachypodium distachyon (Mandadi and Scholthof, 2015), respectively.Besides its pivotal role in increasing the coding and regulatory capacity of the transcriptome, AS finetunes gene expression by varying the output ratios of splicing variants. The full extent of AS regulation likely exceeds the current estimates, as the production of many transcript variants can be specifically controlled under certain conditions, such as cell and tissue types, developmental stages, and in response to stresses and other environmental factors (Reddy et al., 2013;Staige...

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RNA Binding Proteins RZ-1B and RZ-1C Play Critical Roles in Regulating Pre-mRNA Splicing and Gene Expression during Development in Arabidopsis

Cited by 77 publications

References 64 publications

Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes

Depletion of Arabidopsis SC35 and SC35-like serine/arginine-rich proteins affects the transcription and splicing of a subset of genes

The ALBA RNA-binding proteins function redundantly to promote growth and flowering in Arabidopsis

Subcellular Compartmentation of Alternatively Spliced Transcripts Defines SERINE/ARGININE-RICH PROTEIN30 Expression

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