Structural basis of nucleic acid binding by<i>Nicotiana tabacum</i>glycine-rich RNA-binding protein: implications for its RNA chaperone function

Khan, Feroz; Daniëls, Mark A.; Folkers, Gert E.; Boelens, Rolf; Naqvi, Syed Muhammad Saqlan; Ingen, Hugo van

doi:10.1093/nar/gku468

Cited by 22 publications

(31 citation statements)

References 51 publications

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“…Deletion of AtGR-RBP7 leads to low-temperature sensitive phenotypes, highlighting its role in optimal plant adjustment to cold stress [245]. NMR analysis confirms the structural disorder of the GR domain for NtGR-RBP1, an AtGR-RBP7 orthologue from Nicotiana tabacum [246]. As expected, NtGR-RBP1 is shown to bind RNA and single stranded DNA through the RRM.…”

Section: Glycine Rich-rna Binding Proteins (Gr-rbps)supporting

confidence: 66%

“…Furthermore, the NtGR-RBP1 GR interacts transiently with its RRM domain, promoting self-association to effectively increase its local concentration and hence its affinity for nucleic acids. These findings suggest a mechanism for the unfolding of nonnative structures in RNA by NtGR-RBP1, which may be involved in enhancing its RNA chaperone activity [246].…”

Section: Glycine Rich-rna Binding Proteins (Gr-rbps)mentioning

confidence: 81%

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Structural disorder in plant proteins: where plasticity meets sessility

Covarrubias

Cuevas-Velazquez

Romero-Pérez

et al. 2017

Cell. Mol. Life Sci.

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Plants are sessile organisms. This intriguing nature provokes the question of how they survive despite the continual perturbations caused by their constantly changing environment. The large amount of knowledge accumulated to date demonstrates the fascinating dynamic and plastic mechanisms, which underpin the diverse strategies selected in plants in response to the fluctuating environment. This phenotypic plasticity requires an efficient integration of external cues to their growth and developmental programs that can only be achieved through the dynamic and interactive coordination of various signaling networks. Given the versatility of intrinsic structural disorder within proteins, this feature appears as one of the leading characters of such complex functional circuits, critical for plant adaptation and survival in their wild habitats. In this review, we present information of those intrinsically disordered proteins (IDPs) from plants for which their high level of predicted structural disorder has been correlated with a particular function, or where there is experimental evidence linking this structural feature with its protein function. Using examples of plant IDPs involved in the control of cell cycle, metabolism, hormonal signaling and regulation of gene expression, development and responses to stress, we demonstrate the critical importance of IDPs throughout the life of the plant.

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Section: Glycine Rich-rna Binding Proteins (Gr-rbps)supporting

confidence: 66%

Section: Glycine Rich-rna Binding Proteins (Gr-rbps)mentioning

confidence: 81%

Structural disorder in plant proteins: where plasticity meets sessility

Covarrubias

Cuevas-Velazquez

Romero-Pérez

et al. 2017

Cell. Mol. Life Sci.

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“…The interaction between ORRM4 and ORRM3 was shown to be mediated by the C-terminal GR domain of ORRM4. NMR studies of NtGR-RBP1, which contains an N-terminal RRM domain and a C-terminal GR domain like ORRM4, show that the GR domain is responsible for mediating self-association by transient interactions with its RRM domain (NtRRM; Khan et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

RNA Recognition Motif-Containing Protein ORRM4 Broadly Affects Mitochondrial RNA Editing and Impacts Plant Development and Flowering

et al. 2015

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Plant RNA editosomes modify cytidines (C) to uridines (U) at specific sites in plastid and mitochondrial transcripts. Members of the RNA-editing factor interacting protein (RIP) family and Organelle RNA Recognition Motif-containing (ORRM) family are essential components of the Arabidopsis (Arabidopsis thaliana) editosome. ORRM2 and ORRM3 have been recently identified as minor mitochondrial editing factors whose silencing reduces editing efficiency at ;6% of the mitochondrial C targets. Here we report the identification of ORRM4 (for organelle RRM protein 4) as a novel, major mitochondrial editing factor that controls ;44% of the mitochondrial editing sites. C-to-U conversion is reduced, but not eliminated completely, at the affected sites. The orrm4 mutant exhibits slower growth and delayed flowering time. ORRM4 affects editing in a site-specific way, though orrm4 mutation affects editing of the entire transcript of certain genes. ORRM4 contains an RRM domain at the N terminus and a Gly-rich domain at the C terminus. The RRM domain provides the editing activity of ORRM4, whereas the Gly-rich domain is required for its interaction with ORRM3 and with itself. The presence of ORRM4 in the editosome is further supported by its interaction with RIP1 in a bimolecular fluorescence complementation assay. The identification of ORRM4 as a major mitochondrial editing factor further expands our knowledge of the composition of the RNA editosome and reveals that adequate mitochondrial editing is necessary for normal plant development.

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“…While the structural architectures of several eukaryotic RRM-containing proteins have been reported, 20 − 22 our structural and functional understanding of plant RRM and plant glycine-rich RNA-binding proteins is less well developed. To this date, the three-dimensional (3D) structures of only two plant-derived GR-RBPs have been reported, 23 , 24 and none from barley. The present work is the first structural report of a barley GR-RBP protein.…”

mentioning

confidence: 99%

“…Moreover, protein–protein interactions were detected using NMR chemical shift perturbation experiments between the RRM and GR domains of Hv GR-RBP1, suggesting that at least in vitro , these two domains self-associate, results that are consistent with what has been observed for the Nicotiana tabacum Nt GR-RBP1 protein. 24 Nucleic acid interaction assays indicated that the GR domain of Hv GR-RBP1 can bind to single-stranded RNA (ssRNA) in the absence of the RRM domain. As anticipated based on the Hv GR-RBP1 sequence similarity to the Nicotiana tabacum Nt GR-RBP1 protein and a recent report by Khan et al, 24 1 H/ 15 N chemical shift perturbation experiments established that the N-terminal RRM domain of Hv GR-RBP1 can bind, albeit weakly, to a 6-nucleotide single-stranded DNA fragment containing the consensus sequence 5′-TTCTGX-3′, a DNA equivalent of the 5′-UUCUGA-3′ RNA sequence previously identified as a key nucleotide binding motif for the Arabidopsis protein At GRP7.…”

mentioning

confidence: 99%

Structural and Biochemical Analysis of the Hordeum vulgare L. HvGR-RBP1 Protein, a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley Plant Development and Stress Response

et al. 2014

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The timing of whole-plant senescence influences important agricultural traits such as yield and grain protein content. Post-transcriptional regulation by plant RNA-binding proteins is essential for proper control of gene expression, development, and stress responses. Here, we report the three-dimensional solution NMR structure and nucleic acid-binding properties of the barley glycine-rich RNA-binding protein HvGR-RBP1, whose transcript has been identified as being >45-fold up-regulated in early—as compared to late—senescing near-isogenic barley germplasm. NMR analysis reveals that HvGR-RBP1 is a multidomain protein comprising a well-folded N-terminal RNA Recognition Motif (RRM) and a structurally disordered C-terminal glycine-rich domain. Chemical shift differences observed in 2D 1H–15N correlation (HSQC) NMR spectra of full-length HvGR-RBP1 and N-HvGR-RBP1 (RRM domain only) suggest that the two domains can interact both in-trans and intramolecularly, similar to what is observed in the tobacco NtGR-RBP1 protein. Further, we show that the RRM domain of HvGR-RBP1 binds single-stranded DNA nucleotide fragments containing the consensus nucleotide sequence 5′-TTCTGX-3′ with low micromolar affinity in vitro. We also demonstrate that the C-terminal glycine-rich (HvGR) domain of Hv-GR-RBP1 can interact nonspecifically with ssRNA in vitro. Structural similarities with other plant glycine-rich RNA-binding proteins suggest that HvGR-RBP1 may be multifunctional. Based on gene expression analysis following cold stress in barley and E. coli growth studies following cold shock treatment, we conclude that HvGR-RBP1 functions in a manner similar to cold-shock proteins and harbors RNA chaperone activity. HvGR-RBP1 is therefore not only involved in the regulation of barley development including senescence, but also functions in plant responses to environmental stress.

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Structural basis of nucleic acid binding byNicotiana tabacumglycine-rich RNA-binding protein: implications for its RNA chaperone function

Cited by 22 publications

References 51 publications

Structural disorder in plant proteins: where plasticity meets sessility

Structural disorder in plant proteins: where plasticity meets sessility

RNA Recognition Motif-Containing Protein ORRM4 Broadly Affects Mitochondrial RNA Editing and Impacts Plant Development and Flowering

Structural and Biochemical Analysis of the Hordeum vulgare L. HvGR-RBP1 Protein, a Glycine-Rich RNA-Binding Protein Involved in the Regulation of Barley Plant Development and Stress Response

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