skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The Landscape of RNA-Protein Interactions in Plants: Approaches and Current Status

Journal Article · · International Journal of Molecular Sciences (Online)
DOI:https://doi.org/10.3390/ijms22062845· OSTI ID:1851431
 [1];  [1]
  1. Colorado State Univ., Fort Collins, CO (United States). Dept. of Biology. Program in Cell and Molecular Biology

RNAs transmit information from DNA to encode proteins that perform all cellular processes and regulate gene expression in multiple ways. From the time of synthesis to degradation, RNA molecules are associated with proteins called RNA-binding proteins (RBPs). The RBPs play diverse roles in many aspects of gene expression including pre-mRNA processing and post-transcriptional and translational regulation. In the last decade, the application of modern techniques to identify RNA–protein interactions with individual proteins, RNAs, and the whole transcriptome has led to the discovery of a hidden landscape of these interactions in plants. Global approaches such as RNA interactome capture (RIC) to identify proteins that bind protein-coding transcripts have led to the identification of close to 2000 putative RBPs in plants. Interestingly, many of these were found to be metabolic enzymes with no known canonical RNA-binding domains. Here, we review the methods used to analyze RNA–protein interactions in plants thus far and highlight the understanding of plant RNA–protein interactions these techniques have provided us. We also review some recent protein-centric, RNA-centric, and global approaches developed with non-plant systems and discuss their potential application to plants. We also provide an overview of results from classical studies of RNA–protein interaction in plants and discuss the significance of the increasingly evident ubiquity of RNA–protein interactions for the study of gene regulation and RNA biology in plants.

Research Organization:
Colorado State Univ., Fort Collins, CO (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
Grant/Contract Number:
SC0010733; DBI-1949036; MCB-2014542
OSTI ID:
1851431
Journal Information:
International Journal of Molecular Sciences (Online), Vol. 22, Issue 6; ISSN 1422-0067
Publisher:
MDPICopyright Statement
Country of Publication:
United States
Language:
English

References (143)

RNA-Binding Proteins as Targets to Improve Salt Stress Tolerance in Crops journal February 2020
Uridylation of miRNAs by HEN1 SUPPRESSOR1 in Arabidopsis journal April 2012
The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA journal January 2003
Methods to study RNA–protein interactions journal February 2019
The Arabidopsis Nucleotidyl Transferase HESO1 Uridylates Unmethylated Small RNAs to Trigger Their Degradation journal April 2012
Dek42 encodes an RNA‐binding protein that affects alternative pre‐mRNA splicing and maize kernel development journal April 2019
irCLIP platform for efficient characterization of protein–RNA interactions journal April 2016
Laser microdissection of tomato fruit cell and tissue types for transcriptome profiling journal November 2016
UV crosslinked mRNA-binding proteins captured from leaf mesophyll protoplasts journal November 2016
RNA Chaperone Function of a Universal Stress Protein in Arabidopsis Confers Enhanced Cold Stress Tolerance in Plants journal November 2017
iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution journal July 2010
Arabidopsis DRB4 protein in antiviral defense against Turnip yellow mosaic virus infection: DRB4 function in antiviral defense journal October 2011
The Arabidopsis splicing regulator SR45 confers salt tolerance in a splice isoform-dependent manner journal April 2019
Plant Systems Biology at the Single-Cell Level journal November 2017
The RNA-binding protein repertoire of Arabidopsis thaliana journal July 2016
Regulation of Flowering Time by the RNA-Binding Proteins AtGRP7 and AtGRP8 journal May 2019
Dissecting plant defence signal transduction: modifiers of snc1 in Arabidopsis journal March 2010
Beyond CLIP: advances and opportunities to measure RBP–RNA and RNA–RNA interactions journal May 2019
uvCLAP is a fast and non-radioactive method to identify in vivo targets of RNA-binding proteins journal March 2018
A Global View of RNA-Protein Interactions Identifies Post-transcriptional Regulators of Root Hair Cell Fate journal April 2017
Regulation and function of SOC1, a flowering pathway integrator journal April 2010
sCLIP—an integrated platform to study RNA–protein interactomes in biomedical research: identification of CSTF2tau in alternative processing of small nuclear RNAs journal February 2017
Role of Arabidopsis Pumilio RNA binding protein 5 in virus infection journal May 2013
Systematic analysis of plant mitochondrial and chloroplast small RNAs suggests organelle-specific mRNA stabilization mechanisms journal May 2016
RNA Recognition by the MS2 Phage Coat Protein journal January 1997
Targeted Endoplasmic Reticulum Localization of Storage Protein mRNAs Requires the RNA-Binding Protein RBP-L journal January 2019
RNA Processing and Export journal October 2010
Discovering the RNA-Binding Proteome of Plant Leaves with an Improved RNA Interactome Capture Method journal April 2020
MOS2, a Protein Containing G-Patch and KOW Motifs, Is Essential for Innate Immunity in Arabidopsis thaliana journal November 2005
Searching for a Match: Structure, Function and Application of Sequence-Specific RNA-Binding Proteins journal May 2019
OsFKBP20‐1b interacts with the splicing factor OsSR45 and participates in the environmental stress response at the post‐transcriptional level in rice journal February 2020
Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms journal June 2007
The cyclin L homolog MOS12 and the MOS4-associated complex are required for the proper splicing of plant resistance genes: MOS12 and MAC in the splicing of R genes journal June 2012
Role of plant RNA-binding proteins in development, stress response and genome organization journal April 2009
AlSRG1, a novel gene encoding an RRM-type RNA-binding protein (RBP) from Aeluropus littoralis, confers salt and drought tolerance in transgenic tobacco journal June 2018
Pentatricopeptide Repeat Proteins in Plants journal April 2014
Nuclear Speckle RNA Binding Proteins Remodel Alternative Splicing and the Non-coding Arabidopsis Transcriptome to Regulate a Cross-Talk Between Auxin and Immune Responses journal August 2018
Genome-wide comparative analysis of RNA-binding Glycine-rich protein family genes between Gossypium arboreum and Gossypium raimondii journal June 2019
HPR1, a component of the THO/TREX complex, plays an important role in disease resistance and senescence in Arabidopsis: Disease resistance and senescence are affected by HPR1 journal December 2011
Plant RNA Interactome Capture: Revealing the Plant RBPome journal June 2017
Current approaches for RNA-labelling to identify RNA-binding proteins journal March 2019
Mass-spectrometry-based draft of the Arabidopsis proteome journal March 2020
CRISPR-assisted detection of RNA–protein interactions in living cells journal June 2020
Long Noncoding RNA Modulates Alternative Splicing Regulators in Arabidopsis journal July 2014
Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP journal April 2010
The Xist lncRNA Exploits Three-Dimensional Genome Architecture to Spread Across the X Chromosome journal July 2013
THO 2, a core member of the THO / TREX complex, is required for micro RNA production in Arabidopsis journal May 2015
RNA polymerase V transcription guides ARGONAUTE4 to chromatin journal April 2009
Plant polyadenylation factors: conservation and variety in the polyadenylation complex in plants journal November 2012
Interacting protein partners of Arabidopsis RNA-binding protein AtRBP45b journal January 2017
Physiological responses related to increased grain yield under drought in the first biotechnology‐derived drought‐tolerant maize journal November 2014
Zipcode RNA-Binding Proteins and Membrane Trafficking Proteins Cooperate to Transport Glutelin mRNAs in Rice Endosperm journal May 2020
A family of RRM-type RNA-binding proteins specific to plant mitochondria journal April 2002
RNA–protein interaction mapping via MS2- or Cas13-based APEX targeting journal August 2020
Two Prp19-Like U-Box Proteins in the MOS4-Associated Complex Play Redundant Roles in Plant Innate Immunity journal July 2009
Expression of Arabidopsis glycine-rich RNA-binding protein AtGRP2 or AtGRP7 improves grain yield of rice (Oryza sativa) under drought stress conditions journal January 2014
Analysis of long non-coding RNAs produced by a specialized RNA polymerase in Arabidopsis thaliana journal September 2013
A Putative Nucleoporin 96 Is Required for Both Basal Defense and Constitutive Resistance Responses Mediated by suppressor of npr1-1 , constitutive 1   journal April 2005
The RNA-binding protein FPA regulates flg22-triggered defense responses and transcription factor activity by alternative polyadenylation journal October 2013
RNA-Binding Proteins in Plant Immunity journal January 2011
Alternative polyadenylation of mRNA precursors journal September 2016
RNA Regulatory Elements and Polyadenylation in Plants journal January 2012
Adaptation of iCLIP to plants determines the binding landscape of the clock-regulated RNA-binding protein AtGRP7 journal October 2017
Global transcript profiling of transgenic plants constitutively overexpressing the RNA-binding protein AtGRP7 journal October 2010
Molecular Characterization, Expression Pattern and Function Analysis of Glycine-Rich Protein Genes Under Stresses in Chinese Cabbage (Brassica rapa L. ssp. pekinensis) journal July 2020
Systematic Discovery of Xist RNA Binding Proteins journal April 2015
Enod40 , a Short Open Reading Frame–Containing mRNA, Induces Cytoplasmic Localization of a Nuclear RNA Binding Protein in Medicago truncatula journal March 2004
Translational Repression and Specific RNA Binding by the Coat Protein of the Pseudomonas Phage PP7 journal June 2001
Alternative polyadenylation and gene expression regulation in plants: Polyadenylation and gene expression regulation journal November 2010
A nuclear-encoded chloroplast-targeted S1 RNA-binding domain protein affects chloroplast rRNA processing and is crucial for the normal growth of Arabidopsis thaliana journal June 2015
Integrative genome-wide analysis reveals HLP1, a novel RNA-binding protein, regulates plant flowering by targeting alternative polyadenylation journal June 2015
Capturing RNA–protein interaction via CRUIS journal March 2020
Alternative Splicing in Plant Genes: A Means of Regulating the Environmental Fitness of Plants journal February 2017
Transcriptome analyses reveal SR45 to be a neutral splicing regulator and a suppressor of innate immunity in Arabidopsis thaliana journal October 2017
The Arabidopsis SUPPRESSOR OF AUXIN RESISTANCE Proteins Are Nucleoporins with an Important Role in Hormone Signaling and Development journal June 2006
RNA as a long-distance information macromolecule in plants journal November 2001
dCLIP: a computational approach for comparative CLIP-seq analyses journal January 2014
Transgenic overexpression of UIP1, an interactor of the 3′ untranslated region of the Rubisco small subunit mRNA, increases rice tolerance to drought journal June 2012
Identification of an Arabidopsis thaliana protein that binds to tomato mosaic virus genomic RNA and inhibits its multiplication journal October 2008
In Planta Determination of the mRNA-Binding Proteome of Arabidopsis Etiolated Seedlings journal October 2016
Complexity of the Alternative Splicing Landscape in Plants journal October 2013
Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway: Characterization of the hot pepper PR-10 journal December 2003
The Spen Family Protein FPA Controls Alternative Cleavage and Polyadenylation of RNA journal February 2010
RNA-binding protein immunoprecipitation as a tool to investigate plant miRNA processing interference by regulatory proteins of diverse origin journal January 2018
Evolution of the Small Family of Alternative Splicing Modulators Nuclear Speckle RNA-Binding Proteins in Plants journal February 2020
Splitting aptamers and nucleic acid enzymes for the development of advanced biosensors journal February 2020
An Effector of RNA-Directed DNA Methylation in Arabidopsis Is an ARGONAUTE 4- and RNA-Binding Protein journal May 2009
Genomic Maps of Long Noncoding RNA Occupancy Reveal Principles of RNA-Chromatin Interactions journal November 2011
Molecular characterization and expression analysis of a glycine-rich RNA-binding protein gene from Malus hupehensis Rehd. journal July 2011
Changes in the Arabidopsis RNA-binding proteome reveal novel stress response mechanisms journal April 2019
Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress journal October 2005
The Arabidopsis RNA-Binding Protein AtRGGA Regulates Tolerance to Salt and Drought Stress journal March 2015
HITS‐CLIP: panoramic views of protein–RNA regulation in living cells journal July 2010
Robust transcriptome-wide discovery of RNA-binding protein binding sites with enhanced CLIP (eCLIP) journal March 2016
The increasing diversity and complexity of the RNA-binding protein repertoire in plants journal September 2020
Transcriptome-Wide Identification of RNA Targets of Arabidopsis SERINE/ARGININE-RICH45 Uncovers the Unexpected Roles of This RNA Binding Protein in RNA Processing journal November 2015
Drought Stress Causes Specific Changes to the Spliceosome and Stress Granule Components journal January 2020
Cold shock protein 1 chaperones mRNAs during translation in Arabidopsis thaliana journal May 2013
CLIP Identifies Nova-Regulated RNA Networks in the Brain journal November 2003
Bruno‐like proteins modulate flowering time via 3′ UTR‐dependent decay of SOC1 mRNA journal February 2013
mRNA Localization in Plant Cells journal October 2019
Comprehensive identification of RNA–protein interactions in any organism using orthogonal organic phase separation (OOPS) journal January 2019
RNA-Binding Protein RBP-P Is Required for Glutelin and Prolamine mRNA Localization in Rice Endosperm Cells journal September 2018
Bacterial RNA Chaperones Confer Abiotic Stress Tolerance in Plants and Improved Grain Yield in Maize under Water-Limited Conditions journal June 2008
β-Actin mRNA interactome mapping by proximity biotinylation journal June 2019
A SWI/SNF Chromatin-Remodeling Complex Acts in Noncoding RNA-Mediated Transcriptional Silencing journal January 2013
The REM phase of gene regulation journal August 2010
RNA-binding proteins and circadian rhythms in Arabidopsis thaliana journal November 2001
MOS11: A New Component in the mRNA Export Pathway journal December 2010
A Polypyrimidine Tract Binding Protein, Pumpkin RBP50, Forms the Basis of a Phloem-Mobile Ribonucleoprotein Complex journal January 2009
Widespread Translational Inhibition by Plant miRNAs and siRNAs journal May 2008
The Arabidopsis pentatricopeptide repeat protein PDM1 is associated with the intergenic sequence of S11-rpoA for rpoA monocistronic RNA cleavage journal May 2012
An RRM-containing mei2 -like MCT1 plays a negative role in the seed germination and seedling growth of Arabidopsis thaliana in the presence of ABA journal December 2016
Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts journal May 2009
Overexpression of the RNA binding protein MhYTP1 in transgenic apple enhances drought tolerance and WUE by improving ABA level under drought condition journal March 2019
Isolation and identification of cytoskeleton-associated prolamine mRNA binding proteins from developing rice seeds journal March 2010
A Chloroplast-targeted S1 RNA-binding Domain Protein Plays a Role in Arabidopsis Response to Diverse Abiotic Stresses journal February 2019
Aptamers: versatile molecular recognition probes for cancer detection journal January 2016
RNA-Binding Proteins Revisited – The Emerging Arabidopsis mRNA Interactome journal June 2017
Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors journal June 2019
Plant Glycine-Rich Proteins in Stress Response: An Emerging, Still Prospective Story journal March 2018
A Glycine-Rich RNA-Binding Protein, CsGR-RBP3, Is Involved in Defense Responses Against Cold Stress in Harvested Cucumber (Cucumis sativus L.) Fruit journal April 2018
Plant RNA binding proteins for control of RNA virus infection journal January 2013
A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity journal April 2007
Comparative analysis of RNA-binding proteomes under Arabidopsis thaliana-Pst DC3000-PAMP interaction by orthogonal organic phase separation journal October 2020
Evolution of Complex Target SELEX to Identify Aptamers against Mammalian Cell-Surface Antigens journal January 2017
Mechanistic implications of enhanced editing by a HyperTRIBE RNA-binding protein journal November 2017
Discovery of RNA-binding proteins and characterization of their dynamic responses by enhanced RNA interactome capture journal October 2018
RNA 3' processing functions of Arabidopsis FCA and FPA limit intergenic transcription journal May 2011
Overexpression of MpGR-RBP1, a glycine-rich RNA-binding protein gene from Malus prunifolia (Willd.) Borkh., confers salt stress tolerance and protects against oxidative stress in Arabidopsis journal July 2014
5′ UTR m6A Promotes Cap-Independent Translation journal November 2015
The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3 journal April 2015
Auto-regulation of the circadian slave oscillator component At GRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation journal December 2007
TRIBE: Hijacking an RNA-Editing Enzyme to Identify Cell-Specific Targets of RNA-Binding Proteins journal April 2016
PUMPKIN, the Sole Plastid UMP Kinase, Associates with Group II Introns and Alters Their Metabolism journal November 2018
Nanomolar binding affinity of quinine-based antimalarial compounds by the cocaine-binding aptamer journal November 2018
Heterologous expression of an RNA-binding protein affects flowering time as well as other developmental processes in Solanaceae journal May 2016
An ABA-regulated putative RNA-binding protein affects seed germination of Arabidopsis under ABA or abiotic stress conditions journal January 2013
Metabolic Enzymes Enjoying New Partnerships as RNA-Binding Proteins journal December 2015
CmRBP50 Protein Phosphorylation Is Essential for Assembly of a Stable Phloem-mobile High-affinity Ribonucleoprotein Complex journal July 2011
HITS-CLIP yields genome-wide insights into brain alternative RNA processing journal November 2008
The small glycine-rich RNA binding protein At GRP7 promotes floral transition in Arabidopsis thaliana: At GRP7 and the floral transition in A. thaliana journal June 2008
Current challenges and future perspectives of plant and agricultural biotechnology journal June 2015