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Dynamics and Functions of Stress Granules and Processing Bodies in Plants

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Dynamics and Functions of Stress Granules and Processing Bodies in Plants plants Review Dynamics and Functions of Stress Granules and Processing Bodies in Plants 1, 2 1, Geng-Jen Jang y, Jyan-Chyun Jang and Shu-Hsing Wu * 1 Institute of Plant and Microbial Biology, Academia Sinica, Taipei 11529, Taiwan; [email protected] 2 Department of Horticulture and Crop Science, Department of Molecular Genetics, Center for Applied Plant Sciences, Center for RNA Biology, Ohio State University, Columbus, OH 43210, USA; [email protected] * Correspondence: [email protected]; Tel.: +886-2-2787-1178 Current address: Department of Cell and Developmental Biology, John Innes Centre, Norwich Research y Park, Norwich NR4 7UH, UK. Received: 14 July 2020; Accepted: 26 August 2020; Published: 30 August 2020 Abstract: RNA granules, such as stress granules and processing bodies, can balance the storage, degradation, and translation of mRNAs in diverse eukaryotic organisms. The sessile nature of plants demands highly versatile strategies to respond to environmental fluctuations. In this review, we discuss recent findings of the dynamics and functions of these RNA granules in plants undergoing developmental reprogramming or responding to environmental stresses. Special foci include the dynamic assembly, disassembly, and regulatory roles of these RNA granules in determining the fate of mRNAs. Keywords: stress granules; processing bodies; mRNA decay; translation 1. Introduction A healthy balance of mRNA destinies, including decay, translation, and sequestration, is crucial for plants to optimize growth and development and combat biotic/abiotic environmental stresses. A plethora of mechanisms are responsible for mRNAs destined for degradation, including de-adenylation of the polyA tail and mRNA decapping followed by 50 to 30 decay, 30 to 50 mRNA decay, and co-translational decay [1,2]. The translation control of mRNAs often involves the formation of mRNA–ribonucleoprotein (mRNP) complexes, namely ribosomes/polysomes, and membraneless RNA granules formed via liquid–liquid phase separation (LLPS). LLPS is often triggered by proteins with intrinsically disordered regions that induce the aggregation of complex proteins or protein–RNA networks, such as stress granules (SGs) or processing bodies (p-bodies) [3,4]. SGs function primarily to store mRNA–ribosome complexes to halt translation, whereas functions of p-body components have been implicated in both mRNA decay and translation repression [5]. The protein constituents of SGs and p-bodies have been previously reviewed [6,7]. Briefly, in plants, p-bodies contain many RNA-binding proteins (RBPs) and key factors for mRNAs decay, including decapping complexes, 50 to 30 exoribonuclease, de-adenylation factors, small-RNA-dependent slicer protein Argonaute1, and factors involved in nonsense-mediated mRNA decay [7]. SGs are composed of polyadenylated mRNAs, translation initiating factors, the 40S ribosome subunit, RNA-binding proteins, and regulators of gene silencing [6]. A recent study involving the affinity purification of proteins and metabolites co-purified with the GFP-tagged SG marker Rbp47b has significantly expanded the protein repertoire of plant SGs [8]. In addition to the conserved components for SG assembly and dynamics, this study also discovered important regulators and stress-related proteins associated with SGs, including a key cell-cycle regulator cyclin-dependent kinase A. Intriguingly, this study also identified SG-associated metabolites, nucleotides, amino acids, and phospholipids, implying that SGs Plants 2020, 9, 1122; doi:10.3390/plants9091122 www.mdpi.com/journal/plants Plants 2020, 9, x FOR PEER REVIEW 2 of 12 and phospholipids, implying that SGs can also sequester small molecules [8]. Given that the Plants 2020, 9, 1122 2 of 11 composition of both SGs and p-bodies has been reviewed recently [6], the current review focuses on the recent advancements of the dynamic formation and functions of these two types of RNA granules canin plants. also sequester small molecules [8]. Given that the composition of both SGs and p-bodies has been reviewed recently [6], the current review focuses on the recent advancements of the dynamic formation and2. Stress functions Granules of these two types of RNA granules in plants. SGs are membraneless organelles composed of proteins and translationally repressed mRNAs 2. Stress Granules [9,10]. SGs are conserved in eukaryotes such as yeast, plants, and mammals [11–13]. In general, SGs are assembledSGs are membranelesswhen organisms organelles face stresses composed and are often of proteins disassembled and translationallyduring recovery repressed from the mRNAsstress condition,[9,10]. SGs which are conserved is accompanied in eukaryotes by the such restor asation yeast, of plants, active and translation. mammals [In11 plants,–13]. In multiple general, SGsstresses are assembled(heat, hypoxia, when high organisms salt, and face darkness), stresses and oxidative are often phosphorylation disassembled during inhibitors recovery (arsenite, from thepotassium stress condition, cyanide, whichand myxothiazol), is accompanied and by methyl the restoration jasmonate of can active trigger translation. the formation In plants, of multipleSGs [14– stresses18]. (heat, hypoxia, high salt, and darkness), oxidative phosphorylation inhibitors (arsenite, potassiumThe formation cyanide, and and myxothiazol), functions of and SGs methyl under jasmonate heat and can hypoxia trigger the stresses formation have of SGsbeen [14 better–18]. characterizedThe formation and are and summarized functions of SGsbelow. under heat and hypoxia stresses have been better characterized and are summarized below. 2.1. SG and Heat Stress 2.1. SG and Heat Stress When cells are exposed to high temperature stress, some proteins undergo misfolding and aggregation.When cells In areplant exposed cells, toheat high shock temperature proteins stress, (HSPs), some including proteins undergothe low-molecular-mass misfolding and aggregation.chaperones, InHSP70 plant and cells, HSP100, heat shock function proteins together (HSPs), to including interact with the low-molecular-mass denatured proteins chaperones, to prevent HSP70their aggregation and HSP100, and function to disaggregate togetherto and interact refold with the misfolded denatured proteins proteins [19]. to prevent On the their other aggregation hand, SGs andcomposed to disaggregate of mRNAs and and refold translation the misfolded initiation proteins factor eIF4E [19]. Onwere the observed other hand, in tomato SGs composed culture cells of mRNAswithin 30 and min translation of heat shock initiation treatment factor [17] eIF4E (Figure were observed1a). Under in heat tomato stress, culture translation cells within is stalled, 30 min and of heatpre-existing shock treatment mRNAs [ 17are] (Figuretemporarily1a). Under stored heat in SGs stress, to translationreduce the isprotein stalled, influx and pre-existingthat can be a mRNAs burden areto cells temporarily under heat stored stress. in SGs to reduce the protein influx that can be a burden to cells under heat stress. FigureFigure 1.1. Stress granule dynamics and functionsfunctions inin translationtranslation repressionrepression inin responseresponse toto abioticabiotic stresses.stresses. ((aa)) StressStress granulesgranules markedmarked withwith eIF4EeIF4E formedformed afterafter 3030 minmin ofof heatheat stressstress inin tomatotomato cellscells [[17].17]. ((bb)) StressStress granulesgranules markedmarked withwith RFP-PABP2RFP-PABP2 thatthat accumulatedaccumulated afterafter 1-h1-h heatheat treatmenttreatment andand decreaseddecreased afterafter aa 2-h2-h recoveryrecovery atat 2222◦ °CC fromfrom heatheat stressstress in in Arabidopsis Arabidopsisroots roots [ 20[20].]. (c(c)) UBP1C-containing UBP1C-containing stressstress granulesgranules assembledassembled in in response response to to hypoxia hypoxia stress stress in Arabidopsisin Arabidopsis leaves leaves [16]. [16]. Note Note that that the UBP1C-GFPthe UBP1C- subcellularGFP subcellular localization localization pattern pattern changed changed from the from diffused the distributiondiffused distribution in the nucleus in the and nucleus cytoplasm and tocytoplasm stress granules to stress under granules hypoxia. under For hypoxia. each subfigure, For each the uppersubfigure, panels the illustrate upper panels the localizations illustrate the of SGslocalizations within respective of SGs within cells/tissues respective under cells/tissues mock (control), under stress mock (heat, (control), hypoxia), stress or recovery (heat, hypoxia), conditions. or Therecovery lower conditions. panels are graphicalThe lower representations panels are graphical of mRNA representations destinies correlating of mRNA with destinies the functions correlating of SGs.with 4E:the eIF4Efunctions foci; R:of ribosome;SGs. 4E: eIF4E TR: translating foci; R: ribosome; mRNA; TR: NTR: translating non-translating mRNA; mRNA NTR: associatednon-translating with themRNA stress associated granule (SG); with PABP2: the stress RFP-PABP2 granule (SG); foci; PABP2: N: nucleus; RFP-PABP2 U: UBP1C-GFP foci; N: focus.nucleus; U: UBP1C-GFP focus. SGs often disassemble when recovering from stress conditions. For example, SGs were visualized by RFP-taggedSGs often SG disassemble marker polyA-binding when recovering protein from 2 (PABP2) stress after conditions. 1-h heat treatmentFor example, (37 ◦C), SGs and were the SGvisualized signals wereby RFP-tagged reduced with SG amark 2-her recovery polyA-binding from heat protein stress [220 (PABP2] (Figure) after1b). In1-h
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