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Review
. 2021 Aug 9:12:722643.
doi: 10.3389/fpls.2021.722643. eCollection 2021.

Plant Stress Granules: Trends and Beyond

Affiliations
Review

Plant Stress Granules: Trends and Beyond

Israel Maruri-López et al. Front Plant Sci. .

Abstract

Stress granules (SGs) are dynamic membrane-less condensates transiently assembled through liquid-liquid phase separation (LLPS) in response to stress. SGs display a biphasic architecture constituted of core and shell phases. The core is a conserved SG fraction fundamental for its assembly and consists primarily of proteins with intrinsically disordered regions and RNA-binding domains, along with translational-related proteins. The shell fraction contains specific SG components that differ among species, cell type, and developmental stage and might include metabolic enzymes, receptors, transcription factors, untranslated mRNAs, and small molecules. SGs assembly positively correlates with stalled translation associated with stress responses playing a pivotal role during the adaptive cellular response, post-stress recovery, signaling, and metabolic rewire. After stress, SG disassembly releases mRNA and proteins to the cytoplasm to reactivate translation and reassume cell growth and development. However, under severe stress conditions or aberrant cellular behavior, SG dynamics are severely disturbed, affecting cellular homeostasis and leading to cell death in the most critical cases. The majority of research on SGs has focused on yeast and mammals as model organism. Nevertheless, the study of plant SGs has attracted attention in the last few years. Genetics studies and adapted techniques from other non-plant models, such as affinity capture coupled with multi-omics analyses, have enriched our understanding of SG composition in plants. Despite these efforts, the investigation of plant SGs is still an emerging field in plant biology research. In this review, we compile and discuss the accumulated progress of plant SGs regarding their composition, organization, dynamics, regulation, and their relation to other cytoplasmic foci. Lastly, we will explore the possible connections among the most exciting findings of SGs from mammalian, yeast, and plants, which might help provide a complete view of the biology of plant SGs in the future.

Keywords: RNA-binding domains; four-phase assembly model; intrinsically disordered regions; phase separation; plant stress granules; post-translational modifications; preexisting complex; small molecules.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Proposed model stress granule (SG) assembly and disassembly. Schematic representation of SG dynamics based on accumulated evidence of non-plant and plant models. (A) Preexisting protein network, experimental evidence revealed protein–protein interaction (PPI) networks of SG core proteins such as RNA-binding protein 47b (Rbp47), tudor staphylococcal nuclease (TSN), PAB4, and angustifolia (AN) proteins under non-stress conditions. (B) Stalled translation, a global reduction in translation under stress response generates an mRNA-ribonucleoprotein (mRNP) influx essential for SG assembly. (C) Nucleation, high concentrations of mRNP induce liquid–liquid phase separation (LLPS) of mRNP complexes. (D) Core growth, the recruitment of additional SG components to nucleated mRNP drives the establishment of visible core structures; this phase is an ATP- and microtubule (MT)-dependent process. (E) Shell growth phase, once the core structure is defined, additional mRNPs, specific proteins, small molecules, nucleotides, amino acids, and phospholipids are recruited as shell components. (F) Fusion phase, after the formation of individual SGs, fusion events with adjacent SGs take place to assemble a multicore structure immersed in a single shell. (G) SG disassembly occurs after stress during the recovery period. The SGs begin with shell dissociation, followed by the core disassembly, the ATP-dependent remodeling complexes are crucial in this step. The upper box denotes the elements presents in the scheme. Posttranslational modifications (PTMs) and RNA modifications: Ub, ubiquitination; M, methylation; P, phosphorylation; S, SUMOylation; Par, PARylation. Dashed lines indicate confirmed evidence in non-plant models that could also occur in plants but is not yet explored. Created with BioRender.com.
FIGURE 2
FIGURE 2
Role of PTMs in the four-phase SG assembles model. SG nucleation assembly is described on the function of concentration and combination of either protein–protein, RNA–RNA interactions, or protein–RNA interactions. The evidence indicates the presence of preexisting complex under non-stress conditions. In line with this finding, we suggested this complex as a steady–ready interaction in the first step in the four-phase model, where PTMs and RNA modifications might function as a signal to regulate oligomerization, structure, subcellular localization, and protein functions, these evoked changes on SG components could modulate SG assembly or disassembly, independent of concentration. Modified from Van Treeck and Parker (2018). Created with BioRender.com.

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