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. 2023 Sep 1;35(9):3187-3204.
doi: 10.1093/plcell/koad127.

Stress-related biomolecular condensates in plants

Jorge Solis-Miranda  1 , Monika Chodasiewicz  2 , Aleksandra Skirycz  3 , Alisdair R Fernie  4 , Panagiotis N Moschou  5   6   7 , Peter V Bozhkov  8 , Emilio Gutierrez-Beltran  1   9
Affiliations

Stress-related biomolecular condensates in plants

Jorge Solis-Miranda et al. Plant Cell. .

Abstract

Biomolecular condensates are membraneless organelle-like structures that can concentrate molecules and often form through liquid-liquid phase separation. Biomolecular condensate assembly is tightly regulated by developmental and environmental cues. Although research on biomolecular condensates has intensified in the past 10 years, our current understanding of the molecular mechanisms and components underlying their formation remains in its infancy, especially in plants. However, recent studies have shown that the formation of biomolecular condensates may be central to plant acclimation to stress conditions. Here, we describe the mechanism, regulation, and properties of stress-related condensates in plants, focusing on stress granules and processing bodies, 2 of the most well-characterized biomolecular condensates. In this regard, we showcase the proteomes of stress granules and processing bodies in an attempt to suggest methods for elucidating the composition and function of biomolecular condensates. Finally, we discuss how biomolecular condensates modulate stress responses and how they might be used as targets for biotechnological efforts to improve stress tolerance.

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Conflict of interest statement

Conflict of interest: The authors declare no conflict of interest.

Figures

Figure 1.
Figure 1.
Diagram of the major principles underlying biomolecular condensate formation. A certain protein concentration (dependent on various factors, such as temperature, redox state, pH) enables homotypic or heterotypic interactions between sticker domains (e.g. protein 1–protein 2 interaction on the diagram). When reaching a system-specific threshold concentration (Cthreshold), the entire system undergoes phase separation into 2 phases. The “stickiness” (or multivalency) depends on the attraction between residues usually provided by so-called IDRs (e.g. PrLDs or LCDs). Phase separation driven by IDR–IDR interactions can be mediated by noncovalent interactions (boxed area) that include π (aromatic ring)–π, cation (+) –π, charge (−)–charge (+), dipole (±)–dipole (±), or hydrogen bonds (H). Folded domains or nucleic acids also mediate phase separation (e.g. protein 3 with an RNA-binding domain [RBD], in the diagram). Given enough time or at high concentrations, condensates may form filaments/aggregates with solid-like material properties. Created with BioRender.com.
Figure 2.
Figure 2.
Basic principles of LLPS in the assembly of SGs. SGs are believed to assemble through 3 major steps: (1) nucleation, (2) growth, and (3) shell assembly. Stress inhibits translation, which triggers release of mRNAs from the polysomes, which, together with RBPs, promotes nucleation via LLPS. Next, specific recruitment of additional SG components facilitates core growth (2) and thereafter shell assembly (3). The phase-separating biomolecules (usually proteins) can be categorized as scaffold or clients. In this figure, scaffold and client components are represented as spheres (green for scaffolds and blue for clients) with attractive sites on their surface (gray patches). Each patch (valency) allows a protein to participate in one attractive protein–protein or RNA–protein interaction. In the absence of stress, SG components may exist as preformed protein complexes (pre-existing or standby state) serving as seeds for rapid assembly (Gutierrez-Beltran et al. 2021). Upon stress, these complexes may facilitate the recruitment of RNAs and other proteins into phase-separated condensates that become microscopically discernible fluorescent foci if properly labeled. This phase separation may be modulated by posttranslational modifications. Created with BioRender.com.
Figure 3.
Figure 3.
Proteomic analysis of plant SGs and PBs. A) Venn diagram showing the extent of overlap among interactomes for 4 different SG-associated proteins (RGBD2/4, TSN2, RBP47, and CML38) under stress. B) A subset of common and specific interactors of the proteins in (A). C) Percentage of RNA-binding proteins found in the 4 interactomes. D) Protein–protein interaction networks among the RGBD2/4, TSN2, RBP47, and CML38 interactomes. E) Venn diagram showing the extent of overlap among interactomes for 4 different PB-associated proteins (DCP1, DCP2, DCP5, and UPF1) under stress. F) A subset of common and specific interactors of the proteins in (E). For complete lists of Arabidopsis SG and PB proteome components, see Supplemental Data Sets S1 and S2. G) Venn diagram showing the extent of overlap among plant, mammalian and yeast SG proteomes. H) Venn diagram showing the extent of overlap among plant, mammalian and yeast PB proteomes.
Figure 4.
Figure 4.
Crosstalk among plant SGs, PBs and siRNA bodies. A) Venn diagrams showing the extent of overlap among DCP1, DCP5 (both for PBs), and TSN2 (for SGs) interactomes under no-stress (NS) conditions (left) and between DCP1 and TSN2 interactomes under heat stress (HS). B) A subset of common and specific interactors of DCP1, DCP5, and TSN2 at the absence of stress. C) Diagram of the relationships among SGs, PBs, and siRNA bodies under no stress conditions and upon onset of stress. For complete lists of Arabidopsis SG and PB proteome components, see Supplemental Data Sets S1 and S2. Created with BioRender.com.
Figure 5.
Figure 5.
Biomolecular condensates play a key role in stress responses. A) The sequestration of transcription factors and regulators in condensates can regulate transcription, either promoting or inhibiting it. B) Condensates can either increase or decrease translation efficiency. C) Due to mass action, concentration of enzymes and substrates in the condensates can enhance catalysis or even allow formation of metabolons with improved efficiency. D) Condensates can inhibit enzymatic reactions and pathways in the dilute phase (e.g. cytosol) by sequestering enzymes, their ligands or substrates as well as metabolic intermediates. Inhibition of the reaction can also be achieved by separating different components of the common pathway (e.g. enzyme and substrate) via sequestration into different types of biomolecular condensates. Created with BioRender.com.
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