Protein Disorder in Plant Stress Adaptation: History
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An-Shan Hsiao

Global climate change has caused severe abiotic and biotic stresses, affecting plant growth and food security. The mechanical understanding of plant stress responses is critical for achieving sustainable agriculture. Intrinsically disordered proteins (IDPs) are a group of proteins without unique three-dimensional structures. The environmental sensitivity and structural flexibility of IDPs contribute to the growth and developmental plasticity for sessile plants to deal with environmental challenges.

  • intrinsically disordered proteins (IDPs)
  • stress response
  • liquid–liquid phase separation (LLPS)

1. Introduction

Human activities have released large amounts of greenhouse gases into the atmosphere, causing climate change [1]. Global climate change is the main cause of abiotic and biotic stresses for plants that include flooding, drought, heat, cold, salinity, pests, and microbes [2]. These environmental stresses have greatly influenced plant physiological processes and have adverse effects on agriculture productivity [2][3]. To tackle the environmental stresses, sessile plants have evolved multiple processes including stress sensing, hormone regulation, signal transduction, gene expression, and regulatory pathways to adjust growth and development in a spatiotemporal manner [4][5]. Understanding the mechanism of plant stress adaptation to adverse environmental conditions will open new opportunities for agricultural applications and global food security.
Intrinsically disordered proteins (IDPs) are a group of proteins natively lacking defined three-dimensional structures. The peculiarities of their amino acid sequences are known to be depleted in order-promoting residues (tryptophan, cysteine, tyrosine, isoleucine, phenylalanine, valine, asparagine, and leucine) and enriched in disorder-promoting residues (arginine, proline, glutamine, glycine, glutamate, serine, alanine, and lysine) [6][7]. The amino acid biases contribute their exceptional spatiotemporal heterogeneity and low conformational stability, which drive their atypical response to changing environments [6][7]. IDPs can gain structures in the presence of various osmolytes, under the changes in temperature and pH, and perform a disorder-to-order transition when interacting with binding partners (i.e., cellular membranes, proteins, metal ions, and DNA) [6][7][8][9][10]. These features allow IDPs to sense environmental changes, mediate corresponding signalling pathways, and control and fine-tune plant metabolism in response to light, mechanical forces, pH, redox potential, and drought/salt concentration [11][12][13]. Thus, IDPs are thought to play critical roles in dynamic and plastic responses for the survival of sessile plants under the constantly changing environment [14][15][16].
The great importance of IDPs in stress adaptation is shown by extremophiles (i.e., anhydrobiotic tardigrades and resurrection plants) exhibiting extreme tolerance to various environmental stressors. Tardigrades survive in adverse environments via a set of highly disordered proteins that protect biomaterial through vitrification [17][18]. Two plants with relatively high protein disorder abundance, resurrection grass (Oropetium thomaeum) and switch grass (Panicum virgatum), are both stress-tolerant [19]. A proteomics analysis revealed that various IDPs were induced in the resurrection plant Haberlea rhodopensis during stress responses [20], whereas IDPs in wheat and barley are mainly involved in regulating cellular and biological processes in response to stress [21]. The function of IDPs in protecting biomolecules under stress conditions has been proposed [22], but the precise mechanisms of their action are still largely unknown.
Intrinsically disordered regions (IDRs) of transcription factors are highly adaptive and are proposed to provide functional versatility in molecular recognition via their binding plasticity [22][23][24]. IDRs can also serve as signalling hubs that regulate a diverse array of signal transduction pathways [9][25]. IDPs/IDRs are key triggers of liquid–liquid phase separation (LLPS) to form biomolecular condensates, which allow the spatiotemporal organization of biochemical reactions by concentrating macromolecules locally [26][27]. In animal cells, biomolecular condensates contribute to the biogenesis of macromolecular machineries essential for gene expression, the sequestration of specific factors to regulate cellular processes, and the interconnection of various diseases and innate immunity [28][29]. Recent studies revealed that plant biomolecular condensates driven by IDRs switch the defence programming through sequestration and regulate translation and protein quality control machineries in the plant immune response [30][31][32]. The study of LLPS is still an emerging area in plant research [33], and future research providing more mechanistic insights into how LLPS is involved in plant stress adaptation is expected.

2. Late Embryogenesis Abundant (LEA) Proteins Confer Abiotic Stress Tolerance

Plant seeds are desiccation-tolerant organs and physiologically similar to anhydrobiosis [34]. During the late stages of seed maturation, a group of IDPs known as LEA proteins are highly expressed in plant seeds before they enter the desiccation phase [35][36]. LEA proteins are thought to be involved in desiccation tolerance by modulating various clients [10][35][36][37]. LEA proteins are widely studied in model and crop plants such as rice, tomato, and Arabidopsis. There are 34, 60, and 51 LEA genes identified in rice [38], tomato [39], and Arabidopsis [40], respectively. LEA genes in plants are non-randomly distributed within the chromosomes, and segmental and tandem duplications drive LEA gene expansion in the genome during evolution [39][41][42].
Most LEA genes have elements responding to abscisic acid (ABA) and/or a low temperature in their promoter regions, such as ABA response elements (ABREs) and C-repeats (CRTs), which agrees well with LEA genes being induced by abiotic stresses such as drought, salinity, heat, and freezing in vegetative tissues [40]. Drought and salinity stresses trigger ABA signalling, whereas sucrose-nonfermenting-1-related protein kinases (SnRK2s) function upstream of the transcription factors ABA-INSENSITIVE 3 (ABI3), ABI5, and ABFs (ABA-responsive element-binding factors) to regulate the LEA gene expression via ABRE [43][44]. Cold stress activates calcium signalling and the mitogen-activated protein kinase cascade pathway, whereas CBFs (C-repeat binding factors) regulate the expression of the group 2 LEA dehydrins via CRT [44]. Most LEA proteins are part of a more widespread group of proteins called “hydrophilins”, which are desiccation-related IDPs and have been discovered in archeal, eubacterial, and eukaryotic domains, including yeast, nematodes, tardigrades, and plants [34][45][46][47]. Hydrophilins are proposed to be stress effectors against desiccation in anhydrobiotes [48]; therefore, it is not surprising that LEA proteins are often involved in various stress responses such as desiccation resistance in plants [37][44][49].
There are several well-known examples of LEA proteins in stress responses. Arabidopsis dehydrins EARLY RESPONSE TO DEHYDRATION 10 (ERD10) and ERD14 function as chaperones to protect cells under a high salinity, drought, and low temperature [50]; LOW-TEMPERATURE-INDUCED 30 (Lti30) protects the membrane during cold and dehydration stress [51][52]; the group 3 LEA protein COLD-REGULATED 15A (COR15A) confers freezing tolerance by interacting with the membrane [53]; and legume physiologically mature (PM) proteins, which belong to various LEA groups, function in abiotic stress tolerance [54][55][56]. Their proposed mechanism is discussed in the following sections. Besides the reviews summarizing dehydrins in abiotic stress tolerance in various plant species [44][49], recent reports showed that heterologous expression of XsLEA1-8 from the monocot resurrection plant Xerophyta schlechteri [57], MsLEA-D34 from alfalfa (Medicago sativa L.) [58], and dehydrin CdDHN4 from bermudagrass (Cynodon dactylon × Cynodon transvaalensis) [59] increased osmotic and salt tolerance in Arabidopsis. These reports suggest that in general, stress-responsive LEA proteins confer stress tolerance among different plant species.
The analysis of LEA proteins in Arabidopsis, tomato, and orchid revealed their wide subcellular distribution [41][60][61]. Experimental data showed Arabidopsis LEA proteins localized to the cytosol, nucleus, mitochondria, plastid, ER, and pexophagosome [60]. Most of the tomato LEA proteins were predicted to target the nucleus or cytoplasm, with some in the mitochondria, chloroplasts, or extracellular matrix [41]. As well, subcellular localization prediction indicated that orchid LEA proteins are located in the nucleus, cytoplasm, chloroplasts, and mitochondria [61]. LEA proteins are proposed to protect the integrity of membranes and the activity of enzymes and biomolecules under stress conditions [22]. Therefore, their ubiquitous expression might provide protection to the corresponding membranes of various organelles as well as enzymes and sequestering targets localized in different cellular compartments under certain stress conditions [35][60]. Multiple cellular locations were also observed in another IDP, the Stress and Growth Interconnector (SGI), from the oil crop rapeseed (Brassica napus), which enhanced biomass and yield under drought conditions via multifaceted interactions with catalases and dehydrins [62]. A wheat IDP, the Triticum aestivum Fusarium Resistance Orphan Gene (TaFROG), showed spatial transition by changing its nucleus localization to cytosolic bodies when interacting with SnRK1 [63]. Thus, the spatial flexibility of IDPs implies their versatile functions in dual/multiple subcellular localizations.

3. Roles of LLPS in Plant Stress Responses

Disordered proteins have phase transition properties for undergoing LLPS and forming membrane-less biomolecular condensates. These properties enable a rapid assembly, disassembly, and concentration of cellular components and facilitate the dynamic formation of local reaction centres with spatiotemporal specificity [27][64]. Notably, LLPS is also involved in plant developmental phase transition such as flowering and seed germination [11]. The FLOWERING CONTROL LOCUS A (FCA) nuclear body driven by highly disordered FLX-LIKE 2 (FLL2) plays a role in transcriptional regulation to control flowering [65]. Stress granules are among the well-studied membrane-less condensates transiently assembled via LLPS in response to stress [66][67], whereas LLPS is induced when plants encounter various abiotic stresses such as a high temperature (35 °C and 37 °C) [68][69], a low temperature (4 °C) [70], salinity (0.4 M NaCl treatment) [71], and ROS (1 mM H2O2) [72]. LLPS driven by the IDR of phytochrome B (phyB) plays a major role in temperature sensing and thermomorphogenesis, suggesting an emerging mechanism for plants to directly respond to thermal changes [73]. A plant-specific prion-like protein was named FLOE1, the definition of floe being “a sheet of floating ice”, which is a phase-separated body of water [74]. Upon hydration, LLPS of intrinsically disordered FLOE1 allowed the embryo to sense water stress and promoted seed germination [74]. The importance of LLPS in the osmotic stress response was shown by the Arabidopsis transcriptional regulator SEUSS (SEU). The IDR of SEU is responsible for forming liquid-like nuclear condensates, which is indispensable for osmotic stress tolerance [75]. Unlike the well-established mechanism of FCA nuclear condensates in transcriptional control of flowering, researchers do not know whether the components of SEU nuclear condensates contain multiple active transcription regulators for promoting the transcription of osmotic stress-responsive genes.
Besides the aforementioned abiotic stress responses, LLPS is also involved in the biotic stress response as an interacting hub in plant immunity. LLPS is induced by bacterial phytopathogens Pseudomonas syringae pv. Maculicola ES4326 and P. syringae pv. tomato DC3000 as shown by the case of guanylate-binding protein (GBP)-like GTPases (GBPLs) [76]. The IDR of GBPLs is required for the assembly of LLPS-driven condensates within the nucleus and they are called GBPL defence-activated condensates, which coordinate defence-gene transcription for disease resistance [76]. The IDR of the salicylic acid receptor NONEXPRESSOR-OF-PATHOGENESIS-RELATED GENE 1 (NPR1) forms cytoplasmic condensates and serves as an interacting hub to sequester and degrade proteins involved in programmed cell death in infection-adjacent cells with a low pathogen load [30]. LLPS of NPR1 plays a role in switching cellular programming from effector-triggered immunity (ETI) in infected cells to systemic acquired resistance in adjacent cells [30]. A recent report highlighted the importance of LLPS in regulating translational reprogramming in plant immunity [32]. Arabidopsis HEM1 (named for heme biosynthesis in the yeast homologue) contains a plant-specific IDR called the low-complexity domain, which undergoes LLPS to form condensates to interact with translation factors, thus suppressing translation efficiency of the pro-death immune genes during ETI [32]. Although the interaction of HEM1 with NPR1 in the cytoplasmic condensates has not been detected [32], both cases suggest a common role of LLPS in balancing tissue health and disease resistance during the plant immune response.
Protein disorder has a versatile contribution to both the plant immune system and pathogen virulence [77][78]. The N-terminal IDR of prosystemin, the 200-aa precursor of the peptidic hormone systemin responding to wounding and herbivore attack, was able to induce defence-related genes and protect tomato plants against Botrytis cinerea and Spodoptera littoralis larvae [79]. In the plant defence response, RPM1-INTERACTING PROTEIN 4 (RIN4) is a negative regulator and targeted by multiple bacteria effectors [80][81][82]. The IDR of RIN4 was known to fold various conformations when interacting with different partners such as bacterial effectors and be under regulation of post-translational modification [83][84][85][86]. The latest report suggested that the intrinsically disordered nature of RIN4 provides a flexible platform to broaden pathogen recognition specificity by establishing compatibility with otherwise incompatible leucine-rich repeat immune receptor proteins [87][88]. Besides its involvement in plant immunity responses, LLPS is involved in pathogen virulence. The IDR of FgRpd3 (reduced potassium dependency 3) from wheat head blight fungus Fusarium graminearumis undergoes LLPS, which assists its interaction with inhibitor of growth (ING) proteins for regulating histone deacetylation and gene expression, thus affecting fungal development and pathogenicity [89].
Achieving the necessary spatiotemporal resolution to deduce the parameters that govern the assembly and behaviour of LLPS is challenging [90], especially when it involves the dynamics and multiple subcellular locations of IDPs (i.e., LEA proteins). Therefore, as compared with extensive studies of plant LEA proteins in stress tolerance, much less research has investigated plant LEA proteins promoting LLPS [91]. Biomolecular condensates formed by LEA proteins from the anhydrobiotic animal brine shrimp were considered to act as protective compartments for desiccation-sensitive proteins to promote dehydration tolerance during anhydrobiosis [92][93]. Whether LLPS has a similar role in plant LEA protein functioning in stress tolerance still awaits investigation. Despite recent discoveries of novel plant IDPs involved in LLPS to generate biomolecular condensates during stress sensing and signalling, several questions remain. What are the determining factors of LLPS for forming biomolecular condensates (i.e., specific amino acid sequences of IDPs, specific IDP conformation, or biophysical properties)? And what are the components of biomolecular condensates in various stress situations? Future investigation dissecting the spatial and temporal rules guiding biomolecular condensate formation under various stress conditions is important to understand the roles of plant IDP-driven LLPS in stress responses.

This entry is adapted from the peer-reviewed paper 10.3390/ijms25021178

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