Structural disorder in plant proteins: where plasticity meets sessility

Abstract

Plants are sessile organisms. This intriguing nature provokes the question of how they survive despite the continual perturbations caused by their constantly changing environment. The large amount of knowledge accumulated to date demonstrates the fascinating dynamic and plastic mechanisms, which underpin the diverse strategies selected in plants in response to the fluctuating environment. This phenotypic plasticity requires an efficient integration of external cues to their growth and developmental programs that can only be achieved through the dynamic and interactive coordination of various signaling networks. Given the versatility of intrinsic structural disorder within proteins, this feature appears as one of the leading characters of such complex functional circuits, critical for plant adaptation and survival in their wild habitats. In this review, we present information of those intrinsically disordered proteins (IDPs) from plants for which their high level of predicted structural disorder has been correlated with a particular function, or where there is experimental evidence linking this structural feature with its protein function. Using examples of plant IDPs involved in the control of cell cycle, metabolism, hormonal signaling and regulation of gene expression, development and responses to stress, we demonstrate the critical importance of IDPs throughout the life of the plant.

Keywords: Intrinsically disordered proteins; LEA proteins; Plant development; Plant metabolism; Plant signaling; Plant stress responses; Transcription factors.

Fig. 1

Schematic representation of two examples of plant proteins containing IDRs that participate in developmental and metabolic processes. a TCP8 is a plant-specific transcription factor involved in plant shape developmental control. TCP8 contains three IDRs (represented by curved lines). In these IDRs, there are conserved serine residues, from which at least one is phosphorylated (fill blue small circle in the middle IDR). The IDR at the C-terminal region corresponds to a trans-activation domain (TAD) required for the formation of TCP8 homo-oligomers. This TAD is also required to bind different partners, such as TCP15 or PNM (red irregular oval). The IDR at the amino-terminal region (purple irregular line) is part of the TCP8 DNA-binding domain; this disordered region gains structure when TCP8 binds to DNA. b CP12 plays a key role in the regulation of the Calvin cycle by translating changes in light availability into the modulation of GAPDH and PRK enzyme activities. CP12 is a scaffold protein (represented by curved lines at the top of this panel) that forms a ternary complex with GAPDH (blue and red irregular ovals) and PRK (brown irregular oval) (GAPDH-CP12-PRK) (represented by the association of the three components at the bottom of the panel). During the formation of the GAPDH-CP12-PRK complex, GAPDH associates with CP12 by conformational selection. Upon this interaction, the CP12 N-terminal region remains in a fuzzy state, serving as a linker that facilitates the interaction with PRK. Once the complex is formed, it dimerizes to form a native complex in which there are two dimers of PRK, two tetramers of GAPDH and two monomers of CP12 (figure at the bottom right of this panel). Using this mechanism, it seems that CP12 is able to modulate GAPDH and PRK activities

Fig. 2

Schematic representation of two examples of plant IDPs that participate in abiotic and biotic stress responses. A LEA proteins (represented as purple curved lines) belong to a representative group of plant IDPs involved in plant abiotic stress responses. LEA proteins are able to prevent the inactivation of reporter enzymes under in vitro partial dehydration and freeze–thaw treatments. One action mechanism supported by different lines of evidence indicates that LEA proteins function as chaperones during water deficit a by interacting with their protein target(s) (green irregular ovals) and avoiding the damage (denaturation represented by green irregular lines emerging from the green ovals) caused by the effects of low water availability in the cell. The possibility that LEA proteins may bind and recognize their targets by conformational selection under water deficit has been suggested by in vitro data. In addition, there is evidence indicating that LEA proteins are able to stabilize membrane (double blue circles) integrity b during water deficit, by interaction through the amphipathic regions present in some LEA proteins. It has been suggested that LEA proteins might achieve more stable conformations upon membrane association. It has been proposed that this interaction induces LEA protein folding. b An additional attribute of at least some LEA proteins is their ability to bind metal ions (Fe³⁺, Ni²⁺, Cu²⁺, Co²⁺ and Zn²⁺) (small gray fill circles), which in some cases, by these means scavenge reactive oxygen species (c). For some LEA proteins, metal binding promotes a reduction in the content of structural disorder; however, this is not a common observation. In this panel, continue arrows represent the protective effect of LEA proteins, whereas discontinuous arrows indicate the consequent damage produced by stress in the absence of these proteins. B Biotic stress produced by plant pathogens has led to the selection of refined mechanisms to detect their presence and to mount complex inducible responses to efficiently counteract their attack. The participation of IDPs along the different steps of pathogen invasion, from their perception to the plant defense response has been documented. The RbohD protein (green curved lines), which belongs to the NADPH oxidase family, represents an example of this. This protein, partially integrated in the membrane, is responsible for the early generation of ROS, upstream of calcium and phosphorylation signaling. The RbohD cytoplasmic N terminus possesses an IDR, which contains EF-hand motifs involved in calcium binding. The malleable nature of this region results in extended conformational changes induced by the synergistic effect of calcium binding and its phosphorylation, which in turn modulates the interaction with small GTPase proteins (orange irregular oval); a process needed to set up the plant protection response against pathogens