How Plants Sense and Respond to Stressful Environments

Abstract

Plants are exposed to an ever-changing environment to which they have to adjust accordingly. Their response is tightly regulated by complex signaling pathways that all start with stimulus perception. Here, we give an overview of the latest developments in the perception of various abiotic stresses, including drought, salinity, flooding, and temperature stress. We discuss whether proposed perception mechanisms are true sensors, which is well established for some abiotic factors but not yet fully elucidated for others. In addition, we review the downstream cellular responses, many of which are shared by various stresses but result in stress-specific physiological and developmental output. New sensing mechanisms have been identified, including heat sensing by the photoreceptor phytochrome B, salt sensing by glycosylinositol phosphorylceramide sphingolipids, and drought sensing by the specific calcium influx channel OSCA1. The simultaneous occurrence of multiple stress conditions shows characteristic downstream signaling signatures that were previously considered general signaling responses. The integration of sensing of multiple stress conditions and subsequent signaling responses is a promising venue for future research to improve the understanding of plant abiotic stress perception.

Figure 1.

Sensing mechanisms for abiotic stress in plants. The five major abiotic stress conditions described in this article are sensed by separate sensing mechanisms. Key proteins in cold temperature sensing are COLD1 in rice (Oryza sativa) and the OST1 pathway in Arabidopsis. COLD1 interacts with RGA1 during cold temperatures, resulting in increased GTPase activity, which activates an unknown calcium influx channel. OST1 is activated upon NMT1-mediated myristoylation of its interactor EGR2 in response to cold temperatures. OST1 is first autophosphorylated, after which it phosphorylates ICE1, leading to the induction of COR gene expression. High temperatures are sensed through recognition of denatured proteins by HSPs, which subsequently release HSE to induce heat-related gene expression. Alternatively, temperature is perceived by the known red/far-red light receptor phyB. High temperatures increase the speed of conversion of activated phyB (Pfr) into inactive phyB (Pr), resulting in increased PIF4 stabilization and hence repression of light-induced gene expression. Flooding sensing is mediated mainly by ethylene accumulation and decreased NO/oxygen levels. Reduced oxygen levels lead to reduced N-terminal Cys oxidation of ERFVII by PCO1/2. This prevents degradation of C-ERFVII, which can relocalize to the nucleus to mediate expression of genes containing hypoxia-responsive elements to mediate flooding tolerance. Drought is likely sensed by a number of transmembrane proteins. OSCA1 is hypothesized to be activated by increased membrane tension occurring during osmotic stress, resulting in the influx of Ca²⁺ to mediate downstream signaling responses. A homolog of OSCA1, called CSC1, is also described as an osmotic stress-regulated calcium channel. The TSC contains a membrane-localized signaling kinase (SK) domain attached to a His kinase (HK) domain in which the His residue is phosphorylated upon osmotic stress. The His kinase subsequently phosphorylates the Asp of a regulator domain, which initiates the signaling cascade in response to drought and/or osmotic stress. Osmotic stress leads to dissociation of the plasma membrane from the cell wall, which is sensed by RLKs localized in the plasma membrane that contain a sensory domain protruding into the cell wall. High salinity is sensed by binding of monovalent cations to the negatively charged GlcA of the GIPC sphingolipids. Upon Na⁺ binding, an unknown calcium influx channel is activated, which results in the activation of the SOS pathway to exclude excess Na⁺ from the cell. P, Phosphate; Myr, Myristoylation; C₂H₄, ethylene; PGB1, phytoglobin1; ERFVII, ethylene response factor7; C_ox-ERFVII, ERF7 containing the oxidized Cys; MC: monovalent cations.

Figure 2.

Membrane composition-related sensing mechanisms. During both heat and cold, PDAT1 and DGAT1 expression is upregulated respectively, increasing the TAG content serving as a lipid storage of polyunsaturated lipids. Desaturase activity is increased during cold conditions to increase desaturation of lipids in the lipid bilayer of chloroplast and other membranes to maintain membrane fluidity. During heat, unsaturated TAG content in the cytosol increases to maintain membrane fluidity. Drought and/or osmotic stress lead to membrane tension, which is likely sensed by the hyperosmolality-gated calcium-permeable channel OSCA1 (pink). Upon osmotic stress, OSCA1 is activated, facilitating the influx of Ca²⁺, resulting in activation of a drought tolerance signaling cascade. Monovalent cations are likely sensed by GIPCs (orange lipids). The negatively charged GlcA (purple pentagons) in GIPC binds Na⁺ ions, leading to opening of an unidentified calcium channel facilitating the influx of Ca²⁺ in the presence of high extracellular Na⁺ levels. The intracellular Ca²⁺ binds SOS3, which forms a complex with SOS2 to activate the Na⁺/H⁺ antiporter SOS1. MC, Monovalent cations.