Abiotic Stress Signaling and Responses in Plants

Abstract

As sessile organisms, plants must cope with abiotic stress such as soil salinity, drought, and extreme temperatures. Core stress-signaling pathways involve protein kinases related to the yeast SNF1 and mammalian AMPK, suggesting that stress signaling in plants evolved from energy sensing. Stress signaling regulates proteins critical for ion and water transport and for metabolic and gene-expression reprogramming to bring about ionic and water homeostasis and cellular stability under stress conditions. Understanding stress signaling and responses will increase our ability to improve stress resistance in crops to achieve agricultural sustainability and food security for a growing world population.

Figure 1

Stress sensing and signaling in different cell organelles. A. Model of dispersed stress sensing by organelles. Stress causes perturbations in various organelles, generating signals that are integrated to regulate nuclear gene expression and other cellular activities, which helps to restore cellular homeostasis. B. ER stress sensing and signaling. C. Chloroplast stress sensing and signaling. Dashed lines indicate postulated regulation.

Figure 2

The Ca²⁺-CBL-CIPK module mediates signaling of various ionic stresses. High Na⁺, low K⁺, excess Mg²⁺ and high pH (low H⁺) conditions cause cytosolic Ca²⁺ signals, which activate SOS3 (CBL4)/SCaBP8 (CBL10)-SOS2 (CIPK24), CBL1/9-CIPK23, CBL2/3-CIPK3/9/23/26 and SCaBP1 (CBL2)-PKS5/24 (CIPK11/14) to phosphorylate and regulate the activity of SOS1 (Na⁺/H⁺ antiporter), AKT1 (K⁺ channel), a putative Mg²⁺ transporter and H⁺-ATPase, respectively. Also shown is ABI2 and 14-3-3 inhibition of SOS2 and SOS2 regulation of SCaBP8 by phosphorylation. Arrows indicate activation, and bars indicate inhibition.

Figure 3

Osmotic stress and ABA sensing and signaling. The Ca²⁺ channel OSCA1 may participate in osmosensing. The resulting Ca²⁺ signal may activate CPKs and CBLs-CIPKs. Eventually, SnRK2s are activated, which leads to ABA accumulation. ABA binds to PYLs, which then interact with and inhibit class A PP2Cs, resulting in the activation of SnRK2.2/3/6/7/8. The activated SnRK2s phosphorylate effector proteins including TFs (transcription factors), SLAC1 and RbohD/F. RbohD/F generates H₂O₂, which elicits a Ca²⁺ signal through GHR1. This Ca²⁺ signal activates CPKs and CBLs-CIPKs that also phosphorylate effector proteins such as SLAC1. In addition to Ca²⁺, ABA also induces the second messengers NO (nitric oxide), and PA (phosphatidic acid) and other phospholipids. NO inhibits SnRK2s and PYLs, and PA regulates proteins like Rbohs. Also depicted is ABA activation of a MAP kinase module. Components of the core ABA signaling pathway are colored in red. Arrows indicate activation, bars indicate inhibition, and dashed lines indicate postulated regulation.

Figure 4

Cold stress sensing and signaling. Cold stress is sensed by membrane proteins such as COLD1, leading to a cytosolic Ca²⁺ signal. CPKs and CBLs-CIPKs may mediate the Ca²⁺ signal to activate a MAP kinase cascade. The activated MPKs are postulated to phosphorylate TFs such as CAMTAs and ICE1/2, which then activate cold responsive genes. Through an unknown mechanism, cold stress also activates OST1 (SnRK2.6), which inhibits HOS1, and phosphorylates and activates ICE1. Arrows indicate activation, bars indicate inhibition, and dashed lines indicate postulated regulation.

Figure 5

Model of systemic stress signaling. Local exposure to stress generates H₂O₂ and Ca²⁺ signals. The Ca²⁺ signal can activate CPKs and CBLs-CIPKs, which phosphorylate and activate RbohD. Activated RbohD generates H₂O₂ that diffuses through the cell wall to neighoring cells, where it induces a Ca²⁺ signal, through RLKs like GHR1. H₂O₂ may activate Ca²⁺ signaling at the cell surface and may also enter the cell through PIP water channels and then activate Ca²⁺ signaling intracellularly. The mutual activation between the Ca²⁺ and H₂O₂ signals generates a self propagating calcium and ROS waves that can travel to distant tissues to cause systemic acquired acclimation responses. Dashed lines indicate postulated regulation.