Orchestrating rapid long-distance signaling in plants with Ca2+ , ROS and electrical signals

Abstract

Plants show a rapid systemic response to a wide range of environmental stresses, where the signals from the site of stimulus perception are transmitted to distal organs to elicit plant-wide responses. A wide range of signaling molecules are trafficked through the plant, but a trio of potentially interacting messengers, reactive oxygen species (ROS), Ca²⁺ and electrical signaling ('trio signaling') appear to form a network supporting rapid signal transmission. The molecular components underlying this rapid communication are beginning to be identified, such as the ROS producing NAPDH oxidase RBOHD, the ion channel two pore channel 1 (TPC1), and glutamate receptor-like channels GLR3.3 and GLR3.6. The plant cell wall presents a plant-specific route for possible propagation of signals from cell to cell. However, the degree to which the cell wall limits information exchange between cells via transfer of small molecules through an extracellular route, or whether it provides an environment to facilitate transmission of regulators such as ROS or H⁺ remains to be determined. Similarly, the role of plasmodesmata as both conduits and gatekeepers for the propagation of rapid cell-to-cell signaling remains a key open question. Regardless of how signals move from cell to cell, they help prepare distant parts of the plant for impending challenges from specific biotic or abiotic stresses.

Keywords: calcium; cell-to-cell communication; plasmodesmata; reactive oxygen species; systemic signaling.

Figure 1

Salt-stress-associated Ca²⁺ and reactive oxygen species (ROS) wave propagation in plants. A salt-stress-triggered cytosolic Ca²⁺ ([Ca²⁺]_cyt) increase is dependent on the tonoplast-localized TWO PORE CHANNEL 1 (TPC1) cation channel (Choi et al., 2014). The resultant [Ca²⁺]_cyt increase is propagated through the cell in a wave front supported by Ca²⁺-induced Ca²⁺ release (CICR) that is either directly or indirectly supported by TPC1 action. In addition, H₂O₂ accumulation in the apoplast is generated by the PM-localized RBOHD NADPH oxidase, that is itself activated by Ca²⁺ through internal Ca²⁺-binding sites (EF-hands) and a variety of Ca²⁺-dependent, post-translational regulators (reviewed in Choi et al., 2016). The apoplastic transmission of accumulated extracellular H₂O₂ is thought to drive cell-to-cell transmission of the propagating wave (Evans et al., 2016). CW, cell wall; ER, endoplasmic reticulum; RBOHD, respiratory burst oxidase homolog D; EF-hand, Ca²⁺-binding domain; TPC1, two pore channel 1; DT, desmotuble.

Figure 2

Routes of cell-to-cell communication in plant and animal cells. Simplified models for the transmission of signals between two plant (a) and animal (b) cells are shown. Signals are transported between cells via secretion of molecules (a and b) or vesicles (b), or direct physical cell-to-cell connections (PDs in a, and gap junctions and tunneling nanotubes in b). CW, cell wall; ER, endoplasmic reticulum; GJ, gap junction; PD, plasmodesma; PM, plasma membrane; TNT, tunneling nanotubes.

Figure 3

Model of possible propagation of general and stress-specific systemic signals. Local stress stimuli triggers changes in membrane potentials, increases in cytosolic [Ca²⁺] and activation of RBOHD-mediated oxidative burst leading to reactive oxygen species (ROS) accumulation, i.e. trio signaling. The association between the signals generates a wave that rapidly spreads throughout the plant in an auto-propagating manner, traversing through the apoplast outside the cell and/or symplastically through PD. This initial signaling wave acts as a priming signal, which is required, but not sufficient for systemic acquired acclimation (SAA). The priming wave activates the core environmental stress response genes (CESRs). Following the general signaling wave, depending on the type of stress, a second wave of systemic stress-specific systemic signaling starts, activating stress-specific genes and cellular mechanisms that facilitate SAA against the same type of stress that triggered the initial response. APX2, ascorbate peroxidase; GLR, GLUTAMATE RECEPTOR-LIKE channels; JA, jasmonic acid; AsA, ascorbic acid; RBOHD, respiratory burst oxidative homolog D; H₂O₂, hydrogen peroxide; HL, high light; HSR, heat stress response; HS, heat stress; WSR, wounding stress response; HLSR, high light stress response; ABA, abscisic acid; MBF1c, multiprotein bridging factor 1c, PD, plasmodesmata.