Cell Signaling during Cold, Drought, and Salt Stress

Abstract

Low temperature, drought, and high salinity are common stress conditions that adversely affect plant growth and crop production. The cellular and molecular responses of plants to environmental stress have been studied intensively (Thomashow, 1999; Hasegawa et al., 2000). Understanding the mechanisms by which plants perceive environmental signals and transmit the signals to cellular machinery to activate adaptive responses is of fundamental importance to biology. Knowledge about stress signal transduction is also vital for continued development of rational breeding and transgenic strategies to improve stress tolerance in crops. In this review, we first consider common characteristics of stress signal transduction in plants, and then examine some recent studies on the functional analysis of signaling components. Finally, we attempt to put these components and pathways into signal transduction networks that are grouped into three generalized signaling types. A Generic Pathway for the Transduction of Cold, Drought, and Salt Stress Signals in Plants. Examples of signaling components in each of the steps are shown (for more detailed information, see Xiong and Zhu, 2001). Secondary signaling molecules can cause receptor-mediated Ca2+ release (indicated with a feedback arrow). Examples of signaling partners that modulate the main pathway are also shown. These partners can be regulated by the main pathway. Signaling can also bypass Ca2+ or secondary signaling molecules in early signaling steps. GPCR, G-protein coupled receptor; InsP, inositol polyphosphates; RLK, receptor-like kinase. Other abbreviations are given in the text. Repetitive Ca2+ Transients upon the Perception of a Primary Signal. The primary increase in cytosolic Ca2+ facilitates the generation of secondary signaling molecules, which stimulate a second round of transient Ca2+ increases, both locally and globally. These second Ca2+ transients may feedback regulate each of the previous steps (not shown). Ca2+ transients from different sources may have different biological significance and result in different outputs, as shown. Secondary signaling molecules such as ROS can also directly regulate signal transduction without Ca2+ (Output 2). Signal transduction requires the proper spatial and temporal coordination of all signaling molecules. Thus, there are certain molecules that participate in the modification, delivery, or assembly of signaling components, but do not directly relay the signal. They too are critical for the accurate transmission of stress signals. These proteins include protein modifiers (e.g., enzymes for protein lipidation, methylation, glycosylation, and ubiquitination), scaffolds, and adaptors (Xiong and Zhu, 2001) (Figure 1). Low temperature, drought, and high salinity are very complex stimuli that possess many different yet related attributes, each of which may provide the plant cell with quite different information. For example, low temperature may immediately result in mechanical constraints, changes in activities of macromolecules, and reduced osmotic potential in the cellular milieu. High salinity includes both an ionic (chemical) and an osmotic (physical) component. The multiplicity of information embedded in abiotic stress signals underlies one aspect of the complexity of stress signaling. On the basis of this multiplicity, it is unlikely that there is only one sensor that perceives the stress condition and controls all subsequent signaling. Rather, a single sensor might only regulate branches of the signaling cascade that are initiated by one aspect of the stress condition. For example, low temperature is known to change membrane fluidity (Murata and Los, 1997). A sensor detecting this change would initiate a signaling cascade responsive to membrane fluidity but would not necessarily control signaling initiated by an intracellular protein whose conformation/activity is directly altered by low temperature. Thus, there may be multiple primary sensors that perceive the initial stress signal. Secondary signals (i.e., hormones and second messengers) can initiate another cascade of signaling events, which can differ from the primary signaling in time (i.e., lag behind) and in space (e.g., the signals may diffuse within or among cells, and their receptors may be in different subcellular locations from the primary sensors) (Figure 2). These secondary signals may also differ in specificity from primary stimuli, may be shared by different stress pathways, and may underlie the interaction among signaling pathways for different stresses and stress cross-protection. Therefore, one primary stress condition may activate multiple signaling pathways differing in time, space, and outputs. These pathways may connect or interact with one another using shared components generating intertwined networks. Given the multiplicity of stress signals, many different sensors are expected, although none have been confirmed for cold, drought, or salinity. Al