Inter-tissue and inter-organ signaling in drought stress response and phenotyping of drought tolerance

Abstract

Plant response to drought stress includes systems for intracellular regulation of gene expression and signaling, as well as inter-tissue and inter-organ signaling, which helps entire plants acquire stress resistance. Plants sense water-deficit conditions both via the stomata of leaves and roots, and transfer water-deficit signals from roots to shoots via inter-organ signaling. Abscisic acid is an important phytohormone involved in the drought stress response and adaptation, and is synthesized mainly in vascular tissues and guard cells of leaves. In leaves, stress-induced abscisic acid is distributed to various tissues by transporters, which activates stomatal closure and expression of stress-related genes to acquire drought stress resistance. Moreover, the stepwise stress response at the whole-plant level is important for proper understanding of the physiological response to drought conditions. Drought stress is sensed by multiple types of sensors as molecular patterns of abiotic stress signals, which are transmitted via separate parallel signaling networks to induce downstream responses, including stomatal closure and synthesis of stress-related proteins and metabolites. Peptide molecules play important roles in the inter-organ signaling of dehydration from roots to shoots, as well as signaling of osmotic changes and reactive oxygen species/Ca²⁺ . In this review, we have summarized recent advances in research on complex plant drought stress responses, focusing on inter-tissue signaling in leaves and inter-organ signaling from roots to shoots. We have discussed the mechanisms via which drought stress adaptations and resistance are acquired at the whole-plant level, and have proposed the importance of quantitative phenotyping for measuring plant growth under drought conditions.

Keywords: abscisic acid (ABA); drought stress; inter-organ signaling; inter-tissue signaling; peptide signals; phenotyping.

Figure 1

Hierarchy of drought stress responses in plants. Under drought stress conditions, plants perceive water‐deficit via “sensing mechanisms” in roots. Several types of water‐deficit signals are transmitted from roots to leaves via “inter‐organ signaling.” Then, they are distributed between distal tissues in each organ via “inter‐tissue signaling” to adapt to drought stress; for example, abscisic acid functions as an inter‐tissue signal to close stomata and change gene expression in leaves.

Figure 2

Abscisic acid (ABA) functions as an inter‐tissue signal in leaves. Leaf cross‐section showing vascular tissues (sites of ABA biosynthesis) and guard cells (ABA action sites). In Arabidopsis, the ABA transporters ABCG25, ABCG40, NRF4.6, and DTX50, are expressed in vascular cells and/or guard cells. In the leaf section, the movement of ABA is indicated by solid and dashed arrows.

Figure 3

Inter‐organ signaling via the vasculature in drought stress responses. Various inter‐organ signals are transmitted via the vasculature as part of drought stress response. Xylem and phloem are important for inter‐organ signaling. Soil water deficit and low humidity may induce drought stress responses in roots and guard cells, respectively. Osmotic changes, reactive oxygen species (ROS), and Ca²⁺ transients function in stress signaling from roots to leaves. Peptides and metabolites are synthesized in roots in response to drought stress and transported via the xylem to leaves. Among them, the roles of CLE25 peptide have been precisely analyzed (Takahashi et al., 2018b).

Figure 4

Drought stress signaling network from the perception of stress signals to cellular, inter‐organ, and whole‐plant responses and the acquisition of tolerance. Drought imposes water‐deficit stress on plants at the cellular, organ, and whole‐plant levels. Water deficit induces osmotic stress, oxidative stress, and mechanical stress, which are sensed by osmosensors, reactive oxygen species (ROS) sensors, and Ca²⁺ channels. These intra‐ and inter‐tissue stress signals are mediated by phosphorylation, abscisic acid (ABA), and metabolites. Inter‐organ signaling molecules (peptides such as CLE2 and metabolites such as sulfate) are transported between tissues and organs. Stress signals regulate channels, transporters, transcription factors, and hormones to induce stomatal closure, stress‐responsive gene expression, and osmolyte/stress‐protein synthesis to prevent severe dehydration. After long‐term water‐deficit stress, phenotypic changes in plants such as drought tolerance and growth delay can be monitored precisely using quantitative phenotyping.