The role of water in plant-microbe interactions

Abstract

Throughout their life plants are associated with various microorganisms, including commensal, symbiotic and pathogenic microorganisms. Pathogens are genetically adapted to aggressively colonize and proliferate in host plants to cause disease. However, disease outbreaks occur only under permissive environmental conditions. The interplay between host, pathogen and environment is famously known as the 'disease triangle'. Among the environmental factors, rainfall events, which often create a period of high atmospheric humidity, have repeatedly been shown to promote disease outbreaks in plants, suggesting that the availability of water is crucial for pathogenesis. During pathogen infection, water-soaking spots are frequently observed on infected leaves as an early symptom of disease. Recent studies have shown that pathogenic bacteria dedicate specialized virulence proteins to create an aqueous habitat inside the leaf apoplast under high humidity. Water availability in the apoplastic environment, and probably other associated changes, can determine the success of potentially pathogenic microbes. These new findings reinforce the notion that the fight over water may be a major battleground between plants and pathogens. In this article, we will discuss the role of water availability in host-microbe interactions, with a focus on plant-bacterial interactions.

Keywords: high humidity; plant disease; plant immunity; stomata; water-soaking.

Figure 1. Movement of water from soil to the atmosphere through a plant

(a) A land plant uptakes water from soil by roots, distributes water through the xylem to other parts of the plant, and transpires water vapor into the atmosphere from the leaves. Root hairs and epidermal cells are mainly responsible for water uptake. Blue arrows indicate the water flow from soil to atmosphere via a plant. (b) Water enters root cells through three distinct pathways: apoplstic, symplastic and transmembrane pathways. All three pathways converge into a symplastic movement at the endodermis. (c) Water is unloaded into the xylem and subjected to long distant transport. (d) In the leaf, water leaves the vascular bundle and is distributed to mesophyll cells and epidermal cells. Water is then drawn into plant cell walls. The water vapor from cell walls move to the atmosphere through stomata during transpiration. Black arrows indicate the direction of the water flow in a plant.

Figure 2. Pathogenic bacteria create water-soaking spots on host plants during pathogenesis

(a) An Arabidopsis plant is infected with a bacterial pathogen, Pst DC3000. The image was taken one day after infection. Dark areas on the leaves indicate water-soaking spots. (b) A model illustrates how pathogenic bacteria create an aqueous environment in the leaf apoplast to support their aggressive growth. Pst DC3000 utilizes two protein effectors, HopM1 and AvrE, to create an aqueous living space in the apoplast. Once inside the plant cell, HopM1 is targeted to the trans-Golgi network/early endosome (TGN/EE) and degrades a plant ARF-family guanine nucleotide exchange factor protein, AtMIN7, involved in vesicle trafficking. AvrE is localized to the plasma membrane. These two effectors likely affect the plant plasma membrane integrity, creating osmotic sinks to draw water (possibly nutrients) into the apoplast. X. gardneri, on the other hand, employs AvrHah1, which is a transcription activator-like (TAL) effector (TALE), to induce water-soaking symptoms in plants. AvrHah1 up-regulates expression of two basic helix-loop-helix (bHLH) transcription factors, which subsequently induce the expression of two genes that encode pectin-modifying enzymes. The actions of pectin-modifying enzymes might change the composition of plant cell walls, affecting the hygroscopicity of the cell walls. In addition, X. axonopodis pv. manihoti and X. citri subsp. malvacearum delivers TALEs TAL20_Xam668 and Avrb6, respectively, to up-regulate expression of the sugar transporter genes SWEET in plants. By redirecting the distribution of sugar in their host plants, the pathogenic bacteria might facilitate their nutrition as well as increase osmotic potential in the apoplast, leading to an aqueous apoplast environment in the infected leaves.