Molecular battles between plant and pathogenic bacteria in the phyllosphere

Abstract

The phyllosphere, i.e., the aerial parts of the plant, provides one of the most important niches for microbial colonization. This niche supports the survival and, often, proliferation of microbes such as fungi and bacteria with diverse lifestyles including epiphytes, saprophytes, and pathogens. Although most microbes may complete the life cycle on the leaf surface, pathogens must enter the leaf and multiply aggressively in the leaf interior. Natural surface openings, such as stomata, are important entry sites for bacteria. Stomata are known for their vital role in water transpiration and gas exchange between the plant and the environment that is essential for plant growth. Recent studies have shown that stomata can also play an active role in limiting bacterial invasion of both human and plant pathogenic bacteria as part of the plant innate immune system. As counter-defense, plant pathogens such as Pseudomonas syringae pv tomato (Pst) DC3000 use the virulence factor coronatine to suppress stomate-based defense. A novel and crucial early battleground in host-pathogen interaction in the phyllosphere has been discovered with broad implications in the study of bacterial pathogenesis, host immunity, and molecular ecology of bacterial diseases.

Figure 1

Light-conditioned tomato leaf (A) and leaf surface under the microscope prior to exposure to Pst DC3000 showing mostly open stomata (B). The same leaf was exposed to Pseudomonas syringae pv. tomato (Pst DC3000) and after 1 h of exposure most stomata were closed (C).

Figure 2

Model illustrating the signaling components and interactions between molecules that have been experimentally demonstrated to be involved in stomatal defense and bacterial counter defense. In the stomatal guard cell, MAMPs (e.g., flagellin and LPS) are perceived by cognate immune receptors (e.g., flagellin receptor FLS2). Perception of MAMPs triggers stomatal closure, which requires the phytohormones SA and ABA, as well as ABA signaling components listed in the grey rectangle (components are listed in order where the top one is the most upstream. Their localization in the cell is not shown). Flagellin also prevents stomatal opening by inhibiting inwardly rectifying K⁺ channels (K⁺in) through ABA signaling components (GPA1 and possibly others). COR-mediated inhibition of MAMP-triggered stomatal closure requires the plant proteins COI1 (a COR receptor) and RIN4. While COI1 physically binds to COR, RIN4 binds and activates the proton pump (H⁺ATPase) causing membrane hyperpolarization and activation of K⁺ influx (K⁺in), a condition that promotes stomatal opening. Dashed arrows indicate possibly indirect pathways. MAMPs = microbe-associated molecular patterns; LPS = lipopolysaccharide; SA = salicylic acid; ABA = abscisic acid; COR = coronatine.

Figure 3

A model depicting the molecular action of coronatine in plant cells (possibly all cell types). COR is secreted by Pst DC3000 into the plant cell and increases the affinity of the COI1 protein (as part of the SCF^COI1 ubiquitin-ligase complex, not shown here) toward the JAZ repressor. The SCF^COI1 complex catalyzes ubiquitination of JAZ, which is then degraded through the 26S proteasome (denoted as “26S”). JAZ protein is part of a repressor complex that also contains NINJA and TPL, and physically binds to transcriptional activators (such as MYC2) of jasmonate response genes. Upon degradation of JAZ, JA response genes are activated blocking plant innate immune responses including stomatal closure. COR = coronatine; JA = jasmonate; JAZ = jasmonate ZIM-domain; NINJA = novel interactor of JAZ; TPL = TOPLESS.