Pseudomonas syringae AlgU downregulates flagellin gene expression helping evade plant immunity

Authors: Swingle, Bryan; BAO, ZHONGMENG - Cornell University; WEI, HAI-LEI - Chinese Academy Of Agricultural Sciences; MA, XING - Cornell University

Submitted to: Journal of Bacteriology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/8/2019
Publication Date: 1/29/2020
Citation: Swingle, B.M., Bao, Z., Wei, H., Ma, X. 2020. Pseudomonas syringae AlgU downregulates flagellin gene expression helping evade plant immunity. Journal of Bacteriology. https://doi.org/10.1128/JB.00418-19.
DOI: https://doi.org/10.1128/JB.00418-19

Interpretive Summary: Most bacteria have one or more “tails” called flagella that are used to power their movement to access host tissues. Plants and animals detect the proteins in flagella as indicators of bacterial infection. Here we identify the master regulator in the bacteria that represses the production of flagella proteins so that the invading bacteria are not detected by the host. This in turn reduces the activation of host immune responses and allows the bacteria to proliferate and cause a more severe disease. Our results are fundamentally important for understanding how bacteria are adapted to colonize new hosts and cause disease in plants. Additionally, because the proteins responsible for this regulation are widely conserved, it is possible that they serve similar roles in other plant and animal diseases. Our results could stimulate new technologies for controlling bacterial disease in important crops. For example, interfering with this master regulator could disrupt the bacteria’s ability to mask its arrival in plant tissues allowing a more robust response by plant defenses that would reduce bacterial growth and the severity of disease.

Technical Abstract: Flagella power bacterial movement through liquids and over surfaces to access or avoid certain environmental conditions, ultimately increasing a cell’s probability of survival and reproduction. In some cases, flagella and chemotaxis are key virulence factors, enabling pathogens to gain entry and attach to suitable host tissues. But, flagella production is not always beneficial, and both plant and animal immune systems have evolved to sense epitopes within the proteins that make up flagellar filaments as signatures of bacterial infection. Microbes poorly adapted to avoid or counteract these immune functions are unlikely to proliferate in host environments, and this failure can select for diverse and often redundant compensatory mechanisms. We tested the role of AlgU, the Pseudomonas extracytoplasmic function sigma factor E or 22 ortholog, in regulating flagellar expression in the context of Pseudomonas syringae – plant interactions. We found that AlgU is necessary for downregulating bacterial flagellin expression in planta and that this results in a corresponding reduction in plant immune elicitation. This AlgU-dependent regulation of flagellin is beneficial to bacterial growth in the course of plant infection, but eliminating the plant’s ability to detect flagellin makes AlgU irrelevant for bacteria growing in the apoplast. Together, these results add support to an emerging model in which P. syringae AlgU functions at a key control point that serves to optimize expression of bacterial functions during host interactions, including minimizing expression of immunity elicitors and concomitantly upregulating beneficial virulence functions.