Evasion and suppression of plant immunity

Abstract

Every year up to 20% of the crop production with an economical value of almost 200 billion euro is lost due to plant diseases. To be able to develop effective and durable strategies to counteract these plant diseases, understanding the mechanisms that enable pathogens to cause disease is essential. Like animals, plants are equipped with an innate immune system that is activated after recognition of an invading organism. Plant immune receptors are able to recognize attackers by certain conserved microbial molecules, after which an effective defense response is activated. Successful pathogens, however, have developed strategies to prevent activation of effective immune responses in their host. For this, pathogens produce numerous so called effector proteins that (1) are able to interfere with host defense responses, or (2) enable the pathogen to escape from recognition by the host immune system. Firstly, 13 putative RXLR effector proteins of the economically important downy mildew pathogen Hyaloperonospora arabidopsidis were screened for a role in host immune suppression. To this end, the RXLR effector proteins were overexpressed in the model plant Arabidopsis. Almost all tested putative RXLR effectors had an effect on specific immune responses in Arabidopsis. The effects were relatively minor, which suggests that the downy mildew pathogen affects host immunity by utilizing many effectors with weak effects, rather than by using few effectors with strong effects on host immunity. Secondly, the role of the excreted protease AprA of Pseudomonas bacteria in the evasion of the immune system of plant and mammalian hosts was investigated. Many Pseudomonas species cause disease in plant and/or animal hosts. They are recognized by host immune receptors through spilled flagellin molecules, which are the main components of the bacterial tail. AprA was identified as a secreted protease of the opportunistic human pathogen Pseudomonas aeruginosa, and shown to degrade flagellin molecules, which enables the pathogen to escape from detection by the host immune system. The important bacterial plant pathogen Pseudomonas syringae produces AprA as well. We demonstrated that AprA-mediated degradation of flagellin molecules is also important for P. syringae to evade host immunity and successfully infect Arabidopsis and tomato. Interestingly, a similar immune evasion strategy was observed in the beneficial bacterium Pseudomonas fluorescens, which interacts with plant roots and stimulates plant growth, indicating that AprA-mediated evasion of host immunity is a strategy that is utilized by both pathogenic and beneficial Pseudomonads. Finally, we tested whether the AprA inhibitor protein AprI, which is also produced by Pseudomonas bacteria, can be utilized to protect plants against bacterial infections. Indeed, transgenic AprI-producing Arabidopsis plants showed enhanced resistance against the P. syringae pathogen, suggesting that AprI can be utilized to protect plants against bacterial diseases. The described work provides novel insights into how successful pathogens can suppress or evade host immunity. Striking parallels between host-microbe interactions in plant and animal systems were demonstrated. We demonstrated that a detailed understanding of the mechanisms by which pathogens can evade or suppress host immunity enables the development of novel tools to combat infections in plants and mammals.