Ménage à Trois: Unraveling the Mechanisms Regulating Plant–Microbe–Arthropod Interactions

Plant–microbe–arthropod (PMA) three-way interactions have important implications for plant health. However, our poor understanding of the underlying regulatory mechanisms hampers their biotechnological applications. To this end, we searched for potential common patterns in plant responses regarding taxonomic groups or lifestyles. We found that most signaling modules regulating two-way interactions also operate in three-way interactions. Furthermore, the relative contribution of signaling modules to the final plant response cannot be directly inferred from two-way interactions. Moreover, our analyses show that three-way interactions often result in the activation of additional pathways, as well as in changes in the speed or intensity of defense activation. Thus, detailed, basic knowledge of plant–microbe–arthropod regulation will be essential for the design of environmentally friendly crop management strategies.

This paper was inspired by scientific discussions among members of the COST Action FA1405. We thank the COST Action members that contributed to identify relevant publications. We thank Júlia Lidoy and Víctor Lidoy for drawing Figure 1. This work was financially supported by COST Action FA1405 and the Slovenian Research Agency’s research core funding No Z4-706, the Spanish Ministry of Science, Innovation and Universities (grants AGL2016-75819-C2-1-R and RTI2018-094350-B-C31), General Secreterial of Research and Technology, Greece co-financed with EU (T1- RCE-05301), and the Onassis Foundation (RZJ-003-2). A.M.M. Acknowledges funding from the program for attracting talent to Salamanca from the Fundación Salamanca Ciudad de Cultura y Saberes and Ayuntamiento de Salamanca