Antimicrobial effectors of plant-associated fungi: multipurpose proteins with fast-evolving surfaces and structurally conserved cores

Plants are exposed to a variety of devastating pathogens, causing significant yearly yield losses. In order to facilitate infections, plant pathogens secrete an arsenal of molecules termed effectors, which are known to modulate plant immune responses. Plants, on the other hand, possess receptors allowing them to detect invading pathogens by either recognising conserved molecules associated with invading microbes or by perceiving effector molecules. For decades, molecular phytopathology research has been focused on the bilateral molecular crosstalk between plants and pathogens and has deepened our understanding of virulence and defence mechanisms. In recent years, the impact of the plant microbiome on plant-pathogen interactions has gained interest, given the fact that some microbes can aid protection against invading pathogens, and pathogen invasion substantially modulates microbiome composition. Several antimicrobial effectors have been identified in fungal plant pathogens, pointing to direct mechanisms whereby pathogens can alter their hosts' microbiome to promote host colonisation. These new findings highlight that some effectors may have several functions targeting plant processes and fungi or bacteria associated with the plant. Advances in computational biology have greatly enhanced the analysis of predicted effector proteins and revealed that these often are highly conserved among phylogenetically distant fungi. Comparative analyses of protein structures have also revealed that functional divergence may emerge from changes in surface frustration around conserved protein folds. Further, computational simulations of protein evolution indicate that protein properties associated with (antimicrobial) effectors can emerge rapidly around conserved folds. We here summarise and discuss recent studies based on computational biology methods, providing novel insights into effector origin, evolution, and functional divergence.