When Plants and Animals First Met Fungi: Insights from the Evolution of Host Immune Systems

Abstract

Fungi interact with plants and animals, leading variously to mutually beneficial partnerships or to devastating disease. Reflecting the importance of plant–fungal and animal–fungal interactions, the innate immune systems of terrestrial plants and animals detect fungi using inherited recognition receptors. Upon recognition, the receptor proteins stimulate signaling pathways that foster intimate mutualisms or trigger robust, multi-level innate defenses against parasitism. To provide points of discussion about how the evolutionary history of host recognition may have unfolded, we analyze the phylogenetic distributions of pattern-recognition receptors important in plant and animal immunity, and of two groups of enzymes important in defenses: chitinases in plants and β-glucanases in animals. Our analysis takes advantage of recently sequenced genomes of early-diverging host plants and animals. We draw upon experimental studies using model organisms that reveal how some host plants and animals perceive fungi. To infer functional homology, we explore recent studies using experimental approaches to analyze binding interactions between host proteins and pathogen molecules. We contend that phylogenetic ages of the host receptors provide a window, imperfect but intriguing, into the origins of the host systems that have been detecting fungi over hundreds of millions of years of geological time.