Fungal Effector Proteins: Molecular Mediators of Fungal Symbionts of Plants

Plant-fungal symbioses are of great importance to agriculture. Phytopathogenic fungi, which cause disease in plants as they consume host tissues, are a major threat to global food security. Conversely, endophytes and mycorrhizal fungi, which can engage in mutually beneficial relationships with host plants, are capable of promoting plant health, growth, and development. Such plant-fungal symbioses, whether they be harmful or beneficial to host plants, require complex and continuous molecular cross talk, including the secretion of fungal effector proteins into the plant apoplast and cytoplasm. Fungal effectors are broadly defined as proteins which modulate plant physiology in ways which facilitate fungal colonization and growth within the host plant. These proteins typically share three common features: (1) an amino(N)-terminal signal peptide to allow for secretion, (2) high cysteine content that facilitates structural stability, and (3) small molecular mass (typically ≤30 kDa). However, fungi often possess a large number of genes which fit these criteria—only a subset of which truly act as effector proteins. Progress in identifying effector proteins has been hindered by the fact that most apparently do not share significant sequence similarities with effectors of other genera. This is thought to be an adaptive trait within the context of the co-evolutionary arms race between plant-associated fungi and their host plants, in which plants are continually evolving novel variations in their resistance (R) proteins to allow for improved detection of fungal effector proteins, while fungi diversify their effectors to evade detection. Despite this fact, there are a limited number of domains and motifs which have been found in effector proteins from a variety of plant-associated fungi. Some of these conserved sequence features, such as CFEM and LysM domains, are shared among effector proteins of phytopathogenic and mutualistic fungi, while others may be tailored to the unique lifestyles of individual species or genera. Relying upon the common features and few conserved motifs and domains, in silico tools are often relied upon to mine fungal genomes for candidate effector proteins. Although this process is valuable in curating lists of potential effectors, experimental validation of effector status is still required. To that end, many studies have utilized knockout or overexpression of putative effector protein-coding genes in order to elucidate the importance of putative effectors in the establishment and maintenance of fungal-plant symbioses—a method which is susceptible to issues of gene redundancy. The vast majority of literature on fungal effectors has focused on fungal pathogens of above-ground plant tissue; however this chapter also emphasizes the limited state of understanding on effector proteins from rhizospheric fungi.