Smut fungi, such as Ustilago maydis, have been studied extensively as a model for plant-pathogenic basidiomycetes. However, little attention has been paid to smut diseases of agronomic importance that are caused by species of the genus Thecaphora, probably due to their more localized distribution. Peanut smut incited by Thecaphora frezii has been reported only in South America, and Argentina is the only country where this disease has been noted in commercial peanut production. In this work, important advances in deciphering T. frezii specific biology/pathobiology in relation to potato (T. solani), wheat (U. tritici), and barley (U. nuda) smuts are presented. We summarize the state of knowledge of fungal effectors, functionally characterized to date in U. maydis and most recently in T. thlaspeos, as well as the potential to be present in other Thecaphora species involved in dicot-host interactions like T. frezii-peanut. We also discuss applicability and limitations of currently available methods for identification of smut fungi in different situations and management strategies to reduce their impact on agri-food quality. We conclude by describing some of the challenges in elucidating T. frezii strategies that allow it to infect the host and tolerate or evade plant immune defense mechanisms, and assessing other aspects related to pest control and their implications for human health.

Phosphoinositide-specific phospholipases C (PI-PLCs) are signaling enzymes that hydrolyze membrane phosphoinositides to generate lipid- and lipid-derived second messengers. In plants, PI-PLCs have been implicated in various physiological processes, including immunity. Tomato SlPLC2 was previously shown to be implicated in susceptibility to the necrotrophic fungus Botrytis cinerea. However, whether this observation extends to pathogens with different lifestyles and evolutionary origins remains unknown. Here, we investigated SlPLC2 function during infection with Phytophthora infestans, a globally devastating oomycete and causal agent of potato and tomato late blight. CRISPR/Cas9 knockout SlPLC2 plants showed significantly reduced disease symptoms, lower pathogen biomass, and decreased sporangia production, indicating impaired colonization. Upon infection, SlPLC2 knockout lines displayed attenuated expression of salicylic acid- and jasmonic acid-marker genes. Consistent with a role for PLC signaling in plant defense, early immune responses, such as hydrogen peroxide accumulation and callose deposition, were reduced in knockout plants. At the cellular level, these plants allow the formation of fewer infection vesicles by P. infestans, accompanied by an increase in expression of a biotrophy-associated effector gene PiAvrblb2, suggesting impaired establishment of infection. In Nicotiana benthamiana, SlPLC2-GFP displays a localization pattern predominately consistent with plasma membrane association and also localizes to the membranes surrounding P. infestans infection vesicles, where we also detected phosphoinositides PI4P and PI(4,5)P2. As complementary heterologous evidence, transient overexpression of SlPLC2 in N. benthamiana enhanced lesion development after P. infestans inoculations. Together, these findings identify SlPLC2 as a susceptibility factor associated with enhanced P. infestans colonization.