Date Published: July 18, 2019
Publisher: Public Library of Science
Author(s): Margaret Branine, Anna Bazzicalupo, Sara Branco, Deborah A. Hogan.
Endophytic insect-pathogenic fungi (EIPF) are both plant mutualists and insect pathogens, living inside plant tissues without causing any symptoms to their plant partner while also parasitizing and killing insects . These interactions can occur simultaneously and lead to the demise of plant insect pests. The ecology and evolution of EIPF are still not fully understood; however, several studies have investigated their diversity [2,3], the mechanisms of plant and insect infection [4,5], and the nature of plant–insect–fungus relationships [6,7]. These multikingdom interactions are of particular interest not only because EIPF are an ideal model for understanding the mechanisms of symbioses, but they are also widely used for practical applications and particularly relevant to agricultural pest control . Here, we provide an overview on EIPF by reviewing what is currently known about their evolution, ecology, and mechanisms of insect and plant colonization. We also address real-world applications of EIPF and identify possible research directions for the field in the future.
Insect pathogenicity is a relatively common nutritional mode among fungi and has evolved independently multiple times within different lineages [9,10]. However, most insect-pathogenic fungi do not have the ability to establish themselves in living plant tissues. EIPF evolved in the order Hypocreales (Ascomycota) [2,3], with the generalist insect pathogens Beauveria and Metarhizium (in the families Cordycipitaceae and Clavicipitaceae, respectively) as the most well-studied EIPF genera. The evolution of EIPF is currently not fully understood; however, a study investigating divergence of the genes involved in insect and plant associations suggested Metarhizium’s association with plants was more likely to have driven diversification than insect pathogenicity . This genus displays a large number of genes specific to plant degradation that allow the digestion of plant material, suggesting it may have evolved from fungi associated with plants . Ancestral character reconstruction based on broad phylogenetic sampling of the Hypocreales suggests that the order’s ancestral ecology also involved insect pathogenicity but recovered Metarhizium or Beauveria as related to plant-associated clades [2,3]. The limited breadth and depth of sampling throughout the Hypocreales and assigning a single lifestyle to each species (endophytic, plant pathogen, or insect pathogen) may have limited the insight of these results. More intense sampling and comprehensive scoring of species’ endophytic habits and insect pathogenicity abilities would assist in detecting further EIPF lineages and widen our understanding of both their distribution across the fungal tree of life and their evolutionary history. For example, linking environmental surveys of endophytic fungal diversity with phylogenetic studies could be a powerful approach for detecting more EIPF. Given the high diversity of fungal insect pathogens, it is possible that many more are also endophytic and have so far been overlooked as EIPF.
EIPF establish mutualistic associations with plants and parasitize insects. These associations can occur simultaneously, with one single fungal individual colonizing plant tissues and infecting insects, forming a tripartite interaction and allowing for nutrient transfer across the fungus, the plant, and the insect (Fig 1). Most of our understanding of these interactions comes from studies investigating Metarhizium robertsii, whose mycelium colonizes both plant root cells and the soil larvae feeding on root tissue. Elegant experiments using radioactive isotopes showed M. robertsii both receiving carbon from the plant partner  and transferring nitrogen from insects to plant roots . These microcosm experiments tracked 15N and 13C in M. robertsii, plants, and larvae, demonstrating that insect-derived nitrogen is moved to the plant only when the fungus is present and that plant-derived carbon is transferred to the fungus and incorporated in fungal carbohydrates such as chitin and trehalose.
In order for EIPFs to be successful symbionts of plants and insects, they need to be able to invade and establish in both organisms. The insect infection processes in the genera Beauveria and Metarhizium have been well studied and serve as a general model for EIPF [1,13]. These fungi seem to use similar mechanisms to penetrate and establish inside their plant and insect hosts, with similar genes involved in insect infection and establishment in plants. Such genes have been hypothesized to derive from gene duplications  or horizontal gene transfer [14,15], implying shared processes in becoming plant and insect symbionts. We currently know more about the genes involved in EIPF insect infection than the genes involved in plant colonization .
The potential for EIPF in practical applications has been explored since the discovery of Beauveria bassiana in the early nineteenth century . These fungi are well known for promoting plant growth and enhancing insect virulence [27,28,30,31,32] and are currently explored for pest control in agriculture . EIPF are also exploited for their secondary metabolites, which are useful in biotechnology and medicine.