Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi

Abstract

This review examines the symbiotic, evolutionary, proteomic and genetic basis for a group of fungi that occupy a specialized niche as insect pathogens as well as endophytes. We focus primarily on species in the genera Metarhizium and Beauveria, traditionally recognized as insect pathogenic fungi but are also found as plant symbionts. Phylogenetic evidence suggests that these fungi are more closely related to grass endophytes and diverged from that lineage ca. 100 MYA. We explore how the dual life cycles of these fungi as insect pathogens and endophytes are coupled. We discuss the evolution of insect pathogenesis while maintaining an endophytic lifestyle and provide examples of genes that may be involved in the transition toward insect pathogenicity. That is, some genes for insect pathogenesis may have been co-opted from genes involved in endophytic colonization. Other genes may be multifunctional and serve in both lifestyle capacities. We suggest that their evolution as insect pathogens allowed them to effectively barter a specialized nitrogen source (i.e. insects) with host plants for photosynthate. These ubiquitous fungi may play an important role as plant growth promoters and have a potential reservoir of secondary metabolites.

Genome‐wide identification of pathogenicity, conidiation and colony sectorization genes in Metarhizium robertsii

“…The ascomycete genus Metarhizium has a world‐wide distribution from the arctic to the tropics and occupies an impressive array of environments including forests, savannahs, swamps, coastal zones and deserts. The representative species of the genus, Metarhizium robertsii (formerly known as Metarhizium anisopliae ), is extraordinarily versatile being a broad host range pathogen of insects as well as a saprophyte, and in the case of some isolates such as ARSEF2575 (used in this study) able to form mutualistic relationships with plants by colonising the rhizoplane (Barelli et al ., ). Consequently, M. robertsii experiences several distinctive sets of selective pressures, allowing the function of a gene to be assessed during several major fungal lifestyles including parasitism, saprophytism and symbiosis.…”

Back to the future: cordycipitoid fungi in a postgenomic world

“…bassiana could occur as an endophyte in the tissues of maize plants and exerted a degree of natural biological control against European corn borer larvae, Ostrinia nubilalis (Lewis and Cossentine 1986; Bing and Lewis 1991). This endophytic “hidden” life for Beauveria that was so startling when first discovered is now known to be widespread and even rather common in a wide range of herbaceous and woody plants (e.g., Vidal and Jaber 2015; Barelli et al 2016; Greenfield et al 2016). More recently, it has been found that species of Metarhizium in particular can also lead a “secret” lives an endophyte (Behie et al 2015; Barelli et al 2016) but that these entomopathogenic fungi seem much more commonly to form natural rhizosphere associations with plant roots that are mutually beneficial (Bidochka et al 2001; St. Leger 2008); these root–fungus–soil interactions seem to function in a manner that strongly resembles those involving ectomycorrhizal basidiomycetes.…”

“…This endophytic “hidden” life for Beauveria that was so startling when first discovered is now known to be widespread and even rather common in a wide range of herbaceous and woody plants (e.g., Vidal and Jaber 2015; Barelli et al 2016; Greenfield et al 2016). More recently, it has been found that species of Metarhizium in particular can also lead a “secret” lives an endophyte (Behie et al 2015; Barelli et al 2016) but that these entomopathogenic fungi seem much more commonly to form natural rhizosphere associations with plant roots that are mutually beneficial (Bidochka et al 2001; St. Leger 2008); these root–fungus–soil interactions seem to function in a manner that strongly resembles those involving ectomycorrhizal basidiomycetes. The physiological and genomic complexities of these cooperative interactions between plants and entomopathogenic fungi are now being studied actively (Pava-Ripoll et al 2011; Behie and Bidochka 2014a, 2014b; Behie et al 2015) and yielding some remarkable results.…”

Biological Control beneath the Feet: A Review of Crop Protection against Insect Root Herbivores

“…[93,94]. For instance, saprophytic EPFs ( B. bassiana , M. anisopliae ) can establish colonies in plant roots even in the absence of insect hosts [95]. This colonization allows a direct transfer of nutrients such as nitrogen from an insect cadaver to the plant [96].…”