Effects of a maize root pest and fungal pathogen on entomopathogenic fungal rhizosphere colonization, endophytism and induction of plant hormones

Some entomopathogenic fungi, such as Metarhizium spp. and Beauveria spp., closely interact with plants by colonizing the rhizosphere or growing endophytically inside root tissues. These characteristics increase the potential for endophytic entomopathogenic fungi to persist in the root system when used as biological control agents. The mechanism by which endophytic entomopathogenic fungi are capable to colonize the internal plant tissues is also influenced by plants and can be regarded as an adaptive protection acquired by plants against herbivorous insects. The mutual benefits obtained by plants and fungi through this peculiar endophytic association supports the bodyguard hypothesis. The objectives of this study were to evaluate the ability of different isolates of Metarhizium spp. and a single isolate of Beauveria bassiana, coated onto seeds, to colonize the rhizosphere and root tissues of maize (Zea mays) and to assess whether the presence of an insect pest and fungal root pathogen influenced this interaction. All the entomopathogenic fungal isolates tested were able to colonize the rhizosphere to some extent, but one isolate of M. anisopliae and the one of M. robertsii performed best. Overall, the presence of Costelytra giveni (Scarabaeidae) larvae significantly decreased rhizosphere colonization by the entomopathogens, while the phytopathogenic fungus Fusarium graminearum (Nectriaceae: Hypocreales) did not. Similarly, the presence of C. giveni decreased endophytic growth in root tissues by around 75% when considering all entomopathogens together. In contrast, a 112% increase in overall root endophytic colonization occurred in the presence of F. graminearum. Salicylic acid (SA) and jasmonic acid (JA) content in maize plants changed depending on the isolate of M. anisopliae incorporated through seed coating and root herbivory by larval presence. In the absence of C. giveni, plants treated with M. anisopliae A1080 had higher SA and JA root content than control plants. Conversely, when larvae were present, maize plants treated with M. anisopliae F672 had increased levels of both phytohormones, indicating a potentially primed state. The observed decrease in root colonization by some entomopathogenic fungal isolates in the presence of larvae of C. giveni and the increase in endophytic colonization in the presence of F. graminearum are in accordance with the bodyguard hypothesis. Additionally, the changes observed in the SA and JA content in Metarhizium treated plants corresponded to plant responses related to systemic acquired resistance and to induced systemic resistance. Our results demonstrate that biotic soil factors can shape the outcome of endophytic entomopathogenic fungi-plant interaction, as well as affecting the plant physiology.