Contents lists available at ScienceDirect Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants Hexon Angel Contreras-Cornejo a, ⁎ , Lourdes Macías-Rodríguez b , Ek del-Val a,c , John Larsen a a Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Ex-Hacienda de San José de La Huerta, C.P. 58190, Morelia, Michoacán, Mexico b Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, C.P. 58030, Morelia, Michoacán, Mexico c Escuela Nacional de Estudios Superiores Unidad Morelia, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro No. 8701, Ex-Hacienda de San José de La Huerta, C.P. 58190, Morelia, Michoacán, Mexico ARTICLE INFO Keywords: Herbivory Maize S. frugiperda Secondary metabolites T. atroviride ABSTRACT Plant roots naturally associate with Trichoderma spp., which can promote plant health and nutrition. Despite that Trichoderma spp. are well-known biocontrol agents, information on their effects against foliar insect herbivory is limited. Here, we examined the effects of T. atroviride in providing maize (Zea mays) resistance against the insect herbivore Spodoptera frugiperda. Increased plant growth, reduced herbivory and altered insect feeding pattern were observed after maize inoculation with T. atroviride. Plant protection was correlated with increased emission of volatile terpenes and accumulation of jasmonic acid, an activator of defense responses against herbivory. Chemical analyses revealed that T. atroviride produced the volatiles 1-octen-3-ol and 6-pentyl-2H-pyran-2-one. Pharmacological tests showed that both compounds reduced the consumption of foliar tissue and altered the feeding pattern of S. frugiperda in a similar way to T. atroviride. These results provide new insight into the role of T. atroviride in plant health in terms of induction of resistance to insect herbivory and production of antifeedant secondary metabolites. 1. Introduction The fall armyworm, Spodoptera frugiperda, is a serious pest of nu- merous crops including maize (Cruz et al., 1999), where it is re- sponsable for severe yield losses every year in several countries (de Lange et al., 2014). Conventionally, S. frugiperda is managed with chemical insecticides, which have adverse impacts on human health and the environment, such as non-target effects on beneficial insects including pollinators and natural pest enemies (Pimentel, 1995). Fungi of the genus Trichoderma are common rhizosphere inhabitants (Druzhinina et al., 2011). They have been widely studied as biological control agents principally against plant pathogenic fungi, but also the activity against bacteria and nematodes is well documented (Harman et al., 2004; Reino et al., 2008; Martínez-Medina et al., 2017). Bio- control of Trichoderma includes the activity of hydrolytic enzymes that degradate the cell wall of the target organism. Secondary metabolites as peptaibols and isoprenoids from Trichoderma have been involved in the biocontrol of both foliar and root pathogens (Velázquez-Robledo et al., 2011; Contreras-Cornejo et al., 2014). Particularly, the metabolite 6- pentyl-2H-pyran-2-one (6-PP), a pyrone from Trichoderma spp. have been shown to inhibit the growth of the fungal pathogens Rhizoctonia solani, Fusarium oxysporum and Botrytis cinerea (Reino et al., 2008). In the rhizosphere, plant roots recognize molecules derived from micro- organisms as auxin-like metabolites or volatile organic compounds (VOCs), which in turn regulate developmental processes or activate defense responses effective against multiple agressors (Pozo et al., 2005; Garnica-Vergara et al., 2016; Hung et al., 2014). Plants respond to feeding by arthropod herbivores by producing a number of secondary compounds, including VOCs that are not only known to attract natural enemies of the herbivores, but they may also prime inducible defense responses in neighbouring plants, resulting in stronger and faster de- fense responses in plants exposed to those molecules (Dicke et al., 2009; Von Mèrey et al., 2011). In the belowgrownd, Trichoderma virens releases a blend of VOCs that trigger defense responses dependent of jasmonic acid (JA) sig- naling pathway (Contreras-Cornejo et al., 2014). Similarly, chewing insects, such as caterpillars predominantly activate the JA-mediated pathway, whereas feeding phloem-sucking herbivores frequently acti- vates the salicylic acid (SA) pathway (Rodriguez-Saona et al., 2010). The molecular mechanisms activated in response to herbivore at- tack involve several key regulatory proteins (Pieterse and Dicke, 2009; Kim and Felton, 2013). In this sense, the transcription factor MYC2, a http://dx.doi.org/10.1016/j.apsoil.2017.10.004 Received 2 April 2017; Received in revised form 6 October 2017; Accepted 9 October 2017 ⁎ Corresponding author. E-mail address: hcontreras@cieco.unam.mx (H.A. Contreras-Cornejo). Applied Soil Ecology xxx (xxxx) xxx–xxx 0929-1393/ © 2017 Elsevier B.V. All rights reserved. Please cite this article as: Contreras-Cornejo, H.A., Applied Soil Ecology (2017), http://dx.doi.org/10.1016/j.apsoil.2017.10.004