Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Free conidia of entomopathogenic fungi modify quality traits by changing glutathione levels after an oxidant stimulus José Miguel Castillo-Minjarez a , Paul Misael Garza-López b , Javier Barrios-González a , Octavio Loera a, ⁎ a Universidad Autónoma Metropolitana-Iztapalapa, Departamento de Biotecnología, San Rafael Atlixco 186, Col. Vicentina, C. P. 09340 México D.F., Mexico b Instituto de Ciencias Agropecuarias, Universidad Autónoma del Estado de Hidalgo, Tulancingo de Bravo, Hidalgo, Mexico ARTICLE INFO Keywords: Conidia quality Dormant conidia Glutathione Cross protection Stress ABSTRACT Adverse environmental conditions (e.g. high temperature, high osmotic pressure, atmospheric changes, solar radiation, etc.) reduce the efficacy of conidia from entomopathogenic fungi used for biological control. Strategies to improve the quality traits of conidia include the introduction of sub-lethal stress treatments applied to fungal mycelium, which can improve the resistance of generated conidia to several stress factors. This work presents for the first time evidence that free conidia of Metarhizium robertsii Xoch8.1, Beauveria bassiana Tac1.1 and Cordyceps javanica CHE-CNRCB303, subjected directly to oxidant pulses (26% O 2 ), had increased osmotic stress resistance compared to control conidia (maintained at 21% O 2 ). In addition, germination and thermotolerance improved in conidia of M. robertsii Xoch8.1 and B. bassiana Tac1.1. Only one pulse was enough to observe these positive effects on the stress tolerance of the free conidia. However, the Cordyceps genus showed an extreme sensitivity to the treatment, since the quality diminished for Cordyceps fumosorosea ARSEF3302, and in the case of C. javanica CHE-CNRCB303 the treatment affected those tolerance features. In addition, changes in the level of glutathione in the conidia indicated that the treatment could generate oxidative stress, which affects quality. In conclusion, despite the low metabolic activity in free conidia in a latency state, these responded to 26% O 2 pulses, modifying quality traits and in some cases, inducing cross protection in a species-dependent response. The information of this research could be tested in harvested conidia used in the preparation of formulations for biological control. 1. Introduction The use of biopesticides has increased in agricultural production, which has helped to mitigate some of the problems that have arisen from over use of chemical pesticides (Duc et al., 2015; Miranda- Hernández et al., 2016). These include damage to human health (Allen and Levy, 2013; Kamel, 2013) and the environment (Jennings and Li, 2014; Smalling et al., 2013), and the development of resistance (Lai and Su, 2011). Conidia of entomopathogenic fungi have been formulated in several commercial biopesticide products, since they naturally infect insects (Motta-Delgado and Murcia-Ordoñez, 2011; Rechcigl and Rechcigl, 1999; Singh et al., 2011). However, there are difficulties in the application of these biopesticides, since adverse environmental conditions affect the efficacy; these include high temperatures, solar radiation (Inglis et al., 2001; Lacey et al., 2001), hypersaline and water deficient environments that cause osmotic stress (Martínez-Villarreal et al., 2016). In addition, defense mechanisms of insects include be- havioral responses that increase body temperature, grooming and production of reactive oxygen species (ROS), all of which can prevent infection (Inglis et al., 2001; Miranda-Hernández et al., 2016; Ortiz- Urquiza et al., 2015; Vega et al., 2009). The quality of a biological control agent can be defined as the ability to function as intended after release in the field (Leppla, 1984). In the case of entomopathogenic fungi, the factors that affect the quality must be identified, as the quality traits in the conidia to persist in the field. Aspects related to the sensitivity of conidia to adverse biotic and abiotic factors are as important as efficient production and high virulence, since those traits determine persistence in the environment (Posada and Vega, 2005; Ravensberg, 2011). Hence, there is an outstanding interest in finding treatments that improve the quality traits of en- tomopathogenic fungal conidia, especially those amenable to mass production. In this sense, the physical, chemical and nutritional https://doi.org/10.1016/j.biocontrol.2019.104011 Received 26 May 2018; Received in revised form 8 June 2019; Accepted 17 June 2019 Abbreviations: 21%, Normal or control atmosphere; 26%, Oxygen-enriched atmosphere; Bb, B. bassiana Tac1.1; Cf, C. fumosorosea ARSEF3302; Cj, C. javanica CHE- CNRCB303; G, Germination; Mr, M. robertsii Xoch8.1; OS, Resistance to osmotic stress; TS, Resistance to thermic stress ⁎ Corresponding author. E-mail address: loera@xanum.uam.mx (O. Loera). Biological Control 137 (2019) 104011 Available online 18 June 2019 1049-9644/ © 2019 Elsevier Inc. All rights reserved. T