Biological Control xxx (2017) xxx–xxx Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Review Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? ⇑ Lara R. Jaber a, , Bonnie H. Ownley b a Department of Plant Protection, Faculty of Agriculture, The University of Jordan, 11942 Amman, Jordan b Department of Entomology and Plant Pathology, The University of Tennessee, Knoxville, TN 37996-4560, USA highlights Fungal entomopathogens as endophytes are garnering increased research attention. These agents have a promising potential for biocontrol of insect and pathogen pests. Consistent plant colonization must be established to achieve endophytic protection. Interaction with other endophytes should be considered to attain optimal efficacy. Elucidating modes of action is essential to realize their full biocontrol potential. article info abstract Article history: An increasing number of recent studies demonstrate that entomopathogenic fungi, often solely consid- Received 2 December 2016 ered as insect pathogens, play additional roles in nature, including endophytism, plant disease antago- Revised 21 January 2017 nism, plant growth promotion, and rhizosphere colonization. These newly emerging, but not yet fully Accepted 23 January 2017 understood, ecological roles hint at the possibility that we have been overlooking important attributes Available online xxxx in our quest to develop fungal entomopathogens exclusively as inundative biopesticides against insect and other arthropod pests. Such additional roles recently-discovered to be played by entomopathogenic Keywords: fungi provide opportunities for the multiple use of these fungi in integrated pest management (IPM) Dual microbial control agents strategies. Of particular interest is the ability displayed by various genera of entomopathogenic fungi Endophytes Fungal entomopathogens to colonize a wide variety of plant species in different families, both naturally and artificially following Hypocreales inoculation, and confer protection against not only insect pests but also plant pathogens. This article Insect pests reviews the literature currently available on the endophytic colonization of different host plants by fun- Integrated pest management (IPM) gal entomopathogens, and summarizes the negative effects of such colonization on insect pests and plant Mode of action pathogens that have been reported to date. It also addresses the possible mechanisms of protection con- Plant diseases ferred by endophytic fungal entomopathogens and explores the potential use of these fungi as dual microbial control agents against both insect and pathogen pests. Moreover, interactions amongst endo- phytic fungal entomopathogens and other endophytes are discussed. Finally, current limitations and future research directions for the innovative use of endophytic fungal entomopathogens as dual microbial control agents are summarized. Ó 2017 Elsevier Inc. All rights reserved. Contents 1. Introduction . ....................................................................................................... 00 2. Fungal entomopathogens as endophytes . ................................................................. 00 3. Endophytic fungal entomopathogens and potential for biological control of insect pests . .............................. 00 4. Endophytic fungal entomopathogens and potential for biological control of plant diseases . .............................. 00 5. Possible mechanisms of plant disease control by endophytic fungal entomopathogens.............................................. 00 DOI of original article: http://dx.doi.org/10.1016/j.biocontrol.2017.01.013 ⇑ Corresponding author. E-mail address: [email protected] (L.R. Jaber). http://dx.doi.org/10.1016/j.biocontrol.2017.01.018 1049-9644/Ó 2017 Elsevier Inc. All rights reserved. Please cite this article in press as: Jaber, L.R., Ownley, B.H. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens?. Biological Control (2017), http://dx.doi.org/10.1016/j.biocontrol.2017.01.018 2 L.R. Jaber, B.H. Ownley / Biological Control xxx (2017) xxx–xxx 5.1. Direct suppression of plant pathogens. ............................................................................. 00 5.2. Induction of systemic plant resistance. ............................................................................. 00 5.3. Promotion of plant growth . ............................................................................. 00 6. Interaction of endophytic fungal entomopathogens with other endophytes . .................................................... 00 7. Conclusions and future prospects . ....................................................................... 00 Acknowledgments . .......................................................................................... 00 References . .......................................................................................................... 00 1. Introduction Even though many other definitions have been used ever since (see Box 1 in Hyde and Soytong, 2008), one common denominator Fungal entomopathogens, often solely considered as insect amongst them is that endophytes are organisms (fungi or bacteria) pathogens, have been studied for over a hundred years without that colonize internal plant tissues without causing apparent reaching their full potential as effective microbial control agents; symptoms or harm to their plant host. So defined, endophytes especially under field conditions (Vega et al., 2009). A growing comprise a diverse polyphyletic group of microorganisms that body of literature hints at the possibility that we have been over- can exhibit more than one type of life history at distinct life stages looking important attributes of fungal entomopathogens in our (Arnold and Lewis, 2005). quest to develop these microorganisms exclusively as biopesti- Although ubiquitous amongst terrestrial plants (Petrini, 1991; cides. An increasing number of recent studies demonstrate that Arnold et al., 2001), the majority of endophyte research has entomopathogenic fungi play additional roles in nature, including focused to date on the vertically-transmitted endophytes within endophytism, plant disease antagonism, plant growth promotion, the genus Neotyphodium (Clavicipitaceae) that systemically colo- and rhizosphere colonization. These newly emerging, but not yet nize the above-ground parts of some grasses. These clavicipita- fully understood, ecological roles provide opportunities for the ceous endophytes are generally known to confer an array of multiple use of fungal entomopathogens in integrated pest man- potential fitness benefits to their grass host plants (Kuldau and agement (IPM) strategies (Vega et al., 2009; Lacey et al., 2015). Bacon, 2008). Less attention has been given to the horizontally- Various genera of entomopathogenic fungi have recently been transmitted non-clavicipitaceous endophytes, which are wide- shown to act as plant endophytes in a variety of host plants spread in nature and dominated by the Ascomycetes (Arnold and (reviewed in Section 2 below), antagonists to plant pathogens Lutzoni, 2007); of which several genera are fungal ento- (Goettel et al., 2008; Ownley et al., 2008, 2010; Sasan and mopathogens (Ascomycota: Hypocreales). Bidochka, 2013; Jaber and Salem, 2014; Jaber, 2015), plant growth Emerging as an exciting new area of research, ‘fungal ento- promoters (Kabaluk and Ericsson, 2007; Garcia et al., 2011; Sasan mopathogens as endophytes’ has only rather recently been incor- and Bidochka, 2012; Liao et al., 2014; Lopez and Sword, 2015; porated into an over 100-year-old endophyte research base Jaber and Enkerli, 2016, 2017), and beneficial rhizosphere colonizers following the recovery of various genera of fungal ento- (Hu and St. Leger, 2002; St. Leger, 2008; Bruck, 2010; Pava-Ripoll mopathogens as endophytes from different plant species (Vega et al., 2011). Despite these newly discovered attributes, attention et al., 2008). Some of these fungi have been reported as naturally has mainly focused on developing these entomopathogenic fungal occurring endophytes, while others have been introduced into species as inundative biopesticides against insect and other arthro- the plant using different inoculation techniques (reviewed in pod pests (de Faria and Wraight, 2007). Inundative releases of bio- Table 1 in Vega, 2008). Pioneering work on entomopathogenic control agents normally rely on the direct action of the released endophytes was conducted with Beauveria bassiana (Balsamo) agents, but not on successive generations (Vincentetal.,2007). Vuillemin (Ascomycota: Hypocreales), a ubiquitous soil-borne fun- However, the emerging multiple roles played by fungal ento- gus that infects a wide range of different insects (>700 insect spe- mopathogens provide promising potential for their indirect, multi- cies; Inglis et al., 2001) and is one of the most commercialized faceted and cost-effective use in sustainable agriculture, for fungal biopesticides (de Faria and Wraight, 2007). Lewis and instance as biofertilizers (Kabaluk and Ericsson, 2007; Sasan and Cossentine (1986) credited the season-long suppression of the Bidochka, 2012; Jaber and Enkerli, 2016, 2017), vertically- European corn borer Ostrinia nubilalis (Hübner) (Lepidoptera: transmitted fungal endophytes (Quesada-Moraga et al., 2014; Pyralidae) in maize Zea mays L.