Manipulation of belowground scents for the benefit of agriculture 1 I. Hiltpold 1 and T.C.J. Turlings 2 2 3 1 Division of Plant Sciences, University of Missouri, 205 Curtis Hall, Columbia, MO 65211- 4 7020, USA 5 2 FARCE laboratory, University of Neuchâtel, Emile-Argand 11, 2000 Neuchâtel 6 Corresponding author: hiltpoldi@missouri.edu 7 8 ABSTRACT 9 Insect herbivory induces the synthesis and release of specific volatile compounds in plants. 10 These volatiles have been shown to be highly attractive to natural enemies of the herbivores, 11 such as predators, parasitic wasps or entomopathogenic nematodes. A few key compounds 12 mediating these so-called tritrophic interactions are known, but in most cases they remain to 13 be identified. In maize, the volatiles emitted upon feeding by leaf- or root-feeding arthropod 14 herbivores have been particularly well studied in the laboratory. Moreover, several genes and 15 biochemical pathways responsible for the production of the emitted volatiles have been 16 elucidated and described. These advances in understanding volatile emissions and their 17 ecological significance open up novel ways to modify plant volatile blends in order to 18 enhance their attractiveness to natural enemies. Here we briefly describe some of the 19 approaches that can be applied to exploit herbivore-induced volatile blends to enhance 20 biological control of belowground herbivores of maize. Based on the available literature, we 21 conclude that the most promising results can be obtained by manipulating the emission of 22 specific volatile compounds, while simultaneously enhancing the responsiveness of natural 23 enemies to particular compounds. However, such manipulative strategies require great caution 24 and we emphasize the importance of taking a holistic ecological approach and to precisely 25 evaluate risks and benefits of modifying volatile blends in the context of pest management. 26 27 Keywords pest control, pest management, plant protection, plant defense, plant volatile, 28 induce defense, plant secondary metabolite 29 30 INTRODUCTION 31 Thorns and waxes are among the obvious direct defences in plants, but a subtler and out-of - 32 sight defence arsenal is also in place in the long war between plants and herbivores. Indeed, a 33 rapidly increasing number of studies is revealing highly sophisticated chemical- based 34 defence strategies in plants, not only in the form of compounds that have a direct negative 35 impact on herbivores, but also in the form of volatiles that attract the natural enemies of 36 herbivores. This signaling towards a third trophic level is one of the acknowledged roles of 37 the so-called herbivore induced volatiles (HIPV) released during and after herbivory. Having 38 been first hypothesized by Price and colleagues (Price et al. 1980), the first evidence of such 39 interactions between three different trophic levels (Dicke & Sabelis 1988; Turlings et al. 40 1990) opened the door to a new interdisciplinary field of research. The resulting studies has 41 revealed that HIPV play a role in indirect plant defence in a number of systems, involving 42 parasitic wasps (Turlings et al. 1991), predatory arthropods (Dicke & Sabelis 1988), 43 entomopathogenic nematodes (Rasmann et al. 2005), and even birds (Mäntylä et al. 2008). 44 Research on HIPV has initially included maize, Zea mays L., as a model plant that is easy to 45 work with and shows a very strong HIPV production in response to herbivory (Turlings et al. 46 1990). In both the shoot (D'Alessandro & Turlings 2005) and the roots (Rasmann & Turlings 47 2008), HIPV have been well characterized for this important crop. In both biological 48 compartments, the plant has to be induced by insect herbivory before producing HIPV. De 49 novo synthesis of volatiles in the plant is triggered by elicitors present in the salivary or 50