Generalist and Specialist Mite Herbivores Induce Similar Defense Responses in Maize and Barley but Differ in Susceptibility to Benzoxazinoids
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fpls-09-01222 August 18, 2018 Time: 18:56 # 1 ORIGINAL RESEARCH published: 21 August 2018 doi: 10.3389/fpls.2018.01222 Generalist and Specialist Mite Herbivores Induce Similar Defense Responses in Maize and Barley but Differ in Susceptibility to Benzoxazinoids Huyen Bui1†, Robert Greenhalgh1†, Alice Ruckert2, Gunbharpur S. Gill2, Sarah Lee1, Ricardo A. Ramirez2 and Richard M. Clark1,3* 1 School of Biological Sciences, University of Utah, Salt Lake City, UT, United States, 2 Department of Biology, Utah State University, Logan, UT, United States, 3 Center for Cell and Genome Science, University of Utah, Salt Lake City, UT, United States Edited by: While substantial progress has been made in understanding defense responses of Raul Antonio Sperotto, cereals to insect herbivores, comparatively little is known about responses to feeding University of Taquari Valley, Brazil by spider mites. Nevertheless, several spider mite species, including the generalist Reviewed by: Mercedes Diaz-Mendoza, Tetranychus urticae and the grass specialist Oligonychus pratensis, cause damage on Centre for Plant Biotechnology cereals such as maize and wheat, especially during drought stress. To understand and Genomics, Spain Vasileios Fotopoulos, defense responses of cereals to spider mites, we characterized the transcriptomic Cyprus University of Technology, responses of maize and barley to herbivory by both mite species, and included a Cyprus wounding control against which modulation of defenses could be tested. T. urticae and *Correspondence: O. pratensis induced highly correlated changes in gene expression on both maize and Richard M. Clark [email protected] barley. Within 2 h, hundreds of genes were upregulated, and thousands of genes were †These authors have contributed up- or downregulated after 24 h. In general, expression changes were similar to those equally to this work induced by wounding, including for genes associated with jasmonic acid biosynthesis Specialty section: and signaling. Many genes encoding proteins involved in direct defenses, or those This article was submitted to required for herbivore-induced plant volatiles, were strongly upregulated in response Plant Microbe Interactions, to mite herbivory. Further, biosynthesis genes for benzoxazinoids, which are specialized a section of the journal Frontiers in Plant Science compounds of Poaceae with known roles in deterring insect herbivores, were induced Received: 28 May 2018 in maize. Compared to chewing insects, spider mites are cell content feeders and Accepted: 31 July 2018 cause grossly different patterns of tissue damage. Nonetheless, the gene expression Published: 21 August 2018 responses of maize to both mite herbivores, including for phytohormone signaling Citation: Bui H, Greenhalgh R, Ruckert A, pathways and for the synthesis of the benzoxazinoid 2-hydroxy-4,7-dimethoxy- Gill GS, Lee S, Ramirez RA and 1,4-benzoxazin-3-one glucoside, a known defensive metabolite against caterpillars, Clark RM (2018) Generalist resembled those reported for a generalist chewing insect, Spodoptera exigua. On and Specialist Mite Herbivores Induce Similar Defense Responses in Maize maize plants harboring mutations in several benzoxazinoid biosynthesis genes, T. urticae and Barley but Differ in Susceptibility performance dramatically increased compared to wild-type plants. In contrast, no to Benzoxazinoids. Front. Plant Sci. 9:1222. difference in performance was observed between mutant and wild-type plants for the doi: 10.3389/fpls.2018.01222 specialist O. pratensis. Collectively, our data provide little evidence that maize and barley Frontiers in Plant Science| www.frontiersin.org 1 August 2018| Volume 9| Article 1222 fpls-09-01222 August 18, 2018 Time: 18:56 # 2 Bui et al. Maize and Barley Responses to Spider Mite Herbivores defense responses differentiate herbivory between T. urticae and O. pratensis. Further, our work suggests that the likely route to specialization for O. pratensis involved the evolution of a robust mechanism to cope with the benzoxazinoid defenses of its cereal hosts. Keywords: Maize (Zea mays L.), Hordeum vulgare, Tetranychus urticae, Oligonychus pratensis, benzoxazinoid, spider mite, herbivore, HDMBOA INTRODUCTION or to potentially suppress plant defense responses that are broadly conserved (Ali and Agrawal, 2012). Alternatively, some Cereal crops of the grass family (Poaceae) account for the specialists have evolved the ability to suppress or otherwise majority of human calories, and reductions in their yield circumvent plant defenses, potentially ameliorating the role dramatically impact human welfare. Abiotic factors, such as of detoxification, or instead have evolved highly specialized drought, are a major source of unrealized yield (Boyer, 1982), detoxification abilities to cope with the toxins they encounter in while another well-characterized source of loss is from herbivory their preferred plant hosts (Dobler et al., 2012; Glas et al., 2014; by insects (Oerke, 2006). Spider mites (Acari: Tetranychidae) Maag et al., 2014; Wouters et al., 2014). belong to the Chelicerata, an arthropod lineage that diverged Like dicots, monocots, including grasses, are attacked by more than 450 million years ago (Dunlop, 2010), and hence generalist and specialist herbivores of diverse feeding guilds, evolved herbivory independently from insects. Crops including including leaf-chewing (e.g., caterpillars) and piercing-sucking maize (Zea mays) and wheat (Triticum sp.) are susceptible not (e.g., aphids and whiteflies). As for dicots, JA signaling and only to insects but also to spider mites, especially during drought the production of specialized compounds feature prominently conditions (Al-Kaisi et al., 2013), where yield losses as high in monocot responses to insect herbivory (Meihls et al., 2012; as 47.2% for maize have been reported (Bacon et al., 1962). Tzin et al., 2015a, 2017). Of the downstream specialized Nevertheless, relatively little is known about the molecular nature compounds in grasses, the best studied are benzoxazinoids, of the defenses plants use to deter spider mites, especially for which are 1,4-benzoxazin-3-one derivatives produced by cereals grasses. including maize, wheat, and rye (Zúñiga et al., 1983; Niemeyer, As shown by molecular studies of plant–herbivore 2009). In maize, levels of benzoxazinoids are highest in interactions, largely with insects and dicots such as Arabidopsis seedlings (Cambier et al., 2000), but can be locally induced thaliana and tomato (Solanum lycopersicum), many plants at feeding sites in the leaves of older plants (Köhler et al., complement constitutive defenses (like trichomes) with rapid, 2015; Maag et al., 2016). The most studied benzoxazinoid, inducible ones that negatively impact herbivores (Howe and 4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), is Jander, 2008). For instance, herbivore-associated triggers stored in vacuoles as an inactive glucoside (Glc) conjugate. like physical damage, oral secretions, or frass, alone or in Upon tissue damage by herbivores, DIMBOA-Glc, as well as combination, lead to changes in the production of specialized derivatives such as 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3- metabolites or defensive proteins that deter herbivores (Howe one glucoside (HDMBOA-Glc), are exposed to glucosidases in and Jander, 2008; Ray et al., 2015). In dicots, molecular responses plastids (Meihls et al., 2012). This leads to the release of the to insect herbivores are mediated largely by phytohormones, aglucones, which are toxic to herbivores, potentially by several especially jasmonates (jasmonic acid, or JA, and its derivatives or modes of action (Wouters et al., 2016). conjugates), which induce transcriptomic reprogramming within Several spider mite species are significant field pests on cereals. hours (Howe and Jander, 2008). Some defenses act directly, These include Tetranychus urticae (the two-spotted spider mite) such as toxic compounds or protease inhibitors that retard on maize, and Oligonychus pratensis (the Banks grass mite) on digestion in an herbivore’s gut. Others act indirectly, like plant both maize and distant relatives including wheat (Figure 1A; volatiles, which can serve as olfactory cues for predators to locate Brandenburg and Kennedy, 1982; Mansour and Bar-Zur, 1992; herbivores at feeding sites (Turlings and Erb, 2018). Archer and Bynum, 1993; Tadmor et al., 1999; Blasi et al., 2015). The type and magnitude of inducible defenses is influenced by T. urticae is an extreme generalist that has been documented on several factors. One of these is feeding guild. Chewing insects like more than 100 plant families (Grbic´ et al., 2011). In contrast, caterpillars, for instance, cause extensive tissue damage and elicit O. pratensis is a specialist on plants in the Poaceae, though different defense responses compared to phloem-feeding insects it has been reported on a few non-grass hosts including date like aphids, which cause minimal loss of plant tissue (Howe palm (which is also a monocot) (Ward et al., 1972; Foster et al., and Jander, 2008). Additionally, plant responses to generalist 1977; Chandler et al., 1979; Holtzer et al., 1984; Archer and herbivores, to which ∼10% of plant-feeding insects belong (Ali Bynum, 1993; Bynum et al., 2015; Negm et al., 2015). As cell- and Agrawal, 2012), can differ from those induced by specialists. content feeders, spider mites belong to a different feeding guild Generalist herbivores feed on hosts in many plant families. They than the best studied insect herbivores