Metabolomics of Thrips Resistance in Pepper (Capsicum spp.) Reveals Monomer and Dimer Acyclic Diterpene Glycosides as Potential Chemical Defenses

Abstract

The development of pesticide resistance in insects and recent bans on pesticides call for the identification of natural sources of resistance in crops. Here, we used natural variation in pepper ( Capsicum spp.) resistance combined with an untargeted metabolomics approach to detect secondary metabolites related to thrips ( Frankliniella occidentalis ) resistance. Using leaf disc choice assays, we tested 11 Capsicum accessions of C. annuum and C. chinense in both vegetative and flowering stages for thrips resistance. Metabolites in the leaves of these 11 accessions were analyzed using LC-MS based untargeted metabolomics. The choice assays showed significant differences among the accessions in thrips feeding damage. The level of resistance depended on plant developmental stage. Metabolomics analyses showed differences in metabolomes among the Capsicum species and plant developmental stages. Moreover, metabolomic profiles of resistant and susceptible accessions differed. Monomer and dimer acyclic diterpene glycosides (capsianosides) were pinpointed as metabolites that were related to thrips resistance. Sucrose and malonylated flavone glycosides were related to susceptibility. To our knowledge, this is the first time that dimer capsianosides of pepper have been linked to insect resistance. Our results show the potential of untargeted metabolomics as a tool for discovering metabolites that are important in plant – insect interactions. Electronic supplementary material The online version of this article (10.1007/s10886-019-01074-4) contains supplementary material, which is available to authorized users.

High Concentrations of Very Long Chain Leaf Wax Alkanes of Thrips Susceptible Pepper Accessions (Capsicum spp)

“…The classification of relative thrips resistance or susceptibility of the accessions was based on the leaf disc choice assays (Table 1 , Macel et al 2019 ). This resistance classification was compared with resistance in whole plant thrips performance assays and in no-choice leaf discs feeding damage assays (Visschers et al 2019a ) (Table 1 ).…”

“…Recent bans on pesticides and increasing resistance to the insecticides that are still used call for identifying natural sources of resistance in crops. Plant metabolites linked to thrips resistance are amongst others alkaloids (Liu et al 2019 ), chlorogenic acid (Leiss et al 2009 ), tocopherols (Maharijaya et al 2012 ) and diterpene glycosides (Macel et al 2019 ; Maharijaya et al 2018 ). However, in most studies the entire leaf was analyzed and not specifically the wax compounds.…”

Resistance to three thrips species in Capsicum spp. depends on site conditions and geographic regions

“…F I G U R E 1 Schematic overview of previous studies conducted on resistance to thrips in Capsicum (Macel et al, 2019;Visschers et al, 2019) that formed the foundation of the experiments reported here (displayed in bold)…”

“…Previously, we screened 40 Capsicum accessions for resistance to two thrips species using leaf disc assays . This resulted in the identification of 11 accessions that were either relatively resistant or susceptible to F. occidentalis (Macel et al, 2019).…”

Specific decorations of 17-hydroxygeranyllinalool diterpene glycosides solve the autotoxicity problem of chemical defense inNicotiana attenuata

“…Diterpene glycosides (DTGs) are a diverse compound class whose members are often associated with phytotoxic activities (Macias et al, 2008) and have potent antiherbivore resistance/deterrence effects. For example, the abundance of monomers and dimers of capsianosides is correlated with thrips resistance in pepper (Macel et al, 2019) and 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs) in Nicotiana species have been shown to function in resistance against larvae of the specialist herbivore Manduca sexta (Lou and Baldwin, 2003;Jassbi et al, 2008;Heiling et al, 2010) and the generalist herbivore, Heliothis virescens (Snook et al, 1997).…”