Interactions Between a Belowground Herbivore and P

Authors: Moniek Van Geem Jeffrey A Harvey Anne Marie Cortesero Ciska E Raaijmakers Rieta Gols

Publish Date: 2015/08/14

Volume: 41, Issue: 8, Pages: 696-707

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Abstract

Plants are attacked by both above and belowground herbivores Toxic secondary compounds are part of the chemical defense arsenal of plants against a range of antagonists and are subject to genetic variation Plants also produce primary metabolites amino acids nutrients sugars that function as essential compounds for growth and survival Wild cabbage populations growing on the Dorset coast of the UK exhibit genetically different chemical defense profiles even though they are located within a few kilometers of each other As in other Brassicaceae the defensive chemicals in wild cabbages constitute among others secondary metabolites called glucosinolates Here we used five Dorset populations of wild cabbage to study the effect of belowground herbivory by the cabbage root fly on primary and secondary chemistry and whether differences in chemistry affected the performance of the belowground herbivore There were significant differences in total root concentrations and chemical profiles of glucosinolates amino acids and sugars among the five wild cabbage populations Glucosinolate concentrations not only differed among the populations but also were affected by root fly herbivory Amino acid and sugar concentrations also differed among the populations but were not affected by root fly herbivory Overall populationrelated differences in plant chemistry were more pronounced for the glucosinolates than for amino acids and sugars The performance of the root herbivore did not differ among the populations tested Survival of the root fly was low 40  suggesting that other belowground factors may override potential differences in effects related to primary and secondary chemistryThe study of plantinsect interactions is a foundation for understanding evolutionary and community ecology Schoonhoven et al 2005 Early studies on plantinsect interactions focused primarily on the aboveground compartment ignoring the fact that plants through their roots also interact with the biotic environment belowground The importance of biotic interactions in the rhizosphere has become apparent in the past two decades Masters and Brown 1992 Masters et al 1993 van der Putten et al 2001 Moreover the belowground environment has consequences for biotic interactions with aboveground plant tissues and vice versa Wardle et al 2004 Plants are attacked by insect herbivores both in the aboveground and belowground domains often simultaneously It has been shown that belowground herbivores by removing root tissues negatively affect the functioning of roots for instance through a reduction in the uptake and storage of nutrients which cascade to other plant tissues thereby affecting the whole plant Blossey and HuntJoshi 2003 van der Putten 2003Plants tissues produce both primary and secondary chemical compounds metabolites that have different biological functions Primary metabolites are those that plants need in order to grow develop and reproduce and include amino acids and sugars Bidwell 1974 Gibson 2005 Plants also produce secondary metabolites that protect organs especially those that are important for survival and reproduction against herbivores and pathogens Secondary metabolites also are used to complete with other plants to attract pollinators and seed dispersers to mitigate symbiotic interactions and to protect against UVlight or other physical stress Wink 1999 The balance between concentrations of secondary and primary metabolites is a determinant of food plant quality for insect herbivores Awmack and Leather 2002 Scriber and Slansky 1981 Plant primary metabolites provide essential nutrients for insect development whereas secondary metabolites can be repellent and/or toxic for many insects and thus interfere with insect behavior and physiology Schoonhoven et al 2005 Scriber and Slansky 1981 However for many coevolved specialist herbivores hostderived secondary metabolites function as feeding or oviposition stimulants Schoonhoven et al 2005Plant secondary chemistry is phylogenetically conserved and genetic variation among populations often is maintained over different scales of space and time Agrawal et al 2012 Berenbaum and Zangerl 1991 Hartmann 1996 Hoy et al 1998 van Geem et al 2013 Various studies have shown that concentrations and specific compounds differ among species within a plant family individuals and populations within a species and even plant structures of individual plants Fahey et al 2001 Fordyce and Malcolm 2000 Gols et al 2008b Häring et al 2007 Hartmann 1996 Thus far most studies on the evolution of diversity in secondary metabolites driven by insect herbivores have focused on aboveground plant tissues Less is known about variation in defense chemistry in the rhizosphere and effects of defensive chemistry on belowground herbivores Moreover intraspecific variation in primary chemistry has been virtually ignoredWild cabbage Brassica oleracea plants grow naturally along the Atlantic coasts of northwestern Europe and belong to the large family Brassicaceae Plant species within this family all produce glucosinolates hereafter GS inducible secondary metabolites that play a role in mediating plantinsect interactions Gols et al 2009 Hopkins et al 2009 GS profiles not only differ among populations Gols et al 2008b Mithen et al 1995 Moyes et al 2000 Newton et al 2009 van Geem et al 2013 but also between individual plants within a population Mithen et al 1995 and between different plant organs of individual plants Bennett and Wallsgrove 1994 Variation in defense chemistry profiles makes the English wild cabbage populations a good model system for studying the effect of plant secondary metabolites on insect performance while incorporating genetic variation that is maintained over a limited spatial scale eg 20 kmInduction of GS has been wellstudied in aboveground plant tissues Agrawal et al 1999 Agrawal 2000 Gols et al 2008a b Harvey et al 2007 2011 Poelman et al 2008 but less so in belowground tissues Soler et al 2005 van Dam and Raaijmakers 2006 Moreover the number of studies investigating the combined effect of primary and secondary metabolites in leaves on insect performance in wild plants are limited but see Cole 1997 Wurst et al 2006 Even less is known about variation in primary and secondary chemical profiles in roots their effect on root insect development and whether concentrations of these chemicals change in response to belowground herbivory which is the topic of this studyThe main aim of our study was to determine whether the chemical profiles of primary and secondary metabolites in roots differed among the wild cabbage populations in response to belowground herbivory We also were interested whether there was a link between root fly performance and root chemistry In a greenhouse experiment we grew plants from seeds collected from five naturally growing populations in Dorset England that differ in foliar GS chemistry Gols et al 2008b Newton et al 2010 We compared development of a specialist herbivore the cabbage root fly Delia radicum L Diptera Anthomyiidae on these plants In addition to root chemistry we also measured root biomass and insect performance variables Given that previous studies have shown that there is constitutive and inducible variation in GS chemistry in leaf tissues of the cabbage populations we hypothesize that 1 this variation also is present in the roots and that 2 the performance of root flies would differ when grown on different populations as has been demonstrated with aboveground insects

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