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(Phratora Vulgatissima) on Salix F2 Hybrids: the Importance of Phenolics

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(Phratora Vulgatissima) on Salix F2 Hybrids: the Importance of Phenolics J Chem Ecol (2013) 39:516–524 DOI 10.1007/s10886-013-0266-3 Performance of an Herbivorous Leaf Beetle (Phratora vulgatissima)onSalix F2 Hybrids: the Importance of Phenolics Mikaela Torp & Anna Lehrman & Johan A. Stenberg & Riitta Julkunen-Tiitto & Christer Björkman Received: 18 September 2012 /Revised: 30 January 2013 /Accepted: 31 January 2013 /Published online: 1 March 2013 # Springer Science+Business Media New York 2013 Abstract The genotype of the plant determines, through the to Phratora vulgatissima. Synergistic effects of these com- expression of the phenotype, how well it is suited as food for pounds, as well as potential threshold concentrations, are herbivores. Since hybridization often results in profound ge- plausible. In addition, we found considerable variation in both nomic alterations with subsequent changes in phenotypic distributions and concentrations of different phenolics in the traits, it has the potential to significantly affect plant- F2 hybrids. The phenolic profiles of parental genotypes and herbivore interactions. In this study, we used a population of F2 hybrids differed significantly (e.g., novel compounds F2 hybrids that originated from a cross between a Salix appeared in the hybrids) suggesting genomic alterations with viminalis and a Salix dasyclados genotype, which differed in subsequent changes in biosynthetic pathways in the hybrids. both phenolic content and resistance to the herbivorous leaf beetle Phratora vulgatissima. We screened for plants that Keywords Hybridization . Phenolics . Luteolin . showed a great variability in leaf beetle performance (i.e., Salicylates . Phratora vulgatissima performance . oviposition and survival). By correlating leaf phenolics to Resistance . Salix the response of the herbivores, we evaluated the importance of different phenolic compounds for Salix resistance to the targeted insect species. The performance of P. vulgatissima Introduction varied among the F2 hybrids, and two patterns of resistance emerged: leaf beetle oviposition was intermediate on the F2 Hybridization between species is common in nature (Arnold, hybrids compared to the parental genotypes, whereas leaf 1997) and can result in substantial changes in various plant beetle survival demonstrated similarities to one of the parents. characteristics. Parental species and hybrids often differ in The findings indicate that these life history traits are controlled resistance to herbivores. This variation is probably mediated by different resistance mechanisms that are inherited differ- by modifications of plant chemistry, morphology, or phenology ently in the hybrids. Salicylates and a methylated luteolin in hybrid plants compared to their parents (Fritz et al., 1999; derivative seem to play major roles in hybrid resistance Cheng et al., 2011). Patterns of hybrid resistance are diverse: hybrids can express intermediate (Fritz et al., 1998;Czesaket al., 2004; Hochwender and Fritz, 2004), equal (Orians et al., M. Torp (*) : J. A. Stenberg : C. Björkman Department of Ecology, Swedish University of Agricultural 1997; Fritz et al., 1998;Hallgrenetal.,2003), increased (Fritz, Sciences, P.O. Box 7044, 750 07 Uppsala, Sweden 1999; Hjältén and Hallgren, 2002; Hochwender and Fritz, e-mail: [email protected] 2004), or decreased (Whitham, 1989; Orians et al., 1997; Hjältén, 1998; Czesak et al., 2004) resistance compared to A. Lehrman Department of Crop Production Ecology, Swedish University their parents. This is not surprising since different traits that of Agricultural Sciences, P.O. Box 7043, 750 07 Uppsala, Sweden affect herbivore responses, e.g., plant secondary chemistry (Tahvanainen et al., 1985) and nutrient content (Mattson, R. Julkunen-Tiitto 1980), exhibit varying and often complex inheritance patterns Natural Product Research Laboratory, Department of Biology, University of Eastern Finland, P.O. Box 111, (Rieseberg and Ellstrand, 1993; Cheng et al., 2011). The resis- 801 01 Joensuu, Finland tance of parental species and hybrids depends partially on J Chem Ecol (2013) 39:516–524 517 environmental conditions (Hochwender et al., 2000). In 2003). To understand the effect of hybridization from an addition, different herbivore species respond differently ecological point of view, it is important to include the more to variation in plant traits (Matsuki and MacLean, 1994; complex hybrid categories (Arnold, 1997). One way to Orians and Fritz, 1996). elucidate how hybridization influences plant-herbivore in- The importance of plant chemistry for the outcome of teractions is to study how plant characteristics that affect plant-herbivore interactions and plant resistance to herbi- herbivore responses (e.g., plant chemistry) are inherited vore attacks has been thoroughly addressed (e.g., Fraenkel, from parental species to hybrids (Orians et al., 2000). 1959; Haukioja, 1980; Harborne, 2001;Treutter,2006; Furthermore, by correlating variation in plant traits to the Barbehenn and Constabel, 2011). However, much is still response of herbivores, it might be possible to gain knowl- unknown about genetic or regulatory aspects of the biosyn- edge about the complex interactions among genes, traits, thesis of many of these defensive chemical compounds. and patterns on a broader ecological scale. Since small genetic changes can cause large shifts in the In this study, we used hybridization between Salix chemical properties of both plant individuals and species viminalis, which is susceptible to the chrysomelid leaf beetle (Nyman and Julkunen-Tiitto, 2005), hybridization should Phratora vulgatissima,andS. dasyclados, which exhibits a further increase the variability in plant chemical profiles. high degree of resistance to this insect pest. Crossing of two According to classic hybridization theory, a trait, whether it F1 hybrids created a F2 generation that gave us an opportunity is expressed by one or several genes, is expected to show to screen for plants that showed variability in the performance greater variance in the F2 hybrids compared to either of P. vulgatissima. Moreover, by analyzing the phenolic pro- the parental species or the F1 hybrids (Hochwender et al., files of the F2 hybrids, we aimed to find chemical clues that 2000). This is a result of recombination between chromo- explained the varied performance of the targeted insect spe- somes during the production of F2 hybrids (Hochwender cies. This study was done as a part of a Salix molecular and Fritz, 2004). Orians (2000)showedthatF2hybridplants breeding program with the long-term goal of developing demonstrated greater variance in secondary chemistry methods for selecting plants with increased resistance to insect than F1 and parental plants. The variability in plant pests and pathogens. chemical content expressed in the F2 generation can be used to evaluate the effect of plant chemistry on herbivore re- sponses and to identify the mechanisms behind such plant- Methods and Materials herbivore interactions. Willows (Salix spp.) are excellent for investigating the The Study System Willows (Salix spp.) are deciduous trees effects of hybridization on insect herbivore responses. Most or shrubs that are commonly cross-fertile and hybridize of the species of this genus are cross-fertile, and many easily. Cuttings root readily making cultivation and cloning hybrids occur naturally. There is a diverse insect community simple. The foliage of Salix species often is rich in carbon- that feeds on willows; in particular, chrysomelid beetles based phenolics, and generally there is a significant genetic (Coleoptera) may cause severe damage to the plants. effect on the phenolic metabolite content (Julkunen-Tiitto, Willows generally can be divided into two groups based 1986;Baumetal.,2009). Phenolic compounds play a major on their content of phenolics: some species or genotypes role in Salix resistance to herbivory (e.g., Tahvanainen et al., contain high levels of phenolic glycosides (e.g., salicylates) 1985). The two willow species used in this study vary in their and low levels of condensed tannins, whereas other species phenolic profiles; the foliage of S. viminalis is high in con- or genotypes demonstrate high levels of condensed tannins densed tannins but does not contain any salicylates, whereas S. but no phenolic glycosides (Julkunen-Tiitto, 1986, 1989; dasyclados leaves contain high levels of salicylates and small Baum et al., 2009). Insect herbivores vary in their ability amounts of condensed tannins (Julkunen-Tiitto, 1986). The to cope with these compounds; specialists often prefer to variation in phenolic content has been proposed to be respon- feed on willows with high levels of phenolic glycosides, sible for the different resistance of the two species for the while generalists usually avoid these plants (Rowell-Rahier, herbivorous leaf beetle P. vulgatissima; S. viminalis is suscep- 1984; Tahvanainen et al., 1985; Kelly and Curry, 1991; tible while S. dasyclados demonstrates a highdegreeofresis- Orians et al., 1997; Boeckler et al., 2011). tance (Glynn et al., 2004; Lehrman et al., 2012). Salix hybrids previously have been used as a model The blue willow leaf beetle (P. vulgatissima) is a common system in studies that try to correlate the response of her- herbivore on many species of Salix, including short rotation bivorous insects and plant chemical composition. Some of coppice crops such as S. viminalis. The beetles are univoltine these studies have focused on parental species and F1 hy- in Sweden and they overwinter as adults. In early spring, they brids
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