Ecological genomics of plant-insect interactions: from gene to community.

A major challenge for current biology is to integrate research approaches that address different levels of biological organization, from subcellular mechanisms to functions in ecological communities. The study of plant-insect interactions provides interesting options for this. Ample information at the subcellular and the individual level is available on the one hand, while important insight in the (community) ecology of insectplant interactions is available as well (Kessler and Baldwin, 2002; Bezemer and van Dam, 2005; Schoonhoven et al., 2005; Kessler and Halitschke, 2007; Snoeren et al., 2007). A major step forward will be to connect these research fields, and encouraging steps have been made during the past years. Insects make up the most diverse and abundant group of plant consumers. A total of 45% of the approximately 1 million described insect species feed on plants (Schoonhoven et al., 2005). Given that the estimated number of insects species is several times higher (Stork, 2007), the number of herbivorous insect species is likely to be much higher too. Herbivorous insects may attack plants below ground as well as above ground, and not a single organ remains free of potential insect attack (Bezemer and van Dam, 2005; Schoonhoven et al., 2005). Plants have evolved a range of defenses to ward off this diversity of attackers, including constitutive and induced defenses (Walling, 2000; Kessler and Baldwin, 2002; Schoonhoven et al., 2005). Because an individual plant may potentially be under the attack of tens or hundreds of consumer species, it is impossible to have constitutive defenses against all these attackers. Furthermore, whether the potential enemies will indeed attack a certain individual is usually unpredictable. Moreover, constitutive defenses may also select for adaptation in herbivorous insects (Agrawal and Karban, 1999). Thus, inducible defenses may tune the defensive needs to the actual presence of attackers and in addition may transform plants into moving fortresses that have a modified phenotype and consequently retard adaptation in herbivores (Agrawal and Karban, 1999; Kahl et al., 2000). For instance, Nicotiana attenuata plants respond to mechanical damage with the induction of nicotine, a neurotoxin affecting most herbivores (Kahl et al., 2000). However, the plant has an attenuated nicotine induction in response to feeding damage by caterpillars of the specialist tobacco hornworm Manduca sexta, which can tolerate considerable levels of nicotine and furthermore can exploit it in its own defense against pathogens and parasitic wasps (Krischik et al., 1988). Instead, N. attenuata responds to Manduca feeding with the production of volatile terpenoids that can attract parasitic wasps that attack the caterpillars (Kahl et al., 2000). Induced defenses comprise direct defenses, such as secondary metabolites and protease inhibitors that negatively affect herbivore growth and survival, as well as indirect defenses, such as herbivore-induced plant volatiles and herbivore-induced extrafloral nectar that enhance the effectiveness of natural enemies of herbivores, such as parasitoids or predators (Kessler and Baldwin, 2002; Heil et al., 2004; Kappers et al., 2005; D’Alessandro and Turlings, 2006; Mumm and Hilker, 2006). The induction of defenses is often specific for the attacker species (Kahl et al., 2000; Dicke et al., 2003; Arimura et al., 2005) and an individual plant can therefore express a range of different phenotypes where each phenotype has its own effects on the members of the community, such as herbivores, carnivores, and pollinators (Dicke et al., 2004; Kessler et al., 2004; Kessler and Halitschke, 2007; Bruinsma and Dicke, 2008). For instance, previous attack may influence the induction of subsequent defenses in specific ways and thereby affect herbivore and plant fitness (Kessler and Baldwin, 2004; Voelckel and Baldwin, 2004b). As a consequence, the investigation of induced defenses requires an approach that considers the total community as well as individual interactions among community members (Kessler and Baldwin, 2004; Kessler et al., 2004; Bruinsma and Dicke, 2008). Integrating this approach at different levels of biological organization is a major challenge that will link mechanisms in terms of transcriptional induction, metabolite induction, and ecological interactions (Mercke et al., 2004). After identifying genes that are involved in specific interactions, their ecological function should be investigated in in-depth studies addressing e.g. ge1 This work was supported by the Netherlands Organization for Scientific Research, NWO (VICI grant no. 865.03.002 to M.D.). * Corresponding author; e-mail [email protected]. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Marcel Dicke ([email protected]). [C] Some figures in this article are displayed in color online but in black and white in the print edition. www.plantphysiol.org/cgi/doi/10.1104/pp.107.111542