Review TRENDS in Plant Science Vol.9 No.5 May 2004 Interactions of insect pheromones and plant semiochemicals Gadi V.P. Reddy1 and Angel Guerrero2 1Agricultural Experiment Station, College of Natural and Applied Sciences, University of Guam, Mangilao, Guam 96923, USA 2Department of Biological Organic Chemistry, Institute of Chemical and Environmental Research (CSIC), Jordi Girona 18-26, 08034-Barcelona, Spain Plant semiochemicals are known to produce a wide pheromones in certain insects and often synergize or range of behavioral responses in insects. Some insects enhance insect responses to sex pheromones. Host sequester or acquire host plant compounds and use compounds can also have an inhibitory or repellent effect, them as sex pheromones or sex pheromone precursors. interrupting the response of insects to their own phero- Other insects produce or release sex pheromones in mone. In other cases, host-derived compounds resulting response to specific host plant cues, and chemicals from from herbivorous attack can attract predators to the host plants often synergistically enhance the response of attacking insect and therefore serve as a defense mechan- an insect to sex pheromones. Plant volatiles can also ism for the plant. Here, we discuss various interactions have inhibitory or repellent effects that interrupt insect between host semiochemicals and insect pheromones, and responses to pheromones and attract predators and their ecological implications in terms of insect behavior, parasitoids to the attacking species after herbivory feeding and reproduction. injury. Here, we review different interactions between plant semiochemicals and insect pheromones, paying Plant stimulation of pheromone production attention to those that can result in the development of Host plants play a key role in the production and use of sex more efficient and reliable programs for pest control. pheromones by herbivorous insects through larval or adult sequestration of chemically active compounds and phero- Interactions between insect pheromones and semiochemi- mone precursors [2]. One of the best examples of cals (molecules that carry signals from one organism to sequestration of plant chemicals by larvae and their another) from the host plant have been known for nearly subsequent use by adult males in sex attraction or as long as pheromones (substances secreted by an indi- courtship interactions is shown in Utetheisa ornatrix vidual that induce a specific reaction in another individual (Arctiidae), whose courtship pheromone derives from of the same species) have been recognized as a key com- pyrrolizidine alkaloids (PAs) ingested at the larval stage munication system within species. Such interactions are from the host plant Crotalaria spectabilis (Figure 1) [3]. manifested as effects of the host plant on insect physiology U. ornatrix larvae sequester PAs (e.g. monocrotaline) and and behavior, reflecting different types of insect strategies retain the alkaloids through metamorphosis into the adult to optimize feeding, mating and reproduction [1]. Some stage to provide egg protection for the next generation. insects acquire host plant chemicals to use them as sex Females receive PAs from males during copulation and pheromones or sex pheromone precursors. Other host transmit the alkaloids together with their own load to plant volatiles can induce the production or release of the eggs [4]. PA sequestering species are found in the CH3 OH HO CH3 CH3 O O O HO CH2OH HO CHO Aromatization 7 Oxidation 7 O CH2 7 hydrolysis N N N (R)-hydroxydanaidal Monocrotaline (Male pheromone of (Crotalaria spectabilis) Utetheisa ornatrix) TRENDS in Plant Science Figure 1. Example of acquisition of pheromone compounds from host plant precursors. Male Utetheisa ornatrix (Lepidoptera: Arctiidae) produces (R)-hydroxydanaidal from dietary pyrrolizidine alkaloids (e.g. monocrotaline) obtained by larvae from the host plant Crotalaria spectabilis [84]. Corresponding authors: Gadi V.P. Reddy ([email protected]), Angel Guerrero ([email protected]). www.sciencedirect.com 1360-1385/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2004.03.009 254 Review TRENDS in Plant Science Vol.9 No.5 May 2004 Lepidoptera (many butterflies and moths), Coleoptera studies, the association between feeding and sex attraction (some leaf beetles), Orthoptera (certain grasshoppers) and suggested the acquisition of plant compounds and their Homoptera (certain aphids), and are used as strong feed- use as pheromone or pheromone precursors by the insect. ing deterrents against invertebrate predators such as Thus, exposure to myrcene in the volatile headspace spiders, ants, coccinellids and lacewings [2]. In addition, increased the amounts of ipsenol and ipsdienol in hindgut PAs are strongly hepatotoxic and pneumotoxic to verte- tissues of male Ips paraconfusus [14] and other Dendroc- brates and genotoxic to insects [5]. PAs are stored and tonus spp. [15] Application of 2H-labeled myrcene and (2)- maintained in the form of the non-toxic oxides and, upon and (þ)-a-pinene resulted in production of 2H-ipsenol feeding, they are reduced in the gut and adsorbed as and 2H ipsdienol and cis- and trans-verbenol [16] in tertiary alkaloids. They can be detoxified by N-oxidation hindguts of I. paraconfusus, providing convincing evidence with a soluble NADPH-dependent flavin monooxygenase of pheromone biosynthetic relationships in scolytids. The present in the hemolymph of PA-sequestering insects and bioorganic reactions whereby monoterpenes are metab- used them as chemical defense [6] or can be bioactivated olized to oxygenated compounds are likely to involve by microsomal liver cytochrome P450-dependent mono- P450 enzymes [17]. oxygenases into unstable pyrrolic intermediates that are However, many studies of the endocrine regulation of highly reactive alkylating agents [7]. In the case of the pheromone production in scolytids foreshadowed the arctiid Tyria jacobaeae, PAs are oxidized in the hemolymph observation that pheromone compounds are often syn- by senecionine N-oxygenase (SNO), a flavin-dependent thesized from short-chain metabolic building blocks rather monooxygenase (FMO) with high substrate specificity than from host precursors. Strong evidence for de novo for PAs. Peptide microsequences obtained from purified synthesis of isoprenoids by scolytids came from in vivo T. jacobaeae SNO were used to clone the corresponding studies in which ipsenol, ipsdienol and amitinol in cDNA [8]. T. jacobaeae SNO possesses an N-terminal signal I. paraconfusus and ipsdienol and amitinol in Ips pini peptide characteristic of extracellular proteins and belongs appeared to be labeled from 14C-acetate [18,19] or to a large family of FMO-like sequences of mostly unknown 14C-mevalonolactone [19]. As an alternative biosynthetic function. The gene for T. jacobaeae SNO, highly specific for route to an aggregation pheromone component of Dendro- toxic PAs, was probably recruited from a pre-existing insect ctonus frontalis, a fatty-acid-like elongation of leucine or specific FMO gene family of unknown function [8]. catabolism of leucine to acetyl-CoA followed by isoprenoid Adult males can also obtain PAs from plants and use synthesis via 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) them as pheromone precursors. This happens in some has been proposed [20]. arctiids, most Dancinae and Ithomiinae butterflies. Juvenile hormone III (JHIII) appears to play a central Cysseps fulvicollis (Arctiidae) males produce hydroxyda- role as a regulator for pheromone production in Scolytidae. naidal from PAs of dead and damaged plants, and release it For instance, the HMG-CoA reductase (HMG-R) inhibitor as a sex attractant [9]. The butterflies are attracted to PAs compactin and the JH analog methoprene were used to and ingest them with nectar or, most frequently, from dead offer indirect evidence that JH regulates de novo phero- parts or withered twigs of the plants [5]. These butterflies mone biosynthesis in male Ips duplicatus [21].In advertise their unpalatability to potential predators by 14C-acetate- and 14C-mevalonolactone-based experiments, conspicuous warning coloration. Conversion of plant PAs I. pini was found to release JHIII in its corpora allata, and into the pheromone has been suggested to occur in increasing topical JHIII dose resulted in an increase of U. ornatrix through aromatization of the dihydropyrrole radiolabeled acetate into ipsdienol [19]. This unequivo- ring of monocrotaline, followed by ester hydrolysis and cally demonstrated that JHIII regulates de novo phero- oxidation [3] (Figure 1). It should be realized that the mone production (Figure 2). However, incorporation of chiral R configuration of both the alkaloid precursor and radiolabeled mevalonolactone into ipsdienol by this insect the pheromone is maintained. This mechanism was was unaffected by increasing JHIII dose, suggesting that confirmed by feeding labeled PA heliotrine to larvae of JH primarily influences enzymes before mevalonate in Creatonotos transiens [10] and in Estigmene acrea [11]. this pathway [i.e. HMG-CoA synthase (HMG-S) and The acquisition of chemicals from plants and their use HMG-R] [22]. However, it is not clear whether JHIII alone in a sexual context is also known for certain species of is sufficient to upregulate de novo pheromone biosynthesis orchid bees and tephritid fruit flies. Male bees collect a in all Ips spp. Comparative studies of I. paraconfusus and mixture of terpenoids from orchids and use them as an I. pini indicated: (a)