Recruitment of entomopathogenic nematodes by insect-damaged maize roots

Abstract

Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E )-b-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E )-b-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-b-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.Plants are not simply passive victims of attacking herbivores; they have evolved an arsenal of physical and chemical defences to protect themselves. Often these defences are mobilized only in response to herbivory 1,2 . Among the proposed inducible defences is the production and release of volatile chemicals that could serve as signals to attract natural enemies of the herbivores [3][4][5] . Manipulating these signals can help increase the effectiveness of these natural enemies as control agents [6][7][8] . The induced emission of chemical signals is not limited solely to aboveground plant parts. The entomopathogenic nematode Heterorhabditis megidis was found to be attracted to exudates emitted by plant roots after damage by weevil larvae 9,10 , but the nature of the attractants involved is unknown. Here we show that maize roots damaged by larvae of the economically important coleopteran pest Diabrotica virgifera virgifera LeConte are attractive to entomopathogenic nematodes, and we identify the chemical compound responsible for the attraction. D. v. virgifera or Western corn rootworm (WCR) is a voracious pest of maize that is responsible for the use of the bulk of pesticides applied in the cultivation of this crop in the USA 11 . The recent introduction and rapid spread of WCR into Europe has caused major concern for maize production on this continent and has stimulated the search for new methods of maize protection 12,13 . The use of nematodes to control WCR is an ecologically sound option 14,15 , especially if researchers can optimize their efficacy at finding and killing WCR. Attraction of nematodes by WCR-damaged rootsTo determine whether or not WCR-infested maiz...

Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature

“…Indirect defenses are widespread and include domatia, extrafloral nectar, and food bodies which provide shelter and nutrition for predators and parasitoids, as well as herbivory-induced plant volatiles (HIPVs) which convey information about feeding herbivores (Heil, 2008). Field studies with the native tobacco Nicotiana attenuata , a desert annual, and with maize have shown that HIPVs can reduce herbivore loads by 24% to more than 90%, by increasing both predation and parasitization of herbivores (Kessler and Baldwin, 2001; Rasmann et al, 2005; Halitschke et al, 2008; Degenhardt et al, 2009; Allmann and Baldwin, 2010) and deterring herbivore oviposition (Kessler and Baldwin, 2001). …”

“…But because HIPVs can be perceived by many other members of the ecological community—from herbivores, pollinators, predators and parasitoids to competing or parasitic plants—it is not clear whether HIPVs increase plant fitness in nature (Dicke and Baldwin, 2010; Kessler and Heil, 2011). The field studies described above have either spanned too short a time to reveal Darwinian fitness benefits, or have not reported fitness data at all (Kessler and Baldwin, 2001; Rasmann et al, 2005; Halitschke et al, 2008; Degenhardt et al, 2009; Allmann and Baldwin, 2010). Two laboratory studies showed that parasitization of herbivores can increase plant reproduction (van Loon et al, 2000; Hoballah and Turlings, 2001), but the parasitization in these studies was not mediated by HIPVs.…”

“…Thus the inducibility of HIPV emission, which ensures association with herbivore feeding, is likely essential for HIPV function, but it is difficult to engineer (Kos et al, 2009). Engineered constitutive HIPV emissions have been used, either on predators and parasitoids trained to associate target volatiles with prey in short-term laboratory experiments (Kappers et al, 2005; Schnee et al, 2006), or in set-ups in which target volatiles are always associated with prey (Rasmann et al, 2005; Degenhardt et al, 2009). When plants are engineered constitutively to emit HIPVs, they no longer provide accurate information about the location of feeding herbivores, and predators will not associate these signals with prey in nature.…”

Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering

“…Arabidopsis has been shown to emit two terpenoids, (3,S)-(E)-nerolidol and its derivative (E)-4,8-dimethyl-1,3,7-nonatriene, when the strawberry nerolidol synthase gene was introduced into the plants, resulting in greater attraction of the predators of predatory mites (Kappers et al 2005). Caryophyllene, emitted from the roots of Maize plants, is known to be an herbivore-induced below-ground signal, which strongly attracts entomopathogenic nematodes (Rasmann et al 2005;Delory et al 2016). Similarly, Ozawa et al (2000) demonstrated that (Lotus japonicus) shoots infested with spider mites released a blend of volatiles that attracted predators of mites (Phytoseiulus persimilis).…”

“…Although terpenes are mostly studied in the above-ground tissues, recently, their novel function in the below-ground environment, as signaling molecules, has been identified (Karban et al 2014;Delory et al 2016). For example, β-caryophyllene, released from the roots of maize plants against beetle (Diabrotica virgifera) attack, acts as a volatile signal to attract predatory nematodes, which will defend plants indirectly from further damage (Rasmann et al 2005). Similarly, the Hedychium coronarium farnesyl pyrophosphate synthase gene shows a quick response to herbivory and wounding and is involved in floral biosynthesis (Lan et al 2013).…”