Detritivorous crustaceans become herbivores on jasmonate-deficient plants

Abstract

The jasmonate signal pathway is known to control defenses against herbivores, such as leaf eaters (folivores). Does the reach of the pathway extend to defense against other types of animal? Among the arthropods attracted to seed baits placed below flowering Arabidopsis thaliana plants are 2 largely nocturnal isopod crustaceans generally considered as detritivores: Porcellio scaber and Armadillidium vulgare. Parallel laboratory experiments identified the isopods as being capable of predation on intact plants. Isopod feeding was strongly facilitated in jasmonate-deficient Arabidopsis and rice plants. The feeding activity of isopods revealed potentially detritivore-sensitive, jasmonate-protected Achilles' heels in these architecturally different plants (petioles and inflorescence stems in Arabidopsis, and lower stem and mesocotyl in rice). The work addresses the question of what stops 2 detritivores from attacking living plants and provides evidence that it is, in part, the jasmonate signal pathway. Furthermore, senescent leaves from an Arabidopsis jasmonate mutant were consumed more rapidly than senescent wild-type leaves, suggesting that past activity of the jasmonate signal pathway in leaves may slow carbon recycling through detritivory.detritivory ͉ isopods ͉ jasmonic acid ͉ plant defense ͉ senescence H erbivory is one of the most important processes in the biosphere, whereby carbon fixed by plants is transferred to higher trophic levels (1, 2). In many cases the largest category of herbivores on the vegetative tissues of plants tends to be insects (3). Additionally, many organisms are known to prey on seeds or otherwise affect seed fate (4). However, herbivores are not the only organisms associated with plants, and only a proportion of the animals associated with plants eat living plant tissues. Another important category of organisms found associated with plants are the detritivores: feeders on dead and dying material (5). Detritivory of plant material is a second major environmental process releasing carbon from plants to higher trophic levels. Like herbivory, this is one of the truly large-scale processes in nature. Detritivores, generally considered apart from herbivores, may actively survey the plant and its vicinity looking for senescent, decaying, or otherwise compromised plant tissues. Furthermore, there is no clear division in nature between detritivory and herbivory, and many arthropods are omnivores feeding at more than one trophic level (6). It is possible that some detritivores, if given the opportunity, might be facultative herbivores. Indeed, it is conceivable that defense barriers against detritivores would be provided by the jasmonate signal pathway, because this pathway operates on the expression of hundreds of wound-inducible defense and survival genes (7) and underlies a major defense system against many herbivores (8).Through field observations we first identified arthropods potentially capable of devouring Arabidopsis seeds. These were early-stage juveniles of the nocturnal dermapteran (e...

Reexamination of Chlorophyllase Function Implies Its Involvement in Defense against Chewing Herbivores

“…It was shown that jasmonate-insensitive Arabidopsis mutants become susceptible to herbivores or detritivores, such as Porcellio scaber and Armadillidium vulgare, which usually do not feed on Arabidopsis (Farmer and Dubugnon, 2009;Abe et al, 2013). We speculate that the efficiency of the CLH/chlorophyll defense system may vary between insect species and among different plant species.…”

Lipoxygenase6-Dependent Oxylipin Synthesis in Roots Is Required for Abiotic and Biotic Stress Resistance of Arabidopsis

“…S4) and on leaves of dde2 (Supplemental Fig. S4; Farmer and Dubugnon, 2009). The fact that lox6 and dde2 mutations have similar effects indicates that jasmonates are responsible for deterring crustacean feeding in the wild type.…”

“…The detritivore rough woodlouse (Porcellio scaber) was collected and cultivated as described in Farmer and Dubugnon (2009). For the feeding assay, detached leaves and roots of 6-week-old hydroponically cultivated plants were used.…”

Plant-mediated links between detritivores and aboveground herbivores

“…Interestingly, the Collembola Protaphorura fimata has been reported to act as a root herbivore and may predominately feed on roots (Endlweber et al, 2009). Other well-known detritivores, the crustacean isopods Porcellio scaber and Armadillidium vulgare , can become herbivores on jasmonate-deficient plants (Farmer and Dubugnon, 2009). A recent study reported that the anecic earthworm Lumbricus terrestris can act as a shoot herbivore (Griffith et al, 2013).…”