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The roots of defense: plant resistance and tolerance to belowground herbivory.

ABSTRACT: There is conclusive evidence that there are fitness costs of plant defense and that herbivores can drive selection for defense. However, most work has focused on above-ground interactions, even though belowground herbivory may have greater impacts on individual plants than above-ground herbivory. Given the role of belowground plant structures in resource acquisition and storage, research on belowground herbivores has much to contribute to theories on the evolution of plant defense. Pocket gophers (Geomyidae) provide an excellent opportunity to study root herbivory. These subterranean rodents spend their entire lives belowground and specialize on consuming belowground plant parts.We compared the root defenses of native forbs from mainland populations (with a history of gopher herbivory) to island populations (free from gophers for up to 500,000 years). Defense includes both resistance against herbivores and tolerance of herbivore damage. We used three approaches to compare these traits in island and mainland populations of two native California forbs: 1) Eschscholzia californica populations were assayed to compare alkaloid deterrents, 2) captive gophers were used to test the palatability of E. californica roots and 3) simulated root herbivory assessed tolerance to root damage in Deinandra fasciculata and E. californica. Mainland forms of E. californica contained 2.5 times greater concentration of alkaloids and were less palatable to gophers than island forms. Mainland forms of D. fasciculata and, to a lesser extent, E. californica were also more tolerant of root damage than island conspecifics. Interestingly, undamaged island individuals of D. fasciculata produced significantly more fruit than either damaged or undamaged mainland individuals.These results suggest that mainland plants are effective at deterring and tolerating pocket gopher herbivory. Results also suggest that both forms of defense are costly to fitness and thus reduced in the absence of the putative target herbivore.

SUBMITTER: Watts SM

PROVIDER: S-EPMC3071833 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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The roots of defense: plant resistance and tolerance to belowground herbivory.

Watts Sean M SM Dodson Craig D CD Reichman O J OJ

PloS one 20110406 4

<h4>Background</h4>There is conclusive evidence that there are fitness costs of plant defense and that herbivores can drive selection for defense. However, most work has focused on above-ground interactions, even though belowground herbivory may have greater impacts on individual plants than above-ground herbivory. Given the role of belowground plant structures in resource acquisition and storage, research on belowground herbivores has much to contribute to theories on the evolution of plant def ...[more]

PMID: 21494690

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Project description:Insect herbivores can shift the composition of a plant community, but the mechanism underlying such shifts remains largely unexplored. A possibility is that insects alter the competitive symmetry between plant species. The effect of herbivory on competition likely depends on whether the plants are subjected to aboveground or belowground herbivory or both, and also depends on soil nitrogen levels. It is unclear how these biotic and abiotic factors interactively affect competition. In a greenhouse experiment, we measured competition between two coexisting grass species that respond differently to nitrogen deposition: Dactylis glomerata L., which is competitively favoured by nitrogen addition, and Festuca rubra L., which is competitively favoured on nitrogen-poor soils. We predicted: (1) that aboveground herbivory would reduce competitive asymmetry at high soil nitrogen by reducing the competitive advantage of D. glomerata; and (2), that belowground herbivory would relax competition at low soil nitrogen, by reducing the competitive advantage of F. rubra. Aboveground herbivory caused a 46% decrease in the competitive ability of F. rubra, and a 23% increase in that of D. glomerata, thus increasing competitive asymmetry, independently of soil nitrogen level. Belowground herbivory did not affect competitive symmetry, but the combined influence of above- and belowground herbivory was weaker than predicted from their individual effects. Belowground herbivory thus mitigated the increased competitive asymmetry caused by aboveground herbivory. D. glomerata remained competitively dominant after the cessation of aboveground herbivory, showing that the influence of herbivory continued beyond the feeding period. We showed that insect herbivory can strongly influence plant competitive interactions. In our experimental plant community, aboveground insect herbivory increased the risk of competitive exclusion of F. rubra. Belowground herbivory appeared to mitigate the influence of aboveground herbivory, and this mechanism may play a role for plant species coexistence.

Project description:Plants recognize and respond to feeding by herbivorous insects by upregulating their local and systemic defenses. While defense induction by aboveground herbivores has been well studied, far less is known about local and systemic defense responses against attacks by belowground herbivores. Here, we investigated and compared the responses of the maize transcriptome to belowground and aboveground mechanical damage and infestation by two well-adapted herbivores: the soil-dwelling western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) and the leaf-chewing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). In responses to both herbivores, maize plants were found to alter local transcription of genes involved in phytohormone signaling, primary and secondary metabolism. Induction by real herbivore damage was considerably stronger and modified the expression of more genes than mechanical damage. Feeding by the corn rootworm had a strong impact on the shoot transcriptome, including the activation of genes involved in defense and development. By contrast, feeding by the fall armyworm induced only few transcriptional changes in the roots. In conclusion, feeding by a leaf chewer and a root feeder differentially affects the local and systemic defense of maize plants. Besides revealing clear differences in how maize plants respond to feeding by these specialized herbivores, this study reveals several novel genes that may play key roles in plant-insect interactions and thus sets the stage for in depth research into the mechanism that can be exploited for improved crop protection.Significance statementExtensive transcriptomic analyses revealed a clear distinction between the gene expression profiles in maize plants upon shoot and root attack, locally as well as distantly from the attacked tissue. This provides detailed insights into the specificity of orchestrated plant defense responses, and the dataset offers a molecular resource for further genetic studies on maize resistance to herbivores and paves the way for novel strategies to enhance maize resistance to pests.

Project description:Plants can defend themselves against herbivores through activation of defensive pathways and attraction of third-trophic-level predators and parasites. Trophic cascades that mediate interactions in the phytobiome are part of a larger dynamic including the pathogens of the plant itself, which are known to greatly influence plant defenses. As such, we investigated the impact of a phloem-limited bacterial pathogen, Candidatus Liberibacter asiaticus (CLas), in cultivated citrus rootstock on a well-studied belowground tritrophic interaction involving the attraction of an entomopathogenic nematode (EPN), Steinernema diaprepesi, to their root-feeding insect hosts, Diaprepes abbreviatus larvae. Using belowground olfactometers, we show how CLas infection interferes with this belowground interaction by similarly inducing the release of a C12 terpene, pregeijerene, and disconnecting the association of the terpene with insect presence. D. abbreviatus larvae that were not feeding but in the presence of a CLas-infected plant were more likely to be infected by EPN than those near uninfected plants. Furthermore, nonfeeding larvae associated with CLas-infected plants were just as likely to be infected by EPN as those near noninfected plants with D. abbreviatus larval damage. Larvae of two weevil species, D. abbreviatus and Pachnaeus litus, were also more attracted to plants with infection than to uninfected plants. D. abbreviatus larvae were most active when exposed to pregeijerene at a concentration of 0.1 μg/μl. We attribute this attraction to CLas-infected plants to the same signal previously thought to be a herbivore-induced plant volatile specifically induced by root-feeding insects, pregeijerene, by assessing volatiles collected from the roots of infected plants and uninfected plants with and without feeding D. abbreviatus. Synthesis. Phytopathogens can influence the structuring of soil communities extending to the third trophic level. Field populations of EPN may be less effective at host-finding using pregeijerene as a cue in citrus grove agroecosystems with high presence of CLas infection.

Dataset Information

The roots of defense: plant resistance and tolerance to belowground herbivory.

Publications

The roots of defense: plant resistance and tolerance to belowground herbivory.

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