Whiteflies interfere with indirect plant defense against spider mites in Lima bean
15 Dec 2009-Proceedings of the National Academy of Sciences of the United States of America (National Academy of Sciences)-Vol. 106, Iss: 50, pp 21202-21207
TL;DR: Interference by a phloem-feeding insect, the whitefly Bemisia tabaci, with indirect plant defenses induced by spider mites is reported, concluding that in dual-infested Lima bean plants the suppression of the JA signaling pathway by whitefly feeding is not due to enhanced SA levels.
Abstract: Plants under herbivore attack are able to initiate indirect defense by synthesizing and releasing complex blends of volatiles that attract natural enemies of the herbivore. However, little is known about how plants respond to infestation by multiple herbivores, particularly if these belong to different feeding guilds. Here, we report the interference by a phloem-feeding insect, the whitefly Bemisia tabaci, with indirect plant defenses induced by spider mites (Tetranychus urticae) in Lima bean (Phaseolus lunatus) plants. Additional whitefly infestation of spider-mite infested plants resulted in a reduced attraction of predatory mites (Phytoseiulus persimilis) compared to attraction to plants infested by spider mites only. This interference is shown to result from the reduction in (E)-β-ocimene emission from plants infested by both spider mites and whiteflies. When using exogenous salicylic acid (SA) application to mimic B. tabaci infestation, we observed similar results in behavioral and chemical analyses. Phytohormone and gene-expression analyses revealed that B. tabaci infestation, as well as SA application, inhibited spider mite-induced jasmonic acid (JA) production and reduced the expression of two JA-regulated genes, one of which encodes for the P. lunatus enzyme β-ocimene synthase that catalyzes the synthesis of (E)-β-ocimene. Remarkably, B. tabaci infestation concurrently inhibited SA production induced by spider mites. We therefore conclude that in dual-infested Lima bean plants the suppression of the JA signaling pathway by whitefly feeding is not due to enhanced SA levels.
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TL;DR: Evidence is emerging that beneficial root-inhabiting microbes also hijack the hormone-regulated immune signaling network to establish a prolonged mutualistic association, highlighting the central role of plant hormones in the regulation of plant growth and survival.
Abstract: Plant hormones have pivotal roles in the regulation of plant growth, development, and reproduction. Additionally, they emerged as cellular signal molecules with key functions in the regulation of immune responses to microbial pathogens, insect herbivores, and beneficial microbes. Their signaling pathways are interconnected in a complex network, which provides plants with an enormous regulatory potential to rapidly adapt to their biotic environment and to utilize their limited resources for growth and survival in a cost-efficient manner. Plants activate their immune system to counteract attack by pathogens or herbivorous insects. Intriguingly, successful plant enemies evolved ingenious mechanisms to rewire the plant’s hormone signaling circuitry to suppress or evade host immunity. Evidence is emerging that beneficial root-inhabiting microbes also hijack the hormone-regulated immune signaling network to establish a prolonged mutualistic association, highlighting the central role of plant hormones in the regulation of plant growth and survival.
2,132 citations
Cites background from "Whiteflies interfere with indirect ..."
...In lima bean, SAinducing, phloem-feeding sweetpotato whitefly (Bemisia tabaci ) negatively affected JA biosynthesis and JA-dependent indirect plant defenses that were triggered by the twospotted spider mite (Tetranychus urticae) on the same plant (Zhang et al. 2009)....
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TL;DR: Molecular advances in understanding of HIPV signaling and biosynthesis is enabling the creation of HIPv-'mute' and possibly HIPV-'deaf' plants, which could be used for unbiased examination of the fitness value of HIPVs emissions under natural conditions.
977 citations
TL;DR: Evidence for and against adaptive explanations for antagonistic crosstalk are examined, its phylogenetic origins are traced, and a hypothesis-testing framework for future research on the adaptive significance of SA-JA crosStalk is provided.
923 citations
TL;DR: Interestingly, application of larval oral secretion into wounded leaf tissue stimulated the ERF-branch of the JA pathway, suggesting that compounds in the oral secretion have the potential to manipulate the plant response toward the caterpillar-preferred ERf-regulated branch of theJA response.
Abstract: Plant defenses against insect herbivores and necrotrophic pathogens are differentially regulated by different branches of the jasmonic acid (JA) signaling pathway. In Arabidopsis, the basic helix-loop-helix leucine zipper transcription factor (TF) MYC2 and the APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) domain TF ORA59 antagonistically control these distinct branches of the JA pathway. Feeding by larvae of the specialist insect herbivore Pieris rapae activated MYC2 transcription and stimulated expression of the MYC2-branch marker gene VSP2, while it suppressed transcription of ORA59 and the ERF-branch marker gene PDF1.2. Mutant jin1 and jar1-1 plants, which are impaired in the MYC2-branch of the JA pathway, displayed a strongly enhanced expression of both ORA59 and PDF1.2 upon herbivory, indicating that in wild-type plants the MYC2-branch is prioritized over the ERF-branch during insect feeding. Weight gain of P. rapae larvae in a no-choice setup was not significantly affected, but in a two-choice setup the larvae consistently preferred jin1 and jar1-1 plants, in which the ERF-branch was activated, over wild-type Col-0 plants, in which the MYC2-branch was induced. In MYC2- and ORA59-impaired jin1-1/RNAi-ORA59 plants this preference was lost, while in ORA59-overexpressing 35S:ORA59 plants it was gained, suggesting that the herbivores were stimulated to feed from plants that expressed the ERF-branch rather than that they were deterred by plants that expressed the MYC2-branch. The feeding preference of the P. rapae larvae could not be linked to changes in glucosinolate levels. Interestingly, application of larval oral secretion into wounded leaf tissue stimulated the ERF-branch of the JA pathway, suggesting that compounds in the oral secretion have the potential to manipulate the plant response toward the caterpillar-preferred ERF-regulated branch of the JA response. Our results suggest that by activating the MYC2-branch of the JA pathway, plants prevent stimulation of the ERF-branch by the herbivore, thereby becoming less attractive to the attacker.
509 citations
Cites background from "Whiteflies interfere with indirect ..."
...In Lima bean, infestation with the whitefly B. tabaci and the spider mite Tetranychus urticae was shown to suppress indirect JA-dependent defenses that were induced by the spider mites, resulting in reduced attraction of carnivorous enemies of the spider mites (Zhang et al., 2009)....
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TL;DR: The recent discoveries on plant-mediated interactions between beneficial belowground microbes and aboveground insects are reviewed to review the molecular and physiological mechanisms involved.
505 citations
References
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TL;DR: Recent advances in plant immunity research have provided exciting new insights into the underlying defense signaling network, and diverse small-molecule hormones play pivotal roles in the regulation of this network.
Abstract: Plants live in complex environments in which they intimately interact with a broad range of microbial pathogens with different lifestyles and infection strategies. The evolutionary arms race between plants and their attackers provided plants with a highly sophisticated defense system that, like the animal innate immune system, recognizes pathogen molecules and responds by activating specific defenses that are directed against the invader. Recent advances in plant immunity research have provided exciting new insights into the underlying defense signaling network. Diverse small-molecule hormones play pivotal roles in the regulation of this network. Their signaling pathways cross-communicate in an antagonistic or synergistic manner, providing the plant with a powerful capacity to finely regulate its immune response. Pathogens, on the other hand, can manipulate the plant's defense signaling network for their own benefit by affecting phytohormone homeostasis to antagonize the host immune response.
2,019 citations
"Whiteflies interfere with indirect ..." refers background in this paper
...Based on the observations that infestation by phloem-feeding insects may induce SA-dependent genes while suppressing JAdependent genes (19–21), and possible cross-talk between JA and SA signaling pathways (28), we hypothesized that infestations by phloem-feeding insects would affect the emission of HIPVs induced by herbivores whose feeding behavior triggered JA-mediated responses, and will consequently interfere with the induction of HIPV-mediated indirect plant defense....
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...Considering the well-known cross-talk between JA and SA signaling pathways (28), it might be expected that B....
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TL;DR: The authors quantified volatile emissions fromNicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually.
Abstract: Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions fromNicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-α-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.
1,827 citations
TL;DR: Corn seedlings release large amounts of terpenoid volatiles after they have been fed upon by caterpillars, and females of the parasitic wasp Cotesia marginiventris (Cresson) learn to take advantage of those plant-producedvolatiles to locate hosts when exposed to these volatile in association with hosts or host by-products.
Abstract: Corn seedlings release large amounts of terpenoid volatiles after they have been fed upon by caterpillars. Artificially damaged seedlings do not release these volatiles in significant amounts unless oral secretions from the caterpillars are applied to the damaged sites. Undamaged leaves, whether or not they are treated with oral secretions, do not release detectable amounts of the terpenoids. Females of the parasitic wasp Cotesia marginiventris (Cresson) learn to take advantage of those plant-produced volatiles to locate hosts when exposed to these volatiles in association with hosts or host by-products. The terpenoids may be produced in defense against herbivores but may also serve a secondary function in attracting the natural enemies of these herbivores.
1,624 citations
"Whiteflies interfere with indirect ..." refers background in this paper
...A important indirect defense of plants against herbivores is the emission of plant volatiles that provide important foraging cues for natural enemies of the herbivore (1, 2)....
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TL;DR: The production by phylogenetically diverse plant species and the exploitation by parasitoids of highly specific chemical signals, keyed to individual herbivore species, indicates that the interaction between plants and the natural enemies of the herbivores that attack them is more sophisticated than previously realized.
Abstract: 1-3 . Here we use chemical and behavioural assays to show that these plant emissions can transmit herbivore-specific infor- mation that is detectable by parasitic wasps (parasitoids). Tobacco, cotton and maize plants each produce distinct volatile blends in response to damage by two closely related herbivore species, Heliothis virescens and Helicoverpa zea. The specialist parasitic wasp Cardiochiles nigriceps exploits these differences to distinguish infestation by its host, H. virescens, from that by H. zea. The production by phylogenetically diverse plant species and the exploitation by parasitoids of highly specific chemical signals, keyed to individual herbivore species, indicates that the interaction between plants and the natural enemies of the herbi- vores that attack them is more sophisticated than previously realized. Herbivore-induced plant signals are important for the foraging success of parasitoids and for the plants' defence 3-8 . The production and release of volatiles is triggered at least in part by substance(s) in the oral secretion of herbivores 2,9 ; in cotton, this is known to be an active process in which several terpenoids are synthesized de novo in response to insect feeding 10 . The chemical composition of released volatiles varies among plant tissues (cotton leaves, flowers and bolls, for example) 11 , varieties 12 and cultivars 13 . Although volatile emis-
1,237 citations
"Whiteflies interfere with indirect ..." refers background in this paper
...The discovery that combined infestations by phloemfeeding insects and cell-content feeding herbivores that commonly occur under natural circumstances affect plant-carnivore interactions, demonstrates that chemically mediated interactions in nature are more intricate than previously thought (38)....
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TL;DR: It is shown that uninfested lima bean leaves activate five separate defence genes when exposed to volatiles from conspecific leaves infested with T. urticae, but not when exposed with volatile from artificially wounded leaves.
Abstract: In response to herbivore damage, several plant species emit volatiles that attract natural predators of the attacking herbivores. Using spider mites (Tetranychus urticae) and predatory mites (Phytoseiulus persimilis), it has been shown that not only the attacked plant but also neighbouring plants are affected, becoming more attractive to predatory mites and less susceptible to spider mites. The mechanism involved in such interactions, however, remains elusive. Here we show that uninfested lima bean leaves activate five separate defence genes when exposed to volatiles from conspecific leaves infested with T. urticae, but not when exposed to volatiles from artificially wounded leaves. The expression pattern of these genes is similar to that produced by exposure to jasmonic acid. At least three terpenoids in the volatiles are responsible for this gene activation; they are released in response to herbivory but not artificial wounding. Expression of these genes requires calcium influx and protein phosphorylation/dephosphorylation.
682 citations