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Abstract
BackgroundThe adage from Shakespeare, "troubles, not as single spies, but in battalions come," holds true for Nicotiana attenuata, which is commonly attacked by both pathogens (Pseudomonas spp.) and herbivores (Manduca sexta) in its native habitats. Defense responses targeted against the pathogens can directly or indirectly influence the responses against the herbivores. Nadefensin is an effective induced defense gene against the bacterial pathogen Pseudomonas syringae pv tomato (PST DC3000), which is also elicited by attack from M. sexta larvae, but whether this defense protein influences M. sexta's growth and whether M. sexta-induced Nadefensin directly or indirectly influences PST DC3000 resistance are unknown.ResultsM. sexta larvae consumed less on WT and on Nadefensin-silenced N. attenuata plants that had previously been infected with PST DC3000 than on uninfected plants. WT plants infected with PST DC3000 showed enhanced resistance to PST DC3000 and decreased leaf consumption by M. sexta larvae, but larval mass gain was unaffected. PST DC3000-infected Nadefensin-silenced plants were less resistant to subsequent PST DC3000 challenge, and on these plants, M. sexta larvae consumed less and gained less mass. WT and Nadefensin-silenced plants previously damaged by M. sexta larvae were better able to resist subsequent PST DC3000 challenges than were undamaged plants.ConclusionThese results demonstrate that Na-defensin directly mediates defense against PST DC3000 and indirectly against M. sexta in N. attenuata. In plants that were previously infected with PST DC3000, the altered leaf chemistry in PST DC3000-resistant WT plants and PST DC3000-susceptible Nadefensin-silenced plants differentially reduced M. sexta's leaf consumption and mass gain. In plants that were previously damaged by M. sexta, the combined effect of the altered host plant chemistry and a broad spectrum of anti-herbivore induced metabolomic responses was more effective than Nadefensin alone in resisting PST DC3000.
Highlights
The adage from Shakespeare, "troubles, not as single spies, but in battalions come," holds true for Nicotiana attenuata, which is commonly attacked by both pathogens (Pseudomonas spp.) and herbivores (Manduca sexta) in its native habitats
The quantitative real-time PCR analysis (Fig. 1) revealed that Nadefensin transcript accumulation differed significantly across treatments and genotypes (Fig. 1; ANOVA F11,17 = 16.00, P < 0.001): Nadefensin levels in WT plants infected with PST DC3000 and in those attacked by M. sexta did not differ significantly (Fig. 1; p = 0.183)
Larvae that fed on PST DC3000-infected WT plants, which are resistant to PST DC3000, consumed significantly more than those that fed on PST DC3000-infected Nadefensinsilenced plants, which are highly susceptible to PST DC3000 (Fig. 2A and 2B); we found no difference in the titers of PST DC3000 in the guts of the larvae (Fig. 4A and 4B) that had consumed either WT or Nadefensin-silenced plants
Summary
The adage from Shakespeare, "troubles, not as single spies, but in battalions come," holds true for Nicotiana attenuata, which is commonly attacked by both pathogens (Pseudomonas spp.) and herbivores (Manduca sexta) in its native habitats. Nadefensin is an effective induced defense gene against the bacterial pathogen Pseudomonas syringae pv tomato (PST DC3000), which is elicited by attack from M. sexta larvae, but whether this defense protein influences M. sexta's growth and whether M. sexta-induced Nadefensin directly or indirectly influences PST DC3000 resistance are unknown. When plants are attacked by pathogens and herbivores, they mount defense responses which can slow an herbivore's feeding and the rate of disease spread. In response to herbivore attack, plants produce a broad spectrum of defense compounds that are elicited by a jasmonic acid-dependent signaling pathway. In response to damage by the solanaceous specialist herbivore Manduca sexta, Nicotiana attenuata produces anti-herbivore defense metabolites such as nicotine [2,3], caffeoyl putrescine, rutin, and diterpene glycoside [4], as well as anti-digestive trypsin protease inhibitors (TPIs) [5,6]. PR13/Na-defensins in N. attenuata have been shown to suppress Pseudomonas syrinage pvtomato-DC3000 (PST DC3000) [9]
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