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Fatty acid-amino acid conjugates are essential for systemic activation of salicylic acid-induced protein kinase and accumulation of jasmonic acid in Nicotiana attenuata.

Hettenhausen C, Heinrich M, Baldwin IT, Wu J - BMC Plant Biol. (2014)

Bottom Line: Previous studies mainly focused on individual responses and a limited number of systemic leaves, and more research is needed for a better understanding of how different plant parts respond to herbivory.In contrast to the activation of SIPK and elevation of JA in specific systemic leaves, increases in the activity of an important anti-herbivore defense, trypsin proteinase inhibitor (TPI), were observed in all systemic leaves after simulated herbivory, suggesting that systemic TPI induction does not require SIPK activation and JA increases.Leaf ablation experiments demonstrated that within 10 minutes after simulated herbivory, a signal (or signals) was produced and transported out of the treated leaves, and subsequently activated systemic responses.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Herbivory induces the activation of mitogen-activated protein kinases (MAPKs), the accumulation of jasmonates and defensive metabolites in damaged leaves and in distal undamaged leaves. Previous studies mainly focused on individual responses and a limited number of systemic leaves, and more research is needed for a better understanding of how different plant parts respond to herbivory. In the wild tobacco Nicotiana attenuata, FACs (fatty acid-amino acid conjugates) in Manduca sexta oral secretions (OS) are the major elicitors that induce herbivory-specific signaling but their role in systemic signaling is largely unknown.

Results: Here, we show that simulated herbivory (adding M. sexta OS to fresh wounds) dramatically increased SIPK (salicylic acid-induced protein kinase) activity and jasmonic acid (JA) levels in damaged leaves and in certain (but not all) undamaged systemic leaves, whereas wounding alone had no detectable systemic effects; importantly, FACs and wounding are both required for activating these systemic responses. In contrast to the activation of SIPK and elevation of JA in specific systemic leaves, increases in the activity of an important anti-herbivore defense, trypsin proteinase inhibitor (TPI), were observed in all systemic leaves after simulated herbivory, suggesting that systemic TPI induction does not require SIPK activation and JA increases. Leaf ablation experiments demonstrated that within 10 minutes after simulated herbivory, a signal (or signals) was produced and transported out of the treated leaves, and subsequently activated systemic responses.

Conclusions: Our results reveal that N. attenuata specifically recognizes herbivore-derived FACs in damaged leaves and rapidly send out a long-distance signal to phylotactically connected leaves to activate MAPK and JA signaling, and we propose that FACs that penetrated into wounds rapidly induce the production of another long-distance signal(s) which travels to all systemic leaves and activates TPI defense.

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Wounding and FACs are both required for systemic JA accumulation. a JA levels in local leaves 0 after wounding. The leaves 0 were wounded with a pattern wheel and 20 μl of water were immediately applied to wounds (W + W), and the JA contents were analyzed. b JA and JA-Ile contents in local and systemic leaves 90 min after W + W treatment. c and d JA and JA-Ile values in different leaves 90 min after applying FAC or FAC-free OS to wounds. Leaves 0 were wounded with a pattern wheel and 20 μl of FAC (27.6 ng/μl; W + FAC) or 20 μl FAC-free M. sexta OS (W + FAC-free OS) were immediately applied to wounds. e JA contents in different leaves 90 min after pressure infiltration of 100 μl FAC (27.6 ng/μl) into leaves 0. Values are mean ± SE; N = 5; n.d. = not detectable.
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Fig2: Wounding and FACs are both required for systemic JA accumulation. a JA levels in local leaves 0 after wounding. The leaves 0 were wounded with a pattern wheel and 20 μl of water were immediately applied to wounds (W + W), and the JA contents were analyzed. b JA and JA-Ile contents in local and systemic leaves 90 min after W + W treatment. c and d JA and JA-Ile values in different leaves 90 min after applying FAC or FAC-free OS to wounds. Leaves 0 were wounded with a pattern wheel and 20 μl of FAC (27.6 ng/μl; W + FAC) or 20 μl FAC-free M. sexta OS (W + FAC-free OS) were immediately applied to wounds. e JA contents in different leaves 90 min after pressure infiltration of 100 μl FAC (27.6 ng/μl) into leaves 0. Values are mean ± SE; N = 5; n.d. = not detectable.

Mentions: In maize leaves, wounding induces JA accumulation only at the immediate site of damage, whereas insect elicitors also induce JA accumulation in distant tissues [28]. Previous research on N. attenuata revealed that after simulated herbivory, JA levels in distal leaves accumulate to less than 10% of the local maximum [9,23,24], and after wounding alone no increase in JA was detected [9]. To gain insight into the responses of systemic leaves to mechanical wounding, leaves 0 were wounded and 20 μl of water were applied (W + W), and JA and JA-Ile accumulations were determined in all leaves. Local JA levels increased 10 min after the treatment and reached high values between 30 and 90 min (about 550 ng g−1 FM), which were significantly smaller than those detected after W + OS elicitation; after 150 min, JA levels decreased back to almost basal levels (Figure 2a). JA-Ile followed the JA pattern but accumulated to the highest levels after 30 min (137 ng g−1 FM) (Figure 2a). In contrast to W + OS, W + W treatment did not lead to detectably increased JA and JA-Ile levels in any systemic leaves 90 min after treatment (Figure 2b) and other times examined (30, 60, and 150 min; these data are not shown). These findings suggest that the systemic JA accumulation is OS-dependent and wounding alone has non-detectable effect on systemic JA levels. FACs in M. sexta OS are known to be the elicitors for OS-specific plant responses, such as MAPK activation [3], JA burst, and accumulation of defense metabolites [17,29]. Given that applying OS to wounds (W + OS) induced systemic JA accumulation, we next explored whether FACs were responsible for this systemic response.Figure 2


Fatty acid-amino acid conjugates are essential for systemic activation of salicylic acid-induced protein kinase and accumulation of jasmonic acid in Nicotiana attenuata.

Hettenhausen C, Heinrich M, Baldwin IT, Wu J - BMC Plant Biol. (2014)

Wounding and FACs are both required for systemic JA accumulation. a JA levels in local leaves 0 after wounding. The leaves 0 were wounded with a pattern wheel and 20 μl of water were immediately applied to wounds (W + W), and the JA contents were analyzed. b JA and JA-Ile contents in local and systemic leaves 90 min after W + W treatment. c and d JA and JA-Ile values in different leaves 90 min after applying FAC or FAC-free OS to wounds. Leaves 0 were wounded with a pattern wheel and 20 μl of FAC (27.6 ng/μl; W + FAC) or 20 μl FAC-free M. sexta OS (W + FAC-free OS) were immediately applied to wounds. e JA contents in different leaves 90 min after pressure infiltration of 100 μl FAC (27.6 ng/μl) into leaves 0. Values are mean ± SE; N = 5; n.d. = not detectable.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Fig2: Wounding and FACs are both required for systemic JA accumulation. a JA levels in local leaves 0 after wounding. The leaves 0 were wounded with a pattern wheel and 20 μl of water were immediately applied to wounds (W + W), and the JA contents were analyzed. b JA and JA-Ile contents in local and systemic leaves 90 min after W + W treatment. c and d JA and JA-Ile values in different leaves 90 min after applying FAC or FAC-free OS to wounds. Leaves 0 were wounded with a pattern wheel and 20 μl of FAC (27.6 ng/μl; W + FAC) or 20 μl FAC-free M. sexta OS (W + FAC-free OS) were immediately applied to wounds. e JA contents in different leaves 90 min after pressure infiltration of 100 μl FAC (27.6 ng/μl) into leaves 0. Values are mean ± SE; N = 5; n.d. = not detectable.
Mentions: In maize leaves, wounding induces JA accumulation only at the immediate site of damage, whereas insect elicitors also induce JA accumulation in distant tissues [28]. Previous research on N. attenuata revealed that after simulated herbivory, JA levels in distal leaves accumulate to less than 10% of the local maximum [9,23,24], and after wounding alone no increase in JA was detected [9]. To gain insight into the responses of systemic leaves to mechanical wounding, leaves 0 were wounded and 20 μl of water were applied (W + W), and JA and JA-Ile accumulations were determined in all leaves. Local JA levels increased 10 min after the treatment and reached high values between 30 and 90 min (about 550 ng g−1 FM), which were significantly smaller than those detected after W + OS elicitation; after 150 min, JA levels decreased back to almost basal levels (Figure 2a). JA-Ile followed the JA pattern but accumulated to the highest levels after 30 min (137 ng g−1 FM) (Figure 2a). In contrast to W + OS, W + W treatment did not lead to detectably increased JA and JA-Ile levels in any systemic leaves 90 min after treatment (Figure 2b) and other times examined (30, 60, and 150 min; these data are not shown). These findings suggest that the systemic JA accumulation is OS-dependent and wounding alone has non-detectable effect on systemic JA levels. FACs in M. sexta OS are known to be the elicitors for OS-specific plant responses, such as MAPK activation [3], JA burst, and accumulation of defense metabolites [17,29]. Given that applying OS to wounds (W + OS) induced systemic JA accumulation, we next explored whether FACs were responsible for this systemic response.Figure 2

Bottom Line: Previous studies mainly focused on individual responses and a limited number of systemic leaves, and more research is needed for a better understanding of how different plant parts respond to herbivory.In contrast to the activation of SIPK and elevation of JA in specific systemic leaves, increases in the activity of an important anti-herbivore defense, trypsin proteinase inhibitor (TPI), were observed in all systemic leaves after simulated herbivory, suggesting that systemic TPI induction does not require SIPK activation and JA increases.Leaf ablation experiments demonstrated that within 10 minutes after simulated herbivory, a signal (or signals) was produced and transported out of the treated leaves, and subsequently activated systemic responses.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Herbivory induces the activation of mitogen-activated protein kinases (MAPKs), the accumulation of jasmonates and defensive metabolites in damaged leaves and in distal undamaged leaves. Previous studies mainly focused on individual responses and a limited number of systemic leaves, and more research is needed for a better understanding of how different plant parts respond to herbivory. In the wild tobacco Nicotiana attenuata, FACs (fatty acid-amino acid conjugates) in Manduca sexta oral secretions (OS) are the major elicitors that induce herbivory-specific signaling but their role in systemic signaling is largely unknown.

Results: Here, we show that simulated herbivory (adding M. sexta OS to fresh wounds) dramatically increased SIPK (salicylic acid-induced protein kinase) activity and jasmonic acid (JA) levels in damaged leaves and in certain (but not all) undamaged systemic leaves, whereas wounding alone had no detectable systemic effects; importantly, FACs and wounding are both required for activating these systemic responses. In contrast to the activation of SIPK and elevation of JA in specific systemic leaves, increases in the activity of an important anti-herbivore defense, trypsin proteinase inhibitor (TPI), were observed in all systemic leaves after simulated herbivory, suggesting that systemic TPI induction does not require SIPK activation and JA increases. Leaf ablation experiments demonstrated that within 10 minutes after simulated herbivory, a signal (or signals) was produced and transported out of the treated leaves, and subsequently activated systemic responses.

Conclusions: Our results reveal that N. attenuata specifically recognizes herbivore-derived FACs in damaged leaves and rapidly send out a long-distance signal to phylotactically connected leaves to activate MAPK and JA signaling, and we propose that FACs that penetrated into wounds rapidly induce the production of another long-distance signal(s) which travels to all systemic leaves and activates TPI defense.

Show MeSH
Related in: MedlinePlus