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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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TPI activity in local and systemic leaves. Leaves 0 were wounded with a pattern wheel and 20 μl of water (W + W) or M. sexta OS (W + OS) were applied to the wounds. Treated leaves and systemic leaves were harvested 3 days after the treatment and TPI activity was analyzed. Values are mean ± SE; N = 5.
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Fig4: TPI activity in local and systemic leaves. Leaves 0 were wounded with a pattern wheel and 20 μl of water (W + W) or M. sexta OS (W + OS) were applied to the wounds. Treated leaves and systemic leaves were harvested 3 days after the treatment and TPI activity was analyzed. Values are mean ± SE; N = 5.

Mentions: M. sexta attack increases the levels of TPI transcripts and activity in N. attenuata. This response is not limited to attacked leaves but spreads to systemic ones [30,31]. TPI expression is dependent on JA signaling as COI1- and LOX3-silenced plants that are defective in JA perception and production, respectively, have very little TPI activity and do not accumulate TPI after W + OS elicitation [32,33]. To investigate the pattern of TPI activity in local and systemic leaves and to reveal whether it is correlated with MAPK activation and induced JA/JA-Ile levels, we treated leaves 0 with W + W and W + OS and analyzed TPI activity in local and systemic leaves 3 days after elicitation. Without treatment, highest TPI levels were found in young leaves, and the older ones had very low TPI activity (Figure 4). Wounding elicited increased TPI activity levels in leaves 0 and in leaves +2 and +3, with values 2- to 3-fold of those in uninduced respective controls. In contrast, W + OS treatment induced TPI levels in almost all leaves (Figure 4). Similar to W + W treatment, highest values were detected in the local leaves 0 and in leaves +2 and +3, whose TPI activity levels were twice as much as those induced by wounding; remarkably, despite relatively high W + OS-induced JA-Ile levels in systemic leaves −3 and −2 (Figure 1d), these leaves exhibited only minor TPI activity (Figure 4).Figure 4


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)

TPI activity in local and systemic leaves. Leaves 0 were wounded with a pattern wheel and 20 μl of water (W + W) or M. sexta OS (W + OS) were applied to the wounds. Treated leaves and systemic leaves were harvested 3 days after the treatment and TPI activity was analyzed. Values are mean ± SE; N = 5.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4263023&req=5

Fig4: TPI activity in local and systemic leaves. Leaves 0 were wounded with a pattern wheel and 20 μl of water (W + W) or M. sexta OS (W + OS) were applied to the wounds. Treated leaves and systemic leaves were harvested 3 days after the treatment and TPI activity was analyzed. Values are mean ± SE; N = 5.
Mentions: M. sexta attack increases the levels of TPI transcripts and activity in N. attenuata. This response is not limited to attacked leaves but spreads to systemic ones [30,31]. TPI expression is dependent on JA signaling as COI1- and LOX3-silenced plants that are defective in JA perception and production, respectively, have very little TPI activity and do not accumulate TPI after W + OS elicitation [32,33]. To investigate the pattern of TPI activity in local and systemic leaves and to reveal whether it is correlated with MAPK activation and induced JA/JA-Ile levels, we treated leaves 0 with W + W and W + OS and analyzed TPI activity in local and systemic leaves 3 days after elicitation. Without treatment, highest TPI levels were found in young leaves, and the older ones had very low TPI activity (Figure 4). Wounding elicited increased TPI activity levels in leaves 0 and in leaves +2 and +3, with values 2- to 3-fold of those in uninduced respective controls. In contrast, W + OS treatment induced TPI levels in almost all leaves (Figure 4). Similar to W + W treatment, highest values were detected in the local leaves 0 and in leaves +2 and +3, whose TPI activity levels were twice as much as those induced by wounding; remarkably, despite relatively high W + OS-induced JA-Ile levels in systemic leaves −3 and −2 (Figure 1d), these leaves exhibited only minor TPI activity (Figure 4).Figure 4

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