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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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Systemic responses after W + OS elicitation and leaf excision. Local leaves 0 were W + OS-elicited, and these leaves including petioles were ablated at indicated times after treatment and the elicited systemic responses were determined. a TPI activity (mean ± SE, N =5) in different leaves, 3 d after elicitation of leaves 0, which were either not excised or ablated at different times [untreated plants (“no treatment”) served as comparisons]. b JA accumulation (mean ± SE, N = 5) in leaves +3, 90 min after local leaves were elicited with W + OS and ablated at indicated times. c SIPK activity in systemic leaves +3, 60 min after the leaves 0 were treated with W + OS.
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Fig5: Systemic responses after W + OS elicitation and leaf excision. Local leaves 0 were W + OS-elicited, and these leaves including petioles were ablated at indicated times after treatment and the elicited systemic responses were determined. a TPI activity (mean ± SE, N =5) in different leaves, 3 d after elicitation of leaves 0, which were either not excised or ablated at different times [untreated plants (“no treatment”) served as comparisons]. b JA accumulation (mean ± SE, N = 5) in leaves +3, 90 min after local leaves were elicited with W + OS and ablated at indicated times. c SIPK activity in systemic leaves +3, 60 min after the leaves 0 were treated with W + OS.

Mentions: The increased MAPK activity, JA levels, and TPI activity in systemic leaves after W + OS elicitation revealed that certain long-distance signals are propagated from local leaves to systemic ones to activate these responses. To estimate the time required for the TPI-inducing systemic signal to exit from the wounded leaf, we treated leaves 0 with W + OS and then removed them (by excising from petioles) at 0, 1, 5, and 10 min after the treatments; untreated plants and plants treated with W + OS whose local leaves were retained were used for comparisons. Three days after these initial treatments, TPI activity was measured in systemic leaves (Figure 5a). Immediately removing the treated leaves did not induce any changes of TPI activity, and similarly, excision of the damaged leaves in 1 or 5 min also induced very little systemic TPI (Figure 5a). However, when the local leaves were removed 10 min after the treatment, TPI activity levels in systemic leaves almost fully elevated to those in plants whose treated leaves were retained (Figure 5a). These results suggest that systemic TPI induction involves a signal that exits the wounded leaves between 5 to 10 min, and given that the petiole lengths are about 3 cm, the speed of the signal traveling out of the treated leaves is approximately 0.3 cm/min. These findings are consistent with an earlier study in N. attenuata where it was shown that removing a 3-mm-wide zone adjacent to the W + OS treatment site within 40 s did not prevent the induction of JA in the remaining leaf tissue [34].Figure 5


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)

Systemic responses after W + OS elicitation and leaf excision. Local leaves 0 were W + OS-elicited, and these leaves including petioles were ablated at indicated times after treatment and the elicited systemic responses were determined. a TPI activity (mean ± SE, N =5) in different leaves, 3 d after elicitation of leaves 0, which were either not excised or ablated at different times [untreated plants (“no treatment”) served as comparisons]. b JA accumulation (mean ± SE, N = 5) in leaves +3, 90 min after local leaves were elicited with W + OS and ablated at indicated times. c SIPK activity in systemic leaves +3, 60 min after the leaves 0 were treated with W + OS.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Systemic responses after W + OS elicitation and leaf excision. Local leaves 0 were W + OS-elicited, and these leaves including petioles were ablated at indicated times after treatment and the elicited systemic responses were determined. a TPI activity (mean ± SE, N =5) in different leaves, 3 d after elicitation of leaves 0, which were either not excised or ablated at different times [untreated plants (“no treatment”) served as comparisons]. b JA accumulation (mean ± SE, N = 5) in leaves +3, 90 min after local leaves were elicited with W + OS and ablated at indicated times. c SIPK activity in systemic leaves +3, 60 min after the leaves 0 were treated with W + OS.
Mentions: The increased MAPK activity, JA levels, and TPI activity in systemic leaves after W + OS elicitation revealed that certain long-distance signals are propagated from local leaves to systemic ones to activate these responses. To estimate the time required for the TPI-inducing systemic signal to exit from the wounded leaf, we treated leaves 0 with W + OS and then removed them (by excising from petioles) at 0, 1, 5, and 10 min after the treatments; untreated plants and plants treated with W + OS whose local leaves were retained were used for comparisons. Three days after these initial treatments, TPI activity was measured in systemic leaves (Figure 5a). Immediately removing the treated leaves did not induce any changes of TPI activity, and similarly, excision of the damaged leaves in 1 or 5 min also induced very little systemic TPI (Figure 5a). However, when the local leaves were removed 10 min after the treatment, TPI activity levels in systemic leaves almost fully elevated to those in plants whose treated leaves were retained (Figure 5a). These results suggest that systemic TPI induction involves a signal that exits the wounded leaves between 5 to 10 min, and given that the petiole lengths are about 3 cm, the speed of the signal traveling out of the treated leaves is approximately 0.3 cm/min. These findings are consistent with an earlier study in N. attenuata where it was shown that removing a 3-mm-wide zone adjacent to the W + OS treatment site within 40 s did not prevent the induction of JA in the remaining leaf tissue [34].Figure 5

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