Carnivorous Nepenthes x ventrata plants use a naphthoquinone as phytoanticipin against herbivory
Carnivorous plants feed on animal prey, mainly insects, to get additional nutrients. This carnivorous syndrome is widely investigated and reported. In contrast, reports on herbivores feeding on carnivorous plants and related defenses of the plants under attack are rare. Here, we studied the interact...
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Published in | PloS one Vol. 16; no. 10; p. e0258235 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
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Public Library of Science
22.10.2021
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ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/journal.pone.0258235 |
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Abstract | Carnivorous plants feed on animal prey, mainly insects, to get additional nutrients. This carnivorous syndrome is widely investigated and reported. In contrast, reports on herbivores feeding on carnivorous plants and related defenses of the plants under attack are rare. Here, we studied the interaction of a pitcher plant,
Nepenthes x ventrata
, with a generalist lepidopteran herbivore,
Spodoptera littoralis
, using a combination of LC/MS-based chemical analytics, choice and feeding assays. Chemical defenses in
N
.
x ventrata
leaves were analyzed upon
S
.
littoralis
feeding. A naphthoquinone, plumbagin, was identified in
Nepenthes
defense against herbivores and as the compound mainly responsible for the finding that
S
.
littoralis
larvae gained almost no weight when feeding on
Nepenthes
leaves. Plumbagin is constitutively present but further 3-fold increased upon long-term (> 1 day) feeding. Moreover, in parallel
de novo
induced trypsin protease inhibitor (TI) activity was identified. In contrast to TI activity, enhanced plumbagin levels were not phytohormone inducible, not even by defense-related jasmonates although upon herbivory their level increased more than 50-fold in the case of the bioactive jasmonic acid-isoleucine. We conclude that
Nepenthes
is efficiently protected against insect herbivores by naphthoquinones acting as phytoanticipins, which is supported by additional inducible defenses. The regulation of these defenses remains to be investigated. |
---|---|
AbstractList | Carnivorous plants feed on animal prey, mainly insects, to get additional nutrients. This carnivorous syndrome is widely investigated and reported. In contrast, reports on herbivores feeding on carnivorous plants and related defenses of the plants under attack are rare. Here, we studied the interaction of a pitcher plant,
Nepenthes x ventrata
, with a generalist lepidopteran herbivore,
Spodoptera littoralis
, using a combination of LC/MS-based chemical analytics, choice and feeding assays. Chemical defenses in
N
.
x ventrata
leaves were analyzed upon
S
.
littoralis
feeding. A naphthoquinone, plumbagin, was identified in
Nepenthes
defense against herbivores and as the compound mainly responsible for the finding that
S
.
littoralis
larvae gained almost no weight when feeding on
Nepenthes
leaves. Plumbagin is constitutively present but further 3-fold increased upon long-term (> 1 day) feeding. Moreover, in parallel
de novo
induced trypsin protease inhibitor (TI) activity was identified. In contrast to TI activity, enhanced plumbagin levels were not phytohormone inducible, not even by defense-related jasmonates although upon herbivory their level increased more than 50-fold in the case of the bioactive jasmonic acid-isoleucine. We conclude that
Nepenthes
is efficiently protected against insect herbivores by naphthoquinones acting as phytoanticipins, which is supported by additional inducible defenses. The regulation of these defenses remains to be investigated. Carnivorous plants feed on animal prey, mainly insects, to get additional nutrients. This carnivorous syndrome is widely investigated and reported. In contrast, reports on herbivores feeding on carnivorous plants and related defenses of the plants under attack are rare. Here, we studied the interaction of a pitcher plant, Nepenthes x ventrata, with a generalist lepidopteran herbivore, Spodoptera littoralis, using a combination of LC/MS-based chemical analytics, choice and feeding assays. Chemical defenses in N. x ventrata leaves were analyzed upon S. littoralis feeding. A naphthoquinone, plumbagin, was identified in Nepenthes defense against herbivores and as the compound mainly responsible for the finding that S. littoralis larvae gained almost no weight when feeding on Nepenthes leaves. Plumbagin is constitutively present but further 3-fold increased upon long-term (> 1 day) feeding. Moreover, in parallel de novo induced trypsin protease inhibitor (TI) activity was identified. In contrast to TI activity, enhanced plumbagin levels were not phytohormone inducible, not even by defense-related jasmonates although upon herbivory their level increased more than 50-fold in the case of the bioactive jasmonic acid-isoleucine. We conclude that Nepenthes is efficiently protected against insect herbivores by naphthoquinones acting as phytoanticipins, which is supported by additional inducible defenses. The regulation of these defenses remains to be investigated. Carnivorous plants feed on animal prey, mainly insects, to get additional nutrients. This carnivorous syndrome is widely investigated and reported. In contrast, reports on herbivores feeding on carnivorous plants and related defenses of the plants under attack are rare. Here, we studied the interaction of a pitcher plant, Nepenthes x ventrata, with a generalist lepidopteran herbivore, Spodoptera littoralis, using a combination of LC/MS-based chemical analytics, choice and feeding assays. Chemical defenses in N. x ventrata leaves were analyzed upon S. littoralis feeding. A naphthoquinone, plumbagin, was identified in Nepenthes defense against herbivores and as the compound mainly responsible for the finding that S. littoralis larvae gained almost no weight when feeding on Nepenthes leaves. Plumbagin is constitutively present but further 3-fold increased upon long-term (> 1 day) feeding. Moreover, in parallel de novo induced trypsin protease inhibitor (TI) activity was identified. In contrast to TI activity, enhanced plumbagin levels were not phytohormone inducible, not even by defense-related jasmonates although upon herbivory their level increased more than 50-fold in the case of the bioactive jasmonic acid-isoleucine. We conclude that Nepenthes is efficiently protected against insect herbivores by naphthoquinones acting as phytoanticipins, which is supported by additional inducible defenses. The regulation of these defenses remains to be investigated.Carnivorous plants feed on animal prey, mainly insects, to get additional nutrients. This carnivorous syndrome is widely investigated and reported. In contrast, reports on herbivores feeding on carnivorous plants and related defenses of the plants under attack are rare. Here, we studied the interaction of a pitcher plant, Nepenthes x ventrata, with a generalist lepidopteran herbivore, Spodoptera littoralis, using a combination of LC/MS-based chemical analytics, choice and feeding assays. Chemical defenses in N. x ventrata leaves were analyzed upon S. littoralis feeding. A naphthoquinone, plumbagin, was identified in Nepenthes defense against herbivores and as the compound mainly responsible for the finding that S. littoralis larvae gained almost no weight when feeding on Nepenthes leaves. Plumbagin is constitutively present but further 3-fold increased upon long-term (> 1 day) feeding. Moreover, in parallel de novo induced trypsin protease inhibitor (TI) activity was identified. In contrast to TI activity, enhanced plumbagin levels were not phytohormone inducible, not even by defense-related jasmonates although upon herbivory their level increased more than 50-fold in the case of the bioactive jasmonic acid-isoleucine. We conclude that Nepenthes is efficiently protected against insect herbivores by naphthoquinones acting as phytoanticipins, which is supported by additional inducible defenses. The regulation of these defenses remains to be investigated. |
Audience | Academic |
Author | Dávila-Lara, Alberto Mithöfer, Axel Reichelt, Michael Rahman-Soad, Asifur |
AuthorAffiliation | Zhejiang University, CHINA 2 Department of Biochemistry, Max Planck Institute for Chemical Ecology Jena, Germany 1 Research Group Plant Defense Physiology, Max Planck Institute for Chemical Ecology, Jena, Germany |
AuthorAffiliation_xml | – name: 1 Research Group Plant Defense Physiology, Max Planck Institute for Chemical Ecology, Jena, Germany – name: 2 Department of Biochemistry, Max Planck Institute for Chemical Ecology Jena, Germany – name: Zhejiang University, CHINA |
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SubjectTerms | Carnivorous plants Chemical defense Chemical ecology Chemistry Comparative analysis Experiments Feeding Herbivores Herbivory Humidity Insects Isoleucine Jasmonic acid Larvae Leaves Metabolites Naphthalene Nepenthes Nutrients Physiology Plant hormones Plumbagin Polyethylene terephthalate Prey Properties Protease inhibitors Proteinase inhibitors Trypsin |
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Title | Carnivorous Nepenthes x ventrata plants use a naphthoquinone as phytoanticipin against herbivory |
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