Mutation of the Arabidopsis Calmodulin-Like Protein CML37 Deregulates the Jasmonate Pathway and Enhances Susceptibility to Herbivory
Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes i...
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| Published in | Molecular plant Vol. 7; no. 12; pp. 1712 - 1726 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Elsevier Inc
01.12.2014
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca2＋ levels play a key role in mediating stress response pathways. Ca2＋ signals are decoded by Ca2＋ sensor proteins such as calmodulin-like proteins （CMLs）. Here, we demonstrate that recombinant CML37 behaves like a Ca2＋ sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca2＋ sensor protein, CML37, functions as a positive regulator in Ca2＋ signaling during herbivory, connecting Ca2＋ and jasmonate signaling. |
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| AbstractList | Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca2+ levels play a key role in mediating stress response pathways. Ca2+ signals are decoded by Ca2+ sensor proteins such as calmodulin-like proteins (CMLs). Here, we demonstrate that recombinant CML37 behaves like a Ca2+ sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca2+ sensor protein, CML37, functions as a positive regulator in Ca2+ signaling during herbivory, connecting Ca2+ and jasmonate signaling. Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca2+ levels play a key role in mediating stress response pathways. Ca2+ signals are decoded by Ca2+ sensor proteins such as calmodulin-like proteins (CMLs). Here, we demonstrate that recombinant CML37 behaves like a Ca2+ sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca2+ sensor protein, CML37, functions as a positive regulator in Ca2+ signaling during herbivory, connecting Ca2+ and jasmonate signaling. The Ca2+ sensor protein CML37 acts as positive defense regulator upon herbivory in Arabidopsis. After Spodoptera littoralis feeding, CML37 enhances the jasmonate pathway by promoting JAR1 activity and thereby downstream defense activation. Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca(2+) levels play a key role in mediating stress response pathways. Ca(2+) signals are decoded by Ca(2+) sensor proteins such as calmodulin-like proteins (CMLs). Here, we demonstrate that recombinant CML37 behaves like a Ca(2+) sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca(2+) sensor protein, CML37, functions as a positive regulator in Ca(2+) signaling during herbivory, connecting Ca(2+) and jasmonate signaling. Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca(2+) levels play a key role in mediating stress response pathways. Ca(2+) signals are decoded by Ca(2+) sensor proteins such as calmodulin-like proteins (CMLs). Here, we demonstrate that recombinant CML37 behaves like a Ca(2+) sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca(2+) sensor protein, CML37, functions as a positive regulator in Ca(2+) signaling during herbivory, connecting Ca(2+) and jasmonate signaling.Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca(2+) levels play a key role in mediating stress response pathways. Ca(2+) signals are decoded by Ca(2+) sensor proteins such as calmodulin-like proteins (CMLs). Here, we demonstrate that recombinant CML37 behaves like a Ca(2+) sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca(2+) sensor protein, CML37, functions as a positive regulator in Ca(2+) signaling during herbivory, connecting Ca(2+) and jasmonate signaling. Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca2＋ levels play a key role in mediating stress response pathways. Ca2＋ signals are decoded by Ca2＋ sensor proteins such as calmodulin-like proteins （CMLs）. Here, we demonstrate that recombinant CML37 behaves like a Ca2＋ sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca2＋ sensor protein, CML37, functions as a positive regulator in Ca2＋ signaling during herbivory, connecting Ca2＋ and jasmonate signaling. |
| Author | Sandra S. Scholz Jyothilakshmi Vadassery Monika Heyer Michael Reichelt Kyle W. Bender Wayne A. Snedden Wilhelm Boland Axel Mithofer |
| AuthorAffiliation | Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knoll-StraBe 8, 07745 Jena, Germany Department of Biochemistry, Max Planck Institute for Chemica Eco ogy, Hans-Knoll-StraBe 8, 07745 Jena, Germany Department of Plant Biology, University of Illinois, Urbana, IL 61801, USA Department of Biology, Queen＇s University, Kingston, Ontario, Canada, Canada, K7L 3N6 |
| Author_xml | – sequence: 1 givenname: Sandra S. surname: Scholz fullname: Scholz, Sandra S. organization: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany – sequence: 2 givenname: Jyothilakshmi surname: Vadassery fullname: Vadassery, Jyothilakshmi organization: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany – sequence: 3 givenname: Monika surname: Heyer fullname: Heyer, Monika organization: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany – sequence: 4 givenname: Michael surname: Reichelt fullname: Reichelt, Michael organization: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany – sequence: 5 givenname: Kyle W. surname: Bender fullname: Bender, Kyle W. organization: Department of Plant Biology, University of Illinois, Urbana, IL 61801, USA – sequence: 6 givenname: Wayne A. surname: Snedden fullname: Snedden, Wayne A. organization: Department of Biology, Queen's University, Kingston, Ontario, K7L 3N6 Canada – sequence: 7 givenname: Wilhelm surname: Boland fullname: Boland, Wilhelm organization: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany – sequence: 8 givenname: Axel surname: Mithöfer fullname: Mithöfer, Axel email: amithoefer@ice.mpg.de organization: Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, 07745 Jena, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25267731$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2014 The Authors. All rights reserved. The Author 2014. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPB and IPPE, SIBS, CAS. |
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| DocumentTitleAlternate | Mutation of the Arabidopsis Calmodulin-Like Protein CML37 Deregulates the Jasmonate Pathway and Enhances Susceptibility to Herbivory |
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| Keywords | herbivory jasmonates calmodulin-like proteins oral secretion cytosolic calcium |
| Language | English |
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| Notes | 31-2013/Q herbivory; oral secretion; jasmonates; cytosolic calcium; calmodulin-like proteins. Throughout their life, plants are challenged by various abiotic and biotic stress factors. Among those are attacks from herbivorous insects. The molecular mechanisms underlying the detection of herbivores and the subsequent signal transduction are not well understood. As a second messenger, fluxes in intracellular Ca2＋ levels play a key role in mediating stress response pathways. Ca2＋ signals are decoded by Ca2＋ sensor proteins such as calmodulin-like proteins （CMLs）. Here, we demonstrate that recombinant CML37 behaves like a Ca2＋ sensor in vitro and, in Arabidopsis, AtCML37 is induced by mechanical wounding as well as by infestation with larvae of the generalist lepidopteran herbivore Spodoptera littoralis. Loss of function of CML37 led to a better feeding performance of larvae suggesting that CML37 is a positive defense regulator. No herbivory-induced changes in secondary metabolites such as glucosinolates or flavonoids were detected in cml37 plants, although a significant reduction in the accumulation of jasmonates was observed, due to reduced expression of JAR1 mRNA and cellular enzyme activity. Consequently, the expression of jasmonate-responsive genes was reduced as well. Summarizing, our results suggest that the Ca2＋ sensor protein, CML37, functions as a positive regulator in Ca2＋ signaling during herbivory, connecting Ca2＋ and jasmonate signaling. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
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| SubjectTerms | Animals Arabidopsis Arabidopsis - genetics Arabidopsis - physiology Arabidopsis Proteins - genetics biotic stress calcium Calcium Signaling Calmodulin - genetics calmodulin-like proteins Cyclopentanes - chemistry cytosolic calcium enzyme activity flavonoids Gene Expression Regulation, Plant genes glucosinolates Herbivory jasmonates jasmonic acid larvae messenger RNA Mutation oral secretion Oxylipins - chemistry phytophagous insects proteins secondary metabolites Spodoptera Spodoptera littoralis stress response 拟南芥 敏感性 植食性昆虫 次级代谢产物 突变 茉莉酸类 钙调素 钙调蛋白 |
| Title | Mutation of the Arabidopsis Calmodulin-Like Protein CML37 Deregulates the Jasmonate Pathway and Enhances Susceptibility to Herbivory |
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