Mutation of the Arabidopsis Calmodulin-Like Protein CML37 Deregulates the Jasmonate Pathway and Enhances Susceptibility to Herbivory

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 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.

Calmodulin-like protein CML37 is a positive regulator of ABA during drought stress in Arabidopsis

“…12 Recently, several CMLs were identified that are regulated by herbivory or herbivore-related signals present in insect-derived oral secretions. [13][14][15] For 2 particular calmodulin-like proteins, CML37 and CML42, it was demonstrated that they have antagonistic effects. CML42 represents a negative regulator of insect herbivory-induced defense, while CML37 is quite the opposite, a positive regulator of insect herbivoryinduced defense.…”

“…CML42 represents a negative regulator of insect herbivory-induced defense, while CML37 is quite the opposite, a positive regulator of insect herbivoryinduced defense. 13,15 CML37 was shown to connect Ca 2C and jasmonate signaling by affecting the synthesis of jasmonic acidisoleucine conjugate. 15 All those examples demonstrate that almost all CML genes studied so far are involved in more than one stress-responsive pathway, including biotic and abiotic stress, as well as developmental stimuli.…”

Jasmonic acid interacts with abscisic acid to regulate plant responses to water stress conditions

“…17 Recently CML37, a Ca 2C sensor involved in the regulation of herbivore-induced plant defenses mediated by jasmonates was also identified as a positive regulator of ABA in drought stress. 18 The cml37-1 mutant displays a lower expression of JA related genes in response to wounding and, interestingly, this mutant also has a reduced ABA accumulation in response to drought stress, 19 moreover, another member of this Ca 2C sensor family, CML42 has antagonistic effects and Arabidopsis mutant defective in this protein is able to accumulate ABA in response to drought.…”

Respective contribution of CML8 and CML9, two arabidopsis calmodulin-like proteins, to plant stress responses

“…While CML42 acts as a negative regulator of plant defense against herbivorous insects, CML37 acts as a positive regulator. [15][16][17] In response to drought stress, CML37 and CML42 also act as positive and negative regulators respectively. 15,16 Collectively, all these data highlight the complexity of calcium signaling in plant and support the idea that CMLs could be at the crossroads of plant biotic and abiotic stresses signaling pathways.…”

“…[15][16][17] In response to drought stress, CML37 and CML42 also act as positive and negative regulators respectively. 15,16 Collectively, all these data highlight the complexity of calcium signaling in plant and support the idea that CMLs could be at the crossroads of plant biotic and abiotic stresses signaling pathways. CMLs can exhibit a dual function as either positive and/or negative regulators in plant stresses and thus, might be involved in the fine tuning of plant physiological responses to pathogens under fluctuating parameters of the environment (i.e., temperature, water availability).…”