Abstract
In the interaction between Arabidopsis (Arabidopsis thaliana) and the generalist herbivorous insect Spodoptera littoralis, little is known about early events in defense signaling and their link to downstream phytohormone pathways. S. littoralis oral secretions induced both Ca²⁺ and phytohormone elevation in Arabidopsis. Plant gene expression induced by oral secretions revealed up-regulation of a gene encoding a calmodulin-like protein, CML42. Functional analysis of cml42 plants revealed more resistance to herbivory than in the wild type, because caterpillars gain less weight on the mutant, indicating that CML42 negatively regulates plant defense; cml42 also showed increased aliphatic glucosinolate content and hyperactivated transcript accumulation of the jasmonic acid (JA)-responsive genes VSP2 and Thi2.1 upon herbivory, which might contribute to increased resistance. CML42 up-regulation is negatively regulated by the jasmonate receptor Coronatine Insensitive1 (COI1), as loss of functional COI1 resulted in prolonged CML42 activation. CML42 thus acts as a negative regulator of plant defense by decreasing COI1-mediated JA sensitivity and the expression of JA-responsive genes and is independent of herbivory-induced JA biosynthesis. JA-induced Ca²⁺ elevation and root growth inhibition were more sensitive in cml42, also indicating higher JA perception. Our results indicate that CML42 acts as a crucial signaling component connecting Ca²⁺ and JA signaling. CML42 is localized to cytosol and nucleus. CML42 is also involved in abiotic stress responses, as kaempferol glycosides were down-regulated in cml42, and impaired in ultraviolet B resistance. Under drought stress, the level of abscisic acid accumulation was higher in cml42 plants. Thus, CML42 might serve as a Ca²⁺ sensor having multiple functions in insect herbivory defense and abiotic stress responses.
Highlights
In the interaction between Arabidopsis (Arabidopsis thaliana) and the generalist herbivorous insect Spodoptera littoralis, little is known about early events in defense signaling and their link to downstream phytohormone pathways
We used crude oral secretions (OS) from S. littoralis previously fed with Arabidopsis to test for elicitors an insect might produce on a natural diet as opposed to an artificial diet
Microarray analysis of early signaling genes induced upon the perception of S. littoralis OS led us to identify the CML42 transcript, which was up-regulated in a transient manner
Summary
In the interaction between Arabidopsis (Arabidopsis thaliana) and the generalist herbivorous insect Spodoptera littoralis, little is known about early events in defense signaling and their link to downstream phytohormone pathways. CML42 might serve as a Ca2+ sensor having multiple functions in insect herbivory defense and abiotic stress responses. Plants respond actively to insect herbivory by the production of phytohormones and antiherbivore secondary metabolites and proteins (Mithöfer et al, 2009). Many of these defenses are coordinated by a jasmonic acid (JA)-dependent signaling cascade that is a key component in plant defense against herbivores. Arabidopsis has at least 250 proteins with predicted Ca2+-binding EF hand domains Such a large number of genes involved in a single pathway point to the importance of Ca2+ signaling in biological responses. CML9 alters plant responses to ABA and abiotic stress (Magnan et al, 2008), and loss of CML42 function leads to aberrant trichomes with increased branching (Dobney et al, 2009)
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