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The two alpha-dox genes of Nicotiana attenuata: overlapping but distinct functions in development and stress responses.

ABSTRACT: BACKGROUND: Plant fatty acid alpha-dioxygenases (alpha-DOX) are oxylipin-forming enzymes induced by biotic and abiotic stresses, which also participate in developmental processes. In Nicotiana attenuata, herbivory strongly induces the expression of an alpha-dox1 gene. To determine its role, we silenced its expression using Agrobacterium-mediated plant transformation with an inverted repeat construct. More than half of the transformed lines showed a severe dwarf growth phenotype that was very similar to the phenotype of tomato plants mutated at a second alpha-dox isoform. This led us to identify the corresponding alpha-dox2 gene in N. attenuata and examine the regulation of both alpha-dox genes as well as the consequences of their silencing in plant development and anti-herbivore defense. RESULTS: The transformed lines exhibiting a dwarf growth phenotype are co-silenced for both alpha-dox genes resulting in a nearly complete suppression of alpha-DOX activity, which is associated with increases in ABA, JA and anthocyanin levels, all metabolic signatures of oxidative stress. The other lines, only silenced for alpha-dox1, developed similarly to wild-type plants, exhibited a 40% reduction of alpha-DOX activity resulting in a 50% reduction of its main product in planta (2-HOT) and showed no signs of oxidative stress. In contrast to alpha-dox1, the expression of alpha-dox2 gene is not induced by wounding or elicitors in the oral secretions of Manduca sexta. Instead, alpha-dox2 is expressed in roots and flowers which lack alpha-dox1 expression, but both genes are equally regulated during leaf maturation. We transiently silenced alpha-dox gene copies with gene-specific constructs using virus induced gene silencing and determined the consequences for plant development and phytohormone and 2-HOT levels. While individual silencing of alpha-dox1 or alpha-dox2 had no effects on plant growth, the co-suppression of both alpha-dox genes decreased plant growth. Plants transiently silenced for both alpha-dox genes had increased constitutive levels of JA and ABA but silencing alpha-dox1 alone resulted in lower M. sexta-induced levels of JA, 2-HOT and ABA. CONCLUSIONS: Thus, both alpha-dox isoforms function in the development of N. attenuata. In leaf maturation, the two alpha-dox genes have overlapping functions, but only alpha-dox2 is involved in root and flower development and only alpha-dox1 functions in anti-herbivore defense.

SUBMITTER: Steppuhn A

PROVIDER: S-EPMC3017789 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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The two alpha-dox genes of Nicotiana attenuata: overlapping but distinct functions in development and stress responses.

Steppuhn Anke A Gaquerel Emmanuel E Baldwin Ian T IT

BMC plant biology 20100811

<h4>Background</h4>Plant fatty acid alpha-dioxygenases (alpha-DOX) are oxylipin-forming enzymes induced by biotic and abiotic stresses, which also participate in developmental processes. In Nicotiana attenuata, herbivory strongly induces the expression of an alpha-dox1 gene. To determine its role, we silenced its expression using Agrobacterium-mediated plant transformation with an inverted repeat construct. More than half of the transformed lines showed a severe dwarf growth phenotype that was v ...[more]

PMID: 20701756

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Project description:Background and aimsPlants exposed to solar ultraviolet-B radiation (UV-B, 280-315 nm) frequently suffer less insect herbivory than do plants that receive attenuated levels of UV-B. This anti-herbivore effect of solar UV-B exposure, which has been documented in several ecosystems, is in part mediated by changes in plant tissue quality. Exposure to UV-B can modify the abundance of a number of secondary metabolites, including phenolic compounds with potential impacts on insect herbivores. The aim of this study is to assess the potential anti-herbivore role of UV-B-induced phenolic compounds by comparing the phenolic profiles induced by UV-B and simulated insect herbivory in two wild species of the genus Nicotiana.MethodsPlants grown under field and glasshouse conditions were exposed to contrasting levels of UV-B. Half of the plants of the attenuated UV-B treatment were given a simulated herbivory treatment, where leaves were mechanically damaged and immediately treated with oral secretions of Manduca sexta caterpillars. This treatment is known to mimic the impact of real herbivory on the expression of plant defences in Nicotiana. Phenolic profiles induced by UV-B and simulated herbivory were characterized using high-performance liquid chromatography-mass spectrometry (HPLC-MS).Key resultsUV-B induced the accumulation of several UV-absorbing phenolic compounds that are known to play a significant role in UV-B screening. Interestingly, there was a significant convergence in the phenolic profiles induced by UV-B and simulated herbivory: chlorogenic acid and dicaffeoylspermidine isomers, in particular, displayed a similar pattern of response to these stimuli. In contrast, rutin, the only flavonoid that accumulated in significant quantities in the experiments, was only induced by UV-B.ConclusionsThe results suggest that the anti-herbivory effect induced by UV-B may be mediated at least in part by the accumulation of phenylpropanoid derivatives that are similar to those induced by the plant in response to insect herbivory.

Project description:BackgroundTo survive herbivore attack, plants have evolved potent mechanisms of mechanical or chemical defense that are either constitutively present or inducible after herbivore attack. Due to the costs of defense deployment, plants often regulate their biosynthesis using various transcription factors (TFs). MYC2 regulators belong to the bHLH family of transcription factors that are involved in many aspects of plant defense and development. In this study, we identified a novel MYC2 TF from N. attenuata and characterized its regulatory function using a combination of molecular, analytic and ecological methods.ResultsThe transcript and targeted metabolite analyses demonstrated that NaMYC2 is mainly involved in the regulation of the biosynthesis of nicotine and phenolamides in N. attenuata. In addition, using broadly-targeted metabolite analysis, we identified a number of other metabolite features that were regulated by NaMYC2, which, after full annotation, are expected to broaden our understanding of plant defense regulation. Unlike previous reports, the biosynthesis of jasmonates and some JA-/NaCOI1-dependent metabolites (e.g. HGL-DTGs) were not strongly regulated by NaMYC2, suggesting the involvement of other independent regulators. No significant differences were observed in the performance of M. sexta on MYC2-silenced plants, consistent with the well-known ability of this specialist insect to tolerate nicotine.ConclusionBy regulating the biosynthesis of nicotine, NaMYC2 is likely to enhance plant resistance against non-adapted herbivores and contribute to plant fitness; however, multiple JA/NaCOI1-dependent mechanisms (perhaps involving other MYCs) that regulate separate defense responses are likely to exist in N. attenuata. The considerable variation observed amongst different plant families in the responses regulated by jasmonate signaling highlights the sophistication with which plants craft highly specific and fine-tuned responses against the herbivores that attack them.

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The two alpha-dox genes of Nicotiana attenuata: overlapping but distinct functions in development and stress responses.

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The two alpha-dox genes of Nicotiana attenuata: overlapping but distinct functions in development and stress responses.

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