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Abstract
Although phenylpropanoid-polyamine conjugates (PPCs) occur ubiquitously in plants, their biological roles remain largely unexplored. The two major PPCs of Nicotiana attenuata plants, caffeoylputrescine (CP) and dicaffeoylspermidine, increase dramatically in local and systemic tissues after herbivore attack and simulations thereof. We identified NaMYB8, a homolog of NtMYBJS1, which in BY-2 cells regulates PPC biosynthesis, and silenced its expression by RNA interference in N. attenuata (ir-MYB8), to understand the ecological role(s) of PPCs. The regulatory role of NaMYB8 in PPC biosynthesis was validated by a microarray analysis, which revealed that transcripts of several key biosynthetic genes in shikimate and polyamine metabolism accumulated in a NaMYB8-dependent manner. Wild-type N. attenuata plants typically contain high levels of PPCs in their reproductive tissues; however, NaMYB8-silenced plants that completely lacked CP and dicaffeoylspermidine showed no changes in reproductive parameters of the plants. In contrast, a defensive role for PPCs was clear; both specialist (Manduca sexta) and generalist (Spodoptera littoralis) caterpillars feeding on systemically preinduced young stem leaves performed significantly better on ir-MYB8 plants lacking PPCs compared with wild-type plants expressing high levels of PPCs. Moreover, the growth of M. sexta caterpillars was significantly reduced when neonates were fed ir-MYB8 leaves sprayed with synthetic CP, corroborating the role of PPCs as direct plant defense. The spatiotemporal accumulation and function of PPCs in N. attenuata are consistent with the predictions of the optimal defense theory: plants preferentially protect their most fitness-enhancing and vulnerable parts, young tissues and reproductive organs, to maximize their fitness.
Highlights
Phenylpropanoid-polyamine conjugates (PPCs) occur ubiquitously in plants, their biological roles remain largely unexplored
A microarray study conducted with ir-MYB8 and wild-type plants revealed that NaMYB8 protein is required for transcriptional activation of genes involved in phenylpropanoid and polyamine biosynthesis, in addition to several other genes with unknown functions. As both specialist (M. sexta) and generalist (Spodoptera littoralis) caterpillars performed better on ir-MYB8 plants compared with wild-type plants, we propose that phenylpropanoid-polyamine conjugates (PPCs) and their regulation by NaMYB8 are vital parts of the direct defense mechanisms used by plants against attacking herbivores
We examined the transcriptional response of NaMYB8 to wounding and herbivore cues: a fully expanded rosette leaf was wounded with a pattern wheel, and either water (W+W), mimicking mechanical wounding, or M. sexta oral secretions (OS) (W+OS), representing simulated herbivory, was applied to the wounds
Summary
Phenylpropanoid-polyamine conjugates (PPCs) occur ubiquitously in plants, their biological roles remain largely unexplored. Jasmonic acid (JA) is known to mediate wound and herbivore stress signals in plants that activate local and systemic defenses and lead to the accumulation of antifeedants and/or ovipositioning deterrents against herbivores These toxins largely impair insect growth and reduce their survivorship rates, helping plants to diminish further damage (Steppuhn and Baldwin, 2007; Chen, 2008). One of the widespread secondary metabolic pathways in plants activated by stress is the biosynthesis of phenylpropanoid-polyamine conjugates (PPCs), which has been frequently found to be positively correlated with increased plant resistance to pathogens, viruses, and fungi (for review, see Edreva et al, 2007); the exact role and mode of action of these metabolites in plants remain unclear (Cowley and Walters, 2005; Edreva et al, 2007). The enzymes responsible for the conjugation of acetyl-CoA-activated phenylpropanoid moieties to polyamines have only started to be identified (Grienenberger et al, 2009; Luo et al, 2009)
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