Abstract
Catharanthus roseus produces a wide spectrum of monoterpene indole alkaloids (MIAs). MIA biosynthesis requires a tightly coordinated pathway involving more than 30 enzymatic steps that are spatio-temporally and environmentally regulated so that some MIAs specifically accumulate in restricted plant parts. The first regulatory layer involves a complex network of transcription factors from the basic Helix Loop Helix (bHLH) or AP2 families. In the present manuscript, we investigated whether an additional epigenetic layer could control the organ-, developmental- and environmental-specificity of MIA accumulation. We used Whole-Genome Bisulfite Sequencing (WGBS) together with RNA-seq to identify differentially methylated and expressed genes among nine samples reflecting different plant organs and experimental conditions. Tissue specific gene expression was associated with specific methylation signatures depending on cytosine contexts and gene parts. Some genes encoding key enzymatic steps from the MIA pathway were found to be simultaneously differentially expressed and methylated in agreement with the corresponding MIA accumulation. In addition, we found that transcription factors were strikingly concerned by DNA methylation variations. Altogether, our integrative analysis supports an epigenetic regulation of specialized metabolisms in plants and more likely targeting transcription factors which in turn may control the expression of enzyme-encoding genes.
Highlights
The Madagascar Periwinkle (Catharanthus roseus (L.) G.Don) is a well-known producer of Monoterpene Indole Alkaloids (MIAs) [1]
Our present study reports the first methylome using Whole Genome Bisulfite Sequencing (WGBS) for the medicinal plant C. roseus with DNA methylation signatures specific to organs, ontogenesis, and environmental variations and their relationship with gene expression and MIA accumulation
Focusing on genes whose methylation state and expression levels varied significantly between samples, we found significant relationships depending on cytosine context and gene parts between DNA methylation and expression
Summary
The Madagascar Periwinkle (Catharanthus roseus (L.) G.Don) is a well-known producer of Monoterpene Indole Alkaloids (MIAs) [1]. Vindoline results from the 7-step conversion of tabersonine [8], a molecule that is produced in virtually all parts of the plant. Tabersonine is metabolized into vindoline in leaf or alternatively into lochnericine or hörhammericine in roots [9,10]. Flowers have been reported to have a very low content in catharanthine and high amounts of serpentine and ajmalicine [13]. In addition to this tissue specificity, it has been shown that C. roseus subjected to herbivory by the Tobacco Hornworm Manduca sexta underwent an increase of MIA accumulation through a two-step process [14]. The precise nature of the regulatory events remains largely unknown
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