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Article

Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation

by
Thomas Dugé de Bernonville
1,†,
Stéphane Maury
2,*,†,
Alain Delaunay
2,
Christian Daviaud
3,
Cristian Chaparro
4,
Jörg Tost
3,
Sarah Ellen O’Connor
5 and
Vincent Courdavault
1,*
1
Faculté des Sciences et Techniques, Université de Tours, EA2106 Biomolécules et Biotechnologies Végétales, F-37200 Tours, France
2
INRA, EA1207 USC1328 Laboratoire de Biologie des Ligneux et des Grandes Cultures, Université d’Orléans, F-45067 Orléans, France
3
Laboratoire Epigénétique et Environnement, LEE, Centre National de Recherche en Génomique Humaine, Institut de Biologie François Jacob, F-92265 Evry, France
4
CNRS, IFREMER, UMR5244 Interactions Hôtes-Pathogènes-Environnments, Université de Montpellier, Université de Perpignan Via Domitia, F-66860 Perpignan, France
5
Max Planck Institute for Chemical Ecology, Department of Natural Product Biosynthesis, 07745 Jena, Germany
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2020, 21(17), 6028; https://doi.org/10.3390/ijms21176028
Submission received: 21 July 2020 / Revised: 6 August 2020 / Accepted: 18 August 2020 / Published: 21 August 2020
(This article belongs to the Section Molecular Plant Sciences)
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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.
Keywords: alkaloids; DNA methylation; epigenetics; folivory; organs; plant specialized metabolism alkaloids; DNA methylation; epigenetics; folivory; organs; plant specialized metabolism

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MDPI and ACS Style

Dugé de Bernonville, T.; Maury, S.; Delaunay, A.; Daviaud, C.; Chaparro, C.; Tost, J.; O’Connor, S.E.; Courdavault, V. Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation. Int. J. Mol. Sci. 2020, 21, 6028. https://doi.org/10.3390/ijms21176028

AMA Style

Dugé de Bernonville T, Maury S, Delaunay A, Daviaud C, Chaparro C, Tost J, O’Connor SE, Courdavault V. Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation. International Journal of Molecular Sciences. 2020; 21(17):6028. https://doi.org/10.3390/ijms21176028

Chicago/Turabian Style

Dugé de Bernonville, Thomas, Stéphane Maury, Alain Delaunay, Christian Daviaud, Cristian Chaparro, Jörg Tost, Sarah Ellen O’Connor, and Vincent Courdavault. 2020. "Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation" International Journal of Molecular Sciences 21, no. 17: 6028. https://doi.org/10.3390/ijms21176028

APA Style

Dugé de Bernonville, T., Maury, S., Delaunay, A., Daviaud, C., Chaparro, C., Tost, J., O’Connor, S. E., & Courdavault, V. (2020). Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation. International Journal of Molecular Sciences, 21(17), 6028. https://doi.org/10.3390/ijms21176028

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