Characterization of the Cannabis sativa glandular trichome epigenome

Abstract Background The relationship between epigenomics and plant specialised metabolism remains largely unexplored despite the fundamental importance of epigenomics in gene regulation and, potentially, yield of products of plant specialised metabolic pathways. The glandular trichomes of Cannabis s...

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Main Authors: Lee J. Conneely, Bhavna Hurgobin, Sophia Ng, Muluneh Tamiru-Oli, Mathew G. Lewsey
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-024-05787-x
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author Lee J. Conneely
Bhavna Hurgobin
Sophia Ng
Muluneh Tamiru-Oli
Mathew G. Lewsey
author_facet Lee J. Conneely
Bhavna Hurgobin
Sophia Ng
Muluneh Tamiru-Oli
Mathew G. Lewsey
author_sort Lee J. Conneely
collection DOAJ
description Abstract Background The relationship between epigenomics and plant specialised metabolism remains largely unexplored despite the fundamental importance of epigenomics in gene regulation and, potentially, yield of products of plant specialised metabolic pathways. The glandular trichomes of Cannabis sativa are an emerging model system that produce large quantities of cannabinoid and terpenoid specialised metabolites with known medicinal and commercial value. To address this lack of epigenomic data, we mapped H3K4 trimethylation, H3K56 acetylation, H3K27 trimethylation post-translational modifications and the histone variant H2A.Z, using chromatin immunoprecipitation, in C. sativa glandular trichomes, leaf, and stem tissues. Corresponding transcriptomic (RNA-seq) datasets were integrated, and tissue-specific analyses conducted to relate chromatin states to glandular trichome specific gene expression. Results The promoters of cannabinoid and terpenoid biosynthetic genes, specialised metabolite transporter genes, defence related genes, and starch and sucrose metabolism were enriched specifically in trichomes for histone marks H3K4me3 and H3K56ac, consistent with active transcription. We identified putative trichome-specific enhancer elements by identifying intergenic regions of H3K56ac enrichment, a histone mark that maintains enhancer accessibility, then associated these to putative target genes using the tissue specific gene transcriptomic data. Bi-valent chromatin loci specific to glandular trichomes, marked with H3K4 trimethylation and H3K27 trimethylation, were associated with genes of MAPK signalling pathways and plant specialised metabolism pathways, supporting recent hypotheses that implicate bi-valent chromatin in plant defence. The histone variant H2A.Z was largely found in intergenic regions and enriched in chromatin that contained genes involved in DNA homeostasis. Conclusion We report the first genome-wide histone post-translational modification maps for C. sativa glandular trichomes, and more broadly for glandular trichomes in plants. Our findings have implications in plant adaptation and stress responses and provide a basis for enhancer-mediated, targeted, gene transformation studies in plant glandular trichomes.
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spelling doaj-art-717ce6354bda49b9ba121c8089e284ac2025-02-02T12:15:35ZengBMCBMC Plant Biology1471-22292024-11-0124112010.1186/s12870-024-05787-xCharacterization of the Cannabis sativa glandular trichome epigenomeLee J. Conneely0Bhavna Hurgobin1Sophia Ng2Muluneh Tamiru-Oli3Mathew G. Lewsey4La Trobe Institute for Sustainable Agriculture and Food, La Trobe UniversityLa Trobe Institute for Sustainable Agriculture and Food, La Trobe UniversityLa Trobe Institute for Sustainable Agriculture and Food, La Trobe UniversityLa Trobe Institute for Sustainable Agriculture and Food, La Trobe UniversityLa Trobe Institute for Sustainable Agriculture and Food, La Trobe UniversityAbstract Background The relationship between epigenomics and plant specialised metabolism remains largely unexplored despite the fundamental importance of epigenomics in gene regulation and, potentially, yield of products of plant specialised metabolic pathways. The glandular trichomes of Cannabis sativa are an emerging model system that produce large quantities of cannabinoid and terpenoid specialised metabolites with known medicinal and commercial value. To address this lack of epigenomic data, we mapped H3K4 trimethylation, H3K56 acetylation, H3K27 trimethylation post-translational modifications and the histone variant H2A.Z, using chromatin immunoprecipitation, in C. sativa glandular trichomes, leaf, and stem tissues. Corresponding transcriptomic (RNA-seq) datasets were integrated, and tissue-specific analyses conducted to relate chromatin states to glandular trichome specific gene expression. Results The promoters of cannabinoid and terpenoid biosynthetic genes, specialised metabolite transporter genes, defence related genes, and starch and sucrose metabolism were enriched specifically in trichomes for histone marks H3K4me3 and H3K56ac, consistent with active transcription. We identified putative trichome-specific enhancer elements by identifying intergenic regions of H3K56ac enrichment, a histone mark that maintains enhancer accessibility, then associated these to putative target genes using the tissue specific gene transcriptomic data. Bi-valent chromatin loci specific to glandular trichomes, marked with H3K4 trimethylation and H3K27 trimethylation, were associated with genes of MAPK signalling pathways and plant specialised metabolism pathways, supporting recent hypotheses that implicate bi-valent chromatin in plant defence. The histone variant H2A.Z was largely found in intergenic regions and enriched in chromatin that contained genes involved in DNA homeostasis. Conclusion We report the first genome-wide histone post-translational modification maps for C. sativa glandular trichomes, and more broadly for glandular trichomes in plants. Our findings have implications in plant adaptation and stress responses and provide a basis for enhancer-mediated, targeted, gene transformation studies in plant glandular trichomes.https://doi.org/10.1186/s12870-024-05787-xCannabis sativaGlandular trichomesSpecialised metabolismMultiomicsH3K4me3H3K27me3
spellingShingle Lee J. Conneely
Bhavna Hurgobin
Sophia Ng
Muluneh Tamiru-Oli
Mathew G. Lewsey
Characterization of the Cannabis sativa glandular trichome epigenome
BMC Plant Biology
Cannabis sativa
Glandular trichomes
Specialised metabolism
Multiomics
H3K4me3
H3K27me3
title Characterization of the Cannabis sativa glandular trichome epigenome
title_full Characterization of the Cannabis sativa glandular trichome epigenome
title_fullStr Characterization of the Cannabis sativa glandular trichome epigenome
title_full_unstemmed Characterization of the Cannabis sativa glandular trichome epigenome
title_short Characterization of the Cannabis sativa glandular trichome epigenome
title_sort characterization of the cannabis sativa glandular trichome epigenome
topic Cannabis sativa
Glandular trichomes
Specialised metabolism
Multiomics
H3K4me3
H3K27me3
url https://doi.org/10.1186/s12870-024-05787-x
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AT mulunehtamiruoli characterizationofthecannabissativaglandulartrichomeepigenome
AT mathewglewsey characterizationofthecannabissativaglandulartrichomeepigenome