From Structure to Function: Understanding Productivity in Cannabis Glandular Trichomes

Matthew Nolan

doi:10.25918/thesis.533

Cannabis sativa L. glandular trichomes (CsGTs), specialised epidermal structures on female flowers, are the sites of cannabinoid and terpenoid biosynthesis. Over the last decades, selective breeding has driven significant increases in cannabinoid concentrations, with modern cultivars exceeding cannabinoid levels of over 35% of dry flower weight. Despite these advances, molecular mechanisms that support such high levels of secondary metabolite production are not fully understood. This thesis used fluorescent microscopy, quantitative proteomic and metabolomic approaches to investigate drivers of trichome productivity by i) dissecting CsGT development; ii) comparing CsGT from high-yielding modern cultivars with traditional landraces; and iii) exploring the roles of different cell types within CsGTs. The first study identified three distinct CsGT developmental phases: pre-secretory, secretory, and post-secretory. The pre-secretory phase was characterized by smaller secretory cells, limited metabolite accumulation and elevated levels of proteins involved in protein biosynthesis and cellular development. The secretory phase exhibited the highest biosynthetic activity, marked by larger secretory cells, increased plastidal activity, central carbon metabolism, and significant accumulation of cannabinoids and terpenoids. The post-secretory phase showed a decrease in secretory cell size, reduced metabolic activity, and a decrease in primary and secondary metabolism. The second study investigated molecular mechanisms underpinning enhanced productivity in CsGTs of modern cultivars compared to their traditional landrace ancestors. Modern cultivars had larger trichomes, with a greater number of secretory cells. These phenotypic differences were supported by increased metabolic activity, particularly in pathways related to energy production and lipid metabolism. This study highlights the significant morphological and molecular differences between modern and traditional Cannabis cultivars, which are likely the result of selective breeding practices that have largely focused on tetrahydrocannabinol (THC) concentrations in pursuit of increased psychoactivity. The third study explores the functional role of CsGT stalks, which connect secretory heads to flower tissue. While secretory heads are recognized as sites of cannabinoid synthesis, the stalks’ role has remained unclear. Proteomic analysis shows that CsGT stalks serve as sugar sensors, manage resource allocation between the source (flower) and sink (trichome heads) tissues and participate in hormone signalling. Stalks act as regulatory and transport hubs, delivering photo-assimilates and metabolic precursors to meet the high metabolic demands of cannabinoid synthesis in secretory cells. Collectively these studies provide new insights into Cannabis trichome biology and provide targets for the future manipulation of glandular trichome function.

From Structure to Function: Understanding Productivity in Cannabis Glandular Trichomes

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From Structure to Function: Understanding Productivity in Cannabis Glandular Trichomes

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