Glandular trichomes on the plant surface are specialized epidermal cells which can produce and store a variety of plant specialized metabolites. Specialized phytochemicals produced by trichome are extremely diverse among Solanaceae families and a lot of them have been characterized with the advance of plant omics. Due to their benefits for plant defense system and commercial values, biosynthesis and accumulation of trichome metabolites haven been intensively studied. In this study, analytical chemistry and genetic approaches were integrated to explore the remaining questions about mechanism for the production of specialized metabolites in Solanum trichomes. In particular, this study included three studies addressing the dynamics, distribution and development of specialized metabolism in glandular trichomes from tomato and its relatives. This first study presented the development of analytical methods to profile localized metabolites in biological tissues through chemical imaging, and application of this method to investigations of glandular trichomes. Using this mass spectrometry imaging method, single-cell metabolic profiling and spatially preserved chemical information was achieved in tomato leaf trichomes for several type of trichome specialized metabolites, including acylsugar, flavonoids and terpenes. This work extended imaging mass spectrometry to specialized epidermal cells without using dissection or tissue fixation for the first time. The second study described the isotope labeling methodology for tracing specialized metabolites flux in trichomes. In general, an integrated approach combining whole plant 13CO2 labeling and data-independent LC-MS quantitative profiling was developed to monitor the metabolic dynamic flux and turnover rate of protective plant specialized metabolites. This analytical strategy is applicable to a wide range of specialized metabolites. The third study applied the isotopic labeling strategy to discover the dynamics of trichome specialized metabolites accumulation and the effect of developmental stage of tomato leaves. Using flux analysis method, we measured fluctuations in labeling enrichment and metabolite accumulation during different tomato leaf developmental stages, and demonstrated that total acylsugar accumulation reaches a steady state at early stage of development. Evidence was generated to support the concept that degradation of undetected metabolic intermediates provides a key regulatory point in the acylsugar metabolic network offers a new viewpoint for engineering plant metabolic networks for high levels of end product acylsugars. This novel regulation mechanism extends our understanding of catabolic activities of specialized metabolites.
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