Summary Tea trichomes synthesize numerous specialized metabolites to protect plants from environmental stresses and contribute to tea flavours, but little is known about the regulation of trichome development. Here, we showed that CsMYB1 is involved in the regulation of trichome formation and galloylated cis‐catechins biosynthesis in tea plants. The variations in CsMYB1 expression levels are closely correlated with trichome indexes and galloylated cis‐catechins contents in tea plant populations. Genome resequencing showed that CsMYB1 may be selected in modern tea cultivars, since a 192‐bp insertion in CsMYB1 promoter was found exclusively in modern tea cultivars but not in the glabrous wild tea Camellia taliensis. Several enhancers in the 192‐bp insertion increased CsMYB1 transcription in modern tea cultivars that coincided with their higher galloylated cis‐catechins contents and trichome indexes. Biochemical analyses and transgenic data showed that CsMYB1 interacted with CsGL3 and CsWD40 and formed a MYB‐bHLH‐WD40 (MBW) transcriptional complex to activate the trichome regulator genes CsGL2 and CsCPC, and the galloylated cis‐catechins biosynthesis genes anthocyanidin reductase and serine carboxypeptidase‐like 1A. CsMYB1 integratively regulated trichome formation and galloylated cis‐catechins biosynthesis. Results suggest that CsMYB1, trichome and galloylated cis‐catechins are coincidently selected during tea domestication by harsh environments for improved adaption and by breeders for better tea flavours.

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Caffeine is a characteristic bioactive compound in tea and coffee plants, which is synthesized and accumulated extensively in leaves and seeds. However, little is known about the regulatory mechanism of caffeine synthesis in plants. This study compared the caffeine metabolite between tea and coffee plants. We found that tea leaves contained significantly higher caffeine than coffee leaves, which is perhaps due to more members of N-methyltransferase (NMT) genes as well as higher expression levels in tea plants. Substantial numbers of transcription factors were predicted to be involved in caffeine biosynthesis regulation, combining weighted gene co-expression network analysis and the cis-element of NMT promoter analysis in tea and coffee plants. Furthermore, analysis of the transcription factors from the caffeine-related modules suggested that the regulatory mechanism of caffeine biosynthesis was probably partly conservative in tea and coffee plants. This study provides an essential resource for the regulatory mechanism of caffeine biosynthesis in plants.

Stomata perform important functions in plant photosynthesis, respiration, gas exchange, and interactions with environments. However, tea plant stomata development and functions are not known. Here, we show morphological changes during stomata development and genetic dissection of stomata lineage genes regulating stomata formation in tea developing leaves. Different tea plant cultivars displayed clear variations in the stomata development rate, density and size, which are closely related to their tolerance against dehydration capabilities. Whole sets of stomata lineage genes were identified to display predicted functions in regulating stomatal development and formation. The stomata development and lineage genes were tightly regulated by light intensities and high or low temperature stresses, which affected stomata density and function. Furthermore, lower stomatal density and larger size were observed in triploid tea varieties as compared to those in diploid plant. Key stomata lineage genes such as CsSPCHs, CsSCRM, and CsFAMA showed much lower expression levels, whereas negative regulators CsEPF1 and CsYODAs had higher expression levels in triploid than in diploid tea varieties. Our study provides new insight into tea plant stomatal morphological development and the genetic regulatory mechanisms on stomata development under abiotic stresses and genetic backgrounds. The study lays a foundation for future exploring the genetic improvement of water use efficiency in tea plants for living up to the challenging global climate change.

The flowers of tea plants (Camellia sinensis), as well as tea leaves, contain abundant secondary metabolites and are big potential resources for the extraction of bioactive compounds or preparation of functional foods. However, little is known about the biosynthesis and transcriptional regulation mechanisms of those metabolites in tea flowers, such as terpenoid, flavonol, catechins, caffeine, and theanine. This study finely integrated target and nontarget metabolism analyses to explore the metabolic feature of developing tea flowers. Tea flowers accumulated more abundant terpenoid compounds than young leaves. The transcriptome data of developing flowers and leaves showed that a higher expression level of later genes of terpenoid biosynthesis pathway, such as Terpene synthases gene family, in tea flowers was the candidate reason of the more abundant terpenoid compounds than in tea leaves. Differently, even though flavonol and catechin profiling between tea flowers and leaves was similar, the gene family members of flavonoid biosynthesis were selectively expressed by tea flowers and tea leaves. Transcriptome and phylogenetic analyses indicated that the regulatory mechanism of flavonol biosynthesis was perhaps different between tea flowers and leaves. However, the regulatory mechanism of catechin biosynthesis was perhaps similar between tea flowers and leaves. This study not only provides a global vision of metabolism and transcriptome in tea flowers but also uncovered the different mechanisms of biosynthesis and transcriptional regulation of those important compounds.