Novel players in organogenesis of and flavonoid biosynthesis in cucumber glandular trichomes

Authors: FENG, ZHIXUAN - China Agricultural University; SUN, LEI - China Agricultural University; DONG, MINIMIN - China Agricultural University; FAN, SHANAHAN - China Agricultural University; XI, KEIXIN - China Agricultural University; WANG, WUJUN - China Agricultural University; SONG, LIYAN - China Agricultural University; Weng, Yiqun; LIU, XINWANG - China Agricultural University; REN, HUAZHONG - China Agricultural University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2023
Publication Date: 4/26/2023
Citation: Feng, Z., Sun, L., Dong, M., Fan, S., Xi, K., Wang, W., Song, L., Weng, Y., Liu, X., Ren, H. 2023. Novel players in organogenesis of and flavonoid biosynthesis in cucumber glandular trichomes. Plant Physiology. 192 (4), 2723-2736. https://doi.org/10.1093/plphys/kiad236.
DOI: https://doi.org/10.1093/plphys/kiad236

Interpretive Summary: Background The glandular trichomes (GTs) are outgrowths of plant epidermal cells. GTs are able to secrete and store large quantities of specialized secondary metabolites that may play important roles to protect plants from various environmental stresses or are economically import for human use. While extensive work has been done in understanding of the molecular mechanisms of trichome development the model plant Arabidopsis thaliana that has unicellular, non-glandular trichomes (NGTs), little is known on the mechanisms of GT development or regulation of secondary metabolites in plants with multicellular GTs. Major findings In this manuscript, we report identification and functional characterization of genes associated with GT development and secondary metabolism in GTs on developing cucumber ovaries. First an efficient method was developed to separate and isolate cucumber GTs and NGTs. Transcriptomic and metabolomic analyses identified genes and secondary metabolites in the flavonoid biosynthesis pathway that were highly enriched in cucumber GTs. We identified 67 GT development–related genes, and seven of them were characterized for their regulatory functions with multiple approaches in regulating GT development and flavonoid biosynthesis in cucumber. Who cares This work provides novel insights into the development of secondary metabolite biosynthesis in multiple-cellular glandular trichomes of cucumber, which may be of interest for researchers to understand the molecular mechanisms of trichome organogenesis.

Technical Abstract: The glandular trichomes (GTs) are outgrowths of plant epidermal cells that are characterized with secretion and storage of specialized secondary metabolites, which are of protective roles to biotic and abiotic stresses for plants or economic importance for human use. While extensive work has been done in understanding of the molecular mechanisms of trichome organogenesis in Arabidopsis thaliana that has only unicellular, non-glandular trichomes (NGTs), little is known on the mechanisms of GT development or regulation of secondary metabolites in plants with multicellular GTs. Here we report identification and functional characterization of genes associated with GT organogenesis and secondary metabolism in GTs of cucumber (Cucumis sativus). We developed a method for effective separation and isolation of cucumber GTs and NGTs. Transcriptomic and metabolomic analyses identified genes and secondary metabolites in the flavonoid biosynthesis pathway that were highly enriched in cucumber GTs. We identified 67 GT development–related genes, the functions of 7 of which were validated by virus-induced gene silencing. The roles of the cucumber ECERIFERUM1 (CsCER1) gene in GT organogenesis was further validated with overexpressing and RNAi transgenic approaches. We further show that the transcription factor TINY BRANCHED HAIR (TBH) serves as a central regulator of flavonoid biosynthesis in cucumber glandular trichome. Work from this study provides novel insights into the development of secondary metabolite biosynthesis in multiple-cellular glandular trichomes.