GATA and Phytochrome Interacting Factor Transcription Factors Regulate Light-Induced Vindoline Biosynthesis in Catharanthus roseus

Abstract

Catharanthus roseus is the exclusive source of an array of terpenoid indole alkaloids including the anticancer drugs vincristine and vinblastine, derived from the coupling of catharanthine and vindoline. Leaf-synthesized vindoline is regulated by light. A sevenstep enzymatic process is involved in the sequential conversion of tabersonine to vindoline; however, the regulatory mechanism controlling the expression of genes encoding these enzymes has not been elucidated. Here, we identified CrGATA1, an Leu-Leu-Met domain GATA transcription factor that regulates light-induced vindoline biosynthesis in C. roseus seedlings. Expression of CrGATA1 and the vindoline pathway genes T16H2, T3O, T3R, D4H, and DAT was significantly induced by light. In addition, CrGATA1 activated the promoters of five light-responsive vindoline pathway genes in plant cells. Two GATC motifs in the D4H promoter were critical for CrGATA1-mediated transactivation. Transient overexpression of CrGATA1 in C. roseus seedlings resulted in up-regulation of vindoline pathway genes and increased vindoline accumulation. Conversely, virus-induced gene silencing of CrGATA1 in young C. roseus leaves significantly repressed key vindoline pathway genes and reduced vindoline accumulation. Furthermore, we showed that a C. roseus Phytochrome Interacting Factor, CrPIF1, is a repressor of CrGATA1 and vindoline biosynthesis. Transient overexpression or virus-induced gene silencing of CrPIF1 in C. roseus seedlings altered CrGATA1 and vindoline pathway gene expression in the dark. CrPIF1 repressed CrGATA1 and DAT promoter activity by binding to G/E-box/PBE elements. Our findings reveal a regulatory module involving Phytochrome Interacting Factor-GATA that governs light-mediated biosynthesis of specialized metabolites.

The methyl jasmonate-responsive transcription factor SmMYB1 promotes phenolic acid biosynthesis in Salvia miltiorrhiza

“…Metabolic engineering is an efficient approach for improving the production of active ingredients in medicinal plants. This process requires a deep understanding of the biosynthesis pathways of active ingredients, including both biosynthesis-related and regulatory genes 22 – 25 . Although great progress has been made in the isolation and functional identification of biosynthesis-related genes involved in medicinal compounds, little is known about the transcriptional regulation of phenolic acid biosynthesis in S. miltiorrhiza .…”

The regulation of ZCT1, a transcriptional repressor of monoterpenoid indole alkaloid biosynthetic genes in Catharanthus roseus

“…A crucial regulatory mechanism in specialized metabolism is the transcriptional regulation of biosynthetic genes. Several transcription factors (TFs) involved in MIA regulation have been identified in Catharanthus , including the octadecanoid‐responsive Catharanthus AP2‐domain (ORCA) TF family and the zinc finger Catharanthus (ZCT) TF family described below (Menke et al, ; Van der Fits & Memelink, ; Van der Fits, Zhang, Menke, Deneka, & Memelink, ; Sibéril et al, ; Chatel et al, ; Pauw et al, ; Vom Endt, Soares e Silva, Kijne, Pasquali, & Memelink, ; Zhang et al, ; Suttipanta et al, ; Van Moerkercke et al, , ; Paul et al, ; Liu et al, ; Liu, Patra, Pattanaik, Wang, & Yuan, ; Patra, Pattanaik, Schluttenhofer, & Yuan, ; Pan et al, ). Three characterized members ( ZCT1 , ZCT2, and ZCT3 ) of the Cys 2 /His 2 ‐type (C 2 H 2 ) zinc finger family are expressed by the stress‐induced phytohormone jasmonate (Goklany, Rizvi, Loring, Cram, & Lee‐Parsons, ; Pauw et al, ).…”

CrERF5, an AP2/ERF Transcription Factor, Positively Regulates the Biosynthesis of Bisindole Alkaloids and Their Precursors in Catharanthus roseus

“…But both overexpressing and silencing CrERF5 had limited effect on vindoline accumulation, indicating that CrERF5 might not control vindoline pathway. It has been reported that light-induced vindoline biosynthesis is regulated by GATA and PIF transcription factors in C. roseus (Liu et al, 2019). But the genes in the steps from strictosidine to vinblastine, like STR1, Redox1, SAT , and CrPRX1 , were upregulated in CrERF5-overexpressing petals and downregulated in CrERF5-silencing plants, leading to a significant increase of the catharanthine, anhydrovinblastine and vinblastine accumulation.…”