Interference between ER stress-related bZIP-type and jasmonate-inducible bHLH-type transcription factors in the regulation of triterpene saponin biosynthesis in Medicago truncatula

Abstract

Triterpene saponins (TS) are a structurally diverse group of metabolites that are widely distributed in plants. They primarily serve as defense compounds and their production is often triggered by biotic stresses through signaling cascades that are modulated by phytohormones such as the jasmonates (JA). Two JA-modulated basic helix-loop-helix (bHLH) transcription factors (TFs), triterpene saponin biosynthesis activating regulator 1 (TSAR1) and TSAR2, have previously been identified as direct activators of TS biosynthesis in the model legume Medicago truncatula. Here, we report on the involvement of the core endoplasmic reticulum (ER) stress-related basic leucine zipper (bZIP) TFs bZIP17 and bZIP60 in the regulation of TS biosynthesis. Expression and processing of M. truncatula bZIP17 and bZIP60 proteins were altered in roots with perturbed TS biosynthesis or treated with JA. Accordingly, such roots displayed an altered ER network structure. M. truncatula bZIP17 and bZIP60 proteins were shown to localize in the nucleus and appeared to be capable of interfering with the TSAR-mediated transactivation of TS biosynthesis genes. Furthermore, interference between ER stress-related bZIP and JA-modulated bHLH TFs in the regulation of JA-dependent terpene biosynthetic pathways may be widespread in the plant kingdom, as we demonstrate that it also occurs in the regulation of monoterpene indole alkaloid biosynthesis in the medicinal plant Catharanthus roseus.

The saponin bomb: a nucleolar‐localized β‐glucosidase hydrolyzes triterpene saponins in Medicago truncatula

“…For this analysis, a set of characterized M. truncatula TS biosynthesis genes (Table S2) was entered as target pathway and two sets of M. truncatula expression profiles were used. The first dataset consisted of gene expression values generated by RNA‐Seq of M. truncatula hairy roots overexpressing TSAR1 ( TSAR1 OE ) or TSAR2 ( TSAR2 OE ; Mertens et al ., 2016), which was expanded with expression data from M. truncatula hairy roots treated or not with 100 μM of MeJA for 2 or 24 h (Ribeiro et al ., 2022). The second dataset contained all publicly available expression profiles of the M. truncatula Gene Expression Atlas (He et al ., 2009).…”

“…RNA‐Seq analysis of control, TSAR1 OE , and TSAR2 OE lines was reported before (Mertens et al ., 2016). RNA‐Seq analysis of control hairy root lines treated with 100 μM of methyl jasmonate (MeJA) or an equivalent amount of ethanol for 2 or 24 h was carried out as previously described (Mertens et al ., 2016; Ribeiro et al ., 2022). The reported RNA‐Seq read data are available in the ArrayExpress database (http://www.ebi.ac.uk/arrayexpress) under accession nos.…”

The Transcriptional Regulatory Mechanisms Exploration of Jujube Biological Traits through Multi-omics Analysis

“…In jujube, Wen et al (2022) [56] conducted a comprehensive study using metabolite profiling and transcriptomic data analysis on cultivated jujube, which revealed that terpenoids were mainly concentrated in ZjSQS1 (evm.model. Many transcription factors (TFs) have been confirmed roles in regulating terpenes accumulation by affecting the expression of genes related to terpene synthesis in other plants , such as WRKY [59,60], bHLH [61][62][63], AP2/ERF [64][65][66], MYB [67][68][69][70][71], and bZIP [72][73][74], among others. Notable examples of these regulators include PnbHLH1, which controls the biosynthesis of triterpene saponins in Panax notoginseng [61,75], ERF189, an ethylene response factor implicated in the biosynthesis of steroidal glycoalkaloids in potatoes and tomatoes [75,76], and SmERF1L1, which regulates the biosynthesis of tanshinones in Salvia miltiorrhiza Bunge [77].…”

Engineering the plant metabolic system by exploiting metabolic regulation

“…The elucidation of these inducible regulatory sequences coupled with the expression of specific TFs has provided interesting approaches to increase the production of plant metabolites (Colinas & Goossens, 2018; Memelink et al, 2001; Naoumkina et al, 2008). For instance, many jasmonate‐inducible TFs, such as MYC2, have been identified to regulate the production of interesting pharmacological compounds, including glucosinolates (Schweizer et al, 2013), terpenes (Ribeiro et al, 2022), and alkaloids (Sui et al., 2018). Remarkably, the production of artemisinin, a sesquiterpene used for the treatment of malaria, can be stimulated in the glandular trichomes of Artemisia annua by jasmonate (Maes et al, 2011), through a signaling cascade that involves many different TFs (Hassani et al, 2020).…”