SUMMARY
Flavan‐3‐ols are abundant in the tea plant (Camellia sinensis) and confer tea with flavor and health benefits. We recently found that alternative splicing of genes is likely involved in the ...regulation of flavan‐3‐ol biosynthesis; however, the underlying regulatory mechanisms remain unknown. Here, we integrated metabolomics and transcriptomics to construct metabolite–gene networks in tea leaves, collected over five different months and from five spatial positions, and found positive correlations between endogenous jasmonic acid (JA), flavan‐3‐ols, and numerous transcripts. Transcriptome mining further identified CsJAZ1, which is negatively associated with flavan‐3‐ols formation and has three CsJAZ1 transcripts, one full‐length (CsJAZ1‐1), and two splice variants (CsJAZ1‐2 and ‐3) that lacked 3′ coding sequences, with CsJAZ1‐3 also lacking the coding region for the Jas domain. Confocal microscopy showed that CsJAZ1‐1 was localized to the nucleus, while CsJAZ1‐2 and CsJAZ1‐3 were present in both the nucleus and the cytosol. In the absence of JA, CsJAZ1‐1 was bound to CsMYC2, a positive regulator of flavan‐3‐ol biosynthesis; CsJAZ1‐2 functioned as an alternative enhancer of CsJAZ1‐1 and an antagonist of CsJAZ1‐1 in binding to CsMYC2; and CsJAZ1‐3 did not interact with CsMYC2. In the presence of JA, CsJAZ1‐3 interacted with CsJAZ1‐1 and CsJAZ1‐2 to form heterodimers that stabilized the CsJAZ1‐1–CsMYC2 and CsJAZ1‐2–CsMYC2 complexes, thereby repressing the transcription of four genes that act late in the flavan‐3‐ol biosynthetic pathway. These data indicate that the alternative splicing variants of CsJAZ1 coordinately regulate flavan‐3‐ol biosynthesis in the tea plant and improve our understanding of JA‐mediated flavan‐3‐ol biosynthesis.
Significance Statement
Alternative splicing is an important post‐transcriptional mechanism that plays vital roles in plant development and metabolism. This study identified CsJAZ1 and its alternative splicing variants (CsJAZ1‐2 and CsJAZ1‐3) that formed homo‐ and heterodimers, bound to CsMYC2, and coordinately repressed the jasmonic acid‐mediated flavan‐3‐ol biosynthesis. These findings provide evidence that the coordination of JAZ splice variants play important roles in regulating plant secondary metabolism.
SmJAZ8 regulates the biosynthesis of salvianolic acids and tanshinones simultaneously by repressing the transcription factors and biosynthetic pathway genes in Salvia miltiorrhiza hairy roots.
...Abstract
Jasmonates (JAs) are important plant hormones that regulate a variety of plant development and defense processes, including biosynthesis of secondary metabolites. The JASMONATE ZIM DOMAIN (JAZ) proteins act as negative regulators in the JA signaling pathways of plants. We first verified that methyl jasmonate (MeJA) enhanced the accumulation of both salvianolic acids and tanshinones in Salvia miltiorrhiza (Danshen) hairy roots by inducing the expression of their biosynthetic pathway genes. Nine JAZ genes were cloned from Danshen and their expression levels in hairy roots were all increased by treatment with MeJA. When analyzed in detail, however, SmJAZ8 showed the strongest expression in the induced hairy roots. Overexpression or RNAi of SmJAZ8 deregulated or up-regulated the yields of salvianolic acids and tanshinones in the MeJA-induced transgenic hairy roots, respectively, and transcription factors and biosynthetic pathway genes showed an expression pattern that mirrored the production of the compounds. Genetic transformation of SmJAZ8 altered the expression of other SmJAZ genes, suggesting evidence of crosstalk occurring in JAZ-regulated secondary metabolism. Furthermore, the transcriptome analysis revealed a primary-secondary metabolism balance regulated by SmJAZ8. Altogether, we propose a novel role for SmJAZ8 as a negative feedback loop controller in the JA-induced biosynthesis of salvianolic acids and tanshinones.
Jasmonates (JAs) and abscisic acid (ABA) are phytohormones known play important roles in plant response and adaptation to various abiotic stresses including salinity, drought, wounding, and cold. JAZ ...(JASMONATE ZIM-domain) proteins have been reported to play negative roles in JA signaling. However, direct evidence is still lacking that JAZ proteins regulate drought resistance. In this study, OsJAZ1 was investigated for its role in drought resistance in rice. Expression of
was strongly responsive to JA treatment, and it was slightly responsive to ABA, salicylic acid, and abiotic stresses including drought, salinity, and cold. The
-overexpression rice plants were more sensitive to drought stress treatment than the wild-type (WT) rice Zhonghua 11 (ZH11) at both the seedling and reproductive stages, while the
T-DNA insertion mutant plants showed increased drought tolerance compared to the WT plants. The
-overexpression plants were hyposensitive to MeJA and ABA, whereas the
mutant plants were hypersensitive to MeJA and ABA. In addition, there were significant differences in shoot and root length between the OsJAZ1 transgenic and WT plants under the MeJA and ABA treatments. A subcellular localization assay indicated that OsJAZ1 was localized in both the nucleus and cytoplasm. Transcriptome profiling analysis by RNA-seq revealed that the expression levels of many genes in the ABA and JA signaling pathways exhibited significant differences between the
-overexpression plants and WT ZH11 under drought stress treatment. Quantitative real-time PCR confirmed the expression profiles of some of the differentially expressed genes, including
, and
. These results together suggest that OsJAZ1 plays a role in regulating the drought resistance of rice partially via the ABA and JA pathways.
The jasmonic acid (JA) signaling pathway plays an important role in promoting the biosynthesis of tanshinones. While individual transcription factors have been extensively studied in the context of ...tanshinones biosynthesis regulation, the influence of methyl jasmonate (MeJA)-induced transcriptional complexes remains unexplored. This study elucidates the positive regulatory role of the basic helix-loop-helix protein SmMYC2 in tanshinones biosynthesis in Salvia miltiorrhiza. SmMYC2 not only binds to SmGGPPS1 promoters, activating their transcription, but also interacts with SmMYB36. This interaction enhances the transcriptional activity of SmMYC2 on SmGGPPS1, thereby promoting tanshinones biosynthesis. Furthermore, we identified three JA signaling repressors, SmJAZ3, SmJAZ4, and SmJAZ8, which interact with SmMYC2. These repressors hindered the transcriptional activity of SmMYC2 on SmGGPPS1 and disrupted the interaction between SmMYC2 and SmMYB36. MeJA treatment triggered the degradation of SmJAZ3 and SmJAZ4, allowing the SmMYC2-SmMYB36 complex to subsequently activate the expression of SmGGPPS1, whereas SmJAZ8 inhibited MeJA-mediated degradation due to the absence of the LPIARR motif. These results demonstrate that the SmJAZ-SmMYC2-SmMYB36 module dynamically regulates the JA-mediated accumulation of tanshinones. Our results reveal a new regulatory network for the biosynthesis of tanshinones. This study provides valuable insight for future research on MeJA-mediated modulation of tanshinones biosynthesis.
The lipid-derived phytohormone jasmonate (JA) regulates plant growth, development, secondary metabolism, defense against insect attack and pathogen infection, and tolerance to abiotic stresses such ...as wounding, UV light, salt, and drought. JA was first identified in 1962, and since the 1980s many studies have analyzed the physiological functions, biosynthesis, distribution, metabolism, perception, signaling, and crosstalk of JA, greatly expanding our knowledge of the hormone’s action. In response to fluctuating environmental cues and transient endogenous signals, the occurrence of multilayered organization of biosynthesis and inactivation of JA, and activation and repression of the COI1–JAZ-based perception and signaling contributes to the fine-tuning of JA responses. This review describes the JA biosynthetic enzymes in terms of gene families, enzymatic activity, location and regulation, substrate specificity and products, the metabolic pathways in converting JA to activate or inactivate compounds, JA signaling in perception, and the co-existence of signaling activators and repressors.
Plant JASMONATE ZIM-DOMAIN (JAZ) genes play crucial roles in regulating the biosynthesis of specialized metabolites and stressful responses. However, understanding of JAZs controlling these ...biological processes lags due to numerous JAZ copies. Here, we found that two leaf-specific CwJAZ4/9 genes from Curcuma wenyujin are strongly induced by methyl-jasmonate (MeJA) and negatively correlated with terpenoid biosynthesis. Yeast two-hybrid, luciferase complementation imaging and in vitro pull-down assays confirmed that CwJAZ4/9 proteins interact with CwMYC2 to form the CwJAZ4/9-CwMYC2 regulatory cascade. Furthermore, transgenic hairy roots showed that CwJAZ4/9 acts as repressors of MeJA-induced terpenoid biosynthesis by inhibiting the terpenoid pathway and jasmonate response, thus reducing terpenoid accumulation. In addition, we revealed that CwJAZ4/9 decreases salt sensitivity and sustains the growth of hairy roots under salt stress by suppressing the salt-mediated jasmonate responses. Transcriptome analysis for MeJA-mediated transgenic hairy root lines further confirmed that CwJAZ4/9 negatively regulates the terpenoid pathway genes and massively alters the expression of genes related to salt stress signaling and responses, and crosstalks of multiple phytohormones. Altogether, our results establish a genetic framework to understand how CwJAZ4/9 inhibits terpenoid biosynthesis and confers salt tolerance, which provides a potential strategy for producing high-value pharmaceutical terpenoids and improving resistant C. wenyujin varieties by a genetic approach.
The plant hormone jasmonate coordinates immune and growth responses to increase plant survival in unpredictable environments. The core jasmonate signaling pathway comprises several functional ...modules, including a repertoire of COI1-JAZ (CORONATINE INSENSITIVE1-JASMONATE-ZIM DOMAIN) coreceptors that couple jasmonoyl-l-isoleucine perception to the degradation of JAZ repressors, JAZ-interacting transcription factors that execute physiological responses, and multiple negative feedback loops to ensure timely termination of these responses. Here, we review the jasmonate signaling pathway with an emphasis on understanding how transcriptional responses are specific, tunable, and evolvable. We explore emerging evidence that JAZ proteins integrate multiple informational cues and mediate crosstalk by propagating changes in protein-protein interaction networks. We also discuss recent insights into the evolution of jasmonate signaling and highlight how plant-associated organisms manipulate the pathway to subvert host immunity. Finally, we consider how this mechanistic foundation can accelerate the rational design of jasmonate signaling for improving crop resilience and harnessing the wellspring of specialized plant metabolites.
Phytohormones, including jasmonates (JAs), gibberellin, ethylene, abscisic acid, and auxin, integrate endogenous developmental cues with environmental signals to regulate plant growth, development, ...and defense. JAs are well-recognized lipid-derived stress hormones that regulate plant adaptations to biotic stresses, including herbivore attack and pathogen infection, as well as abiotic stresses, including wounding, ozone, and ultraviolet radiation. An increasing number of studies have shown that JAs also have functions in a remarkable number of plant developmental events, including primary root growth, reproductive development, and leaf senescence. Since the 1980s, details of the JA biosynthesis pathway, signaling pathway, and crosstalk during plant growth and development have been elucidated. Here, we summarize recent advances and give an updated overview of JA action and crosstalk in plant growth and development.
Plants as immovable organisms sense the stressors in their environment and respond to them by means of dedicated stress response pathways. In response to stress, jasmonates (jasmonic acid, its ...precursors and derivatives), a class of polyunsaturated fatty acid-derived phytohormones, play crucial roles in several biotic and abiotic stresses. As the major immunity hormone, jasmonates participate in numerous signal transduction pathways, including those of gene networks, regulatory proteins, signaling intermediates, and proteins, enzymes, and molecules that act to protect cells from the toxic effects of abiotic stresses. As cellular hubs for integrating informational cues from the environment, jasmonates play significant roles in alleviating salt stress, drought stress, heavy metal toxicity, micronutrient toxicity, freezing stress, ozone stress, CO
stress, and light stress. Besides these, jasmonates are involved in several developmental and physiological processes throughout the plant life. In this review, we discuss the biosynthesis and signal transduction pathways of the JAs and the roles of these molecules in the plant responses to abiotic stresses.
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