Dual Mechanisms of Coniferyl Alcohol in Phenylpropanoid Pathway Regulation

Guan, Meng-Ling; Li, Changxuan; Shan, Xiaotong; Chen, Fang; Wang, Shufang; Dixon, Richard A.; Zhao, Qiao

doi:10.3389/fpls.2022.896540

Cited by 10 publications

(6 citation statements)

References 39 publications

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“…PAL protein stability in Arabidopsis can be modulated by the KFB (Kelch domain–containing F‐box) proteins (Zhang et al, 2013b). In a previous study, we generated both the pal2 pal3 pal4 triple mutant and the kfb01 kfb20 kfb39 kfb50 quadruple mutant, with much lower or higher PAL abundance, respectively (Guan et al, 2022). Here, we also generated individual PAL overexpression (OE) lines in the kfb quadruple mutant to investigate the contribution of each PAL to SA biosynthesis (Figure S5A).…”

Section: Resultsmentioning

confidence: 99%

Salicylic acid biosynthesis is not from phenylalanine in Arabidopsis

Wu¹,

Zhu

Zhao

2023

JIPB

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The phytohormone salicylic acid (SA) regulates biotic and abiotic stress responses in plants. Two distinct biosynthetic pathways for SA have been well documented in plants: the isochorismate (IC) pathway in the chloroplast and the phenylalanine ammonia-lyase (PAL) pathway in the cytosol. However, there has been no solid evidence that the PAL pathway contributes to SA biosynthesis. Here, we report that feeding Arabidopsis thaliana with Ring-13 C-labeled phenylalanine ( 13 C 6 -Phe) resulted in incorporation of the 13 C label not into SA, but into its isomer 4-hydroxybenzoic acid (4-HBA) instead. We obtained similar results when feeding 13 C 6 -Phe to the SA-deficient ics1 ics2 mutant and the SA-hyperaccumulating mutant s3h s5h. Notably, we detected 13 C 6 -SA when 13 C 6 -benzoic acid (BA) was provided, suggesting that SA can be synthesized from BA. Furthermore, despite the substantial accumulation of SA upon pathogen infection, we did not observe incorporation of 13 C label from Phe into SA. We also did not detect 13 C 6 -SA in PAL-overexpressing lines in the kfb01 kfb02 kfb39 kfb50 background after being fed 13 C 6 -Phe, although endogenous PAL levels were dramatically increased. Based on these combined results, we propose that SA biosynthesis is not from Phe in Arabidopsis. These results have important implications for our understanding of the SA biosynthetic pathway in land plants.

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Section: Resultsmentioning

confidence: 99%

Salicylic acid biosynthesis is not from phenylalanine in Arabidopsis

Wu¹,

Zhu

Zhao

2023

JIPB

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“…S5 ) plants. Exogenous CA was recently reported to lead to the upregulation of MYB4 , ( 42 ) which would be expected to repress expression of our C4H promoter-driven F5H overexpression construct ( 73 ). Instead, under our experimental conditions, transcript levels of the endogenous C4H were unaffected by CA treatment in cadd C4H:F5H seedlings, and the expression of the F5H transgene was only modestly affected and remained 12-fold higher than in wild type ( SI Appendix , Table S2 ).…”

Section: Discussionmentioning

confidence: 95%

“…CA treatment has been reported to lead to the upregulation of the C4H transcriptional repressor MYB4 ( 42 ), which led us to test whether the expression of the C4H:F5H transgene was affected by CA treatment. Although there was a decrease in F5H expression in cadd C4H:F5H seedlings grown in the presence of CA, endogenous C4H mRNA levels were unaffected, and F5H transcript levels were only modestly affected, still being 12 times higher than in wild type ( SI Appendix , Table S2 ).…”

Section: Resultsmentioning

confidence: 99%

Pinoresinol rescues developmental phenotypes of Arabidopsis phenylpropanoid mutants overexpressing FERULATE 5-HYDROXYLASE

Muro-Villanueva,

Pysh,

Kim

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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Most phenylpropanoid pathway flux is directed toward the production of monolignols, but this pathway also generates multiple bioactive metabolites. The monolignols coniferyl and sinapyl alcohol polymerize to form guaiacyl (G) and syringyl (S) units in lignin, components that are characteristic of plant secondary cell walls. Lignin negatively impacts the saccharification potential of lignocellulosic biomass. Although manipulation of its content and composition through genetic engineering has reduced biomass recalcitrance, in some cases, these genetic manipulations lead to impaired growth. The reduced-growth phenotype is often attributed to poor water transport due to xylem collapse in low-lignin mutants, but alternative models suggest that it could be caused by the hyper- or hypoaccumulation of phenylpropanoid intermediates. In Arabidopsis thaliana , overexpression of FERULATE 5-HYDROXYLASE ( F5H ) shifts the normal G/S lignin ratio to nearly pure S lignin and does not result in substantial changes to plant growth. In contrast, when we overexpressed F5H in the low-lignin mutants cinnamyl dehydrogenase c and d ( cadc cadd ), cinnamoyl-CoA reductase 1 , and reduced epidermal fluorescence 3 , plant growth was severely compromised. In addition, cadc cadd plants overexpressing F5H exhibited defects in lateral root development. Exogenous coniferyl alcohol (CA) and its dimeric coupling product, pinoresinol, rescue these phenotypes. These data suggest that mutations in the phenylpropanoid pathway limit the biosynthesis of pinoresinol, and this effect is exacerbated by overexpression of F5H , which further draws down cellular pools of its precursor, CA. Overall, these genetic manipulations appear to restrict the synthesis of pinoresinol or a downstream metabolite that is necessary for plant growth.

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“…In our study, AA treatment of tomato roots induced accumulation of a phenylcoumaran intermediate in lignin biosynthesis, while ANE treatment induced accumulation of coniferyl alcohol, an important monomer unit of lignin. Interestingly, coniferyl alcohol has recently been shown to act in a signaling capacity in a regulatory feedback mechanism to intricately control lignin biosynthesis, an irreversible process that is energetically costly (Guan et al 2022). The findings of our study coincide with the well-characterized role of lignin and its intermediates in plant defense.…”

Section: Discussionmentioning

confidence: 99%

The oomycete MAMP, arachidonic acid, and anAscophyllum nodosum-derived plant biostimulant induce defense metabolome remodeling in tomato

Lewis

Zwan

Richards

et al. 2022

Preprint

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Arachidonic acid (AA) is an oomycete derived MAMP capable of eliciting robust defense responses and inducing resistance in plants. Similarly, extract from the brown seaweed Ascophylum nodosum, a plant biostimulant that contains AA, can also prime plants for defense against pathogen challenge. A previous parallel study comparing the transcriptomes of AA and ANE root-treated tomato demonstrated significant overlap in transcriptional profiles, a shared induced resistance phenotype, and changes in accumulation of various defense-related phytohormones. In this work, untargeted metabolomic analysis via LCMS was conducted to investigate the local and systemic metabolome-wide remodeling events elicited by AA- and ANE-root treatment in tomato. Our study demonstrated AA and ANE's capacity to locally and systemically alter the metabolome of tomato with enrichment of chemical classes and accumulation of metabolites associated with defense-related secondary metabolism. AA and ANE root-treated plants showed enrichment of fatty acyl-glycosides and strong modulation of hydroxycinnamic acids and derivatives. Identification of specific metabolites whose accumulation was affected by AA and ANE treatment revealed shared metabolic changes related to ligno-suberin biosynthesis and the synthesis of phenolic compounds. However, AA- and ANE-induced metabolomes are distinct, and do not share the extensive overlap in their induced transcriptomes that we observed in a previous study. This study highlights the extensive local and systemic metabolic changes in tomato induced by treatment with a fatty acid MAMP and a seaweed-derived plant biostimulant with implications for induced resistance and crop improvement.

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Dual Mechanisms of Coniferyl Alcohol in Phenylpropanoid Pathway Regulation

Cited by 10 publications

References 39 publications

Salicylic acid biosynthesis is not from phenylalanine in Arabidopsis

Salicylic acid biosynthesis is not from phenylalanine in Arabidopsis

Pinoresinol rescues developmental phenotypes of Arabidopsis phenylpropanoid mutants overexpressing FERULATE 5-HYDROXYLASE

The oomycete MAMP, arachidonic acid, and anAscophyllum nodosum-derived plant biostimulant induce defense metabolome remodeling in tomato

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