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Functional analysis of metabolic channeling and regulation in lignin biosynthesis: a computational approach.

ABSTRACT: Lignin is a polymer in secondary cell walls of plants that is known to have negative impacts on forage digestibility, pulping efficiency, and sugar release from cellulosic biomass. While targeted modifications of different lignin biosynthetic enzymes have permitted the generation of transgenic plants with desirable traits, such as improved digestibility or reduced recalcitrance to saccharification, some of the engineered plants exhibit monomer compositions that are clearly at odds with the expected outcomes when the biosynthetic pathway is perturbed. In Medicago, such discrepancies were partly reconciled by the recent finding that certain biosynthetic enzymes may be spatially organized into two independent channels for the synthesis of guaiacyl (G) and syringyl (S) lignin monomers. Nevertheless, the mechanistic details, as well as the biological function of these interactions, remain unclear. To decipher the working principles of this and similar control mechanisms, we propose and employ here a novel computational approach that permits an expedient and exhaustive assessment of hundreds of minimal designs that could arise in vivo. Interestingly, this comparative analysis not only helps distinguish two most parsimonious mechanisms of crosstalk between the two channels by formulating a targeted and readily testable hypothesis, but also suggests that the G lignin-specific channel is more important for proper functioning than the S lignin-specific channel. While the proposed strategy of analysis in this article is tightly focused on lignin synthesis, it is likely to be of similar utility in extracting unbiased information in a variety of situations, where the spatial organization of molecular components is critical for coordinating the flow of cellular information, and where initially various control designs seem equally valid.

SUBMITTER: Lee Y

PROVIDER: S-EPMC3493464 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Functional analysis of metabolic channeling and regulation in lignin biosynthesis: a computational approach.

Lee Yun Y Escamilla-Treviño Luis L Dixon Richard A RA Voit Eberhard O EO

PLoS computational biology 20121108 11

Lignin is a polymer in secondary cell walls of plants that is known to have negative impacts on forage digestibility, pulping efficiency, and sugar release from cellulosic biomass. While targeted modifications of different lignin biosynthetic enzymes have permitted the generation of transgenic plants with desirable traits, such as improved digestibility or reduced recalcitrance to saccharification, some of the engineered plants exhibit monomer compositions that are clearly at odds with the expec ...[more]

PMID: 23144605

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Project description:Asparagus belongs to the Liliaceae family and has important economic and pharmacological value. Lignin plays a crucial role in cell wall structural integrity, stem strength, water transport, mechanical support and plant resistance to pathogens. In this study, various biological methods were used to study the mechanism of shading on the asparagus lignin accumulation pathway. The physiological results showed that shading significantly reduced stem diameter and cell wall lignin content. Microstructure observation showed that shading reduced the number of vascular bundles and xylem area, resulting in decreased lignin content, and thus reducing the lignification of asparagus. Cinnamic acid, caffeic acid, ferulic acid and sinapyl alcohol are crucial intermediate metabolites in the process of lignin synthesis. Metabolomic profiling showed that shading significantly reduced the contents of cinnamic acid, caffeic acid, ferulic acid and sinapyl alcohol. Transcriptome profiling identified 37 differentially expressed genes related to lignin, including PAL, C4H, 4CL, CAD, CCR, POD, CCoAOMT, and F5H related enzyme activity regulation genes. The expression levels of POD, CCoAOMT, and CCR genes were significantly decreased under shading treatment, while the expression levels of CAD and F5H genes exhibited no significant difference with increased shading. The downregulation of POD, CCoAOMT genes and the decrease in CCR gene expression levels inhibited the activities of the corresponding enzymes under shading treatment, resulting in decreased downstream content of caffeic acid, ferulic acid, sinaperol, chlorogenic acid and coniferin. A significant decrease in upstream cinnamic acid content was observed with shading, which also led to decreased downstream metabolites and reduced asparagus lignin content. In this study, transcriptomic and metabolomic analysis revealed the key regulatory genes and metabolites of asparagus lignin under shading treatment. This study provides a reference for further understanding the mechanism of lignin biosynthesis and the interaction of related genes.

Project description:Lignin is a complex polymer in plant cell walls whose proportion is second only to that of cellulose and plays an important role in the mechanical properties of wood and stress resistance of plants. Here, we induced tension wood (TW) formation in Catalpa bungei by artificial bending and analyzed the lignin metabolism of the TW. LC-MS analysis showed that a significantly higher content of coniferyl aldehyde was observed in the TW cell wall than in the opposite wood (OW) and normal wood (NW) cell walls. TW had significantly lower contents of coniferyl alcohol than OW and NW. Raman spectroscopy results indicated that TW had lower total lignin than OW and NW. The transcription and translation levels of most of the differentially expressed genes (DEGs) involved in lignin monomer biosynthesis indicated upregulation in TW/OW and TW/NW. We found no significant difference in the transcription levels of three collision gases (CADs) between TW and OW or between NW, but their translation levels were significantly downregulated in TW, suggesting post-transcriptional control for CAD. We predicted and analyzed transcription factors that could target DEGs involved in lignin monomer biosynthesis in TW. Based on the analysis of the relationships of targeting and coexpression, we found that NAC (evm.model.group1.695) could potentially target 4CLs and CCoAOMT, that HD-Zip (evm.model.group7.1157) had potential targeting relationships with CCoAOMT, F5H, and CCR, and that their expression levels were significantly positive. It is speculated that the upregulation of NAC and HD-ZIP transcription factors activates the expression of downstream target genes, which leads to a significant increase in coniferyl aldehyde in TW. However, the decrease in total lignin in TW may be caused by the significant downregulation of CAD translation and the significant decrease in precursors (coniferyl alcohol). Whether the expression of CAD genes is regulated by post-transcriptional control and affects TW lignin metabolism needs further study.

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Functional analysis of metabolic channeling and regulation in lignin biosynthesis: a computational approach.

Publications

Functional analysis of metabolic channeling and regulation in lignin biosynthesis: a computational approach.

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