Functional Analysis of Metabolic Channeling and Regulation in Lignin Biosynthesis: A Computational Approach

• Type of Material: Article
• Authors: Yun Lee, Georgia Institute of Technology; Luis Escamilla-Trevino, BioEnergy Sciences Center (BESC); Richard A. Dixon, BioEnergy Sciences Center (BESC); Eberhard Voit, Emory University
• Language: English
• Date: 2012-11-01
• Publisher: Public Library of Science
• Publication Version: Final Published Version
• Copyright Statement: © 2012 Lee et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1371/journal.pcbi.1002769
• Title of Journal or Parent Work: PLoS Computational Biology
• ISSN: 1553-734X
• Volume: 8
• Issue: 11
• Start Page: e1002769
• End Page: e1002769
• Grant/Funding Information: This work was funded by DoE-BESC.
• Keywords: PLANTS; PATHWAYS; Mathematical & Computational Biology; MATHEMATICAL & COMPUTATIONAL BIOLOGY; MONOLIGNOLS; ACID; Science & Technology; CHEMICAL SYNTHESES; BIOCHEMICAL RESEARCH METHODS; MEDICAGO-SATIVA L.; Life Sciences & Biomedicine; ARABIDOPSIS; Biochemistry & Molecular Biology; ENZYMES; O-METHYLTRANSFERASE; Biochemical Research Methods; SYRINGYL LIGNIN
• Research Categories: Engineering, Biomedical

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.