Suppression of Chorismate Mutase 1 in Hybrid Poplar to Investigate Potential Redundancy in the Supply of Lignin Precursors

Yaseen Mottiar; Timothy J Tschaplinski; John Ralph; Shawn D Mansfield

doi:10.1002/pld3.70053

Suppression of Chorismate Mutase 1 in Hybrid Poplar to Investigate Potential Redundancy in the Supply of Lignin Precursors

Yaseen Mottiar
, Timothy J Tschaplinski
, John Ralph
, Shawn D Mansfield

Biosciences Division

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Chorismate is an important branchpoint metabolite in the biosynthesis of lignin and a wide array of metabolites in plants. Chorismate mutase (CM), the enzyme responsible for transforming chorismate into prephenate, is a key regulator of metabolic flux towards the synthesis of aromatic amino acids and onwards to lignin. We examined three CM genes in hybrid poplar (Populus alba × grandidentata; P39, abbreviated as Pa×g) and used RNA interference (RNAi) to suppress the expression of Pa×gCM1, the most highly expressed isoform found in xylem tissue. Although this strategy was successful in disrupting Pa×gCM1 transcripts, there was also an unanticipated increase in lignin content, a shift towards guaiacyl lignin units, and more xylem vessels with smaller lumen areas, at least in the most severely affected transgenic line. This was accompanied by compensatory expression of the other two CM isoforms, Pa×gCM2 and Pa×gCM3, as well as widespread changes in gene expression and metabolism. This study investigates potential redundancy within the CM gene family in the developing xylem of poplar and highlights the pivotal role of chorismate in plant metabolism, development, and physiology.

Original language	English
Article number	e70053
Journal	Plant Direct
Volume	9
Issue number	3
DOIs	https://doi.org/10.1002/pld3.70053
State	Published - Mar 2025

Funding

Financial support for this work was provided by a Korea Institute of Science and Technology grant to S.D.M. by the Great Lakes Bioenergy Research Center, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number DE‐SC0018409 to S.D.M. and J.R., and by the Center for Bioenergy Innovation, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number FWP ERKP886 to T.J.T. This manuscript has been supported by UT‐Battelle LLC, under Contract No. DE‐AC05‐00OR22725 with the U.S. Department of Energy. We also gratefully acknowledge the help of Kaye A. Hare with plant maintenance, photography, and harvesting; Charles Hefer with preprocessing of the RNA‐seq data; and Nancy L. Engle, Madhavi Z. Martin, and Audrey D. Labbé with the untargeted analysis of metabolites. Financial support for this work was provided by a Korea Institute of Science and Technology grant to S.D.M. by the Great Lakes Bioenergy Research Center, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number DE‐SC0018409 to S.D.M. and J.R., and by the Center for Bioenergy Innovation, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number FWP ERKP886 to T.J.T. This manuscript has been supported by UT‐Battelle LLC, under Contract No. DE‐AC05‐00OR22725 with the U.S. Department of Energy. Funding: Funding: Financial support for this work was provided by a Korea Institute of Science and Technology grant to S.D.M. by the Great Lakes Bioenergy Research Center, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number DE-SC0018409 to S.D.M. and J.R., and by the Center for Bioenergy Innovation, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number FWP ERKP886 to T.J.T. This manuscript has been supported by UT-Battelle LLC, under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. Financial support for this work was provided by a Korea Institute of Science and Technology grant to S.D.M. by the Great Lakes Bioenergy Research Center, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number DE-SC0018409 to S.D.M. and J.R., and by the Center for Bioenergy Innovation, U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under Award Number FWP ERKP886 to T.J.T. This manuscript has been supported by UT-Battelle LLC, under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. We also gratefully acknowledge the help of Kaye A. Hare with plant maintenance, photography, and harvesting; Charles Hefer with preprocessing of the RNA-seq data; and Nancy L. Engle, Madhavi Z. Martin, and Audrey D. Labbé with the untargeted analysis of metabolites.

Keywords

RNAi
aromatic amino acids
lignin biosynthesis
salicylic acid
shikimate pathway

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10.1002/pld3.70053

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title = "Suppression of Chorismate Mutase 1 in Hybrid Poplar to Investigate Potential Redundancy in the Supply of Lignin Precursors",

abstract = "Chorismate is an important branchpoint metabolite in the biosynthesis of lignin and a wide array of metabolites in plants. Chorismate mutase (CM), the enzyme responsible for transforming chorismate into prephenate, is a key regulator of metabolic flux towards the synthesis of aromatic amino acids and onwards to lignin. We examined three CM genes in hybrid poplar (Populus alba × grandidentata; P39, abbreviated as Pa×g) and used RNA interference (RNAi) to suppress the expression of Pa×gCM1, the most highly expressed isoform found in xylem tissue. Although this strategy was successful in disrupting Pa×gCM1 transcripts, there was also an unanticipated increase in lignin content, a shift towards guaiacyl lignin units, and more xylem vessels with smaller lumen areas, at least in the most severely affected transgenic line. This was accompanied by compensatory expression of the other two CM isoforms, Pa×gCM2 and Pa×gCM3, as well as widespread changes in gene expression and metabolism. This study investigates potential redundancy within the CM gene family in the developing xylem of poplar and highlights the pivotal role of chorismate in plant metabolism, development, and physiology.",

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author = "Yaseen Mottiar and Timothy J Tschaplinski and John Ralph and Shawn D Mansfield",

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AU - Mottiar, Yaseen

AU - Tschaplinski, Timothy J

AU - Ralph, John

AU - Mansfield, Shawn D

N1 - Publisher Copyright: © 2025 Oak Ridge National laboratory and The Author(s). Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd.

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N2 - Chorismate is an important branchpoint metabolite in the biosynthesis of lignin and a wide array of metabolites in plants. Chorismate mutase (CM), the enzyme responsible for transforming chorismate into prephenate, is a key regulator of metabolic flux towards the synthesis of aromatic amino acids and onwards to lignin. We examined three CM genes in hybrid poplar (Populus alba × grandidentata; P39, abbreviated as Pa×g) and used RNA interference (RNAi) to suppress the expression of Pa×gCM1, the most highly expressed isoform found in xylem tissue. Although this strategy was successful in disrupting Pa×gCM1 transcripts, there was also an unanticipated increase in lignin content, a shift towards guaiacyl lignin units, and more xylem vessels with smaller lumen areas, at least in the most severely affected transgenic line. This was accompanied by compensatory expression of the other two CM isoforms, Pa×gCM2 and Pa×gCM3, as well as widespread changes in gene expression and metabolism. This study investigates potential redundancy within the CM gene family in the developing xylem of poplar and highlights the pivotal role of chorismate in plant metabolism, development, and physiology.

AB - Chorismate is an important branchpoint metabolite in the biosynthesis of lignin and a wide array of metabolites in plants. Chorismate mutase (CM), the enzyme responsible for transforming chorismate into prephenate, is a key regulator of metabolic flux towards the synthesis of aromatic amino acids and onwards to lignin. We examined three CM genes in hybrid poplar (Populus alba × grandidentata; P39, abbreviated as Pa×g) and used RNA interference (RNAi) to suppress the expression of Pa×gCM1, the most highly expressed isoform found in xylem tissue. Although this strategy was successful in disrupting Pa×gCM1 transcripts, there was also an unanticipated increase in lignin content, a shift towards guaiacyl lignin units, and more xylem vessels with smaller lumen areas, at least in the most severely affected transgenic line. This was accompanied by compensatory expression of the other two CM isoforms, Pa×gCM2 and Pa×gCM3, as well as widespread changes in gene expression and metabolism. This study investigates potential redundancy within the CM gene family in the developing xylem of poplar and highlights the pivotal role of chorismate in plant metabolism, development, and physiology.

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KW - lignin biosynthesis

KW - salicylic acid

KW - shikimate pathway

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DO - 10.1002/pld3.70053

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ER -

Suppression of Chorismate Mutase 1 in Hybrid Poplar to Investigate Potential Redundancy in the Supply of Lignin Precursors

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