Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression

Abstract Lignin is a key secondary cell wall chemical constituent, and is both a barrier to biomass utilization and a potential source of bioproducts. The Arabidopsis transcription factors MYB58 and MYB63 have been shown to upregulate gene expression of the general phenylpropanoid and monolignol bio...

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Main Authors: Mendel L. Perkins, Mathias Schuetz, Faride Unda, Rebecca A. Smith, Richard Sibout, Natalie J. Hoffmann, Darren C. J. Wong, Simone D. Castellarin, Shawn D. Mansfield, Lacey Samuels
Format: Article
Language:English
Published: Wiley 2020-09-01
Series:Plant Direct
Online Access:https://doi.org/10.1002/pld3.265
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author Mendel L. Perkins
Mathias Schuetz
Faride Unda
Rebecca A. Smith
Richard Sibout
Natalie J. Hoffmann
Darren C. J. Wong
Simone D. Castellarin
Shawn D. Mansfield
Lacey Samuels
author_facet Mendel L. Perkins
Mathias Schuetz
Faride Unda
Rebecca A. Smith
Richard Sibout
Natalie J. Hoffmann
Darren C. J. Wong
Simone D. Castellarin
Shawn D. Mansfield
Lacey Samuels
author_sort Mendel L. Perkins
collection DOAJ
description Abstract Lignin is a key secondary cell wall chemical constituent, and is both a barrier to biomass utilization and a potential source of bioproducts. The Arabidopsis transcription factors MYB58 and MYB63 have been shown to upregulate gene expression of the general phenylpropanoid and monolignol biosynthetic pathways. The overexpression of these genes also results in dwarfism. The vascular integrity, soluble phenolic profiles, cell wall lignin, and transcriptomes associated with these MYB‐overexpressing lines were characterized. Plants with high expression of MYB58 and MYB63 had increased ectopic lignin and the xylem vessels were regular and open, suggesting that the stunted growth is not associated with loss of vascular conductivity. MYB58 and MYB63 overexpression lines had characteristic soluble phenolic profiles with large amounts of monolignol glucosides and sinapoyl esters, but decreased flavonoids. Because loss of function lac4 lac17 mutants also accumulate monolignol glucosides, we hypothesized that LACCASE overexpression might decrease monolignol glucoside levels in the MYB‐overexpressing plant lines. When laccases related to lignification (LAC4 or LAC17) were co‐overexpressed with MYB63 or MYB58, the dwarf phenotype was rescued. Moreover, the overexpression of either LAC4 or LAC17 led to wild‐type monolignol glucoside levels, as well as wild‐type lignin levels in the rescued plants. Transcriptomes of the rescued double MYB63‐OX/LAC17‐OX overexpression lines showed elevated, but attenuated, expression of the MYB63 gene itself and the direct transcriptional targets of MYB63. Contrasting the dwarfism from overabundant monolignol production with dwarfism from lignin mutants provides insight into some of the proposed mechanisms of lignin modification‐induced dwarfism.
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spelling doaj.art-8d1e9c5292904a5e8fb65f3ee7d26dbc2022-12-21T16:58:28ZengWileyPlant Direct2475-44552020-09-0149n/an/a10.1002/pld3.265Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpressionMendel L. Perkins0Mathias Schuetz1Faride Unda2Rebecca A. Smith3Richard Sibout4Natalie J. Hoffmann5Darren C. J. Wong6Simone D. Castellarin7Shawn D. Mansfield8Lacey Samuels9Department of Botany University of British Columbia Vancouver CanadaDepartment of Botany University of British Columbia Vancouver CanadaDepartment of Wood Science University of British Columbia Vancouver CanadaDepartment of Botany University of British Columbia Vancouver CanadaDepartment of Botany University of British Columbia Vancouver CanadaDepartment of Botany University of British Columbia Vancouver CanadaWine Research Centre University of British Columbia Vancouver CanadaWine Research Centre University of British Columbia Vancouver CanadaDepartment of Wood Science University of British Columbia Vancouver CanadaDepartment of Botany University of British Columbia Vancouver CanadaAbstract Lignin is a key secondary cell wall chemical constituent, and is both a barrier to biomass utilization and a potential source of bioproducts. The Arabidopsis transcription factors MYB58 and MYB63 have been shown to upregulate gene expression of the general phenylpropanoid and monolignol biosynthetic pathways. The overexpression of these genes also results in dwarfism. The vascular integrity, soluble phenolic profiles, cell wall lignin, and transcriptomes associated with these MYB‐overexpressing lines were characterized. Plants with high expression of MYB58 and MYB63 had increased ectopic lignin and the xylem vessels were regular and open, suggesting that the stunted growth is not associated with loss of vascular conductivity. MYB58 and MYB63 overexpression lines had characteristic soluble phenolic profiles with large amounts of monolignol glucosides and sinapoyl esters, but decreased flavonoids. Because loss of function lac4 lac17 mutants also accumulate monolignol glucosides, we hypothesized that LACCASE overexpression might decrease monolignol glucoside levels in the MYB‐overexpressing plant lines. When laccases related to lignification (LAC4 or LAC17) were co‐overexpressed with MYB63 or MYB58, the dwarf phenotype was rescued. Moreover, the overexpression of either LAC4 or LAC17 led to wild‐type monolignol glucoside levels, as well as wild‐type lignin levels in the rescued plants. Transcriptomes of the rescued double MYB63‐OX/LAC17‐OX overexpression lines showed elevated, but attenuated, expression of the MYB63 gene itself and the direct transcriptional targets of MYB63. Contrasting the dwarfism from overabundant monolignol production with dwarfism from lignin mutants provides insight into some of the proposed mechanisms of lignin modification‐induced dwarfism.https://doi.org/10.1002/pld3.265
spellingShingle Mendel L. Perkins
Mathias Schuetz
Faride Unda
Rebecca A. Smith
Richard Sibout
Natalie J. Hoffmann
Darren C. J. Wong
Simone D. Castellarin
Shawn D. Mansfield
Lacey Samuels
Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression
Plant Direct
title Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression
title_full Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression
title_fullStr Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression
title_full_unstemmed Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression
title_short Dwarfism of high‐monolignol Arabidopsis plants is rescued by ectopic LACCASE overexpression
title_sort dwarfism of high monolignol arabidopsis plants is rescued by ectopic laccase overexpression
url https://doi.org/10.1002/pld3.265
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