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Title: Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1) releases latent defense signals in stems with reduced lignin content

Abstract

There is considerable interest in engineering plant cell wall components, particularly lignin, to improve forage quality and biomass properties for processing to fuels and bioproducts. However, modifying lignin content and/or composition in transgenic plants through down-regulation of lignin biosynthetic enzymes can induce expression of defense response genes in the absence of biotic or abiotic stress. Arabidopsis thaliana lines with altered lignin through down-regulation of hydroxycinnamoyl CoA:shikimate/quinate hydroxycinnamoyl transferase (HCT) or loss of function of cinnamoyl CoA reductase 1 (CCR1) express a suite of pathogenesis-related (PR) protein genes. The plants also exhibit extensive cell wall remodeling associated with induction of multiple cell wall-degrading enzymes, a process which renders the corresponding biomass a substrate for growth of the cellulolytic thermophile Caldicellulosiruptor bescii lacking a functional pectinase gene cluster. The cell wall remodeling also results in the release of size- and charge-heterogeneous pectic oligosaccharide elicitors of PR gene expression. Genetic analysis shows that both in planta PR gene expression and release of elicitors are the result of ectopic expression in xylem of the gene Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1), which is normally expressed during anther and silique dehiscence. These data highlight the importance of pectin in cell wall integrity and the valuemore » of lignin modification as a tool to interrogate the informational content of plant cell walls.« less

Authors:
 [1];  [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [5];  [6]; ORCiD logo [4];  [7]; ORCiD logo [2]; ORCiD logo [8]; ORCiD logo [8]; ORCiD logo [9]
  1. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst. and Dept. of Biological Sciences
  2. Univ. of Leeds, Leeds (United Kingdom). Faculty of Biological Sciences
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center and Dept. of Plant Biology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation
  5. Univ. of Georgia, Athens, GA (United States). Dept. of Genetics
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation; Univ. of Georgia, Athens, GA (United States). Dept. of Genetics
  7. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst. and Dept. of Biological Sciences; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center
  8. Ghent Univ. (Belguim). Dept. of Plant Biotechnology and Bioinformatics; Vlaams Inst. voor Biotechnologie, Ghent (Belguim). Center for Plant Systems Biology
  9. Univ. of North Texas, Denton, TX (United States). BioDiscovery Inst. and Dept. of Biological Sciences; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center and Center for Bioenergy Innovation
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); USDOE Bioenergy Research Centers (BRC) (United States). Center for Bioenergy Innovation (CBI)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)' National Science Foundation (NSF)
OSTI Identifier:
1625055
Grant/Contract Number:  
AC05-00OR22725; PIEF-GA-2013-625270; DBI-0421683; IOS-0923992
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 117; Journal Issue: 6; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & technology - other topics; cell wall remodeling; lignin modification; defense response; elicitor; polygalacturonase

Citation Formats

Gallego-Giraldo, Lina, Liu, Chang, Pose-Albacete, Sara, Pattathil, Sivakumar, Peralta, Angelo Gabriel, Young, Jenna, Westpheling, Jan, Hahn, Michael G., Rao, Xiaolan, Knox, J. Paul, De Meester, Barbara, Boerjan, Wout, and Dixon, Richard A. Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1) releases latent defense signals in stems with reduced lignin content. United States: N. p., 2020. Web. doi:10.1073/pnas.1914422117.
Gallego-Giraldo, Lina, Liu, Chang, Pose-Albacete, Sara, Pattathil, Sivakumar, Peralta, Angelo Gabriel, Young, Jenna, Westpheling, Jan, Hahn, Michael G., Rao, Xiaolan, Knox, J. Paul, De Meester, Barbara, Boerjan, Wout, & Dixon, Richard A. Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1) releases latent defense signals in stems with reduced lignin content. United States. https://doi.org/10.1073/pnas.1914422117
Gallego-Giraldo, Lina, Liu, Chang, Pose-Albacete, Sara, Pattathil, Sivakumar, Peralta, Angelo Gabriel, Young, Jenna, Westpheling, Jan, Hahn, Michael G., Rao, Xiaolan, Knox, J. Paul, De Meester, Barbara, Boerjan, Wout, and Dixon, Richard A. Thu . "Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1) releases latent defense signals in stems with reduced lignin content". United States. https://doi.org/10.1073/pnas.1914422117. https://www.osti.gov/servlets/purl/1625055.
@article{osti_1625055,
title = {Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1) releases latent defense signals in stems with reduced lignin content},
author = {Gallego-Giraldo, Lina and Liu, Chang and Pose-Albacete, Sara and Pattathil, Sivakumar and Peralta, Angelo Gabriel and Young, Jenna and Westpheling, Jan and Hahn, Michael G. and Rao, Xiaolan and Knox, J. Paul and De Meester, Barbara and Boerjan, Wout and Dixon, Richard A.},
abstractNote = {There is considerable interest in engineering plant cell wall components, particularly lignin, to improve forage quality and biomass properties for processing to fuels and bioproducts. However, modifying lignin content and/or composition in transgenic plants through down-regulation of lignin biosynthetic enzymes can induce expression of defense response genes in the absence of biotic or abiotic stress. Arabidopsis thaliana lines with altered lignin through down-regulation of hydroxycinnamoyl CoA:shikimate/quinate hydroxycinnamoyl transferase (HCT) or loss of function of cinnamoyl CoA reductase 1 (CCR1) express a suite of pathogenesis-related (PR) protein genes. The plants also exhibit extensive cell wall remodeling associated with induction of multiple cell wall-degrading enzymes, a process which renders the corresponding biomass a substrate for growth of the cellulolytic thermophile Caldicellulosiruptor bescii lacking a functional pectinase gene cluster. The cell wall remodeling also results in the release of size- and charge-heterogeneous pectic oligosaccharide elicitors of PR gene expression. Genetic analysis shows that both in planta PR gene expression and release of elicitors are the result of ectopic expression in xylem of the gene Arabidopsis Dehiscence Zone Polygalacturonase 1 (ADPG1), which is normally expressed during anther and silique dehiscence. These data highlight the importance of pectin in cell wall integrity and the value of lignin modification as a tool to interrogate the informational content of plant cell walls.},
doi = {10.1073/pnas.1914422117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 6,
volume = 117,
place = {United States},
year = {Thu Jan 23 00:00:00 EST 2020},
month = {Thu Jan 23 00:00:00 EST 2020}
}

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Expression of polygalacturonases and evidence to support their role during cell separation processes in Arabidopsis thaliana
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journal, April 2010

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journal, September 2012

  • González-Carranza, Zinnia Haydee; Shahid, Ahmad Ali; Zhang, Li
  • Plant Physiology, Vol. 160, Issue 3
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Silencing of Hydroxycinnamoyl-Coenzyme A Shikimate/Quinate Hydroxycinnamoyltransferase Affects Phenylpropanoid Biosynthesis
journal, May 2004

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Convergent Evolution of Syringyl Lignin Biosynthesis via Distinct Pathways in the Lycophyte Selaginella and Flowering Plants
journal, April 2010

  • Weng, Jing-Ke; Akiyama, Takuya; Bonawitz, Nicholas D.
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Elicitors and defense gene induction in plants with altered lignin compositions
journal, June 2018

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  • New Phytologist, Vol. 219, Issue 4
  • DOI: 10.1111/nph.15258

Ethylene production in B otrytis cinerea‐ and oligogalacturonide‐induced immunity requires calcium‐dependent protein kinases
journal, November 2015

  • Gravino, Matteo; Savatin, Daniel Valentin; Macone, Alberto
  • The Plant Journal, Vol. 84, Issue 6
  • DOI: 10.1111/tpj.13057

Altering the Cell Wall and Its Impact on Plant Disease: From Forage to Bioenergy
journal, August 2014


Phytoalexins and their Elicitors-A Defense Against Microbial Infection in Plants
journal, June 1984


Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance
journal, October 2014

  • Chung, Daehwan; Pattathil, Sivakumar; Biswal, Ajaya K.
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/s13068-014-0147-1

Plant cell surface receptor-mediated signaling – a common theme amid diversity
journal, January 2018

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Pectic Cell Wall Fragments Regulate Tobacco Thin-Cell-Layer Explant Morphogenesis
journal, August 1989

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The role of the secondary cell wall in plant resistance to pathogens
journal, August 2014


Cell Wall Ultrastructure of Stem Wood, Roots, and Needles of a Conifer Varies in Response to Moisture Availability
journal, June 2016

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Signaling role of oligogalacturonides derived during cell wall degradation
journal, November 2012

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Works referencing / citing this record:

Pectin-derived immune elicitors in response to lignin modification in plants
journal, February 2020

  • Voxeur, Aline; Höfte, Herman
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 9
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