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Title: Brachypodium Phenylalanine Ammonia Lyase (PAL) Promotes Antiviral Defenses against Panicum mosaic virus and Its Satellites

Abstract

Brachypodium distachyon has recently emerged as a premier model plant for monocot biology, akin to Arabidopsis thaliana. We previously reported genome-wide transcriptomic and alternative splicing changes occurring in Brachypodium during compatible infections with Panicum mosaic virus (PMV) and its satellite virus (SPMV). Here, we dissected the role of Brachypodium phenylalanine ammonia lyase 1 (PAL1), a key enzyme for phenylpropanoid and salicylic acid (SA) biosynthesis and the induction of plant defenses. Targeted metabolomics profiling of PMV-infected and PMV- plus SPMV-infected (PMV/SPMV) Brachypodium plants revealed enhanced levels of multiple defense-related hormones and metabolites such as cinnamic acid, SA, and fatty acids and lignin precursors during disease progression. The virus-induced accumulation of SA and lignin was significantly suppressed upon knockdown of B. distachyon PAL1 (BdPAL1) using RNA interference (RNAi). The compromised SA accumulation in PMV/SPMV-infected BdPAL1 RNAi plants correlated with weaker induction of multiple SA-related defense gene markers (pathogenesis related 1 [PR-1], PR-3, PR-5, and WRKY75) and enhanced susceptibility to PMV/SPMV compared to that of wild-type (WT) plants. Furthermore, exogenous application of SA alleviated the PMV/SPMV necrotic disease phenotypes and delayed plant death caused by single and mixed infections. Together, our results support an antiviral role for BdPAL1 during compatible host-virus interaction, perhapsmore » as a last resort attempt to rescue the infected plant.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [2];  [3];  [4];  [5]
  1. Texas A &M Unive. System, Weslaco, TX (United States). Texas A & M AgriLife Research and Extension Center
  2. U.S. Dept. of Agriculture, Gainesville, FL (United States). Center of Medical, Agricultural, and Veterinary Entomology. Chemistry Unit
  3. Illinois State Univ., Normal, IL (United States). DOE Great Lakes Bioenergy Research Center. School of Biological Sciences
  4. Texas A & M Univ., College Station, TX (United States). Dept. of Plant Pathology and Microbiology
  5. Texas A & M Univ., College Station, TX (United States). Texas A & M AgriLife Research; Texas A & M Univ., College Station, TX (United States). Dept. of Plant Pathology and Microbiology
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA
OSTI Identifier:
1849053
Grant/Contract Number:  
FC02-07ER64494; 2016-67013-24738; 1023984; CSP503406
Resource Type:
Accepted Manuscript
Journal Name:
mBio
Additional Journal Information:
Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 2161-2129
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; microbiology; plant-virus interactions; grasses; defense hormones; bioenergy; metabolic pathways

Citation Formats

Pant, Shankar R., Irigoyen, Sonia, Liu, Jiaxing, Bedre, Renesh, Christensen, Shawn A., Schmelz, Eric A., Sedbrook, John C., Scholthof, Karen-Beth G., and Mandadi, Kranthi K. Brachypodium Phenylalanine Ammonia Lyase (PAL) Promotes Antiviral Defenses against Panicum mosaic virus and Its Satellites. United States: N. p., 2021. Web. doi:10.1128/mbio.03518-20.
Pant, Shankar R., Irigoyen, Sonia, Liu, Jiaxing, Bedre, Renesh, Christensen, Shawn A., Schmelz, Eric A., Sedbrook, John C., Scholthof, Karen-Beth G., & Mandadi, Kranthi K. Brachypodium Phenylalanine Ammonia Lyase (PAL) Promotes Antiviral Defenses against Panicum mosaic virus and Its Satellites. United States. https://doi.org/10.1128/mbio.03518-20
Pant, Shankar R., Irigoyen, Sonia, Liu, Jiaxing, Bedre, Renesh, Christensen, Shawn A., Schmelz, Eric A., Sedbrook, John C., Scholthof, Karen-Beth G., and Mandadi, Kranthi K. Tue . "Brachypodium Phenylalanine Ammonia Lyase (PAL) Promotes Antiviral Defenses against Panicum mosaic virus and Its Satellites". United States. https://doi.org/10.1128/mbio.03518-20. https://www.osti.gov/servlets/purl/1849053.
@article{osti_1849053,
title = {Brachypodium Phenylalanine Ammonia Lyase (PAL) Promotes Antiviral Defenses against Panicum mosaic virus and Its Satellites},
author = {Pant, Shankar R. and Irigoyen, Sonia and Liu, Jiaxing and Bedre, Renesh and Christensen, Shawn A. and Schmelz, Eric A. and Sedbrook, John C. and Scholthof, Karen-Beth G. and Mandadi, Kranthi K.},
abstractNote = {Brachypodium distachyon has recently emerged as a premier model plant for monocot biology, akin to Arabidopsis thaliana. We previously reported genome-wide transcriptomic and alternative splicing changes occurring in Brachypodium during compatible infections with Panicum mosaic virus (PMV) and its satellite virus (SPMV). Here, we dissected the role of Brachypodium phenylalanine ammonia lyase 1 (PAL1), a key enzyme for phenylpropanoid and salicylic acid (SA) biosynthesis and the induction of plant defenses. Targeted metabolomics profiling of PMV-infected and PMV- plus SPMV-infected (PMV/SPMV) Brachypodium plants revealed enhanced levels of multiple defense-related hormones and metabolites such as cinnamic acid, SA, and fatty acids and lignin precursors during disease progression. The virus-induced accumulation of SA and lignin was significantly suppressed upon knockdown of B. distachyon PAL1 (BdPAL1) using RNA interference (RNAi). The compromised SA accumulation in PMV/SPMV-infected BdPAL1 RNAi plants correlated with weaker induction of multiple SA-related defense gene markers (pathogenesis related 1 [PR-1], PR-3, PR-5, and WRKY75) and enhanced susceptibility to PMV/SPMV compared to that of wild-type (WT) plants. Furthermore, exogenous application of SA alleviated the PMV/SPMV necrotic disease phenotypes and delayed plant death caused by single and mixed infections. Together, our results support an antiviral role for BdPAL1 during compatible host-virus interaction, perhaps as a last resort attempt to rescue the infected plant.},
doi = {10.1128/mbio.03518-20},
journal = {mBio},
number = 1,
volume = 12,
place = {United States},
year = {Tue Feb 16 00:00:00 EST 2021},
month = {Tue Feb 16 00:00:00 EST 2021}
}

Works referenced in this record:

A sugarcane mosaic virus vector for gene expression in maize
journal, August 2019

  • Mei, Yu; Liu, Guanjun; Zhang, Chunquan
  • Plant Direct, Vol. 3, Issue 8
  • DOI: 10.1002/pld3.158

Fatty Acid Regulation of Gene Transcription
journal, October 2000

  • Duplus, Eric; Glorian, Martine; Forest, Claude
  • Journal of Biological Chemistry, Vol. 275, Issue 40
  • DOI: 10.1074/jbc.R000015200

Panicum Mosaic Virus and Its Satellites Acquire RNA Modifications Associated with Host-Mediated Antiviral Degradation
journal, August 2019

  • Pyle, Jesse D.; Mandadi, Kranthi K.; Scholthof, Karen-Beth G.
  • mBio, Vol. 10, Issue 4
  • DOI: 10.1128/mBio.01900-19

Metabolic differentiation of Arabidopsis treated with methyl jasmonate using nuclear magnetic resonance spectroscopy
journal, June 2006


Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize
journal, March 2011

  • Schmelz, E. A.; Kaplan, F.; Huffaker, A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
  • DOI: 10.1073/pnas.1014714108

Small-scale and automatable high-throughput compositional analysis of biomass
journal, October 2010

  • DeMartini, Jaclyn D.; Studer, Michael H.; Wyman, Charles E.
  • Biotechnology and Bioengineering, Vol. 108, Issue 2, p. 306-312
  • DOI: 10.1002/bit.22937

Salicylic Acid and its Function in Plant ImmunityF: Defense Signal Molecule Salicylic Acid
journal, June 2011


Dynamics of Responses in Compatible Potato - Potato virus Y Interaction Are Modulated by Salicylic Acid
journal, December 2011


Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew
journal, June 2006


Hormonal Modulation of Plant Immunity
journal, November 2012


BAK1 and BKK1 in Arabidopsis thaliana confer reduced susceptibility to turnip crinkle virus
journal, February 2010


Systemic signaling during plant defense
journal, August 2013


Brachypodium distachyon line Bd3-1 resistance is elicited by the barley stripe mosaic virus triple gene block 1 movement protein
journal, December 2012

  • Lee, Mi Yeon; Yan, Lijie; Gorter, Florien A.
  • Journal of General Virology, Vol. 93, Issue 12
  • DOI: 10.1099/vir.0.045880-0

An update on salicylic acid biosynthesis, its induction and potential exploitation by plant viruses
journal, June 2020


Completion of the cytosolic post-chorismate phenylalanine biosynthetic pathway in plants
journal, January 2019


Acibenzolar- S -Methyl Restricts Infection of Nicotiana benthamiana by Plantago Asiatica Mosaic Virus at Two Distinct Stages
journal, November 2019

  • Matsuo, Yuki; Novianti, Fawzia; Takehara, Miki
  • Molecular Plant-Microbe Interactions®, Vol. 32, Issue 11
  • DOI: 10.1094/MPMI-03-19-0087-R

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Sporogenic Effect of Polyunsaturated Fatty Acids on Development of Aspergillus spp
journal, August 1999


Effects of PHENYLALANINE AMMONIA LYASE ( PAL ) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium
journal, June 2015

  • Cass, Cynthia L.; Peraldi, Antoine; Dowd, Patrick F.
  • Journal of Experimental Botany, Vol. 66, Issue 14
  • DOI: 10.1093/jxb/erv269

Role of β-Oxidation in Jasmonate Biosynthesis and Systemic Wound Signaling in Tomato
journal, February 2005

  • Li, Chuanyou; Schilmiller, Anthony L.; Liu, Guanghui
  • The Plant Cell, Vol. 17, Issue 3
  • DOI: 10.1105/tpc.104.029108

Systemic Acquired Resistance and Salicylic Acid: Past, Present, and Future
journal, September 2018

  • Klessig, Daniel F.; Choi, Hyong Woo; Dempsey, D’Maris Amick
  • Molecular Plant-Microbe Interactions®, Vol. 31, Issue 9
  • DOI: 10.1094/MPMI-03-18-0067-CR

The Role of Salicylic Acid and Jasmonic Acid in Pathogen Defence
journal, May 2006


Induction by Salicylic Acid of Pathogenesis-related Proteins and Resistance to Alfalfa Mosaic Virus Infection in Various Plant Species
journal, October 1986

  • Van Huijsduijnen, R. A. M. H.; Alblas, S. W.; De Rijk, R. H.
  • Journal of General Virology, Vol. 67, Issue 10
  • DOI: 10.1099/0022-1317-67-10-2135

Plant defense signals: Players and pawns in plant-virus-vector interactions
journal, February 2019


Genome-Wide Analysis of Alternative Splicing Landscapes Modulated during Plant-Virus Interactions in Brachypodium distachyon
journal, January 2015


Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


Brachypodium distachyon is a suitable host plant for study of Barley yellow dwarf virus
journal, January 2016


The plant immune system
journal, November 2006

  • Jones, Jonathan D. G.; Dangl, Jeffery L.
  • Nature, Vol. 444, Issue 7117
  • DOI: 10.1038/nature05286

Plant defense in the absence of jasmonic acid: The role of cyclopentenones
journal, October 2001

  • Stintzi, A.; Weber, H.; Reymond, P.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 22
  • DOI: 10.1073/pnas.211311098

Biotic stress globally downregulates photosynthesis genes: Biotic stress downregulates photosynthesis
journal, September 2010


A fatty acid desaturase modulates the activation of defense signaling pathways in plants
journal, July 2001

  • Kachroo, P.; Shanklin, J.; Shah, J.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 16
  • DOI: 10.1073/pnas.151258398

Salicylic Acid Suppresses Jasmonic Acid Signaling Downstream of SCFCOI1-JAZ by Targeting GCC Promoter Motifs via Transcription Factor ORA59    
journal, February 2013

  • Van der Does, Dieuwertje; Leon-Reyes, Antonio; Koornneef, Annemart
  • The Plant Cell, Vol. 25, Issue 2
  • DOI: 10.1105/tpc.112.108548

Complete nucleotide sequences and virion particle association of two satellite RNAs of panicum mosaic virus
journal, August 2017


Primary Metabolism and Plant Defense—Fuel for the Fire
journal, May 2009


Phenylpropanoid Biosynthesis
journal, January 2010


Exploring valid reference genes for gene expression studies in Brachypodium distachyon by real-time PCR
journal, January 2008


RNA: protein interactions associated with satellites of panicum mosaic virus
journal, November 2000


The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PALgene expression
journal, October 2010


Genomic architecture and functional relationships of intronless, constitutively- and alternatively-spliced genes in Brachypodium distachyon
journal, August 2015


Stress-Induced Phenylpropanoid Metabolism.
journal, July 1995


Plant PRRs and the Activation of Innate Immune Signaling
journal, April 2014


To die or not to die? Lessons from lesion mimic mutants
journal, January 2015

  • Bruggeman, Quentin; Raynaud, Cécile; Benhamed, Moussa
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00024

Dietary polyunsaturated fatty acids and regulation of gene transcription
journal, January 2002


Biosynthesis of Jasmonic Acid by Several Plant Species
journal, June 1984

  • Vick, Brady A.; Zimmerman, Don C.
  • Plant Physiology, Vol. 75, Issue 2
  • DOI: 10.1104/pp.75.2.458

Oxylipins Other Than Jasmonic Acid Are Xylem-Resident Signals Regulating Systemic Resistance Induced by Trichoderma virens in Maize
journal, November 2019

  • Wang, Ken-Der; Borrego, Eli J.; Kenerley, Charles M.
  • The Plant Cell, Vol. 32, Issue 1
  • DOI: 10.1105/tpc.19.00487

Salicylic Acid Can Induce Resistance to Plant Virus Movement
journal, September 1998

  • Naylor, Martin; Murphy, Alex M.; Berry, James O.
  • Molecular Plant-Microbe Interactions®, Vol. 11, Issue 9
  • DOI: 10.1094/MPMI.1998.11.9.860

Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure
journal, December 2017

  • Gordon, Sean P.; Contreras-Moreira, Bruno; Woods, Daniel P.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-02292-8

Photosynthesis, photorespiration, and light signalling in defence responses
journal, January 2012

  • Kangasjarvi, S.; Neukermans, J.; Li, S.
  • Journal of Experimental Botany, Vol. 63, Issue 4
  • DOI: 10.1093/jxb/err402

Satellite Panicum Mosaic Virus Capsid Protein Elicits Symptoms on a Nonhost Plant and Interferes with a Suppressor of Virus-Induced Gene Silencing
journal, March 2004


Salicylic acid in plant defence—the players and protagonists
journal, October 2007


Characterization and Biological Function of the ISOCHORISMATE SYNTHASE2 Gene of Arabidopsis
journal, May 2008

  • Garcion, Christophe; Lohmann, Antje; Lamodière, Elisabeth
  • Plant Physiology, Vol. 147, Issue 3
  • DOI: 10.1104/pp.108.119420

A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize
journal, September 2009


Plant Cell Wall Dynamics in Compatible and Incompatible Potato Response to Infection Caused by Potato Virus Y (PVYNTN)
journal, March 2018

  • Otulak-Kozieł, Katarzyna; Kozieł, Edmund; Lockhart, Benham
  • International Journal of Molecular Sciences, Vol. 19, Issue 3
  • DOI: 10.3390/ijms19030862

QuantPrime - a flexible tool for reliable high-throughput primer design for quantitative PCR
journal, January 2008

  • Arvidsson, Samuel; Kwasniewski, Miroslaw; Riano-Pachon, Diego M.
  • BMC Bioinformatics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2105-9-465

Desaturation and Related Modifications of Fatty Acids
journal, June 1998


Nucleotide Sequence and Infectivity of a Full-Length cDNA Clone of Panicum Mosaic Virus
journal, February 1998


Networking by small-molecule hormones in plant immunity
journal, April 2009

  • Pieterse, Corné M. J.; Leon-Reyes, Antonio; Van der Ent, Sjoerd
  • Nature Chemical Biology, Vol. 5, Issue 5
  • DOI: 10.1038/nchembio.164

Salicylic Acid Has Cell-Specific Effects on Tobacco mosaic virus Replication and Cell-to-Cell Movement
journal, February 2002

  • Murphy, Alex M.; Carr, John P.
  • Plant Physiology, Vol. 128, Issue 2
  • DOI: 10.1104/pp.010688

Salicylic Acid-Induced Resistance to Cucumber mosaic virus in Squash and Arabidopsis thaliana : Contrasting Mechanisms of Induction and Antiviral Action
journal, May 2005

  • Mayers, Carl N.; Lee, Kian-Chung; Moore, Catherine A.
  • Molecular Plant-Microbe Interactions®, Vol. 18, Issue 5
  • DOI: 10.1094/MPMI-18-0428

Panicovirus accumulation is governed by two membrane-associated proteins with a newly identified conserved motif that contributes to pathogenicity
journal, March 2006

  • Batten, Jeffrey S.; Turina, Massimo; Scholthof, Karen-Beth G.
  • Virology Journal, Vol. 3, Issue 1
  • DOI: 10.1186/1743-422X-3-12

Plant Immune Responses Against Viruses: How Does a Virus Cause Disease?
journal, May 2013


Oxylipin Signaling: A Distinct Role for the Jasmonic Acid Precursor cis-(+)-12-Oxo-Phytodienoic Acid (cis-OPDA)
journal, January 2012


Comparative Analysis of Antiviral Responses in Brachypodium distachyon and Setaria viridis Reveals Conserved and Unique Outcomes Among C 3 and C 4 Plant Defenses
journal, November 2014

  • Mandadi, Kranthi K.; Pyle, Jesse D.; Scholthof, Karen-Beth G.
  • Molecular Plant-Microbe Interactions®, Vol. 27, Issue 11
  • DOI: 10.1094/MPMI-05-14-0152-R

Biosynthesis and metabolism of salicylic acid.
journal, May 1995

  • Lee, H. I.; Leon, J.; Raskin, I.
  • Proceedings of the National Academy of Sciences, Vol. 92, Issue 10
  • DOI: 10.1073/pnas.92.10.4076

Methyl Salicylate Is a Critical Mobile Signal for Plant Systemic Acquired Resistance
journal, October 2007


Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens
journal, September 2005


Brachypodium as an emerging model for cereal–pathogen interactions
journal, March 2015

  • Fitzgerald, Timothy L.; Powell, Jonathan J.; Schneebeli, Katharina
  • Annals of Botany, Vol. 115, Issue 5
  • DOI: 10.1093/aob/mcv010

Rapid Extraction and Analysis of Nonstructural Carbohydrates in Plant Tissues
journal, January 1993


Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato
journal, January 2014

  • Baebler, Š.; Witek, K.; Petek, M.
  • Journal of Experimental Botany, Vol. 65, Issue 4
  • DOI: 10.1093/jxb/ert447

Brachypodium and plant viruses: entwined tools for discovery
journal, January 2020

  • Scholthof, Karen‐Beth G.
  • New Phytologist, Vol. 227, Issue 6
  • DOI: 10.1111/nph.16388

Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases
journal, November 2012

  • Lionetti, Vincenzo; Cervone, Felice; Bellincampi, Daniela
  • Journal of Plant Physiology, Vol. 169, Issue 16
  • DOI: 10.1016/j.jplph.2012.05.006

A Gene Cluster Encoded by Panicum Mosaic Virus Is Associated with Virus Movement
journal, January 2000

  • Turina, Massimo; Desvoyes, Bénédicte; Scholthof, Karen-Beth G.
  • Virology, Vol. 266, Issue 1
  • DOI: 10.1006/viro.1999.0069

Physiology and Molecular Biology of Phenylpropanoid Metabolism
journal, June 1989


The complex subcellular distribution of satellite panicum mosaic virus capsid protein reflects its multifunctional role during infection
journal, June 2008


A Metabolic Profiling Strategy for the Dissection of Plant Defense against Fungal Pathogens
journal, November 2014


Salicylic acid beyond defence: its role in plant growth and development
journal, February 2011

  • Rivas-San Vicente, M.; Plasencia, J.
  • Journal of Experimental Botany, Vol. 62, Issue 10
  • DOI: 10.1093/jxb/err031

Brachypodium : A Monocot Grass Model Genus for Plant Biology
journal, July 2018

  • Scholthof, Karen-Beth G.; Irigoyen, Sonia; Catalan, Pilar
  • The Plant Cell, Vol. 30, Issue 8
  • DOI: 10.1105/tpc.18.00083

Relationships between Salicylic Acid Content, Phenylalanine Ammonia-lyase (PAL) Activity, and Resistance of Barley to Aphid Infestation
journal, March 2003

  • Chaman, Mercedes E.; Copaja, Sylvia V.; Argandoña, Victor H.
  • Journal of Agricultural and Food Chemistry, Vol. 51, Issue 8
  • DOI: 10.1021/jf020953b

Inhibition of Wound-Induced Accumulation of Allene Oxide Synthase Transcripts in Flax Leaves by Aspirin and Salicylic Acid
journal, November 1998

  • Harms, Karsten; Ramirez, Ingrid; Peña-Cortés, Hugo
  • Plant Physiology, Vol. 118, Issue 3
  • DOI: 10.1104/pp.118.3.1057

The structure of satellite panicum mosaic virus at 1.9 Å resolution
journal, October 1995

  • Ban, Nenad; McPherson, Alexander
  • Nature Structural Biology, Vol. 2, Issue 10
  • DOI: 10.1038/nsb1095-882

Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress
journal, June 2010


Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare : Jasmonate signaling and disease resistance
journal, September 1998


Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean
journal, July 2016

  • Shine, M. B.; Yang, Jung‐Wook; El‐Habbak, Mohamed
  • New Phytologist, Vol. 212, Issue 3
  • DOI: 10.1111/nph.14078

Activities of enzymes involved in the phenylpropanoid pathway in constitutively salicylic acid-producing tobacco plants
journal, September 2002

  • Nugroho, Laurentius H.; Verberne, Marianne C.; Verpoorte, Robert
  • Plant Physiology and Biochemistry, Vol. 40, Issue 9
  • DOI: 10.1016/S0981-9428(02)01437-7

Salicylic Acid, a Multifaceted Hormone to Combat Disease
journal, September 2009


Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping
journal, April 2003


Salicylic Acid Interferes with Tobacco Mosaic Virus Replication via a Novel Salicylhydroxamic Acid-Sensitive Mechanism
journal, April 1997

  • Chivasa, Stephen; Murphy, Alex M.; Naylor, Martin
  • The Plant Cell, Vol. 9, Issue 4
  • DOI: 10.2307/3870506

Cell wall reinforcement in cotton hypocotyls in response to a Verticillium dahliae elicitor
journal, March 1997


A dual gene-silencing vector system for monocot and dicot plants
journal, November 2013

  • Liou, Ming-Ru; Huang, Ying-Wen; Hu, Chung-Chi
  • Plant Biotechnology Journal, Vol. 12, Issue 3
  • DOI: 10.1111/pbi.12140

The Immunity Regulator BAK1 Contributes to Resistance Against Diverse RNA Viruses
journal, November 2013

  • Kørner, Camilla Julie; Klauser, Dominik; Niehl, Annette
  • Molecular Plant-Microbe Interactions®, Vol. 26, Issue 11
  • DOI: 10.1094/MPMI-06-13-0179-R

Distinct Roles of Jasmonates and Aldehydes in Plant-Defense Responses
journal, April 2008


Resistance-related physiological response of rice leaves to the compound stress of enhanced UV-B radiation and Magnaporthe oryzae
journal, January 2018


Plastidial Fatty Acid Signaling Modulates Salicylic Acid– and Jasmonic Acid–Mediated Defense Pathways in the Arabidopsis ssi2 Mutant
journal, November 2003

  • Kachroo, Aardra; Lapchyk, Ludmila; Fukushige, Hirotada
  • The Plant Cell, Vol. 15, Issue 12
  • DOI: 10.1105/tpc.017301

Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways?
journal, April 1999


Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance
journal, August 1993


Role of chloroplast trienoic fatty acids in plant disease defense responses: Chloroplast TAs in defense responses
journal, October 2004


Multi-Year Pathogen Survey of Biofuel Switchgrass Breeding Plots Reveals High Prevalence of Infections by Panicum mosaic virus and Its Satellite Virus
journal, August 2015


Arachidonic Acid: An Evolutionarily Conserved Signaling Molecule Modulates Plant Stress Signaling Networks  
journal, October 2010

  • Savchenko, Tatyana; Walley, Justin W.; Chehab, E. Wassim
  • The Plant Cell, Vol. 22, Issue 10
  • DOI: 10.1105/tpc.110.073858