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Title: Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms

Abstract

Summary Microorganisms, or ‘microbes’, have formed intimate associations with plants throughout the length of their evolutionary history. In extant plant systems microbes still remain an integral part of the ecological landscape, impacting plant health, productivity and long‐term fitness. Therefore, to properly understand the genetic wiring of plants, we must first determine what perception systems plants have evolved to parse beneficial from commensal from pathogenic microbes. In this review, we consider some of the most recent advances in how plants respond at the molecular level to different microbial lifestyles. Further, we cover some of the means by which microbes are able to manipulate plant signaling pathways through altered destructiveness and nutrient sinks, as well as the use of effector proteins and micro‐ RNA s (mi RNA s). We conclude by highlighting some of the major questions still to be answered in the field of plant‐microbe research, and suggest some of the key areas that are in greatest need of further research investment. The results of these proposed studies will have impacts in a wide range of plant research disciplines and will, ultimately, translate into stronger agronomic crops and forestry stock, with immune perception and response systems bred to foster beneficial microbialmore » symbioses while repudiating pathogenic symbioses.« less

Authors:
ORCiD logo [1];  [2]
  1. Hawkesbury Institute for the Environment Western Sydney University Richmond NSW 2753 Australia
  2. Institut National de la Recherche Agronomique (INRA) Unité Mixte de Recherche 1136 INRA‐Université de Lorraine Interactions Arbres/Microorganismes Laboratoire d'excellence ARBRE Centre INRA‐Grand Est‐Nancy 54280 Champenoux France
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1417404
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 93 Journal Issue: 4; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Plett, Jonathan M., and Martin, Francis M. Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. United Kingdom: N. p., 2018. Web. doi:10.1111/tpj.13802.
Plett, Jonathan M., & Martin, Francis M. Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. United Kingdom. https://doi.org/10.1111/tpj.13802
Plett, Jonathan M., and Martin, Francis M. Thu . "Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms". United Kingdom. https://doi.org/10.1111/tpj.13802.
@article{osti_1417404,
title = {Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms},
author = {Plett, Jonathan M. and Martin, Francis M.},
abstractNote = {Summary Microorganisms, or ‘microbes’, have formed intimate associations with plants throughout the length of their evolutionary history. In extant plant systems microbes still remain an integral part of the ecological landscape, impacting plant health, productivity and long‐term fitness. Therefore, to properly understand the genetic wiring of plants, we must first determine what perception systems plants have evolved to parse beneficial from commensal from pathogenic microbes. In this review, we consider some of the most recent advances in how plants respond at the molecular level to different microbial lifestyles. Further, we cover some of the means by which microbes are able to manipulate plant signaling pathways through altered destructiveness and nutrient sinks, as well as the use of effector proteins and micro‐ RNA s (mi RNA s). We conclude by highlighting some of the major questions still to be answered in the field of plant‐microbe research, and suggest some of the key areas that are in greatest need of further research investment. The results of these proposed studies will have impacts in a wide range of plant research disciplines and will, ultimately, translate into stronger agronomic crops and forestry stock, with immune perception and response systems bred to foster beneficial microbial symbioses while repudiating pathogenic symbioses.},
doi = {10.1111/tpj.13802},
journal = {The Plant Journal},
number = 4,
volume = 93,
place = {United Kingdom},
year = {Thu Jan 18 00:00:00 EST 2018},
month = {Thu Jan 18 00:00:00 EST 2018}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1111/tpj.13802

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Verticillium Ave1 effector induces tomato defense gene expression independent of Ve1 protein
journal, November 2016


The Xanthomonas Type III Effector Protein AvrBs3 Modulates Plant Gene Expression and Induces Cell Hypertrophy in the Susceptible Host
journal, July 2002

  • Marois, Eric; Van den Ackerveken, Guido; Bonas, Ulla
  • Molecular Plant-Microbe Interactions, Vol. 15, Issue 7
  • DOI: 10.1094/MPMI.2002.15.7.637

Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis
journal, November 2011

  • Sugio, A.; Kingdom, H. N.; MacLean, A. M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 48
  • DOI: 10.1073/pnas.1105664108

Signaling cross-talk in plant disease resistance
journal, June 2013


The Pseudomonas syringae Type III Effector HopAM1 Enhances Virulence on Water-Stressed Plants
journal, March 2008

  • Goel, Ajay K.; Lundberg, Derek; Torres, Miguel A.
  • Molecular Plant-Microbe Interactions, Vol. 21, Issue 3
  • DOI: 10.1094/MPMI-21-3-0361

Harnessing the rhizosphere microbiome through plant breeding and agricultural management
journal, August 2012


Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis
journal, August 2014

  • Liu, Tingli; Song, Tianqiao; Zhang, Xiong
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5686

Pseudomonas syringae Effector Protein AvrB Perturbs Arabidopsis Hormone Signaling by Activating MAP Kinase 4
journal, February 2010


The Pseudomonas syringae effector protein HopZ1a suppresses effector-triggered immunity
journal, July 2010


Cladosporium fulvum Avr4 Protects Fungal Cell Walls Against Hydrolysis by Plant Chitinases Accumulating During Infection
journal, December 2006

  • van den Burg, Harrold A.; Harrison, Stuart J.; Joosten, Matthieu H. A. J.
  • Molecular Plant-Microbe Interactions, Vol. 19, Issue 12
  • DOI: 10.1094/MPMI-19-1420

Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis-wheat interaction: Research review
journal, July 2010


Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014

  • Plett, J. M.; Daguerre, Y.; Wittulsky, S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
  • DOI: 10.1073/pnas.1322671111

Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis
journal, November 2013

  • Tisserant, E.; Malbreil, M.; Kuo, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
  • DOI: 10.1073/pnas.1313452110

Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3
journal, January 2006

  • Kanneganti, Thirumala-Devi; Özören, Nesrin; Body-Malapel, Mathilde
  • Nature, Vol. 440, Issue 7081
  • DOI: 10.1038/nature04517

Soybean miR172c Targets the Repressive AP2 Transcription Factor NNC1 to Activate ENOD40 Expression and Regulate Nodule Initiation
journal, December 2014


The Downy Mildew Effector Proteins ATR1 and ATR13 Promote Disease Susceptibility in Arabidopsis thaliana
journal, December 2007


The Bacterial Effector HopX1 Targets JAZ Transcriptional Repressors to Activate Jasmonate Signaling and Promote Infection in Arabidopsis
journal, February 2014


LYR3, a high-affinity LCO-binding protein of Medicago truncatula , interacts with LYK3, a key symbiotic receptor
journal, May 2016

  • Fliegmann, Judith; Jauneau, Alain; Pichereaux, Carole
  • FEBS Letters, Vol. 590, Issue 10
  • DOI: 10.1002/1873-3468.12191

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015

  • Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
  • Nature Genetics, Vol. 47, Issue 4
  • DOI: 10.1038/ng.3223

Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review: Fungal carbohydrates in the ectomycorrhizal symbiosis
journal, February 2010


Effectiveness of arbuscular mycorrhizal fungi in the protection of olive plants against oxidative stress induced by drought
journal, June 2014

  • Fouad, Mohamed O.; Essahibi, Abdellatif; Benhiba, Laila
  • Spanish Journal of Agricultural Research, Vol. 12, Issue 3
  • DOI: 10.5424/sjar/2014123-4815

Streptomyces -Induced Resistance Against Oak Powdery Mildew Involves Host Plant Responses in Defense, Photosynthesis, and Secondary Metabolism Pathways
journal, September 2014

  • Kurth, Florence; Mailänder, Sarah; Bönn, Markus
  • Molecular Plant-Microbe Interactions, Vol. 27, Issue 9
  • DOI: 10.1094/MPMI-10-13-0296-R

Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria
journal, May 2017


A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize
journal, January 2014


Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants
journal, October 2012


Both the Extracellular Leucine-Rich Repeat Domain and the Kinase Activity of FLS2 Are Required for Flagellin Binding and Signaling in Arabidopsis
journal, May 2001

  • Gómez-Gómez, Lourdes; Bauer, Zsuzsa; Boller, Thomas
  • The Plant Cell, Vol. 13, Issue 5
  • DOI: 10.1105/tpc.13.5.1155

Lectin Receptor Kinases Participate in Protein-Protein Interactions to Mediate Plasma Membrane-Cell Wall Adhesions in Arabidopsis
journal, December 2005

  • Gouget, Anne; Senchou, Virginie; Govers, Francine
  • Plant Physiology, Vol. 140, Issue 1
  • DOI: 10.1104/pp.105.066464

Fungal Effector Protein AVR2 Targets Diversifying Defense-Related Cys Proteases of Tomato
journal, April 2008

  • Shabab, Mohammed; Shindo, Takayuki; Gu, Christian
  • The Plant Cell, Vol. 20, Issue 4
  • DOI: 10.1105/tpc.107.056325

Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways
journal, October 2013


Os8N3 is a host disease-susceptibility gene for bacterial blight of rice
journal, June 2006

  • Yang, B.; Sugio, A.; White, F. F.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
  • DOI: 10.1073/pnas.0604088103

Sesquiterpene emissions from Alternaria alternata and Fusarium oxysporum: Effects of age, nutrient availability and co-cultivation
journal, February 2016

  • Weikl, Fabian; Ghirardo, Andrea; Schnitzler, Jörg-Peter
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep22152

NopL, an Effector Protein of Rhizobium sp. NGR234, Thwarts Activation of Plant Defense Reactions
journal, February 2004

  • Bartsev, Alexander V.; Deakin, William J.; Boukli, Nawal M.
  • Plant Physiology, Vol. 134, Issue 2
  • DOI: 10.1104/pp.103.031740

Transcriptional Responses of Paxillus involutus and Betula pendula During Formation of Ectomycorrhizal Root Tissue
journal, February 2004

  • Johansson, Tomas; Le Quéré, Antoine; Ahren, Dag
  • Molecular Plant-Microbe Interactions, Vol. 17, Issue 2
  • DOI: 10.1094/MPMI.2004.17.2.202

A Thaumatin-Like Protein, Rj4, Controls Nodule Symbiotic Specificity in Soybean
journal, July 2014

  • Hayashi, Masaki; Shiro, Sokichi; Kanamori, Hiroyuki
  • Plant and Cell Physiology, Vol. 55, Issue 9
  • DOI: 10.1093/pcp/pcu099

Global Patterns of Gene Regulation Associated with the Development of Ectomycorrhiza Between Birch ( Betula pendula Roth.) and Paxillus involutus (Batsch) Fr.
journal, July 2005

  • Le Quéré, Antoine; Wright, Derek P.; Söderström, Bengt
  • Molecular Plant-Microbe Interactions, Vol. 18, Issue 7
  • DOI: 10.1094/MPMI-18-0659

Two Cytoplasmic Effectors of Phytophthora sojae Regulate Plant Cell Death via Interactions with Plant Catalases
journal, November 2014


Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors
journal, October 2013


Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus
journal, November 2004


Plant Stomata Function in Innate Immunity against Bacterial Invasion
journal, September 2006


Role of gibberellins during arbuscular mycorrhizal formation in tomato: new insights revealed by endogenous quantification and genetic analysis of their metabolism in mycorrhizal roots
journal, October 2014

  • Martín-Rodríguez, José Ángel; Ocampo, Juan Antonio; Molinero-Rosales, Nuria
  • Physiologia Plantarum, Vol. 154, Issue 1
  • DOI: 10.1111/ppl.12274

Pep1, a Secreted Effector Protein of Ustilago maydis, Is Required for Successful Invasion of Plant Cells
journal, February 2009


A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data
journal, September 2016

  • Spatafora, Joseph W.; Chang, Ying; Benny, Gerald L.
  • Mycologia, Vol. 108, Issue 5
  • DOI: 10.3852/16-042

Oak Root Response to Ectomycorrhizal Symbiosis Establishment: RNA-Seq Derived Transcript Identification and Expression Profiling
journal, May 2014


A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants
journal, June 2004

  • DebRoy, S.; Thilmony, R.; Kwack, Y. -B.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 26
  • DOI: 10.1073/pnas.0401601101

DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis
journal, December 2013

  • Floss, D. S.; Levy, J. G.; Levesque-Tremblay, V.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 51
  • DOI: 10.1073/pnas.1308973110

The type 3 effector NopL of Sinorhizobium sp. strain NGR234 is a mitogen-activated protein kinase substrate
journal, February 2016

  • Ge, Ying-Ying; Xiang, Qi-Wang; Wagner, Christian
  • Journal of Experimental Botany, Vol. 67, Issue 8
  • DOI: 10.1093/jxb/erw065

Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception
journal, September 2017

  • Bozsoki, Zoltan; Cheng, Jeryl; Feng, Feng
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 38
  • DOI: 10.1073/pnas.1706795114

LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection
journal, October 2003


Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016

  • Martin, Francis; Kohler, Annegret; Murat, Claude
  • Nature Reviews Microbiology, Vol. 14, Issue 12
  • DOI: 10.1038/nrmicro.2016.149