Plasticity of Phymatotrichopsis omnivora infection strategies is dependent on host and nonhost plant responses

Kankanala, Prasanna; Jones, Piet; Nandety, Raja Sekhar; Jacobson, Daniel A.; Mysore, Kirankumar S.

doi:10.1111/pce.13721

Title: Plasticity of Phymatotrichopsis omnivora infection strategies is dependent on host and nonhost plant responses

Journal Article · Fri Feb 14 00:00:00 EST 2020 · Plant, Cell and Environment

DOI:https://doi.org/10.1111/pce.13721· OSTI ID:1599909

Kankanala, Prasanna ^[1]; Jones, Piet ^[2];

^[1]; Jacobson, Daniel A. ^[2];

^[1]

Noble Research Institute LLC Ardmore Oklahoma
Biosciences DivisionOak Ridge National Laboratory Oak Ridge Tennessee, Bredesen Center for Interdisciplinary StudiesUniversity of Tennessee Knoxville Knoxville Tennessee

Necrotrophic fungi constitute the largest group of plant fungal pathogens that cause heavy crop losses worldwide. Phymatotrichopsis omnivora is a broad host, soil–borne necrotrophic fungal pathogen that infects over 2,000 dicotyledonous plants. The molecular basis of such broad host range is unknown. We conducted cell biology and transcriptomic studies in Medicago truncatula (susceptible), Brachypodium distachyon (resistant/nonhost), and Arabidopsis thaliana (partially resistant) to understand P. omnivora virulence mechanisms. We performed defence gene analysis, gene enrichments, and correlational network studies during key infection stages. We identified that P. omnivora infects the susceptible plant as a traditional necrotroph. However, it infects the partially resistant plant as a hemi–biotroph triggering salicylic acid–mediated defence pathways in the plant. Further, the infection strategy in partially resistant plants is determined by the host responses during early infection stages. Mutant analyses in A. thaliana established the role of small peptides PEP1 and PEP2 in defence against P. omnivora . The resistant/nonhost B. distachyon triggered stress responses involving sugars and aromatic acids. Bdwat1 mutant analysis identified the role of cell walls in defence. This is the first report that describes the plasticity in infection strategies of P. omnivora providing insights into broad host range.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1599909

Alternate ID(s):: OSTI ID: 1599911; OSTI ID: 1648904

Journal Information:: Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Vol. 43 Journal Issue: 4; ISSN 0140-7791

Publisher:: WileyCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 3 works

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References (62)

The Role of TIR-NBS and TIR-X Proteins in Plant Basal Defense Responses Nandety, R. S.; Caplan, J. L.; Cavanaugh, K. PLANT PHYSIOLOGY, Vol. 162, Issue 3 https://doi.org/10.1104/pp.113.219162	journal	June 2013
Error and attack tolerance of complex networks Albert, Réka; Jeong, Hawoong; Barabási, Albert-László Nature, Vol. 406, Issue 6794 https://doi.org/10.1038/35019019	journal	July 2000
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
limma: Linear Models for Microarray Data Smyth, G. K. Bioinformatics and Computational Biology Solutions Using R and Bioconductor https://doi.org/10.1007/0-387-29362-0_23	book	January 2005
Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans , causal agent of blackleg disease Staal, Jens; Kaliff, Maria; Bohman, Svante The Plant Journal, Vol. 46, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02688.x	journal	April 2006
Of PAMPs and Effectors: The Blurred PTI-ETI Dichotomy Thomma, Bart P. H. J.; Nürnberger, Thorsten; Joosten, Matthieu H. A. J. The Plant Cell, Vol. 23, Issue 1 https://doi.org/10.1105/tpc.110.082602	journal	January 2011
Plant immunity: towards an integrated view of plant–pathogen interactions Dodds, Peter N.; Rathjen, John P. Nature Reviews Genetics, Vol. 11, Issue 8 https://doi.org/10.1038/nrg2812	journal	June 2010
Novel Markers of Xylogenesis in Zinnia Are Differentially Regulated by Auxin and Cytokinin Pesquet, Edouard; Ranocha, Philippe; Legay, Sylvain Plant Physiology, Vol. 139, Issue 4 https://doi.org/10.1104/pp.105.064337	journal	November 2005
Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis Sinapidou, Eva; Williams, Kevin; Nott, Lucy The Plant Journal, Vol. 38, Issue 6 https://doi.org/10.1111/j.1365-313X.2004.02099.x	journal	June 2004
Sequencing and functional validation of the JGI Brachypodium distachyon T-DNA collection Hsia, Mon Mandy; O'Malley, Ronan; Cartwright, Amy The Plant Journal, Vol. 91, Issue 3 https://doi.org/10.1111/tpj.13582	journal	June 2017
Cytology of Phymatotrichum root rot of Cotton Seedlings Grown in pure Culture Watkins, G. M. American Journal of Botany, Vol. 25, Issue 2 https://doi.org/10.1002/j.1537-2197.1938.tb09195.x	journal	February 1938
When Is Hub Gene Selection Better than Standard Meta-Analysis? Langfelder, Peter; Mischel, Paul S.; Horvath, Steve PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061505	journal	April 2013
Global Gene Expression Profiling During Medicago truncatula–Phymatotrichopsis omnivora Interaction Reveals a Role for Jasmonic Acid, Ethylene, and the Flavonoid Pathway in Disease Development Uppalapati, Srinivasa Rao; Marek, Stephen M.; Lee, Hee-Kyung Molecular Plant-Microbe Interactions, Vol. 22, Issue 1 https://doi.org/10.1094/MPMI-22-1-0007	journal	January 2009
A look at plant immunity through the window of the multitasking coreceptor BAK1 Yasuda, Shigetaka; Okada, Kentaro; Saijo, Yusuke Current Opinion in Plant Biology, Vol. 38 https://doi.org/10.1016/j.pbi.2017.04.007	journal	August 2017
Heat Shock Proteins: A Review of the Molecular Chaperones for Plant Immunity Park, Chang-Jin; Seo, Young-Su The Plant Pathology Journal, Vol. 31, Issue 4 https://doi.org/10.5423/PPJ.RW.08.2015.0150	journal	December 2015
A Receptor Kinase-Like Protein Encoded by the Rice Disease Resistance Gene, Xa21 Song, W. -Y.; Wang, G. -L.; Chen, L. -L. Science, Vol. 270, Issue 5243 https://doi.org/10.1126/science.270.5243.1804	journal	December 1995
Exogenous Trehalose Treatment Enhances the Activities of Defense-Related Enzymes and Triggers Resistance against Downy Mildew Disease of Pearl Millet Govind, Sharathchandra R.; Jogaiah, Sudisha; Abdelrahman, Mostafa Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01593	journal	November 2016
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence Chinchilla, Delphine; Zipfel, Cyril; Robatzek, Silke Nature, Vol. 448, Issue 7152 https://doi.org/10.1038/nature05999	journal	July 2007
Possible rôle of sugars in restriction of lesion development in finger millet leaves infected with Helminthosporium tetramera Vidhyasekaran, P. Physiological Plant Pathology, Vol. 4, Issue 4 https://doi.org/10.1016/0048-4059(74)90031-9	journal	October 1974
Changes in lipid composition of Blumeria graminis f.sp. tritici conidia produced on wheat leaves treated with heptanoyl salicylic acid Muchembled, J.; Sahraoui, A.; Grandmouginferjani, A. Phytochemistry, Vol. 67, Issue 11 https://doi.org/10.1016/j.phytochem.2006.02.025	journal	June 2006
Metabolic flux towards the (iso)flavonoid pathway in lignin modified alfalfa lines induces resistance against Fusarium oxysporum f. sp. medicaginis Gill, Upinder S.; Uppalapati, Srinivasa R.; Gallego-Giraldo, Lina Plant, Cell & Environment https://doi.org/10.1111/pce.13093	journal	November 2017
Non-targeted Colonization by the Endomycorrhizal Fungus, Serendipita vermifera, in Three Weeds Typically Co-occurring with Switchgrass Ray, Prasun; Guo, Yingqing; Kolape, Jaydeep Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02236	journal	January 2018
WRKY transcription factors Rushton, Paul J.; Somssich, Imre E.; Ringler, Patricia Trends in Plant Science, Vol. 15, Issue 5 https://doi.org/10.1016/j.tplants.2010.02.006	journal	May 2010
The Cloned Gene, Xa21, Confers Resistance to Multiple Xanthomonas oryzae pv. oryzae Isolates in Transgenic Plants Wang, Guo-Liang Molecular Plant-Microbe Interactions, Vol. 9, Issue 9 https://doi.org/10.1094/MPMI-9-0850	journal	January 1996
Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein Hubert, D. A. The EMBO Journal, Vol. 22, Issue 21 https://doi.org/10.1093/emboj/cdg547	journal	November 2003
Danger peptide receptor signaling in plants ensures basal immunity upon pathogen‐induced depletion of BAK 1 Yamada, Kohji; Yamashita‐Yamada, Misuzu; Hirase, Taishi The EMBO Journal, Vol. 35, Issue 1 https://doi.org/10.15252/embj.201591807	journal	November 2015
Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data: Mercator: sequence functional annotation server Lohse, Marc; Nagel, Axel; Herter, Thomas Plant, Cell & Environment, Vol. 37, Issue 5 https://doi.org/10.1111/pce.12231	journal	December 2013
Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis Ranocha, Philippe; Dima, Oana; Nagy, Réka Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3625	journal	October 2013
Sucrose-induced lupine defense against Fusarium oxysporum Morkunas, Iwona; Marczak, Łukasz; Stachowiak, Jerzy Plant Physiology and Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1016/j.plaphy.2005.02.011	journal	April 2005
Roles for Rice Membrane Dynamics and Plasmodesmata during Biotrophic Invasion by the Blast Fungus Kankanala, Prasanna; Czymmek, Kirk; Valent, Barbara The Plant Cell, Vol. 19, Issue 2 https://doi.org/10.1105/tpc.106.046300	journal	February 2007
A set of fluorescent protein-based markers expressed from constitutive and arbuscular mycorrhiza-inducible promoters to label organelles, membranes and cytoskeletal elements in Medicago truncatula Ivanov, Sergey; Harrison, Maria J. The Plant Journal, Vol. 80, Issue 6 https://doi.org/10.1111/tpj.12706	journal	December 2014
PKS5, a SNF1-related kinase, interacts with and phosphorylates NPR1, and modulates expression of WRKY38 and WRKY62 Xie, Changgen; Zhou, Xiaona; Deng, Xingwang Journal of Genetics and Genomics, Vol. 37, Issue 6 https://doi.org/10.1016/S1673-8527(09)60054-0	journal	June 2010
Jasmonate Passes Muster: A Receptor and Targets for the Defense Hormone Browse, John Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.092007	journal	June 2009
Dynamics of cell wall components of Magnaporthe grisea during infectious structure development Fujikawa, Takashi; Kuga, Yukari; Yano, Shigekazu Molecular Microbiology, Vol. 73, Issue 4 https://doi.org/10.1111/j.1365-2958.2009.06786.x	journal	August 2009
Necrotroph Attacks on Plants: Wanton Destruction or Covert Extortion? Laluk, Kristin; Mengiste, Tesfaye The Arabidopsis Book, Vol. 8 https://doi.org/10.1199/tab.0136	journal	January 2010
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools Lamesch, Philippe; Berardini, Tanya Z.; Li, Donghui Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1090	journal	December 2011
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update Tian, Tian; Liu, Yue; Yan, Hengyu Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx382	journal	May 2017
Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis Meyers, Blake C.; Kozik, Alexander; Griego, Alyssa The Plant Cell, Vol. 15, Issue 4 https://doi.org/10.1105/tpc.009308	journal	March 2003
Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors Xu, Xinping; Chen, Chunhong; Fan, Baofang The Plant Cell, Vol. 18, Issue 5 https://doi.org/10.1105/tpc.105.037523	journal	April 2006
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
A role for jasmonate in pathogen defense of Arabidopsis Vijayan, P.; Shockey, J.; Levesque, C. A. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.7209	journal	June 1998
Low Oleic Acid-Derived Repression of Jasmonic Acid-Inducible Defense Responses Requires the WRKY50 and WRKY51 Proteins Gao, Qing-Ming; Venugopal, Srivathsa; Navarre, Duroy Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.166876	journal	October 2010
MTGD: The Medicago truncatula Genome Database Krishnakumar, Vivek; Kim, Maria; Rosen, Benjamin D. Plant and Cell Physiology, Vol. 56, Issue 1 https://doi.org/10.1093/pcp/pcu179	journal	November 2014
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Salicylic Acid, a Multifaceted Hormone to Combat Disease Vlot, A. Corina; Dempsey, D'Maris Amick; Klessig, Daniel F. Annual Review of Phytopathology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.phyto.050908.135202	journal	September 2009
NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Century, K. S.; Holub, E. B.; Staskawicz, B. J. Proceedings of the National Academy of Sciences, Vol. 92, Issue 14 https://doi.org/10.1073/pnas.92.14.6597	journal	July 1995
Ecology of Phymatotrichum Omnivorum Lyda, S. D. Annual Review of Phytopathology, Vol. 16, Issue 1 https://doi.org/10.1146/annurev.py.16.090178.001205	journal	September 1978
Biotrophy-necrotrophy switch in pathogen evoke differential response in resistant and susceptible sesame involving multiple signaling pathways at different phases Chowdhury, Supriyo; Basu, Arpita; Kundu, Surekha Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-17248-7	journal	December 2017
Ethylene as a modulator of disease resistance in plants van Loon, Leendert C.; Geraats, Bart P. J.; Linthorst, Huub J. M. Trends in Plant Science, Vol. 11, Issue 4 https://doi.org/10.1016/j.tplants.2006.02.005	journal	April 2006
CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper Cai, Hanyang; Yang, Sheng; Yan, Yan Journal of Experimental Botany, Vol. 66, Issue 11 https://doi.org/10.1093/jxb/erv125	journal	April 2015
An improved genome release (version Mt4.0) for the model legume Medicago truncatula Tang, Haibao; Krishnakumar, Vivek; Bidwell, Shelby BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-312	journal	January 2014
A Study of the Pathogenic Action of Phymatotrichum Omnivorum Watkins, G. M.; Watkins, Matilde Otero American Journal of Botany, Vol. 27, Issue 4 https://doi.org/10.1002/j.1537-2197.1940.tb14681.x	journal	April 1940
Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors Macho, Alberto P.; Zipfel, Cyril Current Opinion in Microbiology, Vol. 23 https://doi.org/10.1016/j.mib.2014.10.009	journal	February 2015
An efficient algorithm for large-scale detection of protein families Enright, A. J. Nucleic Acids Research, Vol. 30, Issue 7 https://doi.org/10.1093/nar/30.7.1575	journal	April 2002
voom: precision weights unlock linear model analysis tools for RNA-seq read counts Law, Charity W.; Chen, Yunshun; Shi, Wei Genome Biology, Vol. 15, Issue 2 https://doi.org/10.1186/gb-2014-15-2-r29	journal	January 2014
Arabidopsis WRKY38 and WRKY62 Transcription Factors Interact with Histone Deacetylase 19 in Basal Defense Kim, Kang-Chang; Lai, Zhibing; Fan, Baofang The Plant Cell, Vol. 20, Issue 9 https://doi.org/10.1105/tpc.107.055566	journal	September 2008
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
The Danger Model: A Renewed Sense of Self Matzinger, P. Science, Vol. 296, Issue 5566 https://doi.org/10.1126/science.1071059	journal	April 2002
Trehalose induces resistance to powdery mildew in wheat Reignault, Ph.; Cogan, A.; Muchembled, J. New Phytologist, Vol. 149, Issue 3 https://doi.org/10.1046/j.1469-8137.2001.00035.x	journal	March 2001
PEPR2 Is a Second Receptor for the Pep1 and Pep2 Peptides and Contributes to Defense Responses in Arabidopsis Yamaguchi, Yube; Huffaker, Alisa; Bryan, Anthony C. The Plant Cell, Vol. 22, Issue 2 https://doi.org/10.1105/tpc.109.068874	journal	February 2010
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Frost De-acclimation of Barley (Hordeum vulgare L.) and Meadow Fescue (Festuca pratensis Huds.). Relationship between Soluble Carbohydrate Content and Resistance to Frost and the Fungal PathogenBipolaris sorokiniana (Sacc.) Shoem. Rapacz, M. Annals of Botany, Vol. 86, Issue 3 https://doi.org/10.1006/anbo.2000.1214	journal	September 2000

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59 BASIC BIOLOGICAL SCIENCES
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Title: Plasticity of Phymatotrichopsis omnivora infection strategies is dependent on host and nonhost plant responses

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