Metabolic patterns in Septoria canker resistant and susceptible Populus trichocarpa genotypes 24 hours post-inoculation

Lenz, Ryan; Louie, Katherine; Sondreli, Kelsey; Galanie, Stephanie; Chen, Jin-Gui; Muchero, Wellington; Bowen, Benjamin; Northen, Trent; Leboldus, Jared

doi:10.1094/phyto-02-21-0053-r

Metabolic patterns in Septoria canker resistant and susceptible Populus trichocarpa genotypes 24 hours post-inoculation

Journal Article · Tue Nov 23 00:00:00 EST 2021 · Phytopathology

DOI:https://doi.org/10.1094/phyto-02-21-0053-r· OSTI ID:1820838

Lenz, Ryan ^[1]; Louie, Katherine ^[2]; Sondreli, Kelsey ^[1]; ^[3]; ^[3]; ^[3]; Bowen, Benjamin ^[2]; Northen, Trent ^[2]; Leboldus, Jared ^[1]

Oregon State Univ., Corvallis, OR (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sphaerulina musiva is an economically and ecologically important fungal pathogen that causes Septoria stem canker and leaf spot disease of Populus species. Here, to bridge the gap between genetic markers and structural barriers previously found to be linked to Septoria (Sphaerulina musiva) canker disease resistance in poplar, we employed hydrophilic interaction liquid chromatography (HILIC) and tandem mass spectrometry (MS/MS) to identify and quantify metabolites involved with signaling and cell wall re-modelling. Fluctuations in signaling molecules, organic acids, amino acids, sterols, phenolics, and saccharides in resistant and susceptible Populus trichocarpa inoculated with Sphaerulina musiva, were observed. The patterns of 222 metabolites in the resistant host implicates systemic acquired resistance (SAR), cell wall apposition, and lignin deposition as modes of resistance to this hemibiotrophic pathogen. This pattern is consistent with the expected response to the biotrophic phase of S. musiva colonization during the first 24 hours post-inoculation. The fungal pathogen metabolized key regulatory signals of SAR, other phenolics, and precursors of lignin biosynthesis which were depleted in the susceptible host. This is the first study to characterize metabolites associated with the response to initial colonization by S. musiva between resistant and susceptible hosts.

View Accepted Manuscript (DOE)

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:: AC02-05CH11231; AC05-00OR22725; SC0018196

OSTI ID:: 1820838

Journal Information:: Phytopathology, Journal Name: Phytopathology Journal Issue: 11 Vol. 111; ISSN 0031-949X

Publisher:: American Phytopathological SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (109)

Using MetaboAnalyst 4.0 for Comprehensive and Integrative Metabolomics Data Analysis Chong, Jasmine; Wishart, David S.; Xia, Jianguo Current Protocols in Bioinformatics, Vol. 68, Issue 1 https://doi.org/10.1002/cpbi.86	journal	September 2019
Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants Smith, Jordan L.; De Moraes, Consuelo M.; Mescher, Mark C. Pest Management Science, Vol. 65, Issue 5 https://doi.org/10.1002/ps.1714	journal	May 2009
The Non-Specific Nature of Defense in Bark and Wood During Wounding, Insect and Pathogen Attack Mullick, D. Bir The Structure, Biosynthesis, and Degradation of Wood https://doi.org/10.1007/978-1-4615-8873-3_10	book	January 1977
Role of castor plant phenolics on performance of its two herbivores and their impact on egg parasitoid behaviour Usha Rani, Pathipati; Pratyusha, Sambangi BioControl, Vol. 59, Issue 5 https://doi.org/10.1007/s10526-014-9590-y	journal	June 2014
Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI) Sumner, Lloyd W.; Amberg, Alexander; Barrett, Dave Metabolomics, Vol. 3, Issue 3 https://doi.org/10.1007/s11306-007-0082-2	journal	September 2007
Flavin Monooxygenase-Generated N-Hydroxypipecolic Acid Is a Critical Element of Plant Systemic Immunity Hartmann, Michael; Zeier, Tatyana; Bernsdorff, Friederike Cell, Vol. 173, Issue 2 https://doi.org/10.1016/j.cell.2018.02.049	journal	April 2018
Pipped at the Post: Pipecolic Acid Derivative Identified as SAR Regulator Shan, Libo; He, Ping Cell, Vol. 173, Issue 2 https://doi.org/10.1016/j.cell.2018.03.045	journal	April 2018
When and how to kill a plant cell: Infection strategies of plant pathogenic fungi Horbach, Ralf; Navarro-Quesada, Aura Rocio; Knogge, Wolfgang Journal of Plant Physiology, Vol. 168, Issue 1 https://doi.org/10.1016/j.jplph.2010.06.014	journal	January 2011
Signaling Mechanisms in Pattern-Triggered Immunity (PTI) Bigeard, Jean; Colcombet, Jean; Hirt, Heribert Molecular Plant, Vol. 8, Issue 4 https://doi.org/10.1016/j.molp.2014.12.022	journal	April 2015
Amino Acid Catabolism in Plants Hildebrandt, Tatjana M.; Nunes Nesi, Adriano; Araújo, Wagner L. Molecular Plant, Vol. 8, Issue 11 https://doi.org/10.1016/j.molp.2015.09.005	journal	November 2015
Signaling cross-talk in plant disease resistance Derksen, Holly; Rampitsch, Christoph; Daayf, Fouad Plant Science, Vol. 207 https://doi.org/10.1016/j.plantsci.2013.03.004	journal	June 2013
Physiology of L-carnitine in plants in light of the knowledge in animals and microorganisms Jacques, Florian; Rippa, Sonia; Perrin, Yolande Plant Science, Vol. 274 https://doi.org/10.1016/j.plantsci.2018.06.020	journal	September 2018
MAGI: A Method for Metabolite Annotation and Gene Integration Erbilgin, Onur; Rübel, Oliver; Louie, Katherine B. ACS Chemical Biology, Vol. 14, Issue 4 https://doi.org/10.1021/acschembio.8b01107	journal	March 2019
Systemic Application of L-Phenylalanine Increases Plant Resistance to Vertebrate Herbivory Grey, Clare B.; Cowan, Dave P.; Langton, Steve D. Journal of Chemical Ecology, Vol. 23, Issue 5 https://doi.org/10.1023/B:JOEC.0000006476.51106.44	journal	May 1997
Networking by small-molecule hormones in plant immunity Pieterse, Corné M. J.; Leon-Reyes, Antonio; Van der Ent, Sjoerd Nature Chemical Biology, Vol. 5, Issue 5 https://doi.org/10.1038/nchembio.164	journal	April 2009
Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants Chanda, Bidisha; Xia, Ye; Mandal, Mihir Kumar Nature Genetics, Vol. 43, Issue 5 https://doi.org/10.1038/ng.798	journal	March 2011
Regulation of pattern recognition receptor signalling in plants Couto, Daniel; Zipfel, Cyril Nature Reviews Immunology, Vol. 16, Issue 9 https://doi.org/10.1038/nri.2016.77	journal	August 2016
Systemic acquired resistance networks amplify airborne defense cues Wenig, Marion; Ghirardo, Andrea; Sales, Jennifer H. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11798-2	journal	August 2019
Exogenous L-Carnitine Promotes Plant Growth and Cell Division by Mitigating Genotoxic Damage of Salt Stress Oney-Birol, Signem Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53542-2	journal	November 2019
Metabolic response induced by parasitic plant-fungus interactions hinder amino sugar and nucleotide sugar metabolism in the host Lee, Dong-Kyu; Ahn, Soohyun; Cho, Hae Yoon Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep37434	journal	November 2016
A medium to enhance identification of Septoria musiva from poplar cankers Stanosz, J. C.; Stanosz, G. R. Forest Pathology, Vol. 32, Issue 3 https://doi.org/10.1046/j.1439-0329.2002.00278.x	journal	June 2002
A molecular mechanism for osmolyte-induced protein stability Street, Timothy O.; Bolen, D. Wayne; Rose, George D. Proceedings of the National Academy of Sciences, Vol. 103, Issue 38 https://doi.org/10.1073/pnas.0606236103	journal	September 2006
Mevalonate governs interdependency of ergosterol and siderophore biosyntheses in the fungal pathogen Aspergillus fumigatus Yasmin, Sabiha; Alcazar-Fuoli, Laura; Gründlinger, Mario Proceedings of the National Academy of Sciences, Vol. 109, Issue 8 https://doi.org/10.1073/pnas.1106399108	journal	November 2011
Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs Hiruma, Kei; Fukunaga, Satoshi; Bednarek, Paweł Proceedings of the National Academy of Sciences, Vol. 110, Issue 23 https://doi.org/10.1073/pnas.1305745110	journal	May 2013
Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen Dhillon, Braham; Feau, Nicolas; Aerts, Andrea L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 11 https://doi.org/10.1073/pnas.1424293112	journal	March 2015
Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns Benedetti, Manuel; Pontiggia, Daniela; Raggi, Sara Proceedings of the National Academy of Sciences, Vol. 112, Issue 17 https://doi.org/10.1073/pnas.1504154112	journal	April 2015
Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant–pathogen interactions in a tree Muchero, Wellington; Sondreli, Kelsey L.; Chen, Jin-Gui Proceedings of the National Academy of Sciences, Vol. 115, Issue 45 https://doi.org/10.1073/pnas.1804428115	journal	October 2018
Isolation of Zeanic Acid, a Natural Plant Growth-regulator from Corn Steep Liquor and Its Chemical Structure Matsushima, Hirochika; Fukumi, Hiroshi; Arima, Kei Agricultural and Biological Chemistry, Vol. 37, Issue 8 https://doi.org/10.1080/00021369.1973.10860910	journal	August 1973
Foliar application of l-phenylalanine and ferulic acids to pea plants: induced phenylalanine ammonia lyase activity and resistance againstErysiphe pisi Bahadur, Amar; Singh, D. P.; Sarma, B. K. Archives Of Phytopathology And Plant Protection, Vol. 45, Issue 4 https://doi.org/10.1080/03235408.2011.587963	journal	February 2012
Recent advances related to poplar leaf spot and canker caused by Septoria musiva : Minireview/Minisynthèse Feau, Nicolas; Mottet, Marie-Josée; Périnet, Pierre Canadian Journal of Plant Pathology, Vol. 32, Issue 2 https://doi.org/10.1080/07060661003740009	journal	June 2010
Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress Slama, Inès; Abdelly, Chedly; Bouchereau, Alain Annals of Botany, Vol. 115, Issue 3 https://doi.org/10.1093/aob/mcu239	journal	January 2015
GlobalANCOVA: exploration and assessment of gene group effects Hummel, M.; Meister, R.; Mansmann, U. Bioinformatics, Vol. 24, Issue 1 https://doi.org/10.1093/bioinformatics/btm531	journal	November 2007
The role of cis -zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions Schäfer, Martin; Brütting, Christoph; Meza-Canales, Ivan David Journal of Experimental Botany, Vol. 66, Issue 16 https://doi.org/10.1093/jxb/erv214	journal	May 2015
Hormonal regulation of secondary cell wall formation Didi, Vojtěch; Jackson, Phil; Hejátko, Jan Journal of Experimental Botany, Vol. 66, Issue 16 https://doi.org/10.1093/jxb/erv222	journal	May 2015
Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner Takagi, Hiroshi; Ishiga, Yasuhiro; Watanabe, Shunsuke Journal of Experimental Botany, Vol. 67, Issue 8 https://doi.org/10.1093/jxb/erw071	journal	March 2016
Modulation of plant autophagy during pathogen attack Leary, Alexandre Y.; Sanguankiattichai, Nattapong; Duggan, Cian Journal of Experimental Botany, Vol. 69, Issue 6 https://doi.org/10.1093/jxb/erx425	journal	December 2017
Combating stress: the interplay between hormone signaling and autophagy in plants Liao, Ching-Yi; Bassham, Diane C. Journal of Experimental Botany, Vol. 71, Issue 5 https://doi.org/10.1093/jxb/erz515	journal	November 2019
MetaboAnalyst 3.0—making metabolomics more meaningful Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv380	journal	April 2015
Populus trichocarpa and Populus deltoides Exhibit Different Metabolomic Responses to Colonization by the Symbiotic Fungus Laccaria bicolor Tschaplinski, Timothy J.; Plett, Jonathan M.; Engle, Nancy L. Molecular Plant-Microbe Interactions, Vol. 27, Issue 6 https://doi.org/10.1094/MPMI-09-13-0286-R	journal	June 2014
Sucrose-Mediated Priming of Plant Defense Responses and Broad-Spectrum Disease Resistance by Overexpression of the Maize Pathogenesis-Related PRms Protein in Rice Plants Gómez-Ariza, Jorge; Campo, Sonia; Rufat, Mar Molecular Plant-Microbe Interactions, Vol. 20, Issue 7 https://doi.org/10.1094/MPMI-20-7-0832	journal	July 2007
Variation in Septoria musiva and Implications for Disease Resistance Screening of Poplars Ward, K. T.; Ostry, M. E. Plant Disease, Vol. 89, Issue 10 https://doi.org/10.1094/PD-89-1077	journal	October 2005
Outbreak of Septoria Canker Caused by Sphaerulina musiva on Populus trichocarpa in Eastern Oregon Søndreli, K. L.; Keriö, S.; Frost, K. Plant Disease, Vol. 104, Issue 12 https://doi.org/10.1094/PDIS-03-20-0494-PDN	journal	December 2020
The Correlation Between Septoria Leaf Spot and Stem Canker Resistance in Hybrid Poplar Dunnell, Kelsey L.; LeBoldus, Jared M. Plant Disease, Vol. 101, Issue 3 https://doi.org/10.1094/PDIS-06-16-0903-RE	journal	March 2017
Identification of Genes Underlying the Resistance to Melampsora larici-populina in an R Gene Supercluster of the Populus deltoides Genome Wei, Suyun; Wu, Huaitong; Li, Xiaoping Plant Disease, Vol. 104, Issue 4 https://doi.org/10.1094/PDIS-08-19-1699-RE	journal	April 2020
The Histology of Hybrid Poplar Clones Inoculated with Septoria musiva Weiland, Jerry E.; Stanosz, Glen R. Plant Disease, Vol. 91, Issue 12 https://doi.org/10.1094/PDIS-91-12-1524	journal	December 2007
Microscopic, Biochemical, and Molecular Comparisons of Moderately Resistant and Susceptible Populus Genotypes Inoculated with Sphaerulina musiva Abraham, Nivi; Chitrampalam, Periasamy; Nelson, Berlin Phytopathology®, Vol. 109, Issue 12 https://doi.org/10.1094/PHYTO-03-19-0105-R	journal	December 2019
Exogenous Trehalose Induces Defenses in Wheat Before and During a Biotic Stress Caused by Powdery Mildew Tayeh, Christine; Randoux, Béatrice; Vincent, Dorothée Phytopathology®, Vol. 104, Issue 3 https://doi.org/10.1094/PHYTO-07-13-0191-R	journal	March 2014
Variability inSeptoria musivain Aggressiveness Krupinsky, J. M. Phytopathology, Vol. 79, Issue 4 https://doi.org/10.1094/Phyto-79-413	journal	January 1989
Vitamin B1 Functions as an Activator of Plant Disease Resistance Ahn, Il-Pyung; Kim, Soonok; Lee, Yong-Hwan Plant Physiology, Vol. 138, Issue 3 https://doi.org/10.1104/pp.104.058693	journal	June 2005
Reduced Carbohydrate Availability Enhances the Susceptibility of Arabidopsis toward Colletotrichum higginsianum Engelsdorf, Timo; Horst, Robin J.; Pröls, Reinhard Plant Physiology, Vol. 162, Issue 1 https://doi.org/10.1104/pp.112.209676	journal	March 2013
A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose Figueroa, Carlos M.; Lunn, John E. Plant Physiology, Vol. 172, Issue 1 https://doi.org/10.1104/pp.16.00417	journal	August 2016
Nucleotide Metabolism in Plants Witte, Claus-Peter; Herde, Marco Plant Physiology, Vol. 182, Issue 1 https://doi.org/10.1104/pp.19.00955	journal	October 2019
The Hot and the Classic Minorsky, Peter V. Plant Physiology, Vol. 128, Issue 1 https://doi.org/10.1104/pp.900014	journal	January 2002
Ethylene Biosynthesis and Signaling Networks Wang, Kevin L. -C.; Li, Hai; Ecker, Joseph R. The Plant Cell, Vol. 14, Issue suppl 1 https://doi.org/10.1105/tpc.001768	journal	May 2002
A Small-Molecule Screen Identifies l-Kynurenine as a Competitive Inhibitor of TAA1/TAR Activity in Ethylene-Directed Auxin Biosynthesis and Root Growth in Arabidopsis He, Wenrong; Brumos, Javier; Li, Hongjiang The Plant Cell, Vol. 23, Issue 11 https://doi.org/10.1105/tpc.111.089029	journal	November 2011
Pipecolic Acid Orchestrates Plant Systemic Acquired Resistance and Defense Priming via Salicylic Acid-Dependent and -Independent Pathways Bernsdorff, Friederike; Döring, Anne-Christin; Gruner, Katrin The Plant Cell, Vol. 28, Issue 1 https://doi.org/10.1105/tpc.15.00496	journal	December 2015
Bacteria Exploit Autophagy for Proteasome Degradation and Enhanced Virulence in Plants Üstün, Suayib; Hafrén, Anders; Liu, Qinsong The Plant Cell, Vol. 30, Issue 3 https://doi.org/10.1105/tpc.17.00815	journal	March 2018
The return of metabolism: biochemistry and physiology of the pentose phosphate pathway: The pentose phosphate pathway Stincone, Anna; Prigione, Alessandro; Cramer, Thorsten Biological Reviews, Vol. 90, Issue 3 https://doi.org/10.1111/brv.12140	journal	September 2014
The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production Ishihara, Atsushi; Hashimoto, Yumi; Tanaka, Chihiro The Plant Journal, Vol. 54, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03441.x	journal	May 2008
Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea Parker, David; Beckmann, Manfred; Zubair, Hassan The Plant Journal, Vol. 59, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.03912.x	journal	September 2009
Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens: Autophagy controls plant basal immunity Lenz, Heike D.; Haller, Eva; Melzer, Eric The Plant Journal, Vol. 66, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04546.x	journal	April 2011
Sugar Alcohols (Polyols) in Fungi and Green Plants. i. Distribution, Physiology and Metabolism Lewis, D. H.; Smith, D. C. New Phytologist, Vol. 66, Issue 2 https://doi.org/10.1111/j.1469-8137.1967.tb05997.x	journal	April 1967
Genome-wide association studies and expression-based quantitative trait loci analyses reveal roles of HCT2 in caffeoylquinic acid biosynthesis and its regulation by defense-responsive transcription factors in Populus Zhang, Jin; Yang, Yongil; Zheng, Kaijie New Phytologist, Vol. 220, Issue 2 https://doi.org/10.1111/nph.15297	journal	July 2018
Salicylic acid activates poplar defense against the biotrophic rust fungus Melampsora larici‐populina via increased biosynthesis of catechin and proanthocyanidins Ullah, Chhana; Tsai, Chung‐Jui; Unsicker, Sybille B. New Phytologist, Vol. 221, Issue 2 https://doi.org/10.1111/nph.15396	journal	August 2018
New insights into the regulation of plant immunity by amino acid metabolic pathways: Amino acid metabolism and plant immunity Zeier, JÜRgen Plant, Cell & Environment, Vol. 36, Issue 12 https://doi.org/10.1111/pce.12122	journal	May 2013
The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism: Purine catabolism in ABA-mediated stress tolerance Watanabe, Shunsuke; Matsumoto, Mayumi; Hakomori, Yuki Plant, Cell & Environment, Vol. 37, Issue 4 https://doi.org/10.1111/pce.12218	journal	November 2013
Metabolomic analysis reveals the potential metabolites and pathogenesis involved in mulberry yellow dwarf disease Gai, Ying-Ping; Han, Xue-Juan; Li, Yi-Qun Plant, Cell & Environment, Vol. 37, Issue 6 https://doi.org/10.1111/pce.12255	journal	January 2014
Signaling by small metabolites in systemic acquired resistance Shah, Jyoti; Chaturvedi, Ratnesh; Chowdhury, Zulkarnain The Plant Journal, Vol. 79, Issue 4 https://doi.org/10.1111/tpj.12464	journal	May 2014
Trehalose metabolism in plants Lunn, John Edward; Delorge, Ines; Figueroa, Carlos María The Plant Journal, Vol. 79, Issue 4 https://doi.org/10.1111/tpj.12509	journal	May 2014
Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms Plett, Jonathan M.; Martin, Francis M. The Plant Journal, Vol. 93, Issue 4 https://doi.org/10.1111/tpj.13802	journal	January 2018
Flavonol rhamnosylation indirectly modifies the cell wall defects of RHAMNOSE BIOSYNTHESIS 1 mutants by altering rhamnose flux Saffer, Adam M.; Irish, Vivian F. The Plant Journal, Vol. 94, Issue 4 https://doi.org/10.1111/tpj.13885	journal	April 2018
A Glucosinolate Metabolism Pathway in Living Plant Cells Mediates Broad-Spectrum Antifungal Defense Bednarek, P.; Pislewska-Bednarek, M.; Svatos, A. Science, Vol. 323, Issue 5910 https://doi.org/10.1126/science.1163732	journal	January 2009
Priming in Systemic Plant Immunity Jung, Ho Won; Tschaplinski, Timothy J.; Wang, Lin Science, Vol. 324, Issue 5923 https://doi.org/10.1126/science.1170025	journal	April 2009
Choline Sulfate in Higher Plants Nissen, Per; Benson, A. A. Science, Vol. 134, Issue 3492 https://doi.org/10.1126/science.134.3492.1759	journal	December 1961
Septoria Canker of Introduced and Native Hybrid Poplars Bier, J. E. Canadian Journal of Research, Vol. 17c, Issue 6 https://doi.org/10.1139/cjr39c-019	journal	June 1939
Discussion: Response of bark tissues to injury and infection Biggs, A. R.; Merrill, W.; Davis, D. D. Canadian Journal of Forest Research, Vol. 14, Issue 3 https://doi.org/10.1139/x84-064	journal	June 1984
Antimicrobial Defenses and Resistance in Forest Trees: Challenges and Perspectives in a Genomic Era Kovalchuk, Andriy; Keriö, Susanna; Oghenekaro, Abbot O. Annual Review of Phytopathology, Vol. 51, Issue 1 https://doi.org/10.1146/annurev-phyto-082712-102307	journal	August 2013
Amino Acids and Plant Diseases van Andel, O. M. Annual Review of Phytopathology, Vol. 4, Issue 1 https://doi.org/10.1146/annurev.py.04.090166.002025	journal	September 1966
Techniques to Study Autophagy in Plants Mitou, Géraldine; Budak, Hikmet; Gozuacik, Devrim International Journal of Plant Genomics, Vol. 2009 https://doi.org/10.1155/2009/451357	journal	August 2009
Integrated transcriptomics and metabolomics decipher differences in the resistance of pedunculate oak to the herbivore Tortrix viridana L. Kersten, Birgit; Ghirardo, Andrea; Schnitzler, Jörg-Peter BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-737	journal	January 2013
Plant hormone-mediated regulation of stress responses Verma, Vivek; Ravindran, Pratibha; Kumar, Prakash P. BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0771-y	journal	April 2016
Identification of a Novel L-rhamnose Uptake Transporter in the Filamentous Fungus Aspergillus niger Sloothaak, Jasper; Odoni, Dorett I.; Martins dos Santos, Vitor A. P. PLOS Genetics, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pgen.1006468	journal	December 2016
The Infection Biology of Sphaerulina musiva: Clues to Understanding a Forest Pathogen Qin, Ruqian; LeBoldus, Jared M. PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0103477	journal	July 2014
Transcriptome Analysis of Poplar during Leaf Spot Infection with Sphaerulina spp. Foster, Adam J.; Pelletier, Gervais; Tanguay, Philippe PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0138162	journal	September 2015
Riboflavin-Induced Disease Resistance Requires the Mitogen-Activated Protein Kinases 3 and 6 in Arabidopsis thaliana Nie, Shengjun; Xu, Huilian PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0153175	journal	April 2016
Characterization of indole-3-pyruvic acid pathway-mediated biosynthesis of auxin in Neurospora crassa Sardar, Puspendu; Kempken, Frank PLOS ONE, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pone.0192293	journal	February 2018
Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi Ohm, Robin A.; Feau, Nicolas; Henrissat, Bernard PLoS Pathogens, Vol. 8, Issue 12 https://doi.org/10.1371/journal.ppat.1003037	journal	December 2012
Biosynthesis of aphidicolin proceeds via the mevalonate pathway in the endophytic fungus Nigrospora sphaerica Lopes, Adriana A.; Pupo, Mônica T. Journal of the Brazilian Chemical Society, Vol. 22, Issue 1 https://doi.org/10.1590/S0103-50532011000100010	journal	January 2011
Systemic Acquired Resistance Ryals, John A.; Neuenschwander, Urs H.; Willits, Michael G. The Plant Cell, Vol. 8, Issue 10 https://doi.org/10.2307/3870231	journal	October 1996
Septoria musiva isolated from cankered stems in hybrid poplar stool beds, Fraser Valley, British Columbia Callan, Brenda North American Fungi https://doi.org/10.2509/pnwf.2007.002.007	journal	January 2007
A Three-Ring Circus: Metabolism of the Three Proteogenic Aromatic Amino Acids and Their Role in the Health of Plants and Animals Parthasarathy, Anutthaman; Cross, Penelope J.; Dobson, Renwick C. J. Frontiers in Molecular Biosciences, Vol. 5 https://doi.org/10.3389/fmolb.2018.00029	journal	April 2018
Insights into Auxin Signaling in Plant?Pathogen Interactions Fu, Jing; Wang, Shiping Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00074	journal	January 2011
Metabolomics of cereals under biotic stress: current knowledge and techniques Balmer, Dirk; Flors, Victor; Glauser, Gaetan Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00082	journal	January 2013
Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs Denancé, Nicolas; Sánchez-Vallet, Andrea; Goffner, Deborah Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00155	journal	January 2013
Source-to-sink transport of sugar and regulation by environmental factors Lemoine, Remi; Camera, Sylvain La; Atanassova, Rossitza Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00272	journal	January 2013
Evaluating plant immunity using mass spectrometry-based metabolomics workflows Heuberger, Adam L.; Robison, Faith M.; Lyons, Sarah Marie A. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00291	journal	June 2014
Metabolic Consequences of Infection of Grapevine (Vitis vinifera L.) cv. “Modra frankinja” with Flavescence Dorée Phytoplasma Prezelj, Nina; Covington, Elizabeth; Roitsch, Thomas Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00711	journal	May 2016
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
Abscisic Acid as Pathogen Effector and Immune Regulator Lievens, Laurens; Pollier, Jacob; Goossens, Alain Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00587	journal	April 2017
Glycans as Modulators of Plant Defense Against Filamentous Pathogens Chaliha, Chayanika; Rugen, Michael D.; Field, Robert A. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00928	journal	July 2018
Signaling Crosstalk between Salicylic Acid and Ethylene/Jasmonate in Plant Defense: Do We Understand What They Are Whispering? Li, Ning; Han, Xiao; Feng, Dan International Journal of Molecular Sciences, Vol. 20, Issue 3 https://doi.org/10.3390/ijms20030671	journal	February 2019
A Guideline to Univariate Statistical Analysis for LC/MS-Based Untargeted Metabolomics-Derived Data Vinaixa, Maria; Samino, Sara; Saez, Isabel Metabolites, Vol. 2, Issue 4 https://doi.org/10.3390/metabo2040775	journal	October 2012
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases Yao, Yushu; Sun, Terence; Wang, Tony Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030431	journal	July 2015
Plant cell wall composition and enzymatic deconstruction Rodrigues Mota, Thatiane; Matias de Oliveira, Dyoni AIMS Bioengineering, Vol. 5, Issue 1 https://doi.org/10.3934/bioeng.2018.1.63	journal	January 2018
Role of glutathione in plant signaling under biotic stress Dubreuil-Maurizi, Carole; Poinssot, Benoît Plant Signaling & Behavior, Vol. 7, Issue 2 https://doi.org/10.4161/psb.18831	journal	February 2012
Toxic and signalling effects of oxalic acid Lehner, Arnaud; Meimoun, Patrice; Errakhi, Rafik Plant Signaling & Behavior, Vol. 3, Issue 9 https://doi.org/10.4161/psb.3.9.6634	journal	September 2008
Amino acid changes during sunflower infection by the necrotrophic fungusB. cinerea Dulermo, Thierry; Bligny, Richard; Gout, Elisabeth Plant Signaling & Behavior, Vol. 4, Issue 9 https://doi.org/10.4161/psb.4.9.9397	journal	September 2009
Phenolic acids act as signaling molecules in plant-microbe symbioses Mandal, Santi M.; Chakraborty, Dipjyoti; Dey, Satyahari Plant Signaling & Behavior, Vol. 5, Issue 4 https://doi.org/10.4161/psb.5.4.10871	journal	April 2010
Glycerol-3-phosphate and systemic immunity Mandal, Mihir K.; Chanda, Bidisha; Xia, Ye Plant Signaling & Behavior, Vol. 6, Issue 11 https://doi.org/10.4161/psb.6.11.17901	journal	November 2011

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