Overexpression of a plasma membrane protein generated broad-spectrum immunity in soybean

Ngaki, Micheline N.; Sahoo, Dipak K.; Wang, Bing; Bhattacharyya, Madan K.

doi:10.1111/pbi.13479

Title: Overexpression of a plasma membrane protein generated broad-spectrum immunity in soybean

Journal Article · Fri Oct 09 00:00:00 EDT 2020 · Plant Biotechnology Journal

DOI:https://doi.org/10.1111/pbi.13479· OSTI ID:1815465

^[1]; Sahoo, Dipak K. ^[1]; Wang, Bing ^[1];

^[1]

Iowa State Univ., Ames, IA (United States)

Plants fight-off pathogens and pests by manifesting an array of defence responses using their innate immunity mechanisms. Here we report the identification of a novel soybean gene encoding a plasma membrane protein, transcription of which is suppressed following infection with the fungal pathogen, Fusarium virguliforme. Overexpression of the protein led to enhanced resistance against not only against F. virguliforme, but also against spider mites (Tetranychus urticae, Koch), soybean aphids (Aphis glycines, Matsumura) and soybean cyst nematode (Heterodera glycines). We, therefore, name this protein as Glycine max disease resistance 1 (GmDR1; Glyma.10g094800). The homologues of GmDR1 have been detected only in legumes, cocoa, jute and cotton. The deduced GmDR1 protein contains 73 amino acids. GmDR1 is predicted to contain an ecto- and two transmembrane domains. Transient expression of the green fluorescent protein fused GmDR1 protein in soybean leaves showed that it is a plasma membrane protein. We investigated if chitin, a pathogen-associated molecular pattern (PAMP), common to all pathogen and pests considered in this study, can significantly enhance defence pathways among the GmDR1-overexpressed transgenic soybean lines. Chitin induces marker genes of the salicylic- and jasmonic acid-mediated defence pathways, but suppresses the defence pathway regulated by ethylene. Chitin induced SA- and JA-regulated defence pathways may be one of the mechanisms involved in generating broad-spectrum resistance among the GmDR1-overexpressed transgenic soybean lines against two serious pathogens and two pests including spider mites, against which no known resistance genes have been identified in soybean and among the most other crop species.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1815465

Journal Information:: Plant Biotechnology Journal, Vol. 19, Issue 3; ISSN 1467-7644

Publisher:: Society for Experimental Biology; Association of Applied BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (83)

Humidity assay for studying plant-pathogen interactions in miniature controlled discrete humidity environments with good throughput Xu, Zhen; Jiang, Huawei; Sahu, Binod Bihari Biomicrofluidics, Vol. 10, Issue 3 https://doi.org/10.1063/1.4950998	journal	May 2016
Role of LysM receptors in chitin-triggered plant innate immunity Tanaka, Kiwamu; Nguyen, Cuong T.; Liang, Yan Plant Signaling & Behavior, Vol. 8, Issue 1 https://doi.org/10.4161/psb.22598	journal	January 2013
Position Effect Variegation and Viability Are Both Sensitive to Dosage of Constitutive Heterochromatin in Drosophila Berloco, Maria; Palumbo, Gioacchino; Piacentini, Lucia G3 Genes\|Genomes\|Genetics, Vol. 4, Issue 9 https://doi.org/10.1534/g3.114.013045	journal	September 2014
Detection of fungal and bacterial carbohydrates: Do the similar structures of chitin and peptidoglycan play a role in immune dysfunction? Dworkin, Jonathan PLOS Pathogens, Vol. 14, Issue 10 https://doi.org/10.1371/journal.ppat.1007271	journal	October 2018
DAMPs, MAMPs, and NAMPs in plant innate immunity Choi, Hyong Woo; Klessig, Daniel F. BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0921-2	journal	October 2016
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
The battle for chitin recognition in plant-microbe interactions Sánchez-Vallet, Andrea; Mesters, Jeroen R.; Thomma, Bart P. H. J. FEMS Microbiology Reviews, Vol. 39, Issue 2 https://doi.org/10.1093/femsre/fuu003	journal	February 2015
Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses Sarowar, Sujon; Kim, Young Jin; Kim, Eui Nam Plant Cell Reports, Vol. 24, Issue 4 https://doi.org/10.1007/s00299-005-0928-x	journal	February 2005
Influence of Potassium Fertility on Soybean Aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), Population Dynamics at a Field and Regional Scale Myers, Scott W.; Gratton, Claudio Environmental Entomology, Vol. 35, Issue 2 https://doi.org/10.1603/0046-225X-35.2.219	journal	April 2006
Induction of ethylene inhibits development of soybean sudden death syndrome by inducing defense-related genes and reducing Fusarium virguliforme growth Abdelsamad, Noor A.; MacIntosh, Gustavo C.; Leandro, Leonor F. S. PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0215653	journal	May 2019
Position effect variegation and chromatin proteins Reute, Gunter; Spierer, Pierre BioEssays, Vol. 14, Issue 9 https://doi.org/10.1002/bies.950140907	journal	September 1992
Protein Structure and Function Prediction Using I‐TASSER Yang, Jianyi; Zhang, Yang Current Protocols in Bioinformatics, Vol. 52, Issue 1 https://doi.org/10.1002/0471250953.bi0508s52	journal	December 2015
Quantitative Peptidomics Study Reveals That a Wound-Induced Peptide from PR-1 Regulates Immune Signaling in Tomato Chen, Ying-Lan; Lee, Chi-Ying; Cheng, Kai-Tan The Plant Cell, Vol. 26, Issue 10 https://doi.org/10.1105/tpc.114.131185	journal	October 2014
Germin and Germin-like Proteins: Evolution, Structure, and Function Dunwell, Jim M.; Gibbings, J. George; Mahmood, Tariq Critical Reviews in Plant Sciences, Vol. 27, Issue 5 https://doi.org/10.1080/07352680802333938	journal	September 2008
The Stress-Induced Soybean NAC Transcription Factor GmNAC81 Plays a Positive Role in Developmentally Programmed Leaf Senescence Pimenta, Maiana Reis; Silva, Priscila Alves; Mendes, Giselle Camargo Plant and Cell Physiology, Vol. 57, Issue 5 https://doi.org/10.1093/pcp/pcw059	journal	March 2016
Systemic acquired resistance in soybean is regulated by two proteins, Orthologous to Arabidopsis NPR1 Sandhu, Devinder; Tasma, I. Made; Frasch, Ryan BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-105	journal	August 2009
The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject to Chitin-induced Phosphorylation Petutschnig, Elena K.; Jones, Alexandra M. E.; Serazetdinova, Liliya Journal of Biological Chemistry, Vol. 285, Issue 37 https://doi.org/10.1074/jbc.M110.116657	journal	July 2010
Enhanced resistance to soybean cyst nematode Heterodera glycines in transgenic soybean by silencing putative CLE receptors Guo, Xiaoli; Chronis, Demosthenis; De La Torre, Carola M. Plant Biotechnology Journal, Vol. 13, Issue 6 https://doi.org/10.1111/pbi.12313	journal	January 2015
Comparative transcriptome analysis of soybean response to bean pyralid larvae Zeng, Weiying; Sun, Zudong; Cai, Zhaoyan BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4256-7	journal	November 2017
Wheat PR-1 proteins are targeted by necrotrophic pathogen effector proteins Breen, Susan; Williams, Simon J.; Winterberg, Britta The Plant Journal, Vol. 88, Issue 1 https://doi.org/10.1111/tpj.13228	journal	August 2016
Performance and prospects of Rag genes for management of soybean aphid Hesler, Louis S.; Chiozza, Mariana V.; O'Neal, Matthew E. Entomologia Experimentalis et Applicata, Vol. 147, Issue 3 https://doi.org/10.1111/eea.12073	journal	May 2013
Bacterial disease resistance in Arabidopsis through flagellin perception Zipfel, Cyril; Robatzek, Silke; Navarro, Lionel Nature, Vol. 428, Issue 6984 https://doi.org/10.1038/nature02485	journal	April 2004
Can Plant Defence Mechanisms Provide New Approaches for the Sustainable Control of the Two-Spotted Spider Mite Tetranychus urticae? Agut, Blas; Pastor, Victoria; Jaques, Josep International Journal of Molecular Sciences, Vol. 19, Issue 2 https://doi.org/10.3390/ijms19020614	journal	February 2018
An Acidic PATHOGENESIS-RELATED1 Gene of Oryza grandiglumis is Involved in Disease Resistance Response Against Bacterial Infection Shin, Sang Hyun; Pak, Jung-Hun; Kim, Mi Jin The Plant Pathology Journal, Vol. 30, Issue 2 https://doi.org/10.5423/PPJ.NT.11.2013.0112	journal	June 2014
Cross talk between signaling pathways in pathogen defense Kunkel, Barbara N.; Brooks, David M. Current Opinion in Plant Biology, Vol. 5, Issue 4 https://doi.org/10.1016/S1369-5266(02)00275-3	journal	August 2002
LysM, a widely distributed protein motif for binding to (peptido)glycans Buist, Girbe; Steen, Anton; Kok, Jan Molecular Microbiology, Vol. 68, Issue 4 https://doi.org/10.1111/j.1365-2958.2008.06211.x	journal	May 2008
Elicitors and defense gene induction in plants with altered lignin compositions Gallego-Giraldo, Lina; Posé, Sara; Pattathil, Sivakumar New Phytologist, Vol. 219, Issue 4 https://doi.org/10.1111/nph.15258	journal	June 2018
Soybean Aphid (Hemiptera: Aphididae) Development on Soybean With Rag1 Alone, Rag2 Alone, and Both Genes Combined Wiarda, S. L.; Fehr, W. R.; O'Neal, M. E. Journal of Economic Entomology, Vol. 105, Issue 1 https://doi.org/10.1603/EC11020	journal	February 2012
Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Alexander, D.; Goodman, R. M.; Gut-Rella, M. Proceedings of the National Academy of Sciences, Vol. 90, Issue 15 https://doi.org/10.1073/pnas.90.15.7327	journal	August 1993
Reduced variation in transgene expression from a binary vector with selectable markers at the right and left T-DNA borders Bhattacharyya, Madan K.; Stermer, Bruce A.; Dixon, Richard A. The Plant Journal, Vol. 6, Issue 6 https://doi.org/10.1046/j.1365-313X.1994.6060957.x	journal	December 1994
A LysM Receptor-Like Kinase Plays a Critical Role in Chitin Signaling and Fungal Resistance in Arabidopsis Wan, Jinrong; Zhang, Xue-Cheng; Neece, David The Plant Cell, Vol. 20, Issue 2 https://doi.org/10.1105/tpc.107.056754	journal	February 2008
The MAPK Kinase Kinase GmMEKK1 Regulates Cell Death and Defense Responses Xu, Hui-Yang; Zhang, Chi; Li, Zhen-Chao Plant Physiology, Vol. 178, Issue 2 https://doi.org/10.1104/pp.18.00903	journal	August 2018
The plant immune system Jones, Jonathan D. G.; Dangl, Jeffery L. Nature, Vol. 444, Issue 7117 https://doi.org/10.1038/nature05286	journal	November 2006
Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity Gouhier-Darimont, Caroline; Schmiesing, André; Bonnet, Christelle Journal of Experimental Botany, Vol. 64, Issue 2 https://doi.org/10.1093/jxb/ers362	journal	January 2013
Recognition of Herbivory-Associated Molecular Patterns Mithöfer, Axel; Boland, Wilhelm Plant Physiology, Vol. 146, Issue 3 https://doi.org/10.1104/pp.107.113118	journal	March 2008
RNA-Seq Analysis of a Soybean Near-Isogenic Line Carrying Bacterial Leaf Pustule-Resistant and -Susceptible Alleles Kim, K. H.; Kang, Y. J.; Kim, D. H. DNA Research, Vol. 18, Issue 6 https://doi.org/10.1093/dnares/dsr033	journal	October 2011
Transcriptome profiling of soybean (Glycine max) roots challenged with pathogenic and non-pathogenic isolates of Fusarium oxysporum Lanubile, Alessandra; Muppirala, Usha K.; Severin, Andrew J. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2318-2	journal	December 2015
Revisiting the Soybean GmNAC Superfamily Melo, Bruno P.; Fraga, Otto T.; Silva, José Cleydson F. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01864	journal	December 2018
Conserved nematode signalling molecules elicit plant defenses and pathogen resistance Manosalva, Patricia; Manohar, Murli; von Reuss, Stephan H. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8795	journal	July 2015
Emerging Insights into the Functions of Pathogenesis-Related Protein 1 Breen, Susan; Williams, Simon J.; Outram, Megan Trends in Plant Science, Vol. 22, Issue 10 https://doi.org/10.1016/j.tplants.2017.06.013	journal	October 2017
Transmissibility of Field Isolates of Soybean Viruses by Aphis glycines Clark, A. J.; Perry, K. L. Plant Disease, Vol. 86, Issue 11 https://doi.org/10.1094/PDIS.2002.86.11.1219	journal	November 2002
The Fusarium virguliforme Toxin FvTox1 Causes Foliar Sudden Death Syndrome-Like Symptoms in Soybean Brar, Hargeet K.; Swaminathan, Sivakumar; Bhattacharyya, Madan K. Molecular Plant-Microbe Interactions®, Vol. 24, Issue 10 https://doi.org/10.1094/MPMI-12-10-0285	journal	October 2011
Making a Better Home: Modulation of Plant Defensive Response by Brevipalpus Mites Arena, Gabriella D.; Ramos-González, Pedro L.; Rogerio, Luana A. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01147	journal	August 2018
An Oomycete CRN Effector Reprograms Expression of Plant HSP Genes by Targeting their Promoters Song, Tianqiao; Ma, Zhenchuan; Shen, Danyu PLOS Pathogens, Vol. 11, Issue 12 https://doi.org/10.1371/journal.ppat.1005348	journal	December 2015
Antifungal Proteins Selitrennikoff, Claude P. Applied and Environmental Microbiology, Vol. 67, Issue 7 https://doi.org/10.1128/AEM.67.7.2883-2894.2001	journal	July 2001
Agrobacterium tumefaciens -Mediated Transformation of Maize Embryos Using a Standard Binary Vector System Frame, Bronwyn R.; Shou, Huixia; Chikwamba, Rachel K. Plant Physiology, Vol. 129, Issue 1 https://doi.org/10.1104/pp.000653	journal	May 2002
Integrating marker assisted background analysis with foreground selection for identification of superior bacterial blight resistant recombinants in Basmati rice Gopalakrishnan, S.; Sharma, R. K.; Anand Rajkumar, K. Plant Breeding, Vol. 127, Issue 2 https://doi.org/10.1111/j.1439-0523.2007.01458.x	journal	April 2008
Economic Threshold for Soybean Aphid (Hemiptera: Aphididae) Ragsdale, D. W.; McCornack, B. P.; Venette, R. C. Journal of Economic Entomology, Vol. 100, Issue 4 https://doi.org/10.1093/jee/100.4.1258	journal	August 2007
The Leucine-Rich Repeat Receptor-Like Kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the Cytochrome P450 PHYTOALEXIN DEFICIENT3 Contribute to Innate Immunity to Aphids in Arabidopsis Prince, David C.; Drurey, Claire; Zipfel, Cyril Plant Physiology, Vol. 164, Issue 4 https://doi.org/10.1104/pp.114.235598	journal	February 2014
Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane Bleckmann, Andrea; Weidtkamp-Peters, Stefanie; Seidel, Claus A. M. Plant Physiology, Vol. 152, Issue 1 https://doi.org/10.1104/pp.109.149930	journal	November 2009
A Functional Genomics Approach Identifies Candidate Effectors from the Aphid Species Myzus persicae (Green Peach Aphid) Bos, Jorunn I. B.; Prince, David; Pitino, Marco PLoS Genetics, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pgen.1001216	journal	November 2010
Investigation of the Fusarium virguliforme fvtox1 mutants revealed that the FvTox1 toxin is involved in foliar sudden death syndrome development in soybean Pudake, Ramesh N.; Swaminathan, Sivakumar; Sahu, Binod B. Current Genetics, Vol. 59, Issue 3 https://doi.org/10.1007/s00294-013-0392-z	journal	May 2013
Assessment of conditions affecting Agrobacterium-mediated soybean transformation using the cotyledonary node explant Paz, Margie M.; Shou, Huixia; Guo, Zibiao Euphytica, Vol. 136, Issue 2 https://doi.org/10.1023/B:EUPH.0000030670.36730.a4	journal	January 2004
Plant PRRs and the Activation of Innate Immune Signaling Macho, Alberto P.; Zipfel, Cyril Molecular Cell, Vol. 54, Issue 2 https://doi.org/10.1016/j.molcel.2014.03.028	journal	April 2014
Expression of pathogenesis-related proteins in transplastomic tobacco plants confers resistance to filamentous pathogens under field trials Boccardo, Noelia Ayelen; Segretin, María Eugenia; Hernandez, Ingrid Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-39568-6	journal	February 2019
Disease Resistance Mechanisms in Plants Andersen, Ethan; Ali, Shaukat; Byamukama, Emmanuel Genes, Vol. 9, Issue 7 https://doi.org/10.3390/genes9070339	journal	July 2018
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
Chitosan and chitin oligomers increase phenylalanine ammonia-lyase and tyrosine ammonia-lyase activities in soybean leaves Khan, Wajahatullah; Prithiviraj, Balakrishnan; Smith, Donald L. Journal of Plant Physiology, Vol. 160, Issue 8 https://doi.org/10.1078/0176-1617-00905	journal	January 2003
Beyond the Nucleosome: Epigenetic Aspects of Position–Effect Variegation in Drosophila Wakimoto, Barbara T. Cell, Vol. 93, Issue 3 https://doi.org/10.1016/S0092-8674(00)81159-9	journal	May 1998
Germins: A diverse protein family important for crop improvement Davidson, Rebecca M.; Reeves, Patrick A.; Manosalva, Patricia M. Plant Science, Vol. 177, Issue 6 https://doi.org/10.1016/j.plantsci.2009.08.012	journal	December 2009
Inverse effects of Arabidopsis NPR1 gene on fusarium seedling blight and fusarium head blight in transgenic wheat: Effects of NPR1 on FSB and FHB in wheat Gao, C. -S.; Kou, X. -J.; Li, H. -P. Plant Pathology, Vol. 62, Issue 2 https://doi.org/10.1111/j.1365-3059.2012.02656.x	journal	July 2012
Enhanced Disease Susceptibility1 Mediates Pathogen Resistance and Virulence Function of a Bacterial Effector in Soybean Wang, Jialin; Shine, M. B.; Gao, Qing-Ming Plant Physiology, Vol. 165, Issue 3 https://doi.org/10.1104/pp.114.242495	journal	May 2014
Tanscriptomic Study of the Soybean-Fusarium virguliforme Interaction Revealed a Novel Ankyrin-Repeat Containing Defense Gene, Expression of Whose during Infection Led to Enhanced Resistance to the Fungal Pathogen in Transgenic Soybean Plants Ngaki, Micheline N.; Wang, Bing; Sahu, Binod B. PLOS ONE, Vol. 11, Issue 10 https://doi.org/10.1371/journal.pone.0163106	journal	October 2016
Expression of a Single-Chain Variable-Fragment Antibody Against a Fusarium virguliforme Toxin Peptide Enhances Tolerance to Sudden Death Syndrome in Transgenic Soybean Plants Brar, Hargeet K.; Bhattacharyya, Madan K. Molecular Plant-Microbe Interactions®, Vol. 25, Issue 6 https://doi.org/10.1094/MPMI-12-11-0317	journal	June 2012
Characterization and Biological Function of the ISOCHORISMATE SYNTHASE2 Gene of Arabidopsis Garcion, Christophe; Lohmann, Antje; Lamodière, Elisabeth Plant Physiology, Vol. 147, Issue 3 https://doi.org/10.1104/pp.108.119420	journal	May 2008
Pathogen Effectors Target Arabidopsis EDS1 and Alter Its Interactions with Immune Regulators Bhattacharjee, S.; Halane, M. K.; Kim, S. H. Science, Vol. 334, Issue 6061 https://doi.org/10.1126/science.1211592	journal	December 2011
A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens Liu, Shiming; Kandoth, Pramod K.; Warren, Samantha D. Nature, Vol. 492, Issue 7428 https://doi.org/10.1038/nature11651	journal	October 2012
Investigation of the Fusarium virguliforme Transcriptomes Induced during Infection of Soybean Roots Suggests that Enzymes with Hydrolytic Activities Could Play a Major Role in Root Necrosis Sahu, Binod B.; Baumbach, Jordan L.; Singh, Prashant PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0169963	journal	January 2017
Position effect variegation and imprinting of transgenes in lymphocytes Williams, A.; Harker, N.; Ktistaki, E. Nucleic Acids Research, Vol. 36, Issue 7 https://doi.org/10.1093/nar/gkn085	journal	February 2008
Multiple Phytohormone Signals Control the Transcriptional Response to Soybean Aphid Infestation in Susceptible and Resistant Soybean Plants Studham, Matthew E.; MacIntosh, Gustavo C. Molecular Plant-Microbe Interactions, Vol. 26, Issue 1 https://doi.org/10.1094/MPMI-05-12-0124-FI	journal	January 2013
Effect of Soybean Cultivars Moderately Resistant to Soybean Cyst Nematode on SCN Populations and Yield Adee, Eric A.; Johnson, Martin L.; Niblack, Terry L. Plant Health Progress, Vol. 9, Issue 1 https://doi.org/10.1094/PHP-2008-0618-03-RS	journal	January 2008
Soybean Yield Loss Estimates Due to Diseases in the United States and Ontario, Canada, from 2010 to 2014 Allen, Tom W.; Bradley, Carl A.; Sisson, Adam J. Plant Health Progress, Vol. 18, Issue 1 https://doi.org/10.1094/PHP-RS-16-0066	journal	January 2017
Biochemical and molecular characterization of three barley seed proteins with antifungal properties Leah, R.; Tommerup, H.; Svendsen, I. Journal of Biological Chemistry, Vol. 266, Issue 3 https://doi.org/10.1016/S0021-9258(18)52331-0	journal	January 1991
Hexaacetyl-chitohexaose, a chitin-derived oligosaccharide, transiently activates citrus defenses and alters the feeding behavior of Asian citrus psyllid Shi, Qingchun; George, Justin; Krystel, Joseph Horticulture Research, Vol. 6, Issue 1 https://doi.org/10.1038/s41438-019-0158-y	journal	June 2019
Chitin signaling and plant disease resistance Wan, Jinrong; Zhang, Xue-Cheng; Stacey, Gary Plant Signaling & Behavior, Vol. 3, Issue 10 https://doi.org/10.4161/psb.3.10.5916	journal	October 2008
Overexpression of a soybean salicylic acid methyltransferase gene confers resistance to soybean cyst nematode Lin, Jingyu; Mazarei, Mitra; Zhao, Nan Plant Biotechnology Journal, Vol. 11, Issue 9 https://doi.org/10.1111/pbi.12108	journal	August 2013
Role of Nematode Peptides and Other Small Molecules in Plant Parasitism Mitchum, Melissa G.; Wang, Xiaohong; Wang, Jianying Annual Review of Phytopathology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-phyto-081211-173008	journal	September 2012
Suppression of Soybean Aphid by Generalist Predators Results in a Trophic Cascade in Soybeans Costamagna, Alejandro C.; Landis, Douglas A.; Difonzo, Christina D. Ecological Applications, Vol. 17, Issue 2 https://doi.org/10.1890/06-0284	journal	March 2007
Plant pattern-recognition receptors Zipfel, Cyril Trends in Immunology, Vol. 35, Issue 7 https://doi.org/10.1016/j.it.2014.05.004	journal	July 2014
Characterization of 40 soybean (Glycine max) promoters, isolated from across 5 thematic gene groups Gunadi, Andika; Rushton, Paul J.; McHale, Leah K. Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 127, Issue 1 https://doi.org/10.1007/s11240-016-1038-x	journal	July 2016
Silencing Chitinase Genes Increases Susceptibility of Tetranychus cinnabarinus (Boisduval) to Scopoletin Zhou, Hong; Zhang, Yong-qiang; Lai, Ting BioMed Research International, Vol. 2017 https://doi.org/10.1155/2017/9579736	journal	January 2017
Plant immunity: the EDS1 regulatory node Wiermer, Marcel; Feys, Bart J.; Parker, Jane E. Current Opinion in Plant Biology, Vol. 8, Issue 4 https://doi.org/10.1016/j.pbi.2005.05.010	journal	August 2005
A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat: PR-1 potentially mediates ToxA-induced necrosis Lu, Shunwen; Faris, Justin D.; Sherwood, Robert Molecular Plant Pathology, Vol. 15, Issue 7 https://doi.org/10.1111/mpp.12122	journal	April 2014

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59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES
PAMP
MAMP
HAMP
pattern recognition receptors
PTI
plasma membrane
soybean sudden death syndrome
soybean cyst nematode
spider mites
soybean aphids
disease resistance
chitin

Title: Overexpression of a plasma membrane protein generated broad-spectrum immunity in soybean

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