Use of virus‐induced gene silencing to characterize genes involved in modulating hypersensitive cell death in maize

Murphree, Colin; Kim, Saet‐Byul; Karre, Shailesh; Samira, Rozalynne; Balint‐Kurti, Peter

doi:10.1111/mpp.12999

Title: Use of virus‐induced gene silencing to characterize genes involved in modulating hypersensitive cell death in maize

Journal Article · Sat Oct 10 00:00:00 EDT 2020 · Molecular Plant Pathology

DOI:https://doi.org/10.1111/mpp.12999· OSTI ID:1671835

Murphree, Colin ^[1];

^[1];

^[1]; Samira, Rozalynne ^[2];

^[3]

Department of Entomology and Plant Pathology NC State University Raleigh North Carolina USA
Department of Entomology and Plant Pathology NC State University Raleigh North Carolina USA, Fiber and Biopolymer Research Institute (FBRI) Department of Plant and Soil Science Texas Tech University Texas USA
Department of Entomology and Plant Pathology NC State University Raleigh North Carolina USA, Plant Science Research Unit USDA‐ARS Raleigh North Carolina USA

Abstract Plant disease resistance proteins (R‐proteins) detect specific pathogen‐derived molecules, triggering a defence response often including a rapid localized cell death at the point of pathogen penetration called the hypersensitive response (HR). The maize Rp1‐D21 gene encodes a protein that triggers a spontaneous HR causing spots on leaves in the absence of any pathogen. Previously, we used fine mapping and functional analysis in a Nicotiana benthamiana transient expression system to identify and characterize a number of genes associated with variation in Rp1‐D21 ‐induced HR. Here we describe a system for characterizing genes mediating HR, using virus‐induced gene silencing (VIGS) in a maize line carrying Rp1‐D21 . We assess the roles of 12 candidate genes. Three of these genes, SGT1 , RAR1 , and HSP90 , are required for HR induced by a number of R‐proteins across several plant–pathogen systems. We confirmed that maize HSP90 was required for full Rp1‐D21 ‐induced HR. However, suppression of SGT1 expression unexpectedly increased the severity of Rp1‐D21 ‐induced HR while suppression of RAR1 expression had no measurable effect. We confirmed the effects on HR of two genes we had previously validated in the N. benthamiana system, hydroxycinnamoyltransferase and caffeoyl CoA O‐methyltransferase . We further showed the suppression the expression of two previously uncharacterized, candidate genes, IQ calmodulin binding protein ( IQM3 ) and vacuolar protein sorting protein 37 , suppressed Rp1‐D21 ‐induced HR. This approach is an efficient way to characterize the roles of genes modulating the hypersensitive defence response and other dominant lesion phenotypes in maize.

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Research Organization:: North Carolina State University, Raleigh, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Defense Advanced Research Projects Agency (DARPA); National Science Foundation (NSF)

Grant/Contract Number:: DE‐SC0014116; SC0014116; 60066428; IOS-1444503

OSTI ID:: 1671835

Alternate ID(s):: OSTI ID: 1787152; OSTI ID: 1816588

Journal Information:: Molecular Plant Pathology, Journal Name: Molecular Plant Pathology Vol. 21 Journal Issue: 12; ISSN 1464-6722

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (75)

Maize Homologs of CCoAOMT and HCT, Two Key Enzymes in Lignin Biosynthesis, Form Complexes with the NLR Rp1 Protein to Modulate the Defense Response Wang, Guan-Feng; Balint-Kurti, Peter J. Plant Physiology, Vol. 171, Issue 3 https://doi.org/10.1104/pp.16.00224	journal	May 2016
MAMP (microbe-associated molecular pattern) triggered immunity in plants Newman, Mari-Anne; Sundelin, Thomas; Nielsen, Jon T. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00139	journal	January 2013
Gateway Binary Vectors with the Bialaphos Resistance Gene, bar , as a Selection Marker for Plant Transformation Nakamura, Shinya; Mano, Shoji; Tanaka, Yuji Bioscience, Biotechnology, and Biochemistry, Vol. 74, Issue 6 https://doi.org/10.1271/bbb.100184	journal	June 2010
The HSP90-SGT1 Chaperone Complex for NLR Immune Sensors Shirasu, Ken Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092906	journal	June 2009
Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity Lu, D.; Lin, W.; Gao, X. Science, Vol. 332, Issue 6036 https://doi.org/10.1126/science.1204903	journal	June 2011
Development of a Virus-Induced Gene-Silencing System for Hexaploid Wheat and Its Use in Functional Analysis of the Lr21 -Mediated Leaf Rust Resistance Pathway Scofield, Steven R.; Huang, Li; Brandt, Amanda S. Plant Physiology, Vol. 138, Issue 4 https://doi.org/10.1104/pp.105.061861	journal	July 2005
Molecular and Functional Analyses of a Maize Autoactive NB-LRR Protein Identify Precise Structural Requirements for Activity Wang, Guan-Feng; Ji, Jiabing; EI-Kasmi, Farid PLOS Pathogens, Vol. 11, Issue 2 https://doi.org/10.1371/journal.ppat.1004674	journal	February 2015
Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90: RPS4 expression induces HR in tobacco Zhang, Yan; Dorey, Stephan; Swiderski, Michal The Plant Journal, Vol. 40, Issue 2 https://doi.org/10.1111/j.1365-313X.2004.02201.x	journal	August 2004
Plant Receptor-Like Serine Threonine Kinases: Roles in Signaling and Plant Defense Afzal, Ahmed J.; Wood, Andrew J.; Lightfoot, David A. Molecular Plant-Microbe Interactions®, Vol. 21, Issue 5 https://doi.org/10.1094/MPMI-21-5-0507	journal	May 2008
Developmental programmed cell death in plants Kuriyama, Hideo; Fukuda, Hiroo Current Opinion in Plant Biology, Vol. 5, Issue 6 https://doi.org/10.1016/S1369-5266(02)00305-9	journal	December 2002
Innate Immunity Signaling: Cytosolic Ca ²⁺ Elevation Is Linked to Downstream Nitric Oxide Generation through the Action of Calmodulin or a Calmodulin-Like Protein Ma, Wei; Smigel, Andries; Tsai, Yu-Chang Plant Physiology, Vol. 148, Issue 2 https://doi.org/10.1104/pp.108.125104	journal	August 2008
Genetic Properties of the Maize Nested Association Mapping Population McMullen, M. D.; Kresovich, S.; Villeda, H. S. Science, Vol. 325, Issue 5941 https://doi.org/10.1126/science.1174320	journal	August 2009
Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions Bent, Andrew F.; Mackey, David Annual Review of Phytopathology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.phyto.45.062806.094427	journal	September 2007
Maize death acids, 9-lipoxygenase–derived cyclopente(a)nones, display activity as cytotoxic phytoalexins and transcriptional mediators Christensen, Shawn A.; Huffaker, Alisa; Kaplan, Fatma Proceedings of the National Academy of Sciences, Vol. 112, Issue 36 https://doi.org/10.1073/pnas.1511131112	journal	August 2015
A Connected Set of Genes Associated with Programmed Cell Death Implicated in Controlling the Hypersensitive Response in Maize Olukolu, Bode A.; Negeri, Adisu; Dhawan, Rahul Genetics, Vol. 193, Issue 2 https://doi.org/10.1534/genetics.112.147595	journal	December 2012
siRNA-Finder (si-Fi) Software for RNAi-Target Design and Off-Target Prediction Lück, Stefanie; Kreszies, Tino; Strickert, Marc Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01023	journal	August 2019
Virus-Induced Gene Silencing in Maize with a Foxtail mosaic virus Vector Mei, Yu; Whitham, Steven A. Maize https://doi.org/10.1007/978-1-4939-7315-6_7	book	September 2017
Genetic and Genomic Toolbox of Zea mays Nannas, Natalie J.; Dawe, R. Kelly Genetics, Vol. 199, Issue 3 https://doi.org/10.1534/genetics.114.165183	journal	March 2015
RAR1 Positively Controls Steady State Levels of Barley MLA Resistance Proteins and Enables Sufficient MLA6 Accumulation for Effective Resistance Bieri, Stéphane; Mauch, Stefan; Shen, Qian-Hua The Plant Cell, Vol. 16, Issue 12 https://doi.org/10.1105/tpc.104.026682	journal	November 2004
The pan-genome effector-triggered immunity landscape of a host-pathogen interaction Laflamme, Bradley; Dillon, Marcus M.; Martel, Alexandre Science, Vol. 367, Issue 6479 https://doi.org/10.1126/science.aax4079	journal	February 2020
Recombinant Rp1 genes confer necrotic or nonspecific resistance phenotypes Smith, Shavannor M.; Steinau, Martin; Trick, Harold N. Molecular Genetics and Genomics, Vol. 283, Issue 6 https://doi.org/10.1007/s00438-010-0536-5	journal	May 2010
Optimized cDNA libraries for virus-induced gene silencing (VIGS) using tobacco rattle virus Liu, Enwu; Page, Jonathan E. Plant Methods, Vol. 4, Issue 1 https://doi.org/10.1186/1746-4811-4-5	journal	January 2008
SGT1 and HSP90 are essential for age-related non-host resistance of Nicotiana benthamiana against the oomycete pathogen Phytophthora infestans Shibata, Yusuke; Kawakita, Kazuhito; Takemoto, Daigo Physiological and Molecular Plant Pathology, Vol. 75, Issue 3 https://doi.org/10.1016/j.pmpp.2010.10.001	journal	January 2011
Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes Svitashev, Sergei; Schwartz, Christine; Lenderts, Brian Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13274	journal	November 2016
New Insights into Plant Responses to the Attack from Insect Herbivores Wu, Jianqiang; Baldwin, Ian T. Annual Review of Genetics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-genet-102209-163500	journal	December 2010
A common plant cell-wall protein HyPRP1 has dual roles as a positive regulator of cell death and a negative regulator of basal defense against pathogens: Dual function of plant cell-wall protein HyPRP Yeom, Seon-In; Seo, Eunyoung; Oh, Sang-Keun The Plant Journal, Vol. 69, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04828.x	journal	November 2011
Calmodulin signaling via the IQ motif Bähler, Martin; Rhoads, Allen FEBS Letters, Vol. 513, Issue 1 https://doi.org/10.1016/S0014-5793(01)03239-2	journal	December 2001
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
Resources for Virus-Induced Gene Silencing in the Grasses Scofield, Steven R.; Nelson, Richard S. Plant Physiology, Vol. 149, Issue 1 https://doi.org/10.1104/pp.108.128702	journal	January 2009
Advances in Maize Transformation Technologies and Development of Transgenic Maize Yadava, Pranjal; Abhishek, Alok; Singh, Reeva Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01949	journal	January 2017
The plant hypersensitive response: concepts, control and consequences Balint‐Kurti, Peter Molecular Plant Pathology https://doi.org/10.1111/mpp.12821	journal	July 2019
Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation Cheng, Y. T.; Li, Y.; Huang, S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 35 https://doi.org/10.1073/pnas.1105685108	journal	August 2011
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Molecular Chaperone Hsp90 Associates with Resistance Protein N and Its Signaling Proteins SGT1 and Rar1 to Modulate an Innate Immune Response in Plants Liu, Yule; Burch-Smith, Tessa; Schiff, Michael Journal of Biological Chemistry, Vol. 279, Issue 3 https://doi.org/10.1074/jbc.M310029200	journal	October 2003
Genetic Design and Statistical Power of Nested Association Mapping in Maize Yu, Jianming; Holland, James B.; McMullen, Michael D. Genetics, Vol. 178, Issue 1 https://doi.org/10.1534/genetics.107.074245	journal	January 2008
A maize polygalacturonase functions as a suppressor of programmed cell death in plants He, Yijian; Karre, Shailesh; Johal, Gurmukh S. BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1897-5	journal	July 2019
Silencing of Hydroxycinnamoyl-Coenzyme A Shikimate/Quinate Hydroxycinnamoyltransferase Affects Phenylpropanoid Biosynthesis Hoffmann, Laurent; Besseau, Sébastien; Geoffroy, Pierrette The Plant Cell, Vol. 16, Issue 6 https://doi.org/10.1105/tpc.020297	journal	May 2004
The Development of an Efficient Multipurpose Bean Pod Mottle Virus Viral Vector Set for Foreign Gene Expression and RNA Silencing Zhang, Chunquan; Bradshaw, Jeffrey D.; Whitham, Steven A. Plant Physiology, Vol. 153, Issue 1 https://doi.org/10.1104/pp.109.151639	journal	March 2010
Sgt1p Is a Unique Co-chaperone That Acts as a Client Adaptor to Link Hsp90 to Skp1p Catlett, Michael G.; Kaplan, Kenneth B. Journal of Biological Chemistry, Vol. 281, Issue 44 https://doi.org/10.1074/jbc.M603847200	journal	August 2006
Foxtail Mosaic Virus -Induced Gene Silencing in Monocot Plants Liu, Na; Xie, Ke; Jia, Qi Plant Physiology, Vol. 171, Issue 3 https://doi.org/10.1104/pp.16.00010	journal	May 2016
Characterization of temperature and light effects on the defense response phenotypes associated with the maize Rp1-D21 autoactive resistance gene Negeri, Adisu; Wang, Guan-Feng; Benavente, Larissa BMC Plant Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2229-13-106	journal	January 2013
Reassessing apoptosis in plants Dickman, Martin; Williams, Brett; Li, Yurong Nature Plants, Vol. 3, Issue 10 https://doi.org/10.1038/s41477-017-0020-x	journal	September 2017
Plant Lipoxygenases. Physiological and Molecular Features Porta, Helena; Rocha-Sosa, Mario Plant Physiology, Vol. 130, Issue 1 https://doi.org/10.1104/pp.010787	journal	September 2002
An Alternative Methylation Pathway in Lignin Biosynthesis in Zinnia Ye, Zheng-Hua; Kneusel, Richard E.; Matern, Ulrich The Plant Cell, Vol. 6, Issue 10 https://doi.org/10.2307/3869979	journal	October 1994
Rapid Determination of Gene Function by Virus-induced Gene Silencing in Wheat and Barley Cakir, Cahid; Gillespie, Megan E.; Scofield, Steven R. Crop Science, Vol. 50 https://doi.org/10.2135/cropsci2009.10.0567	journal	March 2010
A Genome-Wide Association Study of the Maize Hypersensitive Defense Response Identifies Genes That Cluster in Related Pathways Olukolu, Bode A.; Wang, Guan-Feng; Vontimitta, Vijay PLoS Genetics, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pgen.1004562	journal	August 2014
A maize cytochrome b–c1 complex subunit protein ZmQCR7 controls variation in the hypersensitive response He, Yijian; Kim, Saet-Byul; Balint-Kurti, Peter Planta, Vol. 249, Issue 5 https://doi.org/10.1007/s00425-019-03092-8	journal	January 2019
A new optical leaf‐clip meter for simultaneous non‐destructive assessment of leaf chlorophyll and epidermal flavonoids Cerovic, Zoran G.; Masdoumier, Guillaume; Ghozlen, NaÏma Ben Physiologia Plantarum, Vol. 146, Issue 3 https://doi.org/10.1111/j.1399-3054.2012.01639.x	journal	June 2012
Characterization of a Brome mosaic virus Strain and Its Use as a Vector for Gene Silencing in Monocotyledonous Hosts Ding, Xin Shun; Schneider, William L.; Chaluvadi, Srinivasa Rao Molecular Plant-Microbe Interactions, Vol. 19, Issue 11 https://doi.org/10.1094/MPMI-19-1229	journal	November 2006
Antagonistic Control of Disease Resistance Protein Stability in the Plant Immune System Holt, B. F. Science, Vol. 309, Issue 5736 https://doi.org/10.1126/science.1109977	journal	August 2005
High-Throughput CRISPR/Cas9 Mutagenesis Streamlines Trait Gene Identification in Maize Liu, Hai-Jun; Jian, Liumei; Xu, Jieting The Plant Cell, Vol. 32, Issue 5 https://doi.org/10.1105/tpc.19.00934	journal	February 2020
Role of SGT1 in resistance protein accumulation in plant immunity Azevedo, Cristina; Betsuyaku, Shigeyuki; Peart, Jack The EMBO Journal, Vol. 25, Issue 9 https://doi.org/10.1038/sj.emboj.7601084	journal	April 2006
The Coiled-Coil and Leucine-Rich Repeat Domain of the Potyvirus Resistance Protein Pvr4 Has a Distinct Role in Signaling and Pathogen Recognition Kim, Saet-Byul; Lee, Hye-Young; Choi, Eun-Hye Molecular Plant-Microbe Interactions®, Vol. 31, Issue 9 https://doi.org/10.1094/MPMI-12-17-0313-R	journal	September 2018
Plant programmed cell death: can't live with it; can't live without it Williams, Brett; Dickman, Marty Molecular Plant Pathology, Vol. 9, Issue 4 https://doi.org/10.1111/j.1364-3703.2008.00473.x	journal	June 2008
Spotted leaf11 , a Negative Regulator of Plant Cell Death and Defense, Encodes a U-Box/Armadillo Repeat Protein Endowed with E3 Ubiquitin Ligase Activity Zeng, Li-Rong; Qu, Shaohong; Bordeos, Alicia The Plant Cell, Vol. 16, Issue 10 https://doi.org/10.1105/tpc.104.025171	journal	September 2004
Arabidopsis E3 ubiquitin ligase PLANT U-BOX13 (PUB13) regulates chitin receptor LYSIN MOTIF RECEPTOR KINASE5 (LYK5) protein abundance Liao, Dehua; Cao, Yangrong; Sun, Xun New Phytologist, Vol. 214, Issue 4 https://doi.org/10.1111/nph.14472	journal	February 2017
The ESCRT machinery Schmidt, Oliver; Teis, David Current Biology, Vol. 22, Issue 4 https://doi.org/10.1016/j.cub.2012.01.028	journal	February 2012
Molecular Characterization of the Maize Rp1-D Rust Resistance Haplotype and Its Mutants Collins, Nicholas; Drake, Jeff; Ayliffe, Michael The Plant Cell, Vol. 11, Issue 7 https://doi.org/10.1105/tpc.11.7.1365	journal	July 1999
Integration of omic networks in a developmental atlas of maize Walley, J. W.; Sartor, R. C.; Shen, Z. Science, Vol. 353, Issue 6301 https://doi.org/10.1126/science.aag1125	journal	August 2016
The U-Box/ARM E3 Ligase PUB13 Regulates Cell Death, Defense, and Flowering Time in Arabidopsis Li, Wei; Ahn, Il-Pyung; Ning, Yuese Plant Physiology, Vol. 159, Issue 1 https://doi.org/10.1104/pp.111.192617	journal	March 2012
To die or not to die? Lessons from lesion mimic mutants Bruggeman, Quentin; Raynaud, CÃ©cile; Benhamed, Moussa Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00024	journal	January 2015
Reconstitution and structure of a plant NLR resistosome conferring immunity Wang, Jizong; Hu, Meijuan; Wang, Jia Science, Vol. 364, Issue 6435 https://doi.org/10.1126/science.aav5870	journal	April 2019
A role for 9-lipoxygenases in maize defense against insect herbivory Woldemariam, Melkamu G.; Ahern, Kevin; Jander, Georg Plant Signaling & Behavior, Vol. 13, Issue 1 https://doi.org/10.1080/15592324.2017.1422462	journal	January 2018
Use of mutant-assisted gene identification and characterization (MAGIC) to identify novel genetic loci that modify the maize hypersensitive response Chaikam, Vijay; Negeri, Adisu; Dhawan, Rahul Theoretical and Applied Genetics, Vol. 123, Issue 6 https://doi.org/10.1007/s00122-011-1641-5	journal	July 2011
ESCRT-I Mediates FLS2 Endosomal Sorting and Plant Immunity Spallek, Thomas; Beck, Martina; Ben Khaled, Sara PLoS Genetics, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pgen.1004035	journal	December 2013
Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking: Oomycete host cell reprogramming Lu, Yi-Ju; Schornack, Sebastian; Spallek, Thomas Cellular Microbiology, Vol. 14, Issue 5 https://doi.org/10.1111/j.1462-5822.2012.01751.x	journal	February 2012
The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana Bos, Jorunn I. B.; Kanneganti, Thirumala-Devi; Young, Carolyn The Plant Journal, Vol. 48, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02866.x	journal	October 2006
The Pepper Calmodulin Gene CaCaM1 Is Involved in Reactive Oxygen Species and Nitric Oxide Generation Required for Cell Death and the Defense Response Choi, Hyong Woo; Lee, Dong Hyuk; Hwang, Byung Kook Molecular Plant-Microbe Interactions®, Vol. 22, Issue 11 https://doi.org/10.1094/MPMI-22-11-1389	journal	November 2009
Staying alive – is cell death dispensable for plant disease resistance during the hypersensitive response? Künstler, András; Bacsó, Renáta; Gullner, Gábor Physiological and Molecular Plant Pathology, Vol. 93 https://doi.org/10.1016/j.pmpp.2016.01.003	journal	January 2016
STRUCTURE AND EVOLUTION OF THE rp1 COMPLEX CONFERRING RUST RESISTANCE IN MAIZE Hulbert, S. H. Annual Review of Phytopathology, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.phyto.35.1.293	journal	September 1997
Structural Basis for Assembly of Hsp90-Sgt1-CHORD Protein Complexes: Implications for Chaperoning of NLR Innate Immunity Receptors Zhang, Minghao; Kadota, Yasuhiro; Prodromou, Chrisostomos Molecular Cell, Vol. 39, Issue 2 https://doi.org/10.1016/j.molcel.2010.05.010	journal	July 2010
Disease Lesion Mimicry Caused by Mutations in the Rust Resistance Gene rp1 Hu, Gongshe; Richter, Todd E.; Hulbert, Scot H. The Plant Cell, Vol. 8, Issue 8 https://doi.org/10.2307/3870307	journal	August 1996
Calmodulin-like Proteins from Arabidopsis and Tomato are Involved in Host Defense Against Pseudomonas syringae pv. tomato Chiasson, David; Ekengren, Sophia K.; Martin, Gregory B. Plant Molecular Biology, Vol. 58, Issue 6 https://doi.org/10.1007/s11103-005-8395-x	journal	August 2005
Recombination at the Rp1 locus of maize Hulbert, Scot H.; Bennetzen, Jeffrey L. Molecular and General Genetics MGG, Vol. 226, Issue 3 https://doi.org/10.1007/BF00260649	journal	May 1991
Programmed cell death in the plant immune system Coll, N. S.; Epple, P.; Dangl, J. L. Cell Death & Differentiation, Vol. 18, Issue 8 https://doi.org/10.1038/cdd.2011.37	journal	April 2011

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59 BASIC BIOLOGICAL SCIENCES
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VIGS

Title: Use of virus‐induced gene silencing to characterize genes involved in modulating hypersensitive cell death in maize

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