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1
Nissinen, R., F. M. Lai, M. J. Laine, et al. "Clavibacter michiganensis subsp. Sepedonicus Elicits a Hypersensitive Response in Tobacco and Secretes Hypersensitive Response-Inducing Protein(s)." Phytopathology® 87, no. 7 (1997): 678–84. http://dx.doi.org/10.1094/phyto.1997.87.7.678.
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Strains of Clavibacter michiganensis subsp. sepedonicus, causal agent of bacterial ring rot of potato, showed marked differences in virulence on host plants. When infiltrated into tobacco leaves, virulent strains caused a rapid localized necrotic response (within 24 to 48 h) characteristic of the hypersensitive response (HR), whereas nonpathogenic strains did not. Concentrated cell-free culture supernatants (CCS) from virulent strains caused a necrotic reaction on tobacco, whereas CCS from nonpathogenic strains did not. The necrosis-inducing activity was heat stable and protease sensitive. Inhibitors of eukaryotic metabolism suppressed the necrotic reaction of tobacco to CCS. No necrotic response was observed when host plants were infiltrated with either cells or CCS from virulent strains. HR-inducing protein(s) from a virulent strain separated from the majority of other proteins on DEAE cellulose at 250 to 300 mM NaCl. Ammonium sulfate-precipitated proteins from a virulent strain produced a necrotic reaction at a total protein concentration of 18 μg/ml, whereas those from a nonpathogenic strain did not, even at a concentration of 180 μg/ml. We conclude that virulent strains of C. michiganensis subsp. sepedonicus elicit a typical HR in tobacco and secrete proteinaceous elicitor(s) of the nonhost HR.
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Zhang, Chu, Annie Tang Gutsche, and Allan D. Shapiro. "Feedback Control of the Arabidopsis Hypersensitive Response." Molecular Plant-Microbe Interactions® 17, no. 4 (2004): 357–65. http://dx.doi.org/10.1094/mpmi.2004.17.4.357.
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The plant hypersensitive response (HR) to avirulent bacterial pathogens results from programmed cell death of plant cells in the infected region. Ion leakage and changes in signaling components associated with HR progression were measured. These studies compared Arabidopsis mutants affecting feedback loops with wild-type plants, with timepoints taken hourly. In response to Pseudomonas syringae pv. tomato DC3000·avrB, npr1-2 mutant plants showed increased ion leakage relative to wild-type plants. Hydrogen peroxide accumulation was similar to that in wild type, but salicylic acid accumulation was reduced at some timepoints. With DC3000·avrRpt2, similar trends were seen. In response to DC3000·avrB, ndr1-1 mutant plants showed more ion leakage than wild-type or npr1-2 plants. Hydrogen peroxide accumulation was delayed by approximately 1 h and reached half the level seen with wild-type plants. Salicylic acid accumulation was similar to npr1-2 mutant plants. With DC3000·avrRpt2, ndr1-1 mutant plants showed no ion leakage, no hydrogen peroxide accumulation, and minimal salicylic acid accumulation. Results with a ndr1-1 and npr1-2 double mutant were similar to ndr1-1. A model consistent with these data is presented, in which one positive and two negative regulatory circuits control HR progression. Understanding this circuitry will facilitate HR manipulation for enhanced disease resistance.
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Kenton, Paul, Luis A. J. Mur, Rainer Atzorn, Claus Wasternack, and John Draper. "(—)-Jasmonic Acid Accumulation in Tobacco Hypersensitive Response Lesions." Molecular Plant-Microbe Interactions® 12, no. 1 (1999): 74–78. http://dx.doi.org/10.1094/mpmi.1999.12.1.74.
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Tobacco infected with Pseudomonas syringae pv. phaseolicola undergoes a hypersensitive response (HR). Jasmonic acid (JA) accumulated within the developing lesion 3 to 9 h after infection and this accumulation preceded protein loss, cell death, and malondialdehyde accumulation. Accumulating JA consisted largely of the (—)-JA stereoisomer and was essentially restricted to the HR lesion.
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Yu, Gong-Xin, Ed Braun, and Roger P. Wise. "Rds and Rih Mediate Hypersensitive Cell Death Independent of Gene-for-Gene Resistance to the Oat Crown Rust Pathogen Puccinia coronata f. sp. avenae." Molecular Plant-Microbe Interactions® 14, no. 12 (2001): 1376–83. http://dx.doi.org/10.1094/mpmi.2001.14.12.1376.
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The Pca crown rust resistance cluster in the diploid Avena genus confers gene-for-gene specificity to numerous isolates of Puccinia coronata f. sp. avenae. Recombination breakpoint analysis indicates that specificities conferred by the Pca cluster are controlled by at least five distinct genes, designated Pc81, Pc82, Pc83, Pc84, and Pc85. Avena plants with the appropriate genotype frequently respond to P. coronata by undergoing hypersensitive cell death at the sites of fungal infection. Autofluorescence of host cells in response to P. coronata occurs in plants that develop visible necrotic lesions but not in plants that lack this phenotype. Two newly described, non-Pc loci were shown to control hypersensitive cell death. Rds (resistance-dependent suppressor of cell death) suppresses the hypersensitive response (HR), but not the resistance, mediated by the Pc82 resistance gene. In contrast, Rih (resistance-independent hypersensitive cell death) confers HR in both resistant and susceptible plants. Linkage analysis indicates that Rds is unlinked to the Pca cluster, whereas Rih is tightly linked to it. These results indicate that multiple synchronous pathways affect the development of hypersensitive cell death and that HR is not essential for resistance to crown rust. Further characterization of these genes will clarify the relationship between plant disease resistance and localized hypersensitive cell death.
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Costet, Laurent, Sylvain Cordelier, Stéphan Dorey, Fabienne Baillieul, Bernard Fritig, and Serge Kauffmann. "Relationship Between Localized Acquired Resistance (LAR) and the Hypersensitive Response (HR): HR Is Necessary for LAR to Occur and Salicylic Acid Is Not Sufficient to Trigger LAR." Molecular Plant-Microbe Interactions® 12, no. 8 (1999): 655–62. http://dx.doi.org/10.1094/mpmi.1999.12.8.655.
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In tobacco plants reacting hypersensitively to pathogen infection, localized acquired resistance (LAR) is induced in a sharp zone surrounding hypersensitive response (HR) lesions. Using a fungal glycoprotein inducing HR and LAR when infiltrated at 50 nM into tobacco leaves, we have shown previously that a plant signal(s) is released by HR cells and diffuses to induce LAR. Here we address two questions: does LAR occur when HR is not induced, and is salicylic acid the (or one of the) mobile LAR signal? We found that application to tobacco leaves of 0.25 nM glycoprotein triggered defense responses without HR and without an H2O2 burst. The analyzed responses include changes in expression of O-methyltransferase (OMT), 3-hydroxy-3-methylglutarylCoA reductase, pathogenesis-related (PR) proteins, and changes in levels of the signal salicylic acid. No defense responses and no increased resistance to tobacco mosaic virus infection were found beyond the elicitor-infiltrated tissue, providing strong evidence that there is no LAR without HR. Treatments of NahG tobacco leaves with 50 nM elicitor induced the HR and, in the sharp zone surrounding the HR lesion, a strong activation of OMT and of basic PR proteins, but not of acidic PR-1 proteins. This indicates that a signal different from salicylic acid is diffusing.
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Dardick, Christopher D., and James N. Culver. "Tobamovirus Coat Proteins: Elicitors of the Hypersensitive Response in Solanum melongena (Eggplant)." Molecular Plant-Microbe Interactions® 10, no. 6 (1997): 776–78. http://dx.doi.org/10.1094/mpmi.1997.10.6.776.
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Solanum melongena (eggplant) exhibits a hypersensitive response (HR) when infected with tobacco mosaic tobamovirus (TMV). In contrast, a TMV mutant unable to express coat protein (CP) did not elicit the HR, while a potexvirus vector engineered to express TMV CP did elicit the eggplant HR. The CPs of U2 and odontoglossum ringspot tobamoviruses also elicited the HR. However, the HR was not elicited by the CP of cucumber green mottle mosaic tobamovirus. Taken together, these findings demonstrate that specific tobamovirus CPs function as elicitors of the eggplant HR.
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Johansson, Oskar N., Anders K. Nilsson, Mikael B. Gustavsson, Thomas Backhaus, Mats X. Andersson, and Mats Ellerström. "A quick and robust method for quantification of the hypersensitive response in plants." PeerJ 3 (December 1, 2015): e1469. http://dx.doi.org/10.7717/peerj.1469.
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One of the most studied defense reactions of plants against microbial pathogens is the hypersensitive response (HR). The HR is a complex multicellular process that involves programmed cell death at the site of infection. A standard method to quantify plant defense and the HR is to measure the release of cellular electrolytes into water after infiltration with pathogenic bacteria. In this type of experiment, the bacteria are typically delivered into the plant tissue through syringe infiltration. Here we report the development of a vacuum infiltration protocol that allows multiple plant lines to be infiltrated simultaneously and assayed for defense responses. Vacuum infiltration did not induce more wounding response in Arabidopsis leaf tissue than syringe inoculation, whereas throughput and reproducibility were improved. The method was used to study HR-induced electrolyte loss after treatment with the bacteriumPseudomonas syringaepv.tomatoDC3000 harboring the effector AvrRpm1, AvrRpt2 or AvrRps4. Specifically, the influence of bacterial titer on AvrRpm1-induced HR was investigated. Not only the amplitude, but also the timing of the maximum rate of the HR reaction was found to be dose-dependent. Finally, using vacuum infiltration, we were able quantify induction of phospholipase D activity after AvrRpm1 recognition in leaves labeled with33PO4.
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Hajimorad, M. R., and J. H. Hill. "Rsv1-Mediated Resistance Against Soybean mosaic virus-N Is Hypersensitive Response-Independent at Inoculation Site, but Has the Potential to Initiate a Hypersensitive Response-like Mechanism." Molecular Plant-Microbe Interactions® 14, no. 5 (2001): 587–98. http://dx.doi.org/10.1094/mpmi.2001.14.5.587.
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Rsv1, a single dominant gene in soybean PI 96983, confers resistance to most strains of Soybean mosaic virus (SMV), including strain G2. The phenotypic response includes the lack of symptoms and virus recovery from mechanically inoculated leaves. To study the resistance mechanism, SMV-N (an isolate of strain G2) was introduced into PI 96983 by grafting. Hypersensitive response (HR)-like lesions occurred on the stems, petioles, and leaf veins, and virus was recovered from these lesions. The response demonstrated the cytological and histological characteristics of HR as well as elevated transcription of a soybean salicylic acid-inducible, pathogenesis-related (PR-1) protein gene. Mechanical inoculation of PI 96983 primary leaves with a high level of SMV-N virions caused no symptoms or up regulation of the PR-1 protein gene transcript. Furthermore, inoculation with infectious viral RNA did not alter the resistance phenotype. The data suggest that interaction of SMV-N with Rsv1 has the potential to induce an HR-like defense reaction. Rsv1-mediated resistance in the inoculated leaf, however, is HR-independent and operates after virion disassembly.
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Gassmann, Walter. "Natural Variation in the Arabidopsis Response to the Avirulence Gene hopPsyA Uncouples the Hypersensitive Response from Disease Resistance." Molecular Plant-Microbe Interactions® 18, no. 10 (2005): 1054–60. http://dx.doi.org/10.1094/mpmi-18-1054.
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The plant hypersensitive response (HR) is tightly associated with gene-for-gene resistance and has been proposed to function in containing pathogens at the invasion site. This tight association has made it difficult to unequivocally evaluate the importance of HR for plant disease resistance. Here, hopPsyA from Pseudomonas syringae pv. syringae 61 is identified as a new avirulence gene for Arabidopsis that triggers resistance in the absence of macroscopic HR. Resistance to P. syringae pv. tomato DC3000 expressing hopPsyA was EDS1-dependent and NDR1-independent. Intriguingly, several Arabidopsis accessions were resistant to DC3000(hopPsyA) in the absence of HR. This is comparable to the Arabidopsis response to avrRps4, but it is shown that hopPsyA does not signal through RPS4. In a cross between two hopPsyA-resistant accessions that differ in their HR response, the HR segregated as a recessive phenotype regulated by a single locus. This locus, HED1 (HR regulator in EDS1 pathway), is proposed to encode a protein whose activity can cause suppression of the EDS1-dependent HR signaling pathway. HED1-regulated symptomless gene-for-gene resistance responses may explain some cases of Arabidopsis resistance to bacteria that are classified as nonhost resistance.
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Guidetti-Gonzalez, Simone, Juliana Freitas-Astúa, Alexandre Morais do Amaral, et al. "Genes associated with hypersensitive response (HR) in the citrus EST database (CitEST)." Genetics and Molecular Biology 30, no. 3 suppl (2007): 943–56. http://dx.doi.org/10.1590/s1415-47572007000500022.
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Wang, Wei-Chang, and Zin-Huang Liu. "HarpinPSS-induced peroxidase and lignin accumulation in tobacco during the hypersensitive response." Functional Plant Biology 26, no. 3 (1999): 265. http://dx.doi.org/10.1071/pp98130.
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Harpinpss, a pathogenic protein encoded by hrpZ in the hrp gene cluster of Pseudomonas syringae pv. syringae, induces the hypersensitive response (HR) in tobacco (Nicotiana tabacum L. cv. Xanthi). An increase in peroxidase activity, lignin content and salicylic acid was observed during the HR elicited by harpin. The increase in anionic, moderately anionic and cationic peroxidase isozymes is positively correlated with the HR in tobacco. In addition, the increase of the anionic peroxidase isozyme (pI 3.5) is correlated with a rise of the transcript of the encoding gene.
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Jakobek, J. L., J. A. Smith-Becker, and P. B. Lindgren. "A Bean cDNA Expressed During a Hypersensitive Reaction Encodes a Putative Calcium-Binding Protein." Molecular Plant-Microbe Interactions® 12, no. 8 (1999): 712–19. http://dx.doi.org/10.1094/mpmi.1999.12.8.712.
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The hypersensitive reaction (HR) is an inducible plant response that is associated with disease resistance. It is characterized by rapid, localized cell death at the site of infection and is believed to inhibit the spread of invading pathogens. We have isolated a cDNA clone, designated Hra32 (for hypersensitive reaction associated), corresponding to an RNA transcript that accumulates in bean during an HR. The predicted protein product of the Hra32 cDNA is an approximately 17 kDa protein of 161 amino acids, with four putative EF-hand calcium-binding domains. The temporal pattern of Hra32 transcript accumulation correlated closely with the onset of the HR in bean after inoculation with incompatible Pseudomonas syringae pv. tabaci and pv. tomato and with tobacco necrosis virus. Hra32 transcript also accumulated in bean in response to compatible P. syringae pv. phaseolicola and was correlated with necrotic cell death associated with disease lesion formation. A more transient pattern of Hra32 transcript accumulation occurred in bean in response to general stimuli that did not result in the HR or host cell death. These treatments included infiltration with a P. syringae pv. tabaci Hrp¯ mutant, P. syringae pv. tabaci cells treated with kanamycin, Escherichia coli, P. fluorescens, or glutathione, and in response to wounding. Thus, there was differential accumulation of the Hra32 transcript in response to specific stimuli resulting in the HR, compared with general stimuli that did not result in cell death. We hypothesize that the Hra32 product may be a component of the pathway that leads to hypersensitive cell death.
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Kamoun, Sophien, Walid Hamada, and Edgar Huitema. "Agrosuppression: A Bioassay for the Hypersensitive Response Suited to High-Throughput Screening." Molecular Plant-Microbe Interactions® 16, no. 1 (2003): 7–13. http://dx.doi.org/10.1094/mpmi.2003.16.1.7.
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We describe a novel method, agrosuppression, that addresses the need for an assay of the hypersensitive response (HR) in intact plants that is rapid and adapted to high-throughput functional screening of plant and pathogen genes. The agrosuppression assay is based on inoculation of intact plants with a mixture of Agrobacterium tumefaciens strains carrying (i) a binary plasmid with one or more candidate HR-inducing genes and (ii) a tumor-inducing (oncogenic) T-DNA. In the absence of HR induction, tumor formation is initiated, resulting in a typical crown gall phenotype. However, upon induction of the HR, tumor formation by the oncogenic T-DNA is suppressed, resulting in a phenotype that can be readily scored. We tested and optimized agrosuppression in Nicotiana benthamiana using the inf1 elicitin gene from the oomycete pathogen Phytophthora infestans, which specifically induces the HR in Nicotiana spp., and the gene-for-gene pair Avr9/Cf-9 from the fungal pathogen Cladosporium fulvum and Lycopersicon pimpinellifolium (currant tomato), respectively. Agrosuppression protocols that can be rapidly performed using simple mechanical wounding of petioles of intact N. benthamiana plants were developed and appeared particularly adapted to intensive high-throughput screening. This assay promises to greatly facilitate the cloning of novel plant R genes and pathogen Avr genes and to accelerate functional analyses and structure-function studies of these genes.
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Palanichelvam, Karuppaiah, Anthony B. Cole, Monir Shababi, and James E. Schoelz. "Agroinfiltration of Cauliflower mosaic virus Gene VI Elicits Hypersensitive Response in Nicotiana Species." Molecular Plant-Microbe Interactions® 13, no. 11 (2000): 1275–79. http://dx.doi.org/10.1094/mpmi.2000.13.11.1275.
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Cauliflower mosaic virus strain W260 induces hypersensitive response (HR) in Nicotiana edwardsonii and systemic cell death in N. clevelandii. In contrast, the D4 strain of Cauliflower mosaic virus evades the host defenses in Nicotiana species; it induces chlorotic primary lesions and a systemic mosaic in both hosts. Previous studies with chimeric viruses had indicated that gene VI of W260 was responsible for elicitation of HR or cell death. To prove conclusively that W260 gene VI is responsible, we inserted gene VI of W260 and D4 into the Agrobacterium tumefaciens binary vector pKYLX7. Agroinfiltration of these constructs into the leaves of N. edwardsonii and N. clevelandii revealed that gene VI of W260 elicited HR in N. edwardsonii 4 to 5 days after infiltration and cell death in N. clevelandii approximately 9 to 12 days after infiltration. In contrast, gene VI of D4 did not elicit HR or cell death in either Nicotiana species. A frameshift mutation introduced into gene VI of W260 abolished its ability to elicit HR or cell death in both Nicotiana species, demonstrating that the elicitor is the gene VI protein.
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Padgett, Hal S., Yuichiro Watanabe, and Roger N. Beachy. "Identification of the TMV Replicase Sequence That Activates the N Gene-Mediated Hypersensitive Response." Molecular Plant-Microbe Interactions® 10, no. 6 (1997): 709–15. http://dx.doi.org/10.1094/mpmi.1997.10.6.709.
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The N gene-mediated hypersensitive response (HR) in tobacco provides a high degree of resistance against most tobamoviruses by halting the progress of infection at the site of inoculation. A previous report indicated a role for the 126/183-kDa replicase in induction of the HR in tobacco containing the N gene (H. S. Padgett and R. N. Beachy, Plant Cell 5:577-586, 1993). Chimeric virus genomes were constructed in which the genes encoding the 126/183-kDa proteins of the HR-eliciting pathogen, tobacco mosaic virus (TMV), and the resistance breaking tobamovirus, Ob, were exchanged. Inoculation of the chimeric viruses to leaves of Nicotiana tabacum cv. Xanthi NN confirmed that either the replicase protein of TMV or its mRNA was responsible for induction of HR. An expression vector based on the Ob virus was used to express fragments of various replicase genes. With this approach, it was determined that the HR is caused by a portion of the replicase protein extending from amino acid 692 to 1116. Consistent with this result, Ob mutants that induce the HR on NN tobacco were found to carry mutations within the same portion of the replicase gene. The N gene-mediated HR is inactive at high temperatures, yet these mutants were able to overcome the HR at significantly lower temperatures than could TMV, indicating that the temperature sensitivity of the N gene response is manifested at the level of interaction between the virus and the defense response mechanism.
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Zhu, Yu-Xiu, Chunxia Ge, Shijun Ma, et al. "Maize ZmFNSI Homologs Interact with an NLR Protein to Modulate Hypersensitive Response." International Journal of Molecular Sciences 21, no. 7 (2020): 2529. http://dx.doi.org/10.3390/ijms21072529.
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Nucleotide binding, leucine-rich-repeat (NLR) proteins are the major class of resistance (R) proteins used by plants to defend against pathogen infection. The recognition between NLRs and their cognate pathogen effectors usually triggers a rapid localized cell death, termed the hypersensitive response (HR). Flavone synthase I (FNSI) is one of the key enzymes in the flavone biosynthesis pathway. It also displays salicylic acid (SA) 5-hydroxylase (S5H) activity. A close homolog of FNSI/S5H displays SA 3-hydroxylase (S3H) activity. Both FNSI/S5H and S3H play important roles in plant innate immunity. However, the underlying molecular mechanisms and the relationship between S5H and S3H with the NLR-mediated HR are not known in any plant species. In this study, we identified three genes encoding ZmFNSI-1, ZmFNSI-2 and ZmS3H that are significantly upregulated in a maize line carrying an autoactive NLR Rp1-D21 mutant. Functional analysis showed that ZmFNSI-1 and ZmFNSI-2, but not ZmS3H, suppressed HR conferred by Rp1-D21 and its signaling domain CCD21 when transiently expressed in N. benthamiana. ZmFNSI-1 and ZmFNSI-2 physically interacted with CCD21. Furthermore, ZmFNSI-1 and ZmFNSI-2 interacted with HCT, a key enzyme in lignin biosynthesis pathway, which can also suppress Rp1-D21-mediated HR. These results lay the foundation for the further functional analysis of the roles of FNSI in plant innate immunity.
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Gabriëls, Suzan H. E. J., Frank L. W. Takken, Jack H. Vossen, et al. "cDNA-AFLP Combined with Functional Analysis Reveals Novel Genes Involved in the Hypersensitive Response." Molecular Plant-Microbe Interactions® 19, no. 6 (2006): 567–76. http://dx.doi.org/10.1094/mpmi-19-0567.
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To identify genes required for the hypersensitive response (HR), we performed expression profiling of tomato plants mounting a synchronized HR, followed by functional analysis of differentially expressed genes. By cDNA-AFLP analysis, the expression profile of tomato plants containing both the Cf-4 resistance gene against Cladosporium fulvum and the matching Avr4 avirulence gene of this fungus was compared with that of control plants. About 1% of the transcript-derived fragments (442 out of 50,000) were derived from a differentially expressed gene. Based on their sequence and expression, 192 fragments, referred to as Avr4-responsive tomato (ART) fragments, were selected for VIGS (virus-induced gene silencing) in Cf-4-transgenic Nicotiana benthamiana. Inoculated plants were analyzed for compromised HR by agroinfiltration of either the C. fulvum Avr4 gene or the Inf1 gene of Phytophthora infestans, which invokes a HR in wild-type N. benthamiana. VIGS using 15 of the ART fragments resulted in a compromised HR, whereas VIGS with fragments of ART genes encoding HSP90, a nuclear GTPase, an L19 ribosomal protein, and most interestingly, a nucleotide binding-leucine rich repeat (NB-LRR)-type protein severely suppressed the HR induced both by Avr4 and Inf1. Requirement of an NB-LRR protein (designated NRC1, for NB-LRR protein required for HR-associated cell death 1) for Cf resistance protein function as well as Inf1-mediated HR suggests a convergence of signaling pathways and supports the recent observation that NB-LRR proteins play a role in signal transduction cascades downstream of resistance proteins.
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Yu, Z. H., J. F. Wang, R. E. Stall, and C. E. Vallejos. "Genomic localization of tomato genes that control a hypersensitive reaction to Xanthomonas campestris pv. vesicatoria (Doidge) dye." Genetics 141, no. 2 (1995): 675–82. http://dx.doi.org/10.1093/genetics/141.2.675.
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Abstract Xanthomonas campestris pv. vesicatoria causes bacterial spot, one of the most serious diseases of tomatoes. The lycopersicon esculentum accession 'Hawaii 7998' is the only reliable source of resistance to race 1 strains of the pathogen. This resistance is associated with a hypersensitive reaction controlled by multiple nondominant genes. The inoculated area becomes fully necrotic 24 hr after inoculation in 'Hawaii 7998,' whereas full necrosis is observed 5 and 4 days after inoculation in the susceptible species L. pennellii (LA 716) and their F1, respectively. An interspecific backcross population, using 'Hawaii 7998' as the recurrent parent, was analyzed to determine the linkage relationships between the resistance genes and 135 molecular marker loci. The range of responses of the BC1 population included those of the parents. Linkage to a hypersensitive response factor was assessed by comparing the rates of necrosis development between homozygous and heterozygous plants at 8 hr-intervals. Three factors that affect the hypersensitive response of 'Hawaii 7998' were detected. One factor is on the short arm of chromosome I, another on the long arm of chromosome I, and a third on the long arm of chromosome 5. These factors appeared to act independently and to have additive effects.
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Ramachandran, Sowmya R., Chuntao Yin, Joanna Kud, et al. "Effectors from Wheat Rust Fungi Suppress Multiple Plant Defense Responses." Phytopathology® 107, no. 1 (2017): 75–83. http://dx.doi.org/10.1094/phyto-02-16-0083-r.
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Fungi that cause cereal rust diseases (genus Puccinia) are important pathogens of wheat globally. Upon infection, the fungus secretes a number of effector proteins. Although a large repository of putative effectors has been predicted using bioinformatic pipelines, the lack of available high-throughput effector screening systems has limited functional studies on these proteins. In this study, we mined the available transcriptomes of Puccinia graminis and P. striiformis to look for potential effectors that suppress host hypersensitive response (HR). Twenty small (<300 amino acids), secreted proteins, with no predicted functions were selected for the HR suppression assay using Nicotiana benthamiana, in which each of the proteins were transiently expressed and evaluated for their ability to suppress HR caused by four cytotoxic effector‐R gene combinations (Cp/Rx, ATR13/RPP13, Rpt2/RPS‐2, and GPA/RBP‐1) and one mutated R gene—Pto(Y207D). Nine out of twenty proteins, designated Shr1 to Shr9 (suppressors of hypersensitive response), were found to suppress HR in N. benthamiana. These effectors varied in the effector-R gene defenses they suppressed, indicating these pathogens can interfere with a variety of host defense pathways. In addition to HR suppression, effector Shr7 also suppressed PAMP-triggered immune response triggered by flg22. Finally, delivery of Shr7 through Pseudomonas fluorescens EtHAn suppressed nonspecific HR induced by Pseudomonas syringae DC3000 in wheat, confirming its activity in a homologous system. Overall, this study provides the first evidence for the presence of effectors in Puccinia species suppressing multiple plant defense responses.
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Tada, Yasuomi, Tomoyo Mori, Takeshi Shinogi, et al. "Nitric Oxide and Reactive Oxygen Species Do Not Elicit Hypersensitive Cell Death but Induce Apoptosis in the Adjacent Cells During the Defense Response of Oat." Molecular Plant-Microbe Interactions® 17, no. 3 (2004): 245–53. http://dx.doi.org/10.1094/mpmi.2004.17.3.245.
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Nitric oxide (NO) acts as a signaling molecule in many cellular responses in plants and animals. Oat plants (Avena sativa L.) evoke the hypersensitive response (HR), which shares morphological and biochemical features with mammalian apoptosis, such as DNA laddering and heterochromatin condensation, in response to the avirulent crown rust fungus (Puccinia coronata f. sp. avenae). We examined the role of NO and reactive oxygen species (ROS) in the initiation of hypersensitive cell death, which is induced by direct contact with the pathogen, and apoptotic cell death in the adjacent cells. Cytofluorimetric analysis using the fluorescent NO probe DAF and the H2O2 probe DCF demonstrated that NO and H2O2 were generated simultaneously in primary leaves at an early stage of the defense response. The NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) markedly enhanced H2O2 accumulation detected by 3,3-diaminobenzidine staining and DCF, whereas treatment with the NO donor S-nitroso-N-acetylpenicillamine (SNAP) strongly suppressed it. Superoxide dismutase (SOD) increased NO accumulation, suggesting that endogenous NO may modulate the level of H2O2 by interacting with O2 - in the HR lesion. Cytological observation showed that administration of cPTIO, SNAP, or SOD had no effect on elicitation of hypersensitive cell death, but clearly reduced heterochromatin condensation in the nearby cells and DNA laddering. These findings indicate that NO and ROS are not essential mediators for the initiation of hypersensitive cell death. However, NO and O2 - but not H2O2 are required for the onset of apoptotic cell death in the adjacent cells, where excess NO may exert its anti-apoptotic function by regulating cellular redox state.
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Ciardi, Joseph A., Denise M. Tieman, Jeffrey B. Jones, and Harry J. Klee. "Reduced Expression of the Tomato Ethylene Receptor Gene LeETR4 Enhances the Hypersensitive Response to Xanthomonas campestris pv. vesicatoria." Molecular Plant-Microbe Interactions® 14, no. 4 (2001): 487–95. http://dx.doi.org/10.1094/mpmi.2001.14.4.487.
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The hypersensitive response (HR) involves rapid death of cells at the site of pathogen infection and is thought to limit pathogen growth through the plant. Ethylene regulates senescence and developmental programmed cell death, but its role in hypersensitive cell death is less clear. Expression of two ethylene receptor genes, NR and LeETR4, is induced in tomato (Lycopersicon esculentum cv. Mill) leaves during an HR to Xanthomonas campestris pv. vesicatoria, with the greatest increase observed in LeETR4. LeETR4 antisense plants previously were shown to exhibit increased sensitivity to ethylene. These plants also exhibit greatly reduced induction of LeETR4 expression during infection and an accelerated HR at inoculum concentrations ranging from 105 to 107 CFU/ml. Increases in ethylene synthesis and pathogenesis-related gene expression are greater and more rapid in infected LeETR4 antisense plants, indicating an enhanced defense response. Populations of avirulent X. campestris pv. vesicatoria decrease more quickly and to a lower level in the transgenic plants, indicating a greater resistance to this pathogen. Because the ethylene action inhibitor 1-methylcyclopropene alleviates the enhanced HR phenotype in LeETR4 antisense plants, these changes in pathogen response are a result of increased ethylene sensitivity.
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Yu, I.-ching, Kevin A. Fengler, Steven J. Clough, and Andrew F. Bent. "Identification of Arabidopsis Mutants Exhibiting an Altered Hypersensitive Response in Gene-for-Gene Disease Resistance." Molecular Plant-Microbe Interactions® 13, no. 3 (2000): 277–86. http://dx.doi.org/10.1094/mpmi.2000.13.3.277.
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A mutational study was carried out to isolate Arabidopsis thaliana plants that exhibit full or partial disruption of the RPS2-mediated hypersensitive response (HR) to Pseudomonas syringae that express avrRpt2. Five classes of mutants were identified including mutations at RPS2, dnd mutations causing a “defense, no death” loss-of-HR phenotype, a lesion-mimic mutant that also exhibited an HR¯phenotype, and a number of intermediate or partial-loss-of-HR mutants. Surprisingly, many of these mutants displayed elevated resistance to virulent P. syringae and, in some cases, to Peronospora parasitica. Constitutively elevated levels of pathogenesis-related (PR) gene expression and salicylic acid were also observed. In the lesion-mimic mutant, appearance of elevated resistance was temporally correlated with appearance of lesions. For one of the intermediate lines, resistance was shown to be dependent on elevated levels of salicylic acid. A new locus was identified and named IHR1, after the mutant phenotype of “intermediate HR.” Genetic analysis of the intermediate-HR plant lines was difficult due to uncertainties in distinguishing the partial/intermediate mutant phenotypes from wild type. Despite this difficulty, the intermediate-HR mutants remain of interest because they reveal potential new defense-related loci and because many of these lines exhibit partially elevated disease resistance without dwarfing or other apparent growth defects.
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Farahani, Ali Safaie, and Seyyed Mohsen Taghavi. "Effects of bacterial populations, temperature and exogenous hydrogen peroxide on the induction of the hypersensitive response in Nicotiana tabacum against Xanthomonas perforans." Journal of Plant Protection Research 57, no. 2 (2017): 201–4. http://dx.doi.org/10.1515/jppr-2017-0019.
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AbstractThe objective of this study was to investigate the effects of inoculum concentration, plant post-inoculation incubation temperature and exogenous hydrogen peroxide (H2O2) on the induction of the hypersensitive response (HR) inNicotiana tabacumagainstXanthomonas perforans. Inoculation of leaves withX. perforansat a concentration of 108CFU · ml−1and incubation of plants at 30°C resulted in the strongest HR elicitation. Furthermore, an exogenous supply of H2O2acceleratedX. perforans-induced HR, whereasin plantaH2O2removal by application of catalase led to a delay in HR development. Our data suggest that H2O2has an important role in HR ofN. tabacumagainstX. perforans.
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Lu, You, Noriyuki Hatsugai, Fumiaki Katagiri, Carol A. Ishimaru, and Jane Glazebrook. "Putative Serine Protease Effectors of Clavibacter michiganensis Induce a Hypersensitive Response in the Apoplast of Nicotiana Species." Molecular Plant-Microbe Interactions® 28, no. 11 (2015): 1216–26. http://dx.doi.org/10.1094/mpmi-02-15-0036-r.
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Clavibacter michiganensis subspp. michiganensis and sepedonicus cause diseases on solanaceous crops. The genomes of both subspecies encode members of the pat-1 family of putative serine proteases known to function in virulence on host plants and induction of hypersensitive responses (HR) on nonhosts. One gene of this family in C. michiganensis subsp. sepedonicus, chp-7, is required for triggering HR in Nicotiana tabacum. Here, further investigation revealed that mutation of the putative catalytic serine residue at position 232 to threonine abolished the HR induction activity of Chp-7, suggesting that enzymatic activity is required. Purified Chp-7 triggered an HR in N. tabacum leaves in the absence of the pathogen, indicating Chp-7 itself is the HR elicitor from C. michiganensis subsp. sepedonicus. Ectopic expression of chp-7 constructs in N. tabacum leaves revealed that Chp-7 targeted to the apoplast triggered an HR while cytoplasmic Chp-7 did not, indicating that Chp-7 induces the HR in the apoplast of N. tabacum leaves. Chp-7 also induced HR in N. sylvestris, a progenitor of N. tabacum, but not in other Nicotiana species tested. ChpG, a related protein from C. michiganensis subsp. michiganensis, also triggered HR in N. tabacum and N. sylvestris. Unlike Chp-7, ChpG triggered HR in N. clevelandii and N. glutinosa.
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Ger, Mang-jye, Cheng-hsien Chen, Shaw-yhi Hwang, et al. "Constitutive Expression of hrap Gene in Transgenic Tobacco Plant Enhances Resistance Against Virulent Bacterial Pathogens by Induction of a Hypersensitive Response." Molecular Plant-Microbe Interactions® 15, no. 8 (2002): 764–73. http://dx.doi.org/10.1094/mpmi.2002.15.8.764.
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Hypersensitive response-assisting protein (HRAP) has been previously reported as an amphipathic plant protein isolated from sweet pepper that intensifies the harpinPss-mediated hypersensitive response (HR). The hrap gene has no appreciable similarity to any other known sequences, and its activity can be rapidly induced by incompatible pathogen infection. To assess the function of the hrap gene in plant disease resistance, the CaMV 35S promoter was used to express sweet pepper hrap in transgenic tobacco. Compared with wild-type tobacco, transgenic tobacco plants exhibit more sensitivity to harpinPss and show resistance to virulent pathogens (Pseudomonas syringae pv. tabaci and Erwinia carotovora subsp. carotovora). This disease resistance of transgenic tobacco does not originate from a constitutive HR, because endogenous level of salicylic acid and hsr203J mRNA showed similarities in transgenic and wild-type tobacco under noninfected conditions. However, following a virulent pathogen infection in hrap transgenic tobacco, hsr203J was rapidly induced and a micro-HR necrosis was visualized by trypan blue staining in the infiltration area. Consequently, we suggest that the disease resistance of transgenic plants may result from the induction of a HR by a virulent pathogen infection.
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Bennett, Mark, Monaz Mehta, and Murray Grant. "Biophoton Imaging: A Nondestructive Method for Assaying R Gene Responses." Molecular Plant-Microbe Interactions® 18, no. 2 (2005): 95–102. http://dx.doi.org/10.1094/mpmi-18-0095.
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Plant disease resistance (R) proteins of the nucleotide binding-leucine rich repeat class are responsible for pathogen recognition and activation of defense signaling networks leading to the hypersensitive response (HR). Genetically, R-protein signaling appears to be integrated through a limited set of common downstream components. However, the timing of development of visible HR is unique to individual R proteins. By utilizing the phenomena of ultraweak photon emission from leaves undergoing an incompatible interacttion, a powerful nondestructive and facile assay is described to compare timing of defense responses elicited by different R proteins. We demonstrate that ultraweak photon emission, or “biophoton generation,” is demonstrated to be associated with hypersensitive cell death. Biophoton emission requires an intact R signaling network and increases in cytosolic calcium and nitric oxide, but elevated reactive oxygen species are not necessary. Importantly, the assay is robust and applicable to a range of incompatible interactions in various plant species. The ability to assay R responses nondestructively in real time and a chosen genetic background makes this technique amenable to subtle genetic dissection of plant defense responses.
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Thomas, Colwyn M., Saijun Tang, Kim Hammond-Kosack, and Jonathan D. G. Jones. "Comparison of the Hypersensitive Response Induced by the Tomato Cf-4 and Cf-9 Genes in Nicotiana spp." Molecular Plant-Microbe Interactions® 13, no. 4 (2000): 465–69. http://dx.doi.org/10.1094/mpmi.2000.13.4.465.
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We have previously shown that tomato Cf-9 induces an Avr9-dependent hypersensitive response (HR) in Nicotiana tabacum and potato. We show here that Cf-4 also induces an Avr4-dependent HR in two tobacco species (N. tabacum and N. benthamiana). The HR induced by Cf-4 and Cf-9 was compared in stable tobacco transgenics by a seedling lethal assay and resistance to recombinant Potato virus X expressing Avr4 or Avr9. We also compared HR induction with Agrobacterium-mediated transient expression. The Cf-4/Avr4 combination induced a more rapid HR than Cf-9/Avr9. Sensitive assays for Cf-9 and Cf-4 function should prove useful for structure/function analyses of these resistance proteins in tobacco.
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Mur, Luis A. J., Aprajita Kumari, Yariv Brotman, et al. "Nitrite and nitric oxide are important in the adjustment of primary metabolism during the hypersensitive response in tobacco." Journal of Experimental Botany 70, no. 17 (2019): 4571–82. http://dx.doi.org/10.1093/jxb/erz161.
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Abstract Nitrate and ammonia deferentially modulate primary metabolism during the hypersensitive response in tobacco. In this study, tobacco RNAi lines with low nitrite reductase (NiRr) levels were used to investigate the roles of nitrite and nitric oxide (NO) in this process. The lines accumulate NO2–, with increased NO generation, but allow sufficient reduction to NH4+ to maintain plant viability. For wild-type (WT) and NiRr plants grown with NO3–, inoculation with the non-host biotrophic pathogen Pseudomonas syringae pv. phaseolicola induced an accumulation of nitrite and NO, together with a hypersensitive response (HR) that resulted in decreased bacterial growth, increased electrolyte leakage, and enhanced pathogen resistance gene expression. These responses were greater with increases in NO or NO2– levels in NiRr plants than in the WT under NO3– nutrition. In contrast, WT and NiRr plants grown with NH4+ exhibited compromised resistance. A metabolomic analysis detected 141 metabolites whose abundance was differentially changed as a result of exposure to the pathogen and in response to accumulation of NO or NO2–. Of these, 13 were involved in primary metabolism and most were linked to amino acid and energy metabolism. HR-associated changes in metabolism that are often linked with primary nitrate assimilation may therefore be influenced by nitrite and NO production.
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Jacques, Alban, Ahmed Ghannam, Mathieu Erhardt, Patrice de Ruffray, Fabienne Baillieul, and Serge Kauffmann. "NtLRP1, a Tobacco Leucine-Rich Repeat Gene with a Possible Role as a Modulator of the Hypersensitive Response." Molecular Plant-Microbe Interactions® 19, no. 7 (2006): 747–57. http://dx.doi.org/10.1094/mpmi-19-0747.
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Plant defense responses against pathogens often involve the restriction of the pathogen to its site of penetration achieved through the combined effects of the hypersensitive response (HR) and its tightly connected localized acquired resistance (LAR). The tobacco DD9-3 expressed sequence tag was previously isolated from a screen designed to isolate genes induced early during the HR, thus potentially involved in the induction/regulation of the HR or LAR. Translation of the open reading frame of DD9-3 revealed a leucine-rich repeat (LRR) domain highly homologous with the receptor domain of a receptor kinase, suggesting a potential function in signaling pathways. The full-length cDNA was cloned. It encodes a small (232 amino acids) LRR protein, designated Nicotiana tabacum leucine-rich protein 1 (NtLRP1), containing a signal peptide, four leucine zipper repeats, five LRR repeats, and a C-terminal domain rich in proline. NtLRP1 expression is induced early during the HR initiated by elicitins, Ralstonia solanacearum, or Tobacco mosaic virus. NtLRP1 coupled with the green fluorescent protein localizes to the endoplasmic reticulum (ER). Loss-of-function through virus-induced gene silencing or through RNA interference did not modify the elicitin-induced HR or LAR. Gain-of-function experiments through transient Agrobacterium tu-mefaciens-mediated NtLRP1 expression in tobacco leaves caused the suppression of the HR induced by 2 nM elicitin and delayed the HR when the elicitin was applied at higher concentrations. The results suggest that NtLRP1 acts as a modulator of the HR and that retention in the ER is essential for its function.
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Zhang, Chu, Kirk J. Czymmek, and Allan D. Shapiro. "Nitric oxide Does Not Trigger Early Programmed Cell Death Events but May Contribute to Cell-to-Cell Signaling Governing Progression of the Arabidopsis Hypersensitive Response." Molecular Plant-Microbe Interactions® 16, no. 11 (2003): 962–72. http://dx.doi.org/10.1094/mpmi.2003.16.11.962.
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Nitric oxide (NO) has been suggested to play a role in the hypersensitive response (HR). Single- and double-label fluorescence microscopy experiments were conducted using Arabidopsis leaves infected with Pseudomonas syringae pv. tomato DC3000 carrying either avrB or avrRpt2. Kinetics of NO production were followed by measurement of green 4-amino-5-methylamino-2′,7′-difluorofluorescein (DAF-FM) triazole fluorescence in leaves coinfiltrated with DAF-FM diacetate. Kinetics of hypersensitive cell death were followed by measurement of cytoplasmic red fluorescence following internalization of coinfiltrated propidium iodide through compromised plasma membranes. Neither NO accumulation nor cell death was seen until approximately 3 h postinoculation of Columbia leaves with DC3000·avrB or approximately 5.5 h post-inoculation with DC3000·avrRpt2. Subsequent NO accumulation kinetics closely paralleled HR progression in both Columbia and ndr1-1 mutant plants. These data established that NO accumulation does not happen sufficiently early for NO to be a signaling component controlling HR triggering. NO accumulation did contribute to the HR, as proven by an approximately 1-h delay in cell death kinetics caused by an NO scavenger or an NO synthase inhibitor. NO was first seen as punctate foci at the cell surface. Subsequent NO accumulation patterns were consistent with NO being an intercellular signal that functions in cell-to-cell spread of the HR.
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Singh, Anita, John S. Petrides, Philip W. Gold, George P. Chrousos, and Patricia A. Deuster. "Differential Hypothalamic-Pituitary-Adrenal Axis Reactivity to Psychological and Physical Stress1." Journal of Clinical Endocrinology & Metabolism 84, no. 6 (1999): 1944–48. http://dx.doi.org/10.1210/jcem.84.6.5746.
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Healthy men exhibit a differential hypothalamic-pituitary-adrenal axis (HPA) response to exercise stress and fall into two groups: high responders (HR) and low responders (LR). The present study examined whether HR to physical stress also exhibit higher HPA reactivity to psychological stress than LR. We examined 14 HR and 13 LR classified based on their ACTH responses to high intensity exercise after pretreatment with dexamethasone. Both groups were of similar age, height, weight, and fitness level. Trait anxiety scores on the Spielberger Trait Anxiety Scale were not different. Subjects underwent a psychological stress test consisting of an interview and mental arithmetic. This test raised heart rate, blood pressure, and plasma ACTH and cortisol levels in both HR and LR. HR tended to have higher heart rates and blood pressures in anticipation of the psychological stress test than LR. ACTH responses of HR were higher, although not significantly, throughout the psychological stress test than LR. HR had a significantly (P &lt; 0.05) greater net integrated cortisol response to the psychological stress than LR. This suggests that the adrenal cortexes of the HR are hypertropic and/or hypersensitive to ACTH. We conclude that men who are highly responsive to exercise stress are also highly responsive to psychological stress.
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Wang, Guan-Feng, and Peter J. Balint-Kurti. "Cytoplasmic and Nuclear Localizations Are Important for the Hypersensitive Response Conferred by Maize Autoactive Rp1-D21 Protein." Molecular Plant-Microbe Interactions® 28, no. 9 (2015): 1023–31. http://dx.doi.org/10.1094/mpmi-01-15-0014-r.
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Disease resistance (R) genes have been isolated from many plant species. Most encode nucleotide binding leucine-rich repeat (NLR) proteins that trigger a rapid localized programmed cell death called the hypersensitive response (HR) upon pathogen recognition. Despite their structural similarities, different NLR are distributed in a range of subcellular locations, and analogous domains play diverse functional roles. The autoactive maize NLR gene Rp1-D21 derives from an intragenic recombination between two NLR genes, Rp1-D and Rp1-dp2, and confers a HR independent of the presence of a pathogen. Rp1-D21 and its N-terminal coiled coil (CC) domain (CCD21) confer autoactive HR when transiently expressed in Nicotiana benthamiana. Rp1-D21 was predominantly localized in cytoplasm with a small amount in the nucleus, while CCD21 was localized in both nucleus and cytoplasm. Targeting of Rp1-D21 or CCD21 predominantly to either the nucleus or the cytoplasm abolished HR-inducing activity. Coexpression of Rp1-D21 or CCD21 constructs confined, respectively, to the nucleus and cytoplasm did not rescue full activity, suggesting nucleocytoplasmic movement was important for HR induction. This work emphasizes the diverse structural and subcellular localization requirements for activity found among plant NLR R genes.
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Abbink, Truus E. M., Johan de Vogel, John F. Bol, and Huub J. M. Linthorst. "Induction of a Hypersensitive Response by Chimeric Helicase Sequences of Tobamoviruses U1 and Ob in N-Carrying Tobacco." Molecular Plant-Microbe Interactions® 14, no. 9 (2001): 1086–95. http://dx.doi.org/10.1094/mpmi.2001.14.9.1086.
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Recently, the helicase domain of the Tobacco mosaic virus (TMV)-U1 replicase proteins (designated MOREHEL:U1) was identified as the elicitor of the N gene-mediated hypersensitive response (HR) in tobacco. In this study, we used agroinfiltration to express the equivalent MOREHEL domain of the non-HR-inducing tobamovirus strain TMV-Ob. It appeared that this MOREHEL:Ob sequence did not elicit a HR in N gene-carrying tobacco. Both MOREHEL sequences were divided into eight subdomains, and chimeras of MOREHEL sequences from U1 and Ob were constructed. Expression of these chimeric MOREHEL sequences revealed that, in the TMV-U1 MOREHEL sequence, at least four domains involved in full HR induction were present. The presence of at least three of these four domains seems a minimal requirement for HR induction. Two additional domains may play a minor role in HR induction. To study the elicitor function of the chimeras during the TMV life cycle, chimeric MOREHEL domains were introduced into full-length TMV cDNA clones. These constructs, however, were unable to establish an infection in Nicotiana benthamiana or Nicotiana tabacum plants.
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Szittya, György, and József Burgyán. "Cymbidium Ringspot Tombusvirus Coat Protein Coding Sequence Acts as an Avirulent RNA." Journal of Virology 75, no. 5 (2001): 2411–20. http://dx.doi.org/10.1128/jvi.75.5.2411-2420.2001.
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ABSTRACT Avirulent genes either directly or indirectly produce elicitors that are recognized by specific receptors of plant resistance genes, leading to the induction of host defense responses such as hypersensitive reaction (HR). HR is characterized by the development of a necrotic lesion at the site of infection which results in confinement of the invader to this area. Artificial chimeras and mutants of cymbidium ringspot (CymRSV) and the pepper isolate of tomato bushy stunt (TBSV-P) tombusviruses were used to determine viral factors involved in the HR resistance phenotype of Datura stramonium upon infection with CymRSV. A series of constructs carrying deletions and frameshifts of the CymRSV coat protein (CP) undoubtedly clarified that an 860-nucleotide (nt)-long RNA sequence in the CymRSV CP coding region (between nt 2666 and 3526) is the elicitor of a very rapid HR-like response of D. stramonium which limits the virus spread. This finding provides the first evidence that an untranslatable RNA can trigger an HR-like resistance response in virus-infected plants. The effectiveness of the resistance response might indicate that other nonhost resistance could also be due to RNA-mediated HR. It is an appealing explanation that RNA-mediated HR has evolved as an alternative defense strategy against RNA viruses.
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Yano, Akira, Kaoru Suzuki, Hirofumi Uchimiya, and Hideaki Shinshi. "Induction of Hypersensitive Cell Death by a Fungal Protein in Cultures of Tobacco Cells." Molecular Plant-Microbe Interactions® 11, no. 2 (1998): 115–23. http://dx.doi.org/10.1094/mpmi.1998.11.2.115.
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Treatment of suspension-cultured tobacco (Nicotiana tabacum cv. Xanthi) cells (line XD6S) with fungal proteinaceous elicitors, namely, xylanase (EC 3.2.1.8) from Trichoderma viride (TvX) and xylanase from T. reesei (TrX), induced shrinkage of the cytoplasm, condensation of the nucleus, and, finally, cell death, which were accompanied by typical defense responses that included an oxidative burst and expression of defense genes. A Ca2+ channel blocker, Gd3+, inhibited the typical response of XD6S cells to TvX, which resembled the hypersensitive reaction (HR). These results suggested that the influx of Ca2+ ions plays an important role as a secondary signal. The HR was not observed in TvX-treated tobacco cells (line BY-2) derived from cv. Bright Yellow 2. This result suggests that key features of cultivar-specific interaction can be observed in cultures of tobacco cells. Xylanase from Bacillus circulans (BcX) and B. subtilis (BsX), which has enzymatic properties similar to those of TvX but an amino acid sequence different from that of TvX, did not induce the HR-like response in XD6S cells. These results suggest that the elicitor action of TvX is not due to its ability to hydrolyze cell walls but requires the TvX-specific recognition factors in plant cells. Thus, TvX-induced cell death was not due to some general toxic effect, but seems to be mediated by the activation of a specific cellular signal-transduction cascade that converges with a pathway that activates the intracellular cell death program.
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Kaewnum, S., S. Prathuangwong, and T. J. Burr. "A Pectate Lyase Homolog, xagP, in Xanthomonas axonopodis pv. glycines Is Associated with Hypersensitive Response Induction on Tobacco." Phytopathology® 96, no. 11 (2006): 1230–36. http://dx.doi.org/10.1094/phyto-96-1230.
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Xanthomonas axonopodis pv. glycines is the causal agent of bacterial pustule disease of soybeans. A transposon insertional mutant (KU-P-M670) of X. axonopodis pv. glycines derived from wild-type strain KU-P-34017 lost the ability to induce the hypersensitive response (HR) on tobacco and pepper but retained its HR induction capacity on cucumber, sesame, and tomato. The mutation also resulted in loss of ability to cause a potato soft rot and express pectolytic activity at pH 6.5. An approximate 1.4-kb DNA fragment carrying the transposon insertion contained a single open reading frame that showed high homology with PSTRU-3, a pectate lyase gene in X. axonopodis pv. malvacearum. Complemented KU-P-M670 regained HR induction on tobacco and also pectolytic activity. Treatment of plants with inhibitors of eukaryotic metabolism blocked HR induction by wild-type strains and by complemented KU-P-M670. The presence of the pectate lyase homolog, which we designated xagP, in 26 X. axonopodis pv. glycines strains was highly correlated with their ability to induce an HR on tobacco. To our knowledge, this is the first study indicating a role for a functional pectate lyase in induction of a plant HR.
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Cawly, John, Anthony B. Cole, Lóránt Király, Wenping Qiu, and James E. Schoelz. "The Plant Gene CCD1 Selectively Blocks Cell Death During the Hypersensitive Response to Cauliflower Mosaic Virus Infection." Molecular Plant-Microbe Interactions® 18, no. 3 (2005): 212–19. http://dx.doi.org/10.1094/mpmi-18-0212.
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The P6 protein of Cauliflower mosaic virus (CaMV) W260 elicits a hypersensitive response (HR) on inoculated leaves of Nicotiana edwardsonii. This defense response, common to many plant pathogens, has two key characteristics, cell death within the initially infected tissues and restriction of the pathogen to this area. We present evidence that a plant gene designated CCD1, originally identified in N. bigelovii, can selectively block the cell death pathway during HR, whereas the resistance pathway against W260 remains intact. Suppression of cell death was evident not only macroscopically but also microscopically. The suppression of HR-mediated cell death was specific to CaMV, as Tobacco mosaic virus was able to elicit HR in the plants that contained CCD1. CCD1 also blocks the development of a systemic cell death symptom induced specifically by the P6 protein of W260 in N. clevelandii. Introgression of CCD1 from N. bigelovii into N. clevelandii blocked the development of systemic cell death in response to W260 infection but could not prevent systemic cell death induced by Tomato bushy stunt virus. Thus, CCD1 blocks both local and systemic cell death induced by P6 of W260 but does not act as a general suppressor of cell death induced by other plant viruses. Furthermore, experiments with CCD1 provide further evidence that cell death could be uncoupled from resistance in the HR of Nicotiana edwardsonii to CaMV W260.
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Ahmad, Musharaf, Doris R. Majerczak, Sharon Pike, Mary Elizabeth Hoyos, Anton Novacky, and David L. Coplin. "Biological Activity of Harpin Produced by Pantoea stewartii subsp. stewartii." Molecular Plant-Microbe Interactions® 14, no. 10 (2001): 1223–34. http://dx.doi.org/10.1094/mpmi.2001.14.10.1223.
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Pantoea stewartii subsp. stewartii causes Stewart's wilt of sweet corn. A hypersensitive response and pathogenicity (Hrp) secretion system is needed to produce water-soaking and wilting symptoms in corn and to cause a hypersensitive response (HR) in tobacco. Sequencing of the hrp cluster revealed a putative harpin gene, hrpN. The product of this gene was overexpressed in Escherichia coli and shown to elicit the HR in tobacco and systemic resistance in radishes. The protein was designated HrpNPnss. Like other harpins, it was heat stable and protease sensitive, although it was three- to fourfold less active biologically than Erwinia amylovora harpin. We used antibodies to purified HrpNPnss to verify that hrpN mutants could not produce harpin. This protein was secreted into the culture supernatant and was produced by strains of P. stewartii subsp. indologenes. In order to determine the importance of HrpNPnss in pathogenesis on sweet corn, three hrpN::Tn5 mutants were compared with the wild-type strain with 50% effective dose, disease severity, response time, and growth rate in planta as parameters. In all tests, HrpNPnss was not required for infection, growth, or virulence in corn or endophytic growth in related grasses.
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Hussain, Mazhar, Shahid Mansoor, Shazia Iram, Yusuf Zafar, and Rob W. Briddon. "The Hypersensitive Response to Tomato leaf curl New Delhi virus Nuclear Shuttle Protein Is Inhibited by Transcriptional Activator Protein." Molecular Plant-Microbe Interactions® 20, no. 12 (2007): 1581–88. http://dx.doi.org/10.1094/mpmi-20-12-1581.
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The hypersensitive response (HR) is a common feature of plant disease resistance reactions and a type of programmed cell death (PCD). Many pathogens are able to modulate pathways involved in cell death. In contrast to animal viruses, inhibitors of PCD activity have not been identified for plant-infecting viruses. Previously, we have reported that the nuclear shuttle protein (NSP) of Tomato leaf curl New Delhi virus (ToLCNDV) induces an HR in Nicotiana tabacum and Lycopersicon esculentum plants when expressed under the control of the Cauliflower mosaic virus 35S promoter. However, HR is not evident in plants infected with ToLCNDV, suggesting that the virus encodes a factor (or factors) that counters this response. Analysis of all ToLCNDV-encoded genes pinpointed the transcriptional activator protein (TrAP) as the factor mediating the anti-HR effect. Deletion mutagenesis showed the central region of TrAP, containing a zinc finger domain and nuclear localization signal, to be important in inhibiting the HR. These results demonstrate that TrAP counters HR-induced cell death, the first such activity identified for a plant-infecting virus.
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Yang, Cunchun, Zhongwei Zou, and Wannakuwattewaduge Gerard Dilantha Fernando. "The Effect of Temperature on the Hypersensitive Response (HR) in the Brassica napus–Leptosphaeria maculans Pathosystem." Plants 10, no. 5 (2021): 843. http://dx.doi.org/10.3390/plants10050843.
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Temperature is considered one of the crucial environmental elements in plant pathological interactions, and previous studies have indicated that there is a relationship between temperature change and host–pathogen interactions. The objective of this research is to investigate the link between temperature and the incompatible interactions of the host and pathogen. In this study, two Leptosphaeria maculans isolates (HCRT75 8-1 and HCRT77 7-2) and two Brassica napus genotypes (Surpass400 and 01-23-2-1) were selected. The selected B. napus genotypes displayed intermediate and resistant phenotypes. The inoculated seedlings were tested under three temperature conditions: 16 °C/10 °C, 22 °C/16 °C and 28 °C/22 °C (day/night: 16 h/8 h). Lesion measurements demonstrated that the necrotic lesions from the 28 °C/22 °C treatment were enlarged compared with the other two temperature treatments (i.e., 16 °C/10 °C and 22 °C/16 °C). The results of expression analysis indicated that the three temperature treatments displayed distinct differences in two marker genes (PATHOGENESIS–RELATED (PR) 1 and 2) for plant defense and one temperature-sensitive gene BONZAI 1 (BON1). Additionally, seven dpi at 22 °C/16 °C appeared to be the optimal pre-condition for the induction of PR1 and 2. These findings suggest that B. napus responds to temperature changes when infected with L. maculans.
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Cole, Anthony B., Lóránt Király, Kathleen Ross, and James E. Schoelz. "Uncoupling Resistance from Cell Death in the Hypersensitive Response of Nicotiana Species to Cauliflower mosaic virus Infection." Molecular Plant-Microbe Interactions® 14, no. 1 (2001): 31–41. http://dx.doi.org/10.1094/mpmi.2001.14.1.31.
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Cauliflower mosaic virus strain W260 elicits a hypersensitive response (HR) in leaves of Nicotiana edwardsonii, an interspecific hybrid derived from a cross between N. glutinosa and N. clevelandii. Interestingly, we found that N. glutinosa is resistant to W260, but responds with local chlorotic lesions rather than necrotic lesions. In contrast, N. clevelandii responds to W260 with systemic cell death. The reactions of the progenitors of N. edwardsonii to W260 infection indicated that each contributed a factor toward the development of HR. In this study, we present two lines of evidence to show that the resistance and cell death that comprise the HR elicited by W260 can indeed be uncoupled. First, we showed that the non-necrotic resistance response of N. glutinosa could be converted to HR when these plants were crossed with N. clevelandii. Second, we found that cell death and resistance segregated independently in the F2 population of a cross between N. edwardsonii and N. clevelandii. We concluded that the resistance of N. edwardsonii to W260 infection was conditioned by a gene derived from N. glutinosa, whereas cell death was conditioned by a gene derived from N. clevelandii. An analysis of pathogenesis-related (PR) protein expression in response to W260 infection revealed that elicitation of PR proteins was associated with resistance rather than with the onset of cell death.
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Chen, Yu, and Dennis A. Halterman. "Phenotypic Characterization of Potato Late Blight Resistance Mediated by the Broad-Spectrum Resistance Gene RB." Phytopathology® 101, no. 2 (2011): 263–70. http://dx.doi.org/10.1094/phyto-04-10-0119.
Full textAbstract:
The potato gene RB, cloned from the wild potato species Solanum bulbocastanum, confers partial resistance to late blight, caused by the oomycete pathogen Phytophthora infestans. In order to better characterize this partial resistance phenotype, we have compared host resistance responses mediated by RB with those mediated by the S. demissum-derived R gene R9, which confers immunity to P. infestans carrying the corresponding avirulence gene avrR9. We found that both RB and R9 genes were capable of eliciting a hypersensitive cell death response (HR). However, in RB plants, the pathogen escaped HR lesions and continued to grow beyond the inoculation sites. We also found that callose deposition was negatively correlated with resistance levels in tested plants. Transcription patterns of pathogenesis-related (PR) genes PR-1 basic, PR-2 acidic, and PR-5 indicated that P. infestans inoculation induced transcription of these defense-related genes regardless of the host genotype; however, transcription was reduced in both the susceptible and partially resistant plants later in the infection process but remained elevated in the immune host. Most interestingly, transcription of the HR-associated gene Hin1 was suppressed in both Katahdin and RB-transgenic Katahdin but not in R9 4 days after inoculation. Together, this suggests that suppression of certain defense-related genes may allow P. infestans to spread beyond the site of infection in the partially resistant host despite elicitation of hypersensitive cell death.
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Hemara, Lauren M., Jay Jayaraman, Paul W. Sutherland, et al. "Effector loss drives adaptation of Pseudomonas syringae pv. actinidiae biovar 3 to Actinidia arguta." PLOS Pathogens 18, no. 5 (2022): e1010542. http://dx.doi.org/10.1371/journal.ppat.1010542.
Full textAbstract:
A pandemic isolate of Pseudomonas syringae pv. actinidiae biovar 3 (Psa3) has devastated kiwifruit orchards growing cultivars of Actinidia chinensis. In contrast, A. arguta (kiwiberry) is not a host of Psa3. Resistance is mediated via effector-triggered immunity, as demonstrated by induction of the hypersensitive response in infected A. arguta leaves, observed by microscopy and quantified by ion-leakage assays. Isolates of Psa3 that cause disease in A. arguta have been isolated and analyzed, revealing a 51 kb deletion in the exchangeable effector locus (EEL). This natural EEL-mutant isolate and strains with synthetic knockouts of the EEL were more virulent in A. arguta plantlets than wild-type Psa3. Screening of a complete library of Psa3 effector knockout strains identified increased growth in planta for knockouts of four effectors–AvrRpm1a, HopF1c, HopZ5a, and the EEL effector HopAW1a –suggesting a resistance response in A. arguta. Hypersensitive response (HR) assays indicate that three of these effectors trigger a host species-specific HR. A Psa3 strain with all four effectors knocked out escaped host recognition, but a cumulative increase in bacterial pathogenicity and virulence was not observed. These avirulence effectors can be used in turn to identify the first cognate resistance genes in Actinidia for breeding durable resistance into future kiwifruit cultivars.
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Alarcón, C., J. Castro, F. Muñoz, P. Arce-Johnson, and J. Delgado. "Protein(s) from the Gram-Positive Bacterium Clavibacter michiganensis subsp. michiganensis Induces a Hypersensitive Response in Plants." Phytopathology® 88, no. 4 (1998): 306–10. http://dx.doi.org/10.1094/phyto.1998.88.4.306.
Full textAbstract:
The gram-positive tomato pathogen Clavibacter michiganensis subsp. michiganensis induced a local necrotic response on four-o'clock (Mirabilis jalapa) and tobacco (Nicotiana tabacum) plants. This necrosis response was characteristic of the hypersensitive response (HR). The cell-free culture supernatant from strain CMM623 also induced a necrosis that was phenotypically similar to that induced by the bacteria. Inhibitors of plant metabolism suppressed the necrotic reaction of both M. jalapa and tobacco. The HR-inducing activity present in the supernatant was heat stable, sensitive to proteases, and had an apparent molecular mass in the range of 35 to 50 kDa as determined by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. The properties observed for the necrosis-inducing activity resembled harpin and PopA described from gram-negative phytopathogenic bacteria.
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Garrido-Ramirez, E. R., M. R. Sudarshana, W. J. Lucas, and R. L. Gilbertson. "Bean dwarf mosaic virus BV1 Protein Is a Determinant of the Hypersensitive Response and Avirulence in Phaseolus vulgaris." Molecular Plant-Microbe Interactions® 13, no. 11 (2000): 1184–94. http://dx.doi.org/10.1094/mpmi.2000.13.11.1184.
Full textAbstract:
The capacities of the begomoviruses Bean dwarf mosaic virus (BDMV) and Bean golden yellow mosaic virus (BGYMV) to differentially infect certain common bean (Phaseolus vulgaris) cultivars were used to identify viral determinants of the hypersensitive response (HR) and avirulence (avr) in BDMV. A series of hybrid DNA-B components, containing BDMV and BGYMV sequences, was constructed and coinoculated with BDMV DNA-A (BDMV-A) or BDMVA-green florescent protein into seedlings of cv. Topcrop (susceptible to BDMV and BGYMV) and the BDMV-resistant cvs. Othello and Black Turtle Soup T-39 (BTS). The BDMV avr determinant, in bean hypocotyl tissue, was mapped to the BDMV BV1 open reading frame and, most likely, to the BV1 protein. The BV1 also was identified as the determinant of the HR in Othello. However, the HR was not required for resistance in Othello nor was it associated with BDMV resistance in BTS. BDMV BV1, a nuclear shuttle protein that mediates viral DNA export from the nucleus, represents a new class of viral avr determinant. These results are discussed in terms of the relationship between the HR and resistance.
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Rodríguez-Decuadro, Susana, Paula Silva, Oscar Bentancur, Fernanda Gamba, and Clara Pritsch. "Histochemical Characterization of Early Response to Cochliobolus sativus Infection in Selected Barley Genotypes." Phytopathology® 104, no. 7 (2014): 715–23. http://dx.doi.org/10.1094/phyto-05-13-0133-r.
Full textAbstract:
Much effort is being made to breed barley with durable resistance to leaf spot blotch incited by Bipolaris sorokiniana (teleomorph: Cochliobolus sativus). We hypothesized that susceptibility and resistance traits in 11 diverse barley genotypes inoculated with a single C. sativus isolate might specify a range of distinct host cell responses. Quantitative descriptions of interaction microphenotypes exhibited by different barley genotype seedlings after infection with C. sativus are provided. Early oxidative responses occurring in epidermis and mesophyll leaf tissue were monitored by histochemical analysis of H2O2 accumulation at 8, 24, and 48 h after inoculation. Cell wall apposition (CWA) in epidermal cells and hypersensitive reaction (HR) of epidermal or mesophyll tissue were early defenses in both resistant and susceptible genotypes. There were differences in level, duration, and frequency of occurrence for CWA and HR for the different barley genotypes. Occurrence of HR in epidermal cells at post-penetration stages was indicative of compatibility. Patterns of cell responses were microphenotypically diverse between different resistant and susceptible genotypes. This suggests that timing and level of response are key features of microphenotypic diversity that distinguish different functional mechanisms of resistance and susceptibility present in barley.
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Ali, Muhammad, Quan-Hui Li, Tao Zou, et al. "Chitinase Gene Positively Regulates Hypersensitive and Defense Responses of Pepper to Colletotrichum acutatum Infection." International Journal of Molecular Sciences 21, no. 18 (2020): 6624. http://dx.doi.org/10.3390/ijms21186624.
Full textAbstract:
Anthracnose caused by Colletotrichum acutatum is one of the most devastating fungal diseases of pepper (Capsicum annuum L.). The utilization of chitin-binding proteins or chitinase genes is the best option to control this disease. A chitin-binding domain (CBD) has been shown to be crucial for the innate immunity of plants and activates the hypersensitive response (HR). The CaChiIII7 chitinase gene has been identified and isolated from pepper plants. CaChiIII7 has repeated CBDs that encode a chitinase enzyme that is transcriptionally stimulated by C. acutatum infection. The knockdown of CaChiIII7 in pepper plants confers increased hypersensitivity to C. acutatum, resulting in its proliferation in infected leaves and an attenuation of the defense response genes CaPR1, CaPR5, and SAR8.2 in the CaChiIII7-silenced pepper plants. Additionally, H2O2 accumulation, conductivity, proline biosynthesis, and root activity were distinctly reduced in CaChiIII7-silenced plants. Subcellular localization analyses indicated that the CaChiIII7 protein is located in the plasma membrane and cytoplasm of plant cells. The transient expression of CaChiIII7 increases the basal resistance to C. acutatum by significantly expressing several defense response genes and the HR in pepper leaves, accompanied by an induction of H2O2 biosynthesis. These findings demonstrate that CaChiIII7 plays a prominent role in plant defense in response to pathogen infection.
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Kim, Jung-Gun, Eunkyung Jeon, Jonghee Oh, Jae Sun Moon, and Ingyu Hwang. "Mutational Analysis of Xanthomonas Harpin HpaG Identifies a Key Functional Region That Elicits the Hypersensitive Response in Nonhost Plants." Journal of Bacteriology 186, no. 18 (2004): 6239–47. http://dx.doi.org/10.1128/jb.186.18.6239-6247.2004.
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ABSTRACT HpaG is a type III-secreted elicitor protein of Xanthomonas axonopodis pv. glycines. We have determined the critical amino acid residues important for hypersensitive response (HR) elicitation by random and site-directed mutagenesis of HpaG and its homolog XopA. A plasmid clone carrying hpaG was mutagenized by site-directed mutagenesis, hydroxylamine mutagenesis, and error-prone PCR. A total of 52 mutants were obtained, including 51 single missense mutants and 1 double missense mutant. The HR elicitation activity was abolished in the two missense mutants [HpaG(L50P) and HpaG(L43P/L50P)]. Seven single missense mutants showed reduced activity, and the HR elicitation activity of the rest of the mutants was similar to that of wild-type HpaG. Mutational and deletion analyses narrowed the region essential for elicitor activity to the 23-amino-acid peptide (H2N-NQGISEKQLDQLLTQLIMALLQQ-COOH). A synthetic peptide of this sequence possessed HR elicitor activity at the same concentration as the HpaG protein. This region has 78 and 74% homology with 23- and 27-amino-acid regions of the HrpW harpin domains, respectively, from Pseudomonas and Erwinia spp. The secondary structure of the peptide is predicted to be an α-helix, as is the HrpW region that is homologous to HpaG. The predicted α-helix of HpaG is probably critical for the elicitation of the HR in tobacco plants. In addition, mutagenesis of a xopA gene yielded two gain-of-function mutants: XopA(F48L) and XopA(F48L/M52L). These results indicate that the 12 amino acid residues between L39 and L50 of HpaG have critical roles in HR elicitation in tobacco plants.
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Robbins, Matthew D., Audrey Darrigues, Sung-Chur Sim, Mohammed Abu Taher Masud, and David M. Francis. "Characterization of Hypersensitive Resistance to Bacterial Spot Race T3 (Xanthomonas perforans) from Tomato Accession PI 128216." Phytopathology® 99, no. 9 (2009): 1037–44. http://dx.doi.org/10.1094/phyto-99-9-1037.
Full textAbstract:
Bacterial spot of tomato is caused by four species of Xanthomonas. The accession PI 128216 (Solanum pimpinellifolium) displays a hypersensitive reaction (HR) to race T3 strains (predominately Xanthomonas perforans). We developed an inbred backcross (IBC) population (BC2S5, 178 families) derived from PI 128216 and OH88119 (S. lycopersicum) as the susceptible recurrent parent for simultaneous introgression and genetic analysis of the HR response. These IBC families were evaluated in the greenhouse for HR to race T3 strain Xcv761. The IBC population was genotyped with molecular markers distributed throughout the genome in order to identify candidate loci conferring resistance. We treated the IBC population as a hypothesis forming generation to guide validation in subsequent crosses. Nonparametric analysis identified an association between HR and markers clustered on chromosome 11 (P < 0.05 to 0.0001) and chromosome 6 (0.04 > P > 0.002). Further analysis of the IBC population suggested that markers on chromosome 6 and 11 failed to assort independently, a phenomenon known as gametic phase disequilibrium. Therefore, to validate marker-trait linkages, resistant IBC plants were crossed with OH88119 and BC3F2 progeny were evaluated for HR in the greenhouse. In these subsequent populations, the HR response was associated with the chromosome 11 markers (P < 0.0002) but not with the markers on chromosome 6 (P > 0.25). Independent F2 families were developed by crossing resistant IBC lines to OH8245, OH88119, and OH7530. These populations were genotyped, organized into classes based on chromosome 11 markers, and evaluated for resistance in the field. The PI 128216 locus on chromosome 11 provided resistance that was dependent on gene dosage and genetic background. These results define a single locus, Rx-4, from PI 128216, which provides resistance to bacterial spot race T3, has additive gene action, and is located on chromosome 11.
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Kolomiets, Mikhailo V., Richard J. Gladon, and David J. Hannapel. "Potato Lipoxygenase POTLX-3 Gene is Expressed In Response to Pathogens but Not Wounding." HortScience 33, no. 3 (1998): 499c—499. http://dx.doi.org/10.21273/hortsci.33.3.499c.
Full textAbstract:
Lipoxygenases are the first committed enzymes in biosynthetic pathways that produce jasmonic acid, methyl jasmonate, traumatin, fatty acid hydroperoxides, and volatile aldehydes. These pathways often function in growth- and defense-related processes in plants. Products of lipoxygenases may be the primary cause of the hypersensitive response (HR) because lipoxygenase by-products such as organic free radicals and active oxygen species are involved in cell membrane degradation during resistance responses against pathogens. In order to study lipoxygenase involvement in defense responses against pathogens, we have isolated and characterized a potato lipoxygenase gene that we have designated POTLX-3. POTLX-3 is not expressed in any potato organs, is not induced by wounding, but is strongly induced in leaves treated with ethylene, methyl jasmonate, or inoculum of Phytophthora infestans, the causal agent of potato late blight. In response to infection, POTLX-3 transcripts accumulate more rapidly in resistant lines than in susceptible lines. In resistant lines, the greatest amount of induction preceded the visual appearance of localized necrotic lesions, consistent with possible involvement of POTLX-3 in HR development. Expression of POTLX-3 also is activated in response to inoculation with the bacterial pathogen Pseudomonas syringae pv. phaseolicola, which causes strongly expressed HR in all potato cultivars. Thus, POTLX-3 expression is not a specific response to P. infestans, but rather a common response related to HR development against a broad range of pathogens. Pattern of POTLX-3 expression indicates that it may have a specific role in defense mechanisms against pathogens.