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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Functional study of Csrbohs in defence response against Xanthomonas citri ssp. citri

Pengying Mei https://orcid.org/0000-0002-8870-447X A , Zhen Song B , Zhong’an Li B and Changyong Zhou B C
+ Author Affiliations
- Author Affiliations

A College of Plant Protection, Southwest University, Chongqing 400715, China.

B Citrus Research Institute, Southwest University, Chongqing 400712, China.

C Corresponding author. Email: zhoucy@cric.cn

Functional Plant Biology 46(6) 543-554 https://doi.org/10.1071/FP18243
Submitted: 12 September 2018  Accepted: 1 February 2019   Published: 27 February 2019

Abstract

NADPH oxidases, encoded by rbohs (respiratory burst oxidase homologues), transfer electrons from NADPH to molecular oxygen (O2) to generate superoxide anion (O2•–), which is the first step in the formation of hydrogen peroxide (H2O2) in the plant–pathogen interaction system. In the present work, six citrus rbohs (Csrbohs) genes were identified in citrus, and their possible involvement in resistance to Xanthomonas citri ssp. citri (Xcc) was examined. Inoculation with Xcc promoted the H2O2 production and induced expression of the Csrbohs, especially CsrbohD. Results showed that CsrbohD was markedly induced in the resistant genotype kumquat ‘Luofu’ [Fortunella margarita (Lour.) Swingle] compared with grapefruit ‘Duncan’ [Citrus paradisi (Linn.) Macf.]. Virus-induced gene silencing (VIGS) of CsrbohD resulted in reduced resistance to Xcc in grapefruit, but not in kumquat. Compared with non-silenced plants, canker-like symptoms were observed earlier, and they were more extensive in the CsrbohD-silenced grapefruit. Silencing of CsrbohD also suppressed the Xcc induced reactive oxygen species (ROS) burst, and resulted in accumulation of more Xcc bacterial colonies. Taken together, these data indicate that CsrbohD promotes resistance to Xcc, especially in grapefruit.

Additional keywords: defense, gp91phox, NOX, X. citri.


References

Apel K, Hirt H (2014) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 728–749.

Asai S, Yoshioka H (2009) Nitric oxide as a partner of reactive oxygen species participates in disease resistance to nectrotophic pathogen Botryis cinerea in Nicotiana benthamiana. Molecular Plant-Microbe Interactions 22, 619–629.
Nitric oxide as a partner of reactive oxygen species participates in disease resistance to nectrotophic pathogen Botryis cinerea in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 19445587PubMed |

Benschop JJ, Mohammed S, O’flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Molecular & Cellular Proteomics 6, 1198–1214.
Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379–406.
A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.Crossref | GoogleScholarGoogle Scholar | 19400727PubMed |

Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Molecular Plant Pathology 4, 141–157.
Xanthomonas citri: breaking the surface.Crossref | GoogleScholarGoogle Scholar | 20569374PubMed |

Chen PS, Wang LY, Chen YJ, Tzeng KC, Chang SC, Chung KR, Lee MH (2012) Understanding cellular defence in kumquat and calamondin to citrus canker caused by Xanthomonas citri subsp. citri. Physiological and Molecular Plant Pathology 79, 1–12.
Understanding cellular defence in kumquat and calamondin to citrus canker caused by Xanthomonas citri subsp. citri.Crossref | GoogleScholarGoogle Scholar |

Chen D, Cao Y, Hong L, Kim D, Ahsan N, Thelen J, Stacey G (2017) Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture. Nature Communications 8, 2265–2277.
Extracellular ATP elicits DORN1-mediated RBOHD phosphorylation to regulate stomatal aperture.Crossref | GoogleScholarGoogle Scholar | 29273780PubMed |

Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500.
A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence.Crossref | GoogleScholarGoogle Scholar | 17625569PubMed |

Civerolo E (1984) Bacterial canker disease of citrus. Journal of the Rio Grande Valley Horticultural Society 37, 127–146.

Cui T, Yan J, Bin Y, Li Z, Zhou C, Song Z (2018) Construction of citrus leaf blotch virus infectious cDNA clone by yeast homologous recombination system Zhongguo Nong Ye Ke Xue 51, 1695–1705.

Das A (2003) Citrus canker – a review. Journal of Applied Horticulture 5, 52–60.

Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. The Plant Journal 47, 907–916.
Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis.Crossref | GoogleScholarGoogle Scholar | 16961732PubMed |

Doke N (1983) Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiological Plant Pathology 23, 359–367.
Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity.Crossref | GoogleScholarGoogle Scholar |

Duan S, Jia H, Pang Z, Teper D, White F, Jones J, Zhou C, Wang N (2018) Functional characterization of the citrus canker susceptibility gene CsLOB1. Molecular Plant Pathology 19, 1908–1916.
Functional characterization of the citrus canker susceptibility gene CsLOB1.Crossref | GoogleScholarGoogle Scholar |

Ebel RC, Kumar N (2012) Interference of oxidative metabolism in citrus by Xanthomonas citri pv citri. In ‘Oxidative stress – environmental induction and dietary antioxidants’. (Ed. V Lushchak) pp. 169–188. (In Tech: Rijeka, Croatia)

Francis MI, Redondo A, Burns JK, Graham JH (2009) Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker. European Journal of Plant Pathology 124, 283–292.
Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker.Crossref | GoogleScholarGoogle Scholar |

Gottwald TR, Graham JH, Civerolo EL, Barrett HC, Hearn CJ (1993) Differential host-range reaction of citrus and citrus relatives to citrus canker and citrus bacterial spot determined by leaf mesophyll susceptibility. Plant Disease 77, 1004–1009.
Differential host-range reaction of citrus and citrus relatives to citrus canker and citrus bacterial spot determined by leaf mesophyll susceptibility.Crossref | GoogleScholarGoogle Scholar |

Groom QJ, Torres MA, Fordhamskelton AP, Hammondkosack KE, Robinson NJ, Jones JDG (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. The Plant Journal 10, 515–522.
rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene.Crossref | GoogleScholarGoogle Scholar | 8811865PubMed |

Jia H, Wang N (2014) Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves. Plant Cell Reports 33, 1993–2001.
Xcc-facilitated agroinfiltration of citrus leaves: a tool for rapid functional analysis of transgenes in citrus leaves.Crossref | GoogleScholarGoogle Scholar | 25146436PubMed |

Kaur G, Sharma A, Guruprasad K, Pati PK (2014) Versatile roles of plant NADPH oxidases and emerging concepts. Biotechnology Advances 32, 551–563.
Versatile roles of plant NADPH oxidases and emerging concepts.Crossref | GoogleScholarGoogle Scholar | 24561450PubMed |

Khalaf A, Moore GA, Jones JB, Gmitter FG (2007) New insights into the resistance of Nagami kumquat to canker disease. Physiological and Molecular Plant Pathology 71, 240–250.
New insights into the resistance of Nagami kumquat to canker disease.Crossref | GoogleScholarGoogle Scholar |

Khalaf AA, Gmitter FG, Conesa A, Dopazo J, Moore GA (2011) Fortunella margarita transcriptional reprogramming triggered by Xanthomonas citri subsp. citri. BMC Plant Biology 11, 159–175.
Fortunella margarita transcriptional reprogramming triggered by Xanthomonas citri subsp. citri.Crossref | GoogleScholarGoogle Scholar | 22078099PubMed |

Kumar N, Ebel RC, Roberts PD (2011a) Antioxidant metabolism of grapefruit infected with Xanthomonas axonopodis pv. citri. Environmental and Experimental Botany 71, 41–49.
Antioxidant metabolism of grapefruit infected with Xanthomonas axonopodis pv. citri.Crossref | GoogleScholarGoogle Scholar |

Kumar N, Ebel RC, Roberts PD (2011b) H2O2 metabolism during sweet orange (Citrus sinensis L. Osb.) ‘Hamlin’ Xanthomonas axonopodis pv. citri interaction. Scientia Horticulturae 128, 465–472.
H2O2 metabolism during sweet orange (Citrus sinensis L. Osb.) ‘Hamlin’ Xanthomonas axonopodis pv. citri interaction.Crossref | GoogleScholarGoogle Scholar |

Kumar N, Ebel RC, Roberts PD (2011c) Superoxide dismutase activity in kumquat leaves infected with Xanthomonas axonopodis pv. citri. Journal of Horticultural Science & Biotechnology 86, 62–68.
Superoxide dismutase activity in kumquat leaves infected with Xanthomonas axonopodis pv. citri.Crossref | GoogleScholarGoogle Scholar |

Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275.
The oxidative burst in plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 15012264PubMed |

Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y (2014) The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host & Microbe 15, 329–338.
The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity.Crossref | GoogleScholarGoogle Scholar |

Li X, Zhang H, Tian L, Huang L, Liu S, Li D, Song F (2015) Tomato SlRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress. Frontiers of Plant Science 6, 463–476.
Tomato SlRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress.Crossref | GoogleScholarGoogle Scholar |

Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. Journal of Experimental Botany 60, 3221–3238.
Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling.Crossref | GoogleScholarGoogle Scholar | 19592501PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Lu D, Wu S, Gao X, Zhang Y, Shan L, Ping H (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proceedings of the National Academy of Sciences of the United States of America 107, 496–501.
A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity.Crossref | GoogleScholarGoogle Scholar | 20018686PubMed |

Ma LY, Zhang H, Sun LR, Jiao YH, Zhang GZ, Miao C, Hao FS (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. Journal of Experimental Botany 63, 305–317.
NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress.Crossref | GoogleScholarGoogle Scholar |

Mafra V, Kubo KS, Alves-Ferreira M, Ribeiro-Alves M, Stuart RM, Boava LP, Rodrigues CM, Machado MA (2012) Reference genes for accurate transcript normalization in citrus genotypes under different experimental conditions. PLoS One 7, e31263
Reference genes for accurate transcript normalization in citrus genotypes under different experimental conditions.Crossref | GoogleScholarGoogle Scholar | 22347455PubMed |

Mafra V, Martins PK, Francisco CS, Ribeiro-Alves M, Freitas-Astua J, Machado MA (2013) Candidatus Liberibacter americanus induces significant reprogramming of the transcriptome of the susceptible citrus genotype. BMC Genomics 14, 247–262.
Candidatus Liberibacter americanus induces significant reprogramming of the transcriptome of the susceptible citrus genotype.Crossref | GoogleScholarGoogle Scholar | 23586643PubMed |

Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45
The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.Crossref | GoogleScholarGoogle Scholar | 19690331PubMed |

Mittler R, Herr EH, Orvar BL, Van Camp W, Willekens H, Inze D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proceedings of the National Academy of Sciences of the United States of America 96, 14165–14170.
Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection.Crossref | GoogleScholarGoogle Scholar | 10570216PubMed |

Nühse TS, Bottrill AR, Jones AM, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. The Plant Journal 51, 931–940.
Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses.Crossref | GoogleScholarGoogle Scholar | 17651370PubMed |

Pachten A, Barz W (1999) Elicitor-stimulated oxidative burst and extracellular pH changes in protoplast suspensions prepared from cultured chickpea (Cicer arietinum L.) Cells. Journal of Plant Physiology 155, 795–797.
Elicitor-stimulated oxidative burst and extracellular pH changes in protoplast suspensions prepared from cultured chickpea (Cicer arietinum L.) Cells.Crossref | GoogleScholarGoogle Scholar |

Papadakis AK, Roubelakis-Angelakis KA (2002) Oxidative stress could be responsible for the recalcitrance of plant protoplasts. Plant Physiology and Biochemistry 40, 549–559.
Oxidative stress could be responsible for the recalcitrance of plant protoplasts.Crossref | GoogleScholarGoogle Scholar |

Proels RK, Oberhollenzer K, Pathuri IP, Hensel G, Kumlehn J, Hückelhoven R (2010) RBOHF2 of barley is required for normal development of penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei. Molecular Plant-Microbe Interactions 23, 1143–1150.
RBOHF2 of barley is required for normal development of penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei.Crossref | GoogleScholarGoogle Scholar | 20687804PubMed |

Ranjan A, Jayaraman D, Grau C, Hill JH, Whitham SA, Ané JM, Smith DL, Kabbage M (2018) The pathogenic development of Sclerotinia sclerotiorum in soybean requires specific host NADPH oxidases. Molecular Plant Pathology 19, 700–714.
The pathogenic development of Sclerotinia sclerotiorum in soybean requires specific host NADPH oxidases.Crossref | GoogleScholarGoogle Scholar | 28378935PubMed |

Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. The Plant Cell 12, 1633–1646.
Jasmonic acid signaling modulates ozone-induced hypersensitive cell death.Crossref | GoogleScholarGoogle Scholar | 11006337PubMed |

Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology 141, 336–340.
Production of reactive oxygen species by plant NADPH oxidases.Crossref | GoogleScholarGoogle Scholar | 16760484PubMed |

Schubert T, Sun X (1996) Bacterial citrus canker. Plant Pathology 377, 2–7.

Schubert TS, Rizvi SA, Sun X, Gottwald TR, Graham JH, Dixon WN (2001) Meeting the challenge of eradicating citrus canker in Florida – again. Plant Disease 85, 340–356.
Meeting the challenge of eradicating citrus canker in Florida – again.Crossref | GoogleScholarGoogle Scholar |

Sendín LN, Filippone MP, Orce IG, Rigano L, Enrique R, Peña L, Vojnov AA, Marano MR, Castagnaro AP (2012) Transient expression of pepper Bs2 gene in Citrus limon as an approach to evaluate its utility for management of citrus canker disease. Plant Pathology 61, 648–657.
Transient expression of pepper Bs2 gene in Citrus limon as an approach to evaluate its utility for management of citrus canker disease.Crossref | GoogleScholarGoogle Scholar |

Slisz AM, Rd BA, Mishchuk DO, Mccollum G, Slupsky CM (2012) Metabolomic analysis of citrus infection by ‘Candidatus Liberibacter’ reveals insight into pathogenicity. Journal of Proteome Research 11, 4223–4230.
Metabolomic analysis of citrus infection by ‘Candidatus Liberibacter’ reveals insight into pathogenicity.Crossref | GoogleScholarGoogle Scholar | 22698301PubMed |

Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2–BAK1 immune complex. Science 342, 624–628.
Structural basis for flg22-induced activation of the Arabidopsis FLS2–BAK1 immune complex.Crossref | GoogleScholarGoogle Scholar | 24114786PubMed |

Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Current Opinion in Plant Biology 14, 691–699.
Respiratory burst oxidases: the engines of ROS signaling.Crossref | GoogleScholarGoogle Scholar | 21862390PubMed |

Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397–403.
Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development.Crossref | GoogleScholarGoogle Scholar | 15939662PubMed |

Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America 99, 517–522.
Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.Crossref | GoogleScholarGoogle Scholar | 11756663PubMed |

Torres MA, Jones JDG, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics 37, 1130–1134.
Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 16170317PubMed |

Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiology 141, 373–378.
Reactive oxygen species signaling in response to pathogens.Crossref | GoogleScholarGoogle Scholar | 16760490PubMed |

Torres MA, Morales J, Sánchez-Rodríguez C, Molina A, Dangl JL (2013) Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. Molecular Plant-Microbe Interactions 26, 686–694.
Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein.Crossref | GoogleScholarGoogle Scholar | 23441575PubMed |

Trujillo M, Altschmied L, Schweizer P, Kogel KH, Hückelhoven R (2006) Respiratory burst oxidase homologue A of barley contributes to penetration by the powdery mildew fungus Blumeria graminis f. sp. hordei. Journal of Experimental Botany 57, 3781–3791.
Respiratory burst oxidase homologue A of barley contributes to penetration by the powdery mildew fungus Blumeria graminis f. sp. hordei.Crossref | GoogleScholarGoogle Scholar | 17046982PubMed |

Vives MC, Martín S, Ambrós S, Renovell Á, Navarro L, Pina JA, Moreno P, Guerri J (2008) Development of a full-genome cDNA clone of citrus leaf blotch virus and infection of citrus plants. Molecular Plant Pathology 9, 787–797.
Development of a full-genome cDNA clone of citrus leaf blotch virus and infection of citrus plants.Crossref | GoogleScholarGoogle Scholar | 19019007PubMed |

Wang Y, Fu XZ, Liu JH, Hong N (2011) Differential structure and physiological response to canker challenge between ‘Meiwa’ kumquat and ‘Newhall’ navel orange with contrasting resistance. Scientia Horticulturae 128, 115–123.
Differential structure and physiological response to canker challenge between ‘Meiwa’ kumquat and ‘Newhall’ navel orange with contrasting resistance.Crossref | GoogleScholarGoogle Scholar |

Wang F, Wang M, Liu X, Xu Y, Zhu S, Shen W, Zhao X (2017) Identification of putative genes involved in limonoids biosynthesis in citrus by comparative transcriptomic analysis. Frontiers of Plant Science 8, 782–793.
Identification of putative genes involved in limonoids biosynthesis in citrus by comparative transcriptomic analysis.Crossref | GoogleScholarGoogle Scholar |

Wi SJ, Ji NR, Park KY (2012) Synergistic biosynthesis of biphasic ethylene and reactive oxygen species in response to hemibiotrophic Phytophthora parasitica in tobacco plants. Plant Physiology 159, 251–265.
Synergistic biosynthesis of biphasic ethylene and reactive oxygen species in response to hemibiotrophic Phytophthora parasitica in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 22388490PubMed |

Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamotoa K (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. The Plant Cell 19, 4022–4034.
Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension.Crossref | GoogleScholarGoogle Scholar | 18156215PubMed |

Yoshioka H, Sugie K, Park HJ, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp91phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Molecular Plant-Microbe Interactions 14, 725–736.
Induction of plant gp91phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato.Crossref | GoogleScholarGoogle Scholar | 11386368PubMed |

Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JDG, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. The Plant Cell 15, 706–718.
Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar | 12615943PubMed |

Zhang X, Francis MI, Dawson WO, Graham JH, Orbović V, Triplett EW, Mou Z (2010) Over-expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker. European Journal of Plant Pathology 128, 91–100.
Over-expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker.Crossref | GoogleScholarGoogle Scholar |

Zhu QH, Stephen S, Kazan K, Jin G, Fan L, Taylor J, Dennis ES, Helliwell CA, Wang MB (2013) Characterization of the defense transcriptome responsive to Fusarium oxysporum-infection in Arabidopsis using RNA-seq. Gene 512, 259–266.
Characterization of the defense transcriptome responsive to Fusarium oxysporum-infection in Arabidopsis using RNA-seq.Crossref | GoogleScholarGoogle Scholar | 23107761PubMed |