Identification and characterisation of barley (Hordeum vulgare) respiratory burst oxidase homologue family members
Damien J. Lightfoot A , Annette Boettcher A , Alan Little A , Neil Shirley B and Amanda J. Able A CA School of Agriculture, Food and Wine, The University of Adelaide, Waite Campus, PMB1, Glen Osmond, SA 5064, Australia.
B Australian Centre for Plant Functional Genomics, The University of Adelaide, Waite Campus, PMB 1, Glen Osmond, SA 5064, Australia.
C Corresponding author. Email: amanda.able@adelaide.edu.au
Functional Plant Biology 35(5) 347-359 https://doi.org/10.1071/FP08109
Submitted: 4 April 2008 Accepted: 29 May 2008 Published: 11 July 2008
Abstract
Respiratory burst oxidase homologues (RBOHs) of the human phagocyte gp91phox gene have been isolated from several plant species and the proteins that they encode have been shown to play important roles in the cellular response to biotic stress via the production of superoxide. In this study we have identified and preliminarily characterised six RBOHs from barley (Hordeum vulgare L.). Conservation of the genomic structure and conceptual protein sequence was observed between all six barley RBOH genes when compared with Arabidopsis and rice RBOH gene family members. Four of the six barley RBOH transcripts had wide-spread constitutive spatial expression patterns. The inducible expression profiles of HvRBOHF1 and HvRBOHF2 in response to infection by the necrotrophic fungal pathogens Pyrenophora teres f. teres Drechsler and Rhynchosporium secalis (Oudem) J. Davis were further characterised by quantitative real-time PCR (qPCR). Increased expression of both transcripts was observed in leaf epidermal tissue in response to infection, which is in keeping with a suggested role for both transcripts in the early oxidative burst during the plant response to pathogen invasion. This research provides a basis for further analysis and establishment of the roles of this RBOH family in various reactive oxygen species dependent processes in barley.
Additional keywords: NADPH oxidase, necrotroph, plant–pathogen interaction, reactive oxygen species.
Acknowledgements
We thank Dr Rafiqul Islam (School of Agriculture, Food and Wine, The University of Adelaide) for providing access to the barley : wheat addition lines, Dr Kazuhiro Sato (Research Institute for Bioresources, Okayama University) for supplying the BAC library filters, Margaret Pallotta (Australian Centre for Plant Functional Genomics, The University of Adelaide) for access to, and screening of, the barley BAC library filters, Dr Hugh Wallwork (South Australian Research and Development Institute) for providing the fungal isolates, Andrew Craig for providing the leaf epidermal peel cDNA and Dr Jason Able and Dr William Bovill (School of Agriculture, Food and Wine, The University of Adelaide) and Dr Catherine McLeod (Salk Institute) for reviewing the manuscript. This work was supported by the Molecular Plant Breeding Cooperative Research Centre and funded by the Grains Research and Development Corporation (Project No. CMB00006).
Able AJ
(2003) Role of reactive oxygen species in the response of barley to necrotrophic pathogens. Protoplasma 221, 137–143.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Amicucci E,
Gaschler K, Ward JM
(1999) NADPH oxidase genes from tomato (Lycopersicon esculentum) and curly-leaf pondweed (Potamogeton crispus). Plant Biology 1, 524–528.
| Crossref | GoogleScholarGoogle Scholar |
Baxter-Burrell A,
Yang Z,
Springer PS, Bailey-Serres J
(2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296, 2026–2028.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bedard K, Krause KH
(2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiological Reviews 87, 245–313.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Burton RA,
Shirley NJ,
King BJ,
Harvey AJ, Fincher GB
(2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiology 134, 224–236.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cao H,
Glazebrook J,
Clarke JD,
Volko S, Dong X
(1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chandra S, Low PS
(1995) Role of phosphorylation in elicitation of the oxidative burst in cultured soybean cells. Proceedings of the National Academy of Sciences of the United States of America 92, 4120–4123.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Delledonne M,
Zeier J,
Marocco A, Lamb C
(2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences of the United States of America 98, 13454–13459.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Doke N
(1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiological Plant Pathology 23, 345–357.
El-Benna J,
Dang PM,
Gougerot-Pocidalo MA, Elbim C
(2005) Phagocyte NADPH oxidase: a multicomponent enzyme essential for host defenses. Archivum Immunologiae et Therapiae Experimentalis 53, 199–206.
| PubMed |
Felsenstein J
(1989) PHYLIP – Phylogeny inference package (version 3.2). Cladistics 5, 164–166.
Finegold AA,
Shatwell KP,
Segal AW,
Klausner RD, Dancis A
(1996) Intramembrane bis-heme motif for transmembrane electron transport conserved in a yeast iron reductase and the human NADPH oxidase. Journal of Biological Chemistry 271, 31021–31024.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Foreman J,
Demidchik V,
Bothwell JH,
Mylona P, Miedema H , et al.
(2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grewal TS,
Rossnagel BG,
Pozniak CJ, Scoles GJ
(2007) Mapping quantitative trait loci associated with barley net blotch resistance. Theoretical and Applied Genetics 116, 529–539.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Groom QJ,
Torres MA,
Fordham-Skelton AP,
Hammond-Kosack KE,
Robinson NJ, Jones JD
(1996) rbohA, a rice homologue of the mammalian gp91phox
respiratory burst oxidase gene. The Plant Journal 10, 515–522.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Horton P,
Park KJ,
Obayashi T,
Fujita N,
Harada H,
Adams-Collier CJ, Nakai K
(2007) WoLF PSORT: protein localization predictor. Nucleic Acids Research 35, W585–W587.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hückelhoven R,
Dechert C,
Trujillo M, Kogel KH
(2001) Differential expression of putative cell death regulator genes in near-isogenic, resistant and susceptible barley lines during interaction with the powdery mildew fungus. Plant Molecular Biology 47, 739–748.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
International Rice Genome Sequencing Project
(2005) The map-based sequence of the rice genome. Nature 436, 793–800.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Islam AKMR,
Shepherd KW, Sparrow DHB
(1981) Isolation and characterization of euplasmic wheat–barley chromosome addition lines. Heredity 46, 161–174.
| Crossref | GoogleScholarGoogle Scholar |
Kauss H, Jeblick W
(1995) Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiology 108, 1171–1178.
| PubMed |
Kawasaki T,
Henmi K,
Ono E,
Hatakeyama S,
Iwano M,
Satoh H, Shimamoto K
(1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proceedings of the National Academy of Sciences of the United States of America 96, 10922–10926.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Keller T,
Damude HG,
Werner D,
Doerner P,
Dixon RA, Lamb C
(1998) A plant homolog of the neutrophil NADPH oxidase gp91
phox
subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. The Plant Cell 10, 255–266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Korzun L, Künzel G
(1996) The physical relationship of barley chromosome 5 (1H) to the linkage groups of rice chromosomes 5 and 10. Molecular & General Genetics 253, 225–231.
| Crossref | GoogleScholarGoogle Scholar |
Kwak JM,
Mori IC,
Pei ZM,
Leonhardt N,
Torres MA,
Dangl JL,
Bloom RE,
Bodde S,
Jones JD, Schroeder JI
(2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. The EMBO Journal 22, 2623–2633.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Levine A,
Tenhaken R,
Dixon R, Lamb C
(1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583–593.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mittler R,
Vanderauwera S,
Gollery M, Van Breusegem F
(2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Morel J,
Fromentin J,
Blein JP,
Simon-Plas F, Elmayan T
(2004) Rac regulation of NtrbohD, the oxidase responsible for the oxidative burst in elicited tobacco cell. The Plant Journal 37, 282–293.
| PubMed |
Mori IC, Schroeder JI
(2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiology 135, 702–708.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Murphy AM,
Holcombe LJ, Carr JP
(2000) Characteristics of salicylic acid-induced delay in disease caused by a necrotrophic fungal pathogen in tobacco. Physiological and Molecular Plant Pathology 57, 47–54.
| Crossref | GoogleScholarGoogle Scholar |
Nakai K, Kanehisa M
(1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14, 897–911.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nürnberger T, Scheel D
(2001) Signal transmission in the plant immune response. Trends in Plant Science 6, 372–379.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ohyanagi H,
Tanaka T,
Sakai H,
Shigemoto Y, Yamaguchi K , et al.
(2006) The Rice Annotation Project Database (RAP-DB): hub for Oryza sativa ssp. japonica genome information. Nucleic Acids Research 34, D741–D744.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ono E,
Wong HL,
Kawasaki T,
Hasegawa M,
Kodama O, Shimamoto K
(2001) Essential role of the small GTPase Rac in disease resistance of rice. Proceedings of the National Academy of Sciences of the United States of America 98, 759–764.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Potocký M,
Jones MA,
Bezvoda R,
Smirnoff N, Žárský V
(2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. The New Phytologist 174, 742–751.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rentel MC,
Lecourieux D,
Ouaked F,
Usher SL, Petersen L , et al.
(2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858–861.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rohe M,
Gierlich A,
Hermann H,
Hahn M,
Schmidt B,
Rosahl S, Knogge W
(1995) The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. The EMBO Journal 14, 4168–4177.
| PubMed |
Sagi M, Fluhr R
(2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiology 126, 1281–1290.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sagi M, Fluhr R
(2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiology 141, 336–340.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saisho D,
Myoraku E,
Kawasaki S,
Sato K, Takeda K
(2007) Construction and characterization of a bacterial artificial chromosome (BAC) library from the Japanese malting barley variety ‘Haruna Nijo’. Breeding Science 57, 29–38.
| Crossref | GoogleScholarGoogle Scholar |
Saitou N, Nei M
(1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
| PubMed |
Sarpeleh A,
Wallwork H,
Catcheside DEA,
Tate ME, Able AJ
(2007) Proteinaceous metabolites from Pyrenophora teres contribute to symptom development of barley net blotch. Phytopathology 97, 907–915.
| Crossref | GoogleScholarGoogle Scholar |
Segal AW,
West I,
Wientjes F,
Nugent JH,
Chavan AJ,
Haley B,
Garcia RC,
Rosen H, Scrace G
(1992) Cytochrome b
245 is a flavocytochrome containing FAD and the NADPH-binding site of the microbicidal oxidase of phagocytes. The Biochemical Journal 284, 781–788.
| PubMed |
Simon-Plas F,
Elmayan T, Blein JP
(2002) The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. The Plant Journal 31, 137–147.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smilde WD,
Halukova J,
Sasaki T, Graner A
(2001) New evidence for the synteny of rice chromosome 1 and barley chromosome 3H from rice expressed sequence tags. Genome 44, 361–367.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sutherland MW
(1991) The generation of oxygen radicals during host plant responses to infection. Physiological and Molecular Plant Pathology 39, 79–93.
| Crossref | GoogleScholarGoogle Scholar |
Thomma BP,
Eggermont K,
Tierens KF, Broekaert WF
(1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiology 121, 1093–1102.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thomma BP,
Eggermont K,
Broekaert WF, Cammue BPA
(2000) Disease development of several fungi on Arabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiology and Biochemistry 38, 421–427.
| Crossref | GoogleScholarGoogle Scholar |
Thompson JD,
Higgins DG, Gibson TJ
(1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Torres MA,
Onouchi H,
Hamada S,
Machida C,
Hammond-Kosack KE, Jones JDG
(1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox
). The Plant Journal 14, 365–370.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vignais PV
(2002) The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cellular and Molecular Life Sciences 59, 1428–1459.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Williams KJ,
Platz GJ,
Barr AR,
Cheong J,
Willsmore K,
Cakir M, Wallwork H
(2003) A comparison of the genetics of seedling and adult plant resistance to the spot form of net blotch (Pyrenophora teres f. maculata). Australian Journal of Agricultural Research 54, 1387–1394.
| Crossref | GoogleScholarGoogle Scholar |
Yamamizo C,
Doke N,
Yoshioka H, Kawakita K
(2007) Involvement of mitogen-activated protein kinase in the induction of StrbohC and StrbohD genes in response to pathogen signals in potato. Journal of General Plant Pathology 73, 304–313.
| Crossref | GoogleScholarGoogle Scholar |
Yoshida LS,
Saruta F,
Yoshikawa K,
Tatsuzawa O, Tsunawaki S
(1998) Mutation at histidine 338 of gp91phox depletes FAD and affects expression of cytochrome b
558 of the human NADPH oxidase. Journal of Biological Chemistry 273, 27879–27886.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yoshie Y,
Goto K,
Takai R,
Iwano M,
Takayama S,
Isogai A, Che F
(2005) Function of the rice gp91phox homologs OsrbohA and OsrbohE genes in ROS-dependent plant immune responses. Plant Biotechnology Journal 22, 127–135.
Yoshioka H,
Sugie K,
Park HJ,
Maeda H,
Tsuda N,
Kawakita K, Doke N
(2001) Induction of plant gp91
phox
homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Molecular Plant–Microbe Interactions 14, 725–736.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhao J,
Davis LC, Verpoorte R
(2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23, 283–333.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
