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Hydrogen peroxide is indispensable to Xanthomonas oryzae pv. oryzae-induced hypersensitive response and nonhost resistance in Nicotiana benthamiana

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Abstract

Nonhost resistance is a durable and broad-spectrum resistance in plants that are outside of the given pathogens’ host range. Previously, we reported that the important pathogen Xanthomonas oryzae pv. oryzae (Xoo), which causes bacterial blight disease in rice, rapidly triggers the hypersensitive response (HR) and nonhost resistance in its nonhost plant Nicotiana benthamiana. In this study, we optimized the conditions, including the inoculum concentration, the leaf positions for inoculation and the plant post-inoculation growth temperature, to induce Xoo-triggered HR and nonhost resistance. We demonstrated that inoculating with a Xoo concentration of 1 × 108 cfu mL−1 in fully expanded leaves of N. benthamiana plants resulted in the strongest induction of HR and nonhost resistance. Furthermore, we probed the role of hydrogen peroxide (H2O2) in Xoo-induced HR and nonhost resistance. An exogenous supply of H2O2 accelerated Xoo-induced HR, while the elimination of H2O2 by the application of a catalase blocked the HR-mediated suppression of bacterial growth in N. benthamiana. Moreover, ∆hrpD6 and ∆hrcU Xoo mutants, which are deficient in H2O2 production, did not show an induction of HR, while another Xoo mutant, ∆hpa1, caused a strong H2O2 accumulation prior to its delayed HR induction. Collectively, our results reveal that H2O2 is indispensable to Xoo-induced HR and nonhost resistance in N. benthamiana.

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References

  • Bednarek P, Osbourn A (2009) Plant-microbe interactions: chemical diversity in plant defense. Science 324:746–748

    Article  CAS  PubMed  Google Scholar 

  • Bestwick CS, Brown IR, Bennett M, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209–221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bestwick CS, Brown IR, Mansfield JW (1998) Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiol 118:1067–1078

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bettgenhaeuser J, Gilbert B, Ayliffe M, Moscou MJ (2014) Nonhost resistance to rust pathogens–a continuation of continua. Front Plant Sci 5:664

    Article  PubMed Central  PubMed  Google Scholar 

  • Budde IP, Ullrich MS (2000) Interactions of Pseudomonas syringae pv. glycinea with host and nonhost plants in relation to temperature and phytotoxin synthesis. Mol Plant-Microbe Interact 13:951–961

    Article  CAS  PubMed  Google Scholar 

  • Chang SW, Hwang BK (2003) Effects of plant age, leaf position, inoculum density, and wetness period on Bipolaris coicis infection in adlays of differing resistance. Plant Dis 87:821–826

    Article  Google Scholar 

  • Fan J, Crooks C, Creissen G, Hill L, Fairhurst S, Doerner P, Lamb C (2011) Pseudomonas sax genes overcome aliphatic isothiocyanate–mediated non-host resistance in Arabidopsis. Science 331:1185–1188

    Article  CAS  PubMed  Google Scholar 

  • Glazener JA, Orlandi EW, Baker CJ (1996) The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol 110:759–763

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guo X, Zou H, Li Y, Zou L, Chen G (2010) HrpD6 gene determines Xanthomonas oryzae pv. oryzae to trigger hypersensitive response in tobacco and pathogenicity in rice. Acta Microbiol Sin 50:1155–1163

  • Jahnen W, Hahlbrock K (1988) Cellular localization of nonhost resistance reactions of parsley (Petroselinum crispum) to fungal infection. Planta 173:197–204

    Article  CAS  PubMed  Google Scholar 

  • Li W, Xu YP, Zhang ZX, Cao WY, Li F, Zhou X, Chen GY, Cai XZ (2012) Identification of genes required for nonhost resistance to Xanthomonas oryzae pv. oryzae reveals novel signaling components. PLoS One 7, e42796

  • Lu M, Tang X, Zhou JM (2001) Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell 13:437–447

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A (2010) S-glycoprotein-like protein regulates defense responses in Nicotiana plants against Ralstonia solanacearum. Plant Physiol 152:2023–2035

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant–fungal interactions. Plant J 29:257–268

    Article  CAS  PubMed  Google Scholar 

  • Mysore KS, Ryu CM (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97–104

    Article  CAS  PubMed  Google Scholar 

  • Niks RE, Marcel TC (2009) Nonhost and basal resistance: how to explain specificity? New Phytol 182:817–828

    Article  PubMed  Google Scholar 

  • Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H, Ellerström M, Andersson MX (2013) Arabidopsis phospholipase Dδ is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol 163:896–906

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pullman G, DeVay J (1982) Epidemiology of verticillium wilt of cotton: a relationship between inoculum density and disease progression. Phytopathol 72:549–554

    Article  Google Scholar 

  • Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A, Mysore KS (2012) Glycolate oxidase modulates reactive oxygen species–mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24:336–352

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16:117–125

    Article  CAS  PubMed  Google Scholar 

  • Senthil-kumar M, Mysore KS (2012) Ornithine–delta–aminotransferase and proline dehydrogenase genes play a role in non–host disease resistance by regulating pyrroline–5–carboxylate metabolism–induced hypersensitive response. Plant Cell Environ 35:1329–1343

    Article  CAS  PubMed  Google Scholar 

  • Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu Rev Phytopathol 51:407–427

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99:517–522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • VanEtten HD, Mansfield JW, Bailey JA, Farmer EE (1994) Two classes of plant antibiotics: phytoalexins versus “Phytoanticipins”. Plant Cell 6:1191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JD, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15:706–718

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zurbriggen MD, Carrillo N, Tognetti VB, Melzer M, Peisker M, Hause B, Hajirezaei MR (2009) Chloroplast–generated reactive oxygen species play a major role in localized cell death during the non–host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J 60:962–973

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Program for the Genetically Modified Organisms Breeding Major Projects under Grant (number 2014ZX0800905B); the Changjiang Scholars and Innovative Research Team in University under Grant (number IRT0943); and the Program for New Century 151 Talents of Zhejiang Province.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou, 310058, China

    Wen Li, Juan Yang & Xin-Zhong Cai

  2. Center of Analysis and Measurement, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou, 310058, China

    You-Ping Xu

  3. State Key Laboratory of Rice Biology, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou, 310058, China

    Xin-Zhong Cai

  4. School of Agriculture and Biology, Shanghai Jiaotong University/Key Laboratory of Urban (South) by Ministry of Agriculture, Shanghai, 200240, China

    Gong-You Chen

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  1. Wen Li
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  2. You-Ping Xu
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  3. Juan Yang
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  4. Gong-You Chen
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  5. Xin-Zhong Cai
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Correspondence to Xin-Zhong Cai.

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Fig. S1

The toxicity of exogenous H2O2 at different concentrations to leaf tissues in N. benthamiana. (DOC 161 kb)

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Li, W., Xu, YP., Yang, J. et al. Hydrogen peroxide is indispensable to Xanthomonas oryzae pv. oryzae-induced hypersensitive response and nonhost resistance in Nicotiana benthamiana . Australasian Plant Pathol. 44, 611–617 (2015). https://doi.org/10.1007/s13313-015-0376-1

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  • DOI: https://doi.org/10.1007/s13313-015-0376-1

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