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TAL effector-dependent Bax gene expression in transgenic rice confers disease resistance to Xanthomonas oryzae pv. oryzae

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The hypersensitive response (HR) is a form of programmed cell death of plant cells occurring in the local region surrounding pathogen infection site to prevent the spread of infection by pathogens. Bax, a mammalian pro-apoptotic member of Bcl-2 family, triggers HR-like cell death when expressed in plants. However, constitutive expression of the Bax gene negatively affects plant growth and development. The Xa10 gene in rice (Oryza sativa) is an executor resistance (R) gene that confers race-specific disease resistance to Xanthomonas oryzae pv. oryzae strains harboring TAL effector gene AvrXa10. In this study, the Xa10 promoter was used to regulate heterologous expression of the Bax gene from mouse (Mus musculus) in Nicotiana benthamiana and rice. Cell death was induced in N. benthamiana after co-infiltration with the PXa10:Bax:TXa10 gene and the PPR1:AvrXa10:TNos gene. Transgenic rice plants carrying the PXa10:Bax:TXa10 gene conferred specific disease resistance to Xa10-incompatible X. oryzae pv. oryzae strain PXO99A(pHM1AvrXa10), but not to the Xa10-compatible strain PXO99A(pHM1). The resistance specificity was confirmed by the AvrXa10-dependent induction of the PXa10:Bax:TXa10 gene in transgenic rice. Our results demonstrated that the inducible expression of the Bax gene in transgenic rice was achieved through the control of the executor R gene promoter and the heterologous expression of the pro-apoptosis regulator gene in rice conferred disease resistance to X. oryzae pv. oryzae.

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Hypersensitive response


Programmed cell death

R :



Effector binding element


Bcl-2-associated X protein


  • Balint-Kurti P (2019) The plant hypersensitive response: concepts, control and consequences. Mol Plant Pathol 20:1163–1178

    PubMed  PubMed Central  Google Scholar 

  • Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J, Kim J-G, Underwood W, Chaudhuri B (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532

    Article  CAS  Google Scholar 

  • Danial NN (2007) BCL-2 family proteins: critical checkpoints of apoptotic cell death. Clin Cancer Res 13:7254–7263

    Article  CAS  Google Scholar 

  • Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205–219

    Article  CAS  Google Scholar 

  • 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. Proc Natl Acad Sci USA 98:13454–13459

    Article  CAS  Google Scholar 

  • Dong S, Zhang Z, Zheng X, Wang Y (2008) Mammalian pro-apoptotic bax gene enhances tobacco resistance to pathogens. Plant Cell Rep 27:1559–1569

    Article  CAS  Google Scholar 

  • Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG, Green DR (1999) Bax-induced caspase activation and apoptosis via cytochromec release from mitochondria is inhibitable by Bcl-xL. J Biol Chem 274:2225–2233

    Article  CAS  Google Scholar 

  • Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang G, White FF, Yin Z (2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–1125

    Article  CAS  Google Scholar 

  • Gu K, Sangha JS, Li Y, Yin Z (2008) High-resolution genetic mapping of bacterial blight resistance gene Xa10. Theor Appl Genet 116:155–163

    Article  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  CAS  Google Scholar 

  • Kauffman H (1973) An improved technique for evaluation of resistance of rice varieties to Xanthomonas oryzae. Plant Dis Rep 57:537–541

    Google Scholar 

  • Kawai-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300

    Article  CAS  Google Scholar 

  • Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648–651

    Article  CAS  Google Scholar 

  • Lacomme C, Santa Cruz S (1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc Natl Acad Sci USA 96:7956–7961

    Article  CAS  Google Scholar 

  • Luo D, Huguet-Tapia JC, Raborn RT, White FF, Brendel VP, Yang B (2021) The Xa7 resistance gene guards the rice susceptibility gene SWEET14 against exploitation by the bacterial blight pathogen. Plant Commun 2:100164

    Article  Google Scholar 

  • Nino-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324

    Article  CAS  Google Scholar 

  • Oltval ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell 74:609–619

    Article  Google Scholar 

  • Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819

    Article  CAS  Google Scholar 

  • Tian D, Yin Z (2009) Constitutive heterologous expression of avrXa27 in rice containing the R gene Xa27 confers enhanced resistance to compatible Xanthomonas oryzae strains. Mol Plant Pathol 10:29–39

    Article  CAS  Google Scholar 

  • Tian D, Wang J, Zeng X, Gu K, Qiu C, Yang X, Zhou Z, Goh M, Luo Y, Murata-Hori M, White FF, Yin Z (2014) The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell 26:497–515

    Article  CAS  Google Scholar 

  • Wang C, Zhang X, Fan Y, Gao Y, Zhu Q, Zheng C, Qin T, Li Y, Che J, Zhang M (2015) XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Mol Plant 8:290–302

    Article  CAS  Google Scholar 

  • Wang J, Zeng X, Tian D, Yang X, Wang L, Yin Z (2018) The pepper Bs4C proteins are localized to the endoplasmic reticulum (ER) membrane and confer disease resistance to bacterial blight in transgenic rice. Mol Plant Pathol 19:2025–2035

    Article  Google Scholar 

  • Wolter KG, Hsu Y-T, Smith CL, Nechushtan A, Xi X-G, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281–1292

    Article  CAS  Google Scholar 

  • Yoshinaga K, Arimura S-i, Hirata A, Niwa Y, Yun D-J, Tsutsumi N, Uchimiya H, Kawai-Yamada M (2005) Mammalian Bax initiates plant cell death through organelle destruction. Plant Cell Rep 24:408–417

    Article  CAS  Google Scholar 

  • Zeng X, Tian D, Gu K, Zhou Z, Yang X, Luo Y, White FF, Yin Z (2015) Genetic engineering of the Xa10 promoter for broad-spectrum and durable resistance to Xanthomonas oryzae pv. oryzae. Plant Biotechnol J 13:993–1001

    Article  CAS  Google Scholar 

  • Zhang J, Yin Z, White F (2015) TAL effectors and the executor R genes. Front Plant Sci 6:641

    CAS  PubMed  PubMed Central  Google Scholar 

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This work was supported by intramural research funds from Temasek Life Sciences Laboratory and a fund from the National Research Foundation (NRF), Prime Minister’s Office, Singapore, on the Disruptive & Sustainable Technology for Agricultural Precision (DiSTAP).

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THE authors thank RM for editing the manuscript. DT and ZY designed the experiments. YG, DT, JT and KHO conducted the experiments. YG, DT, JT and ZY wrote the article. All authors read and approved the article for publication.

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Correspondence to Zhongchao Yin.

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Gui, Y., Tian, D., Ong, K.H. et al. TAL effector-dependent Bax gene expression in transgenic rice confers disease resistance to Xanthomonas oryzae pv. oryzae. Transgenic Res 31, 119–130 (2022).

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