XopR TTSS-effector regulates in planta growth, virulence of Indian strain of Xanthomonas oryzae pv. oryzae via suppressing reactive oxygen species production and cell wall-associated rice immune responses during blight induction
Geeta Verma A , Manju Sharma B and Kalyan K. Mondal A C
+ Author Affiliations
- Author Affiliations
A Division of Plant Pathology, ICAR-Indian Agricultural Research Institute, Pusa Campus, New Delhi, 110 012, India.
B Amity institute of Biotechnology, Amity University, Gurgaon (Manesar), Haryana 122 413, India.
C Corresponding author. Email: mondal_kk@rediffmail.com
Functional Plant Biology 45(5) 561-574 https://doi.org/10.1071/FP17147
Submitted: 18 May 2017 Accepted: 28 November 2017 Published: 8 January 2018
Abstract
Xanthomonas oryzae pv. oryzae (Xoo) causing bacterial blight of rice is a global problem in rice production. Phytopathogenic Xanthomonads overpower PAMP-triggered immunity (PTI) through secreting effectors via type III secretion system (TTSS). We previously screened the TTSS effector repository of an Indian strain of Xoo (race 4), a predominant strain from north-west India that contains 21 Xop and 18 TALE effectors. Here, we demonstrate that Xoo race 4 employs XopR for in planta colonisation, virulence and for the suppression of cell wall-associated immune responses in its natural host. XopR null mutant (Xoo ΔxopR) produced 2.6-fold less-severe lesion as compared with Xoo wild type. Xoo ΔxopR showed 1.58-fold reduced colonisation compared with wild indicating that XopR is required for maximum colonisation in rice. Xoo ΔxopR produced 3.8-fold more callose deposits compared with wild. Xoo ΔxopR caused significantly higher production of ROS in rice. RT-qPCR expression analysis of immune responsive genes of rice indicated 10- to 43-fold upregulation upon challenged inoculation with Xoo ΔxopR over wild. Altogether, our study revealed that XopR of Indian Xoo strain supports its in planta growth and contributes immensely for successful blight development through suppressing defence related events like reactive oxygen species production, callose deposition and transcript abundance of immune responsive genes during rice::Xoo interaction.
Additional keywords: callose, null mutant, ROS, TTSS, XopR.
References
Akimoto-Tomiyama C, Furutani A, Tsuge S, Washington Erica J, Nishizawa Y, Minami E, Ochiai H (2012) XopR, a Type III effector secreted by Xanthomonas oryzae pv. oryzae, suppresses microbe-associated molecular pattern triggered immunity in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 25, 505–514.| XopR, a Type III effector secreted by Xanthomonas oryzae pv. oryzae, suppresses microbe-associated molecular pattern triggered immunity in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkslSkt7w%3D&md5=c379b0cea54b0f94ae7add68f3a85ba2CAS |
Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annual Review of Phytopathology 42, 385–414.
| Type III secretion system effector proteins: double agents in bacterial disease and plant defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotFyrurw%3D&md5=0020cd05ae4fcf764347e230778440b3CAS |
Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.
| Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KlsLg%3D&md5=07b97418dc4ee2f6b02a050b43d5c873CAS |
An C, Mou Z (2012) Non-host defense response in a novel Arabidopsis-Xanthomonas citri subsp. citri pathosystem. PLoS One 7, e31130
| Non-host defense response in a novel Arabidopsis-Xanthomonas citri subsp. citri pathosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xitlyqtrg%3D&md5=7712ef3243f83e92987cc4d1a9c5725cCAS |
Bakshi M, Oelmüller R (2014) WRKY transcription factors: Jack of many trades in plants. Plant Signaling & Behavior 9, e27700
| WRKY transcription factors: Jack of many trades in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtFygt7c%3D&md5=c13a4349d5d56870a3b0b58796433923CAS |
Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R, Hammes UZ, Börnke F (2009) The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. Molecular Plant-Microbe Interactions 22, 655–664.
| The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlGkt74%3D&md5=41b07f50ddf8c5c79b4fce45c919a645CAS |
Bindschedler LV, Minibayeva F, Gardber SL, Gerrish C, Davies DR, Bolwell GP (2001) Early signaling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca21. New Phytologist 151, 185–194.
| Early signaling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca21.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltFGrsr4%3D&md5=92227b2bbce5e695afd33b247bd5e473CAS |
Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Bolwell GP (2006) Peroxidase dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. The Plant Journal 47, 851–863.
| Peroxidase dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsL7E&md5=7a8504983acb279f77172515269e71a6CAS |
Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor and wound induced oxidative cross linking of a proline rich plant cell wall protein, a novel, rapid defense response. Cell 70, 21–30.
| Elicitor and wound induced oxidative cross linking of a proline rich plant cell wall protein, a novel, rapid defense response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvVygtLk%3D&md5=a4431dfd21b571c9fc55185a328bbd14CAS |
Buttner D, He SY (2009) Type III protein secretion in plant pathogenic bacteria. Plant Physiology 150, 1656–1664.
| Type III protein secretion in plant pathogenic bacteria.Crossref | GoogleScholarGoogle Scholar |
Cheong H, Kim CY, Jeon JS, Lee BM, Sun Moon J, Hwang I (2013) Xanthomonas oryzae pv. oryzae type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice. PLoS One 8, e73346
| Xanthomonas oryzae pv. oryzae type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVCku7fJ&md5=d69863fdcae11d4bdddd578c6e452459CAS |
Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiology 145, 890–904.
| Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlemsrbN&md5=3ee1c301f3531a95b91e074568912d4cCAS |
Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences of the United States of America 97, 6640–6645.
| One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFais7c%3D&md5=b85cdd728366321900548da6f4e3baceCAS |
Didsbury J, Weber RF, Bokoch GM, Evans T, Snyderman R (1989) rac, A novel ras-related family of proteins that are botulinum toxin substrates. Journal of Biological Chemistry 264, 16378–16382.
Do Amaral AM, Toledo CP, Baptista JC, Machado JC (2005) Transformation of Xanthomonas axonopodis pv. citri by electroporation. Fitopatologia Brasileira 30, 292–294.
| Transformation of Xanthomonas axonopodis pv. citri by electroporation.Crossref | GoogleScholarGoogle Scholar |
Ellur RK, Khanna A, Gopala Krishnan S, Bhowmick PK, Vinod KK, Nagarajan M, Mondal KK, Singh NK, Prabhu KV, Singh AK (2016) Marker-aided incorporation of Xa38, a novel bacterial blight resistance gene, in PB1121 and comparison of its resistance spectrum with xa13 + Xa21. Scientific Reports 6, 29188
| Marker-aided incorporation of Xa38, a novel bacterial blight resistance gene, in PB1121 and comparison of its resistance spectrum with xa13 + Xa21.Crossref | GoogleScholarGoogle Scholar |
Gay C, Collins J, Gebicki JM (1999) Hydroperoxide assay with the ferric xylenol orange complex. Analytical Biochemistry 273, 149–155.
| Hydroperoxide assay with the ferric xylenol orange complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFyitrs%3D&md5=b6f19859e4d133c04f41a332028c3019CAS |
Goel AK, Lundberg D, Torres MA, Matthews R, Akimoto-Tomiyama C, Farmer L, Dangl JL, Grant SR (2008) The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants. Molecular Plant-Microbe Interactions 21, 361–370.
| The Pseudomonas syringae type III effector HopAM1 enhances virulence on water-stressed plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlyguro%3D&md5=d923569d273d5872c192f0c9f9207e70CAS |
Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000) RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for oxidative burst and hypersensitive cell death. The Plant Journal 23, 441–450.
| RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for oxidative burst and hypersensitive cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1eht7g%3D&md5=ac4e5a55634fd5b5fb3dd3a81e28a676CAS |
Hückelhoven R, Kogel KH (2003) Reactive oxygen intermediates in plant microbe interactions: who is who in powdery mildew resistance? Planta 216, 891–902.
Hückelhoven R, Fodor J, Preis C, Kogel KH (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiology 119, 1251–1260.
| Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation.Crossref | GoogleScholarGoogle Scholar |
Jabs T, Tschöpe M, Colling C, Hahlbrock K, Scheel D (1997) Elicitor stimulated ion fluxes and O2 – from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proceedings of the National Academy of Sciences of the United States of America 94, 4800–4805.
| Elicitor stimulated ion fluxes and O2 – from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVykur0%3D&md5=72e654737ff2f6623df18a2b8e167ca9CAS |
Jiang BL, He YQ, Cen WJ, Wei HY, Jiang GF, Jiang W, Hang XH, Feng JX, Lu GT, Tang DJ, Tang JL (2008) The type III secretion effector XopXccN of Xanthomonas campestris pv. campestris is required for full virulence. Research in Microbiology 159, 216–220.
| The type III secretion effector XopXccN of Xanthomonas campestris pv. campestris is required for full virulence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslaqsL0%3D&md5=54ba10604d9d0aec7cdadef827960b23CAS |
Jiang L, Wu J, Fan S, Li W, Dong L, Cheng Q, Xu P, Zhang S (2015) Isolation and characterization of a novel pathogenesis-related protein gene (GmPRP) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae. PLoS One 10, e0129932
| Isolation and characterization of a novel pathogenesis-related protein gene (GmPRP) with induced expression in soybean (Glycine max) during infection with Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar |
Jones JD, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=baefe36d1f9637835e022377466434abCAS |
Kauffman HE, Reddy APK, Hsieh SPY, Merca SD (1973) An improved technique for evaluating resistance to rice varieties of Xanthomonas oryzae. Plant Disease Reporter 57, 537–541.
Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports 21, 829–837.
Kim JG, Taylor KW, Hotson A, Keegan M, Schmelz EA, Mudgett MB (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas infected tomato leaves. The Plant Cell 20, 1915–1929.
| XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas infected tomato leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyrsbfO&md5=45915e8e91eb9715031708d53af2c4a4CAS |
Kim J, Li X, Roden JA, Taylor KW, Aakre CD, Su B, Lalonde S, Kirik A, Chen Y, Baranage G, McLane H, Martin GB, Mudgett MB (2009) Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato a typical receptor-like kinase and TFT1. The Plant Cell 21, 1305–1323.
| Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato a typical receptor-like kinase and TFT1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFamsLk%3D&md5=7ce9da94a33bec2e0bc2ee7ce053c63fCAS |
Kim JG, Stork W, Mudgett MB (2013) Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host & Microbe 13, 143–154.
| Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVyju7o%3D&md5=323e84c1f8ee8b2bc615af93435bd961CAS |
Kumar R, Mondal KK (2013) XopN T3SS effector is required for growth and pathogenicity by Xanthomonas axonopodis pv. punicae, the causal agent of bacterial blight of pomegranate. Physiological and Molecular Plant Pathology 84, 36–43.
| XopN T3SS effector is required for growth and pathogenicity by Xanthomonas axonopodis pv. punicae, the causal agent of bacterial blight of pomegranate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVaksr%2FM&md5=cefa257e8b154c5ad26fd10ef7e41a48CAS |
Kumar R, Soni M, Mondal KK (2016) XopN-TTSS effector of Xanthomonas axonopodis pv. punicae localizes to the plasma membrane and modulates ROS accumulation events during blight pathogenesis in pomegranate. Microbiological Research 193, 111–120.
| XopN-TTSS effector of Xanthomonas axonopodis pv. punicae localizes to the plasma membrane and modulates ROS accumulation events during blight pathogenesis in pomegranate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1ajtLbN&md5=b2956c0ffe183eea8d019f825e29c28cCAS |
Laloi C, Apel K, Danon A (2004) Reactive oxygen signaling: the latest news. Current Opinion in Plant Biology 7, 323–328.
| Reactive oxygen signaling: the latest news.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVamsLg%3D&md5=c7c0ed986d558f11577b7d92a437dfafCAS |
Lee SC, Hwang BK (2005) Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221, 790–800.
| Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXos1emt7c%3D&md5=cf46f3ef828394105b4f133b8fe9a54eCAS |
Lee BM, Park YJ, Park DS, Kang HW, Kim JG, Song ES, Park IC, Yoon UH, Hahn JH, Koo BS, Lee GB, Kim H, Park HS, Yoon KO, Kim JH, Jung C, Koh NH, Seo JS, Go SJ (2005) The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Research 33, 577–586.
| The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2qtrs%3D&md5=be7b5d655b6e004355b237c7a398f455CAS |
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.
| H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1Glu7Y%3D&md5=59ff84783819a9cb67c52ad8d4bf786aCAS |
Lewis MW, Leslie ME, Fulcher EH, Darnielle L, Healy PN, Youn JY, Liljegren SJ (2010) The SERK1 receptor-like kinase regulates organ separation in Arabidopsis flowers. The Plant Journal 62, 817–828.
| The SERK1 receptor-like kinase regulates organ separation in Arabidopsis flowers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslCgsrY%3D&md5=2c99e169ec30f7e98bc1561d3cae5f9aCAS |
Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in Brassinosteroid signal transduction. Cell 90, 929–938.
| A putative leucine-rich repeat receptor kinase involved in Brassinosteroid signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtV2htr0%3D&md5=f454923c841b3c73d67bd9a59eb47f9dCAS |
Metz M, Dahlbeck D, Morales CQ, Sady BA, Clark ET, Staskawicz BJ (2005) The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. The Plant Journal 41, 801–814.
| The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisleitr0%3D&md5=adb77ba33a0e04f676359f4fccfddc0dCAS |
Mondal KK (2016) Emerging phytobacterial diseases in India: research status and challenges. In ‘Perspectives of plant pathology in genomic era’. (Eds P Chowdappa, P Sharma, D Singh, AK Misra) pp. 167–178. (India Phytopathological Society: New Delhi)
Mondal KK, Meena BR, Junaid A, Verma G, Mani C, Majumder D, Khicher M, Kumar S, Banik S (2014) Pathotyping and genetic screening of type III effectors in Indian strains of Xanthomonas oryzae pv. oryzae causing bacterial leaf blight of rice. Physiological and Molecular Plant Pathology 86, 98–106.
| Pathotyping and genetic screening of type III effectors in Indian strains of Xanthomonas oryzae pv. oryzae causing bacterial leaf blight of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVags7fK&md5=86315151087bd7c9f3a254d349cf4239CAS |
Mondal KK, Verma G, Manju , Junaid A, Mani C (2016) Rice pathogen Xanthomonas oryzae pv. oryzae employs inducible hrp-dependent XopF type III effector protein for its growth, pathogenicity and for suppression of PTI response to induce blight disease. European Journal of Plant Pathology 144, 311–323.
| Rice pathogen Xanthomonas oryzae pv. oryzae employs inducible hrp-dependent XopF type III effector protein for its growth, pathogenicity and for suppression of PTI response to induce blight disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFKktL7L&md5=8579c95b23c85dd6c0c8a9b67a07cf31CAS |
Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annual Review of Plant Biology 56, 509–531.
| New insights to the function of phytopathogenic bacterial type III effectors in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVaqsrk%3D&md5=db24bac2f3842e485fce6e8e22e5c14fCAS |
Ochiai H, Inoue Y, Takeya M, Sasaki A, Kaku H (2005) Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Japan Agricultural Research Quarterly 39, 275–287.
| Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFKnsro%3D&md5=d389bef0ca0a2bd693fd3d84c86f1fe9CAS |
Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, Tsuge S, Furutani A, Ochiai H, Delcher AL, Kelley D, Madupu R, Puiu D, Radune D, Shumway M, Trapnell C, Aparna G, Jha G, Pandey A, Patil PB, Ishihara H, Meyer DF, Szurek B, Verdier V, Koebnik R, Dow JM, Ryan RP, Hirata H, Tsuyumu S, Won Lee S, Seo YS, Sriariyanum M, Ronald PC, Sonti RV, Van Sluys MA, Leach JE, White FF, Bogdanove AJ (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9, 204
| Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A.Crossref | GoogleScholarGoogle Scholar |
Sibanda T, Okoh AI (2008) In vitro evaluation of interactions between acetone extracts of Garcinia kola seeds and some antibiotics. African Journal of Biotechnology 7, 1672–1678.
| In vitro evaluation of interactions between acetone extracts of Garcinia kola seeds and some antibiotics.Crossref | GoogleScholarGoogle Scholar |
Song C, Yang B (2010) Mutagenesis of 18 Type III effectors reveals virulence function of XopZPXO99 in Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions 23, 893–902.
| Mutagenesis of 18 Type III effectors reveals virulence function of XopZPXO99 in Xanthomonas oryzae pv. oryzae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVart7o%3D&md5=b74091dc581ce1b2f1a76ddd7a5bdba5CAS |
Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. Proceedings of the National Academy of Sciences of the United States of America 92, 4158–4163.
| Function of the oxidative burst in hypersensitive disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXls1alt7s%3D&md5=915e5f39078b3a11b5bb851a98fc32a3CAS |
Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Planta 11, 1187–1194.
Vijayakumar H, Thamilarasan SK, Shanmugam A, Natarajan S, Jung HJ, Park JI, Kim HR, Chung MY, Nou IS (2016) Glutathione transferases superfamily: cold-inducible expression of distinct GST genes in Brassica oleracea. International Journal of Molecular Sciences 17, 1211
| Glutathione transferases superfamily: cold-inducible expression of distinct GST genes in Brassica oleracea.Crossref | GoogleScholarGoogle Scholar |
Wang L, Yang L, Zhang JX, Dong J, Yu J, Zhou J, Zhuge Q (2013) Cloning and characterization of a thaumatin-like protein gene PeTLP in Populus deltoides × P. euramericana cv. ‘Nanlin895’. Acta Physiologiae Plantarum 35, 2985–2998.
| Cloning and characterization of a thaumatin-like protein gene PeTLP in Populus deltoides × P. euramericana cv. ‘Nanlin895’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptlWktA%3D%3D&md5=dcdb7f679097dd6fbdd8e1966957d2ddCAS |
Wang S, Sun J, Fan F, Tan Z, Zou Y, Lu DA (2016) Xanthomonas oryzae pv. oryzae effector, XopR, associates with receptor-like cytoplasmic kinases and suppresses PAMP-triggered stomatal closure. Science China. Life Sciences 59, 897
| Xanthomonas oryzae pv. oryzae effector, XopR, associates with receptor-like cytoplasmic kinases and suppresses PAMP-triggered stomatal closure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtlyjs7fM&md5=63c5c20e9baec79266925e2e8b92f4a4CAS |
White FF, Potnis N, Jones JB, Koebnik R (2009) The type III effectors of Xanthomonas. Molecular Plant Pathology 10, 749–766.
| The type III effectors of Xanthomonas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFaitLfP&md5=7c0d98a8ebe574b5e1b228d4b0a24cb3CAS |
Yang B, Sugio A, White FF (2005) Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions 18, 142–149.
| Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXptFCktA%3D%3D&md5=dfe5094050b7ba23ba046b614fee6406CAS |
Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Sang X, Zhou JMA (2007) Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host & Microbe 1, 175–185.
| Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVGlur0%3D&md5=03d4218fb1409c6c26d0948720a3b06dCAS |
