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Silencing of an aquaporin gene diminishes bacterial blight disease in rice

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Abstract

The translocation of type III effectors of plant-pathogenic bacteria is required both for the expression of their role in virulence, and for the triggering of plant defenses. The effector translocation needs molecular associations between bacterial translocators and their recognition compounds situated in plant plasma membranes. We show here that rice aquaporin PIP1;3, a member of the plasma membrane intrinsic protein family, is implicated in translocation of a transcription activator-like (TAL) effector from the bacterial blight pathogen into the cytosol of rice cells. The TAL protein PthXo1 targets rice disease-susceptible gene SWEET11 to determine virulence of the bacterial strain PXO99A on susceptible rice variety Nipponbare. In Nipponbare, post-transcriptional gene silencing of PIP1;3 results in highly alleviated susceptibility and concomitantly decreased expression of SWEET11 as compared to levels of the bacterial virulence and the plant SWEET11 expression in the wild-type plant with normal transcription of PIP1;3. In coincidence, the efficiency in PthXo1 translocation is substantially reduced in PIP1;3-silenced rice lines in contrast to the wild-type plant. In the case of PIP1;3 silencing, moreover, the bacterial type III translocator Hpa1 loses the ability to mediate PthXo1 translocation from the bacterial cells into the cytosol of rice cells. By contrast, PIP1;3 silencing does not affect the performance of isolated Hpa1 as a pattern molecule to induce immune responses in rice. Our data suggest that rice aquaporin PIP1;3 is a candidate of disease-susceptible factor with functional relevance to PthXo1 translocation as a prerequisite of the bacterial virulence on the susceptible rice variety.

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References

  • Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414

    Article  CAS  Google Scholar 

  • Aljaafri WAR, McNeece BT, Lawaju BR, Sharma K, Niruala PM, Pant SR, Long DH, Lawrence KS, Lawrence GW, Klink VP (2017) A harpin elicitor induces the expression of a coiled-coil nucleotide binding leucine rich repeat (CC-NB-LRR) defense signaling gene and others functioning during defense to parasitic nematodes. Plant Physiol Biochem 121:161–175

    Article  CAS  Google Scholar 

  • Baumgart F, Rossi A, Verkman AS (2012) Light inactivation of water transport and protein-protein interactions of aquaporin-Killer Red chimeras. J Gen Physiol 139:83–91

    Article  PubMed Central  CAS  Google Scholar 

  • Bocsanczy AM, Nissinen RM, Oh CS, Beer SV (2008) HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol Plant Pathol 9:425–434

    Article  CAS  Google Scholar 

  • Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA targeting. Science 333:1843–1846

    Article  CAS  Google Scholar 

  • Büttner D (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76:262–310

    Article  PubMed Central  Google Scholar 

  • Büttner D (2016) Behind the lines-actions of bacterial type III effector proteins in plant cells. FEMS Microbiol Rev 40:894–937

    Article  PubMed Central  Google Scholar 

  • Büttner D, Nennstiel D, Klüsener B, Bonas U (2002) Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J Bacteriol 184:2389–2398

    Article  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Charkowski AO, Alfano JR, Preston G, Yuan J, He SY, Collmer A (1998) The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J Bacteriol 180:5211–5217

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chatterjee S, Chaudhury S, McShan AC, Kaur K, De GR (2013) Structure and biophysics of type III secretion in bacteria. Biochemistry 52:2508–2517

    Article  PubMed Central  CAS  Google Scholar 

  • Chen L, Qian J, Qu S, Long J, Yin Q, Zhang C, Wu X, Sun F, Wu T, Hayes M, Beer SV, Dong H (2008) Identification of specific fragments of HpaGXooc, a harpin protein from Xanthomonas oryzae pv. oryzicola, that induce disease resistance and enhanced growth in rice. Phytopathology 98:781–791

    Article  CAS  Google Scholar 

  • Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532

    Article  PubMed Central  CAS  Google Scholar 

  • Chen W, Yin X, Wang L, Tian J, Yang R, Liu D, Yu Z, Ma N, Gao J (2013) Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol Biol 83:219–233

    Article  CAS  Google Scholar 

  • Chen H, Chen J, Li M, Chang M, Xu K, Shang Z, Zhao Y, Palmer I, Zhang Y, McGill J, Alfano JR, Nishimura MT, Liu F, Fu ZQ (2017) A bacterial type III effector targets the master regulator of salicylic acid signalling, NPR1, to subvert plant immunity. Cell Host Microbe 22:777–788

    Article  CAS  Google Scholar 

  • Choi MS, Kim W, Lee C, Oh CS (2013) Harpins, multifunctional proteins secreted by gram-negative plant-pathogenic bacteria. Mol Plant-Microbe Interact 26:1115–1122

    Article  CAS  Google Scholar 

  • Cortes VA, Busso D, Maiz A, Arteaga A, Nervi F, Rigotti A (2014) Physiological and pathological implications of cholesterol. Fronti Biosci Landm 19:416–428

    Article  CAS  Google Scholar 

  • Dik DA, Marous DR, Fisher JF, Mobashery S (2017) Lytic transglycosylases: concinnity in concision of the bacterial cell wall. Crit Rev Biochem Mol Biol 52:503–542

    Article  PubMed Central  Google Scholar 

  • Domingues L, Ismail A, Charro N, Rodríguez-Escudero I, Holden DW, Molina M, Cid VJ, Mota LJ (2016) The Salmonella effector SteA binds phosphatidylinositol 4-phosphate for subcellular targeting within host cells. Cell Microbiol 18:949–969

    Article  CAS  Google Scholar 

  • Dong N, Niu M, Hu L, Yao Q, Zhou R, Shao F (2016) Modulation of membrane phosphoinositide dynamics by the phosphatidylinositide 4-kinase activity of the Legionella LepB effector. Nat Microbiol 12:16236

    Google Scholar 

  • Dortet L, Lombardi C, Cretin F, Dessen A, Filloux A (2018) Pore-forming activity of the Pseudomonas aeruginosa type III secretion system translocon alters the host epigenome. Nat Microbiol 3:378–386

    Article  CAS  Google Scholar 

  • Espina M, Ausar SF, Middaugh CR, Picking WD, Picking WL (2006) Spectroscopic and calorimetric analyses of invasion plasmid antigen D (IpaD) from Shigella flexneri reveal the presence of two structural domains. Biochemistry 45:9219–9227

    Article  CAS  Google Scholar 

  • Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863

    Article  CAS  Google Scholar 

  • Fu M, Xu M, Zhou T, Wang D, Tian S, Han L, Dong H, Zhang C (2014) Transgenic expression of a functional fragment of harpin protein Hpa1 in wheat induces the phloem-based defense to English grain aphid. J Exp Bot 65:1439–1453

    Article  PubMed Central  CAS  Google Scholar 

  • Furini A, Koncz C, Salamini F, Bartels D (1994) Agrobacterium-mediated transformation of the desiccation-tolerant plant Craterostigma plantagineum. Plant Cell Rep 14:102–1066

    CAS  PubMed  Google Scholar 

  • Gaytán MO, Martínez-Santos VI, Soto E, González-Pedrajo B (2016) Type three secretion system in attaching and effacing pathogens. Front Cell Infect Microbiol 6:129

    Article  PubMed Central  Google Scholar 

  • Gomes D, Agasse A, Thiébaud P, Delrot S, Gerós H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788:1213–1228

    Article  CAS  Google Scholar 

  • Guignot J, Tran VNG (2016) Bacterial control of pores induced by the type III secretion system: mind the gap. Front Immunol 7:84

    Article  PubMed Central  Google Scholar 

  • Gupta MK, Nathawat R, Sinha D, Haque AS, Sankaranarayanan R, Sonti RV (2015) Mutations in the predicted active site of Xanthomonas oryzae pv. oryzae XopQ differentially affect virulence, suppression of host innate immunity, and induction of the HR in a nonhost plant. Mol Plant-Microbe Interact 28:195–206

    Article  Google Scholar 

  • Haapalainen M, Engelhardt S, Küfner I, Li CM, Nürnberger T, Lee J, Romantschuk M, Taira S (2011) Functional mapping of harpin HrpZ of Pseudomonas syringae reveals the sites responsible for protein oligomerization, lipid interactions and plant defence induction. Mol Plant-Microbe Interact 12:151–166

    CAS  Google Scholar 

  • Hartmann N, Büttner D (2013) The inner membrane protein HrcV from Xanthomonas spp. is involved in substrate docking during type III secretion. Mol Plant-Microbe Interact 26:1176–1189

    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 

  • Hu S, Wang B, Qi Y, Lin H (2012) The Arg233Lys AQP0 mutation disturbs aquaporin 0-calmodulin interaction causing polymorphic congenital cataract. PLoS One 7:e37637

    Article  PubMed Central  CAS  Google Scholar 

  • Huang CT, Peretti SW, Bryers JD (1993) Plasmid retention and gene expression in suspended and biofilm cultures of recombinant Escherichia coli DH5α (pMJR1750). Biotechnol Bioeng 41:211–220

    Article  CAS  Google Scholar 

  • Ishii H, Hayashi F, Iyobe S, Hashimoto H (1991) Characterization and classification of Actinobacillus (Haemophilus) pleuropneumoniae plasmids. Am J Vet Res 52:1816–1820

    CAS  PubMed  Google Scholar 

  • Ji H, Dong H (2015a) Biological significance and topological basis of aquaporin-partnering protein-protein interactions. Plant Signal Behav 10:e1011947

    Article  Google Scholar 

  • Ji H, Dong H (2015b) Key steps in type III secretion system (T3SS) towards translocon assembly with potential sensor at plant plasma membrane. Mol Plant Pathol 16:762–773

    Article  CAS  Google Scholar 

  • Ji ZL, Song CF, Lu XZ, Wang JS (2011) Two coiled-coil regions of Xanthomonas oryzae pv. oryzae harpin differ in oligomerization and hypersensitive response induction. Amino Acids 40:381–392

    Article  CAS  Google Scholar 

  • Jin M, Berrout J, Chen L, O'Neil RG (2012) Hypotonicity-induced TRPV4 function in renal collecting duct cells: modulation by progressive cross-talk with Ca2+-activated K+ channels. Cell Calcium 51:131–139

    Article  CAS  Google Scholar 

  • Kim JF, Beer SV (1998) HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class. J Bacteriol 180:5203–5210

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kvitko BH, Ramos AR, Morello JE, Oh HS, Collmer A (2007) Identification of harpins in Pseudomonas syringae pv. tomato DC3000, which are functionally similar to HrpK1 in promoting translocation of type III secretion system effectors. J Bacteriol 189:8059–8072

    Article  PubMed Central  CAS  Google Scholar 

  • Lee J, Klessig DF, Nurnberger T (2001a) A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13:1079–1093

    Article  PubMed Central  CAS  Google Scholar 

  • Lee J, Klusener B, Tsiamis G, Stevens C, Neyt C, Tampakaki AP, Panopoulos NJ, Nöller J, Weiler EW, Cornelis GR, Mansfield JW, Nürnberger T (2001b) HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore in vitro. Proc Natl Acad Sci U S A 98:289–294

    CAS  PubMed  Google Scholar 

  • Lei Y, Kang SK, Gao J, Jia XS, Chen LL (2013) Improved annotation of a plant pathogen genome Xanthomonas oryzae pv. oryzae PXO99A. J Biomol Struct Dyn 31:342–450

    Article  CAS  Google Scholar 

  • Li YR, Che YZ, Zou HS, Cui YP, Guo W, Zou LF, Biddle EM, Yang CH, Chen GY (2011) Hpa2 required by HrpF to translocate Xanthomonas oryzae transcriptional activator-like effectors into rice for pathogenicity. Appl Environ Microbiol 77(11):3809–3818

    Article  PubMed Central  CAS  Google Scholar 

  • Li L, Wang H, Gago J, Cui H, Qian Z, Kodama N, Ji H, Tian S, Shen D, Chen Y, Sun F, Xia Z, Ye Q, Sun W, Flexas J, Dong H (2015) Harpin Hpa1 interacts with aquaporin PIP1;4 to promote the substrate transport and photosynthesis in Arabidopsis. Sci Rep 5:17207

    Article  PubMed Central  CAS  Google Scholar 

  • Lindsey Rose KM, Gourdie RG, Prescott AR, Quinlan RA, Crouch RK, Schey KL (2006) The C terminus of lens aquaporin 0 interacts with the cytoskeletal proteins filensin and CP49. Invest Ophthalmol Vis Sci 47:1562–1570

    Article  Google Scholar 

  • Matteï PJ, Faudry E, Job V, Izoré T, Attree I, Dessen A (2011) Membrane targeting and pore formation by the type III secretion system translocon. FEBS J 278:414–426

    Article  Google Scholar 

  • McQuate SE, Young AM, Silva-Herzog E, Bunker E, Hernandez M, de Chaumont F, Liu X, Detweiler CS, Palmer AE (2017) Long-term live-cell imaging reveals new roles for Salmonella effector proteins SseG and SteA. Cell Microbiol 19(1):e12641. https://doi.org/10.1111/cmi.12641

    Article  CAS  Google Scholar 

  • McShan AC, Kaur K, Chatterjee S, Knight KM, De Guzman RN (2016) NMR identification of the binding surfaces involved in the Salmonella and Shigella type III secretion tip-translocon protein-protein interactions. Proteins 84:1097–10107

    Article  PubMed Central  CAS  Google Scholar 

  • Mueller CA, Broz P, Cornelis GR (2008) The type III secretion system tip complex and translocon. Mol Microbiol 68:1085–1095

    Article  CAS  Google Scholar 

  • Nakazawa Y, Oka M, Furuki K, Mitsuishi A, Nakashima E, Takehana M (2011) The effect of the interaction between aquaporin 0 (AQP0) and the filensin tail region on AQP0 water permeability. Mol Vis 17:3191–3199

    PubMed Central  CAS  PubMed  Google Scholar 

  • Obrdlik P, El-Bakkoury M, Hamacher T, Cappellaro C, Vilarino C, Fleische C, Ellerbrok H, Kamuzinzi R, Ledent V, Blaudez D, Sanders D, Revuelta JL, Boles E, André B, Frommer WB (2004) K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. Proceeding of the National Academy of Sciences of the United States of America 101:12242–12247

    Article  CAS  Google Scholar 

  • Oh CS, Beer SV (2007) AtHIPM, an ortholog of the apple HrpN-interacting protein, is a negative regulator of plant growth and mediates the growth-enhancing effect of HrpN in Arabidopsis. Plant Physiol 145:426–436

    Article  PubMed Central  CAS  Google Scholar 

  • Peng J, Bao Z, Ren H, Wang J, Dong H (2004) Expression of harpinXoo in transgenic tobacco induces pathogen defense in the absence of hypersensitive response. Phytopathology 94:1048–1055

    Article  CAS  Google Scholar 

  • Péret B, Li G, Zhao J, Band LR, Voß U, Postaire O, Luu DT, Da IO, Casimiro I, Lucas M, Wells DM, Lazzerini L, Nacry P, King JR, Jensen OE, Schäffner AR, Maurel C, Bennett MJ (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 4:991–998

    Article  Google Scholar 

  • Piscatelli HL, Li M, Zhou D (2016) Dual 4- and 5-phosphatase activities regulate SopB-dependent phosphoinositide dynamics to promote bacterial entry. Cell Microbiol 18:705–719

    Article  CAS  Google Scholar 

  • Preston GM, Agre P (1991) Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proceeding of the National Academy of Sciences of the United States of America 88:11110–11114

    Article  CAS  Google Scholar 

  • Roden JA, Belt B, Ross JB, Tachibana T, Vargas J, Mudgett MB (2004) A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc Natl Acad Sci USA 101:16624–16629

    Article  CAS  Google Scholar 

  • Sang S, Li X, Gao R, You Z, Lü B, Liu P, Ma Q, Dong H (2012) Apoplastic and cytoplasmic location of harpin protein Hpa1Xoo plays different roles in H2O2 generation and pathogen resistance in Arabidopsis. Plant Mol Biol 79:375–391

    Article  CAS  Google Scholar 

  • Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Pühler A (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69–73

    Article  Google Scholar 

  • Scheibner F, Marillonnet, Büttner D (2017) The TAL effector AvrBs3 from Xanthomonas campestris pv. vesicatoria contains multiple export signals and can enter plant cells in the absence of the type III secretion translocon. Front Microbiol 8:2180

    Article  PubMed Central  Google Scholar 

  • Shi LW (2012) SPSS19.0 statistical analysis from accidence to conversance Tsinghua. University Press, Beijing, pp 109–143

    Google Scholar 

  • Sinha D, Gupta MK, Patel HK, Ranjan A, Sonti RV (2013) Cell wall degrading enzyme induced rice innate immune responses are suppressed by the type 3 secretion system effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLoS One 26:e75867

    Article  Google Scholar 

  • Sjöhamn J, Hedfalk K (2014) Unraveling aquaporin interaction partners. Biochim Biophys Acta 1840:1614–1623

    Article  Google Scholar 

  • Tamma G, Lasorsa D, Ranieri M, Mastrofrancesco L, Valenti G, Svelto M (2011) Integrin signalling modulates AQP2 trafficking via Arg-Gly-Asp (RGD) motif. Cell Physiol Biochem 27:739–748

    Article  CAS  Google Scholar 

  • Tejeda-Dominguez F, Huerta-Cantillo J, Chavez-Dueñas L, Navarro-Garcia F (2017) A novel mechanism for protein delivery by the type 3 secretion system for extracellularly secreted proteins. MBio 8:2

    Article  Google Scholar 

  • Tian S, Wang X, Li P, Wang H, Ji H, Xie J, Qiu Q, Shen D, Dong H (2016) Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–1650

    Article  PubMed Central  CAS  Google Scholar 

  • Tsuge S, Furutani A, Fukunaka R, Oku T, Tsuno K, Ochiai H, Inoue Y, Kaku H, Kubo Y (2002) Expression of Xanthomonas oryzae pv. oryzae hrp genes in XOM2, a novel synthetic medium. J Gen Plant Pathol 68:363–371

    Article  CAS  Google Scholar 

  • Verkman AS (2013) Aquaporins. Curr Biol 23:R52–R55

    Article  PubMed Central  CAS  Google Scholar 

  • Wang XY, Song CF, Miao WG, Ji ZL, Wang X, Zhang Y, Zhang JH, Hu JS, Borth W, Wang JS (2008) Mutations in the N-terminal coding region of the harpin protein Hpa1 from Xanthomonas oryzae cause loss of hypersensitive reaction induction in tobacco. Appl Microbiol Biotechnol 81:359–369

    Article  CAS  Google Scholar 

  • Wang X, Zhang L, Ji H, Mo X, Li P, Wang J, Dong H (2018) Hpa1 is a type III translocator in Xanthomonas oryzae pv. oryzae. BMC Microbiol 18:105

    Article  PubMed Central  Google Scholar 

  • Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85–88

    Article  CAS  Google Scholar 

  • White FF, Potnis N, Jones JB, Koebnik R (2009) The type III effectors of Xanthomonas. Mol Plant Pathol 10:749–766

    Article  CAS  Google Scholar 

  • Wudick MM, Luu DT, Maurel C (2009) A look inside: localization patterns and functions of intracellular plant aquaporins. New Phytol 184:289–302

    Article  CAS  Google Scholar 

  • Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N, Uchihashi K, Ishihama N, Kishi-Kaboshi M, Takahashi A, Tsuge S, Ochiai H, Tada Y, Shimamoto K, Yoshioka H, Kawasaki T (2013) A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 13:347–357

    Article  CAS  Google Scholar 

  • Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proceeding of the National Academy of Sciences of the United States of America 103:10503–10508

    Article  CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao Y, Li C, Ge J, Xu M, Zhu Q, Wu T, Guo A, Xie J, Dong H (2014) Recessive mutation identifies auxin-repressed protein ARP1 that regulates growth and disease resistance in tobacco. Mol Plant-Microbe Interact 27:638–654

    Article  CAS  Google Scholar 

  • Zhu WG, MaGbanua MM, White FF (2000) Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J Bacteriol 182:1844–1853

    Article  PubMed Central  CAS  Google Scholar 

  • Zwack EE, Feeley EM, Burton AR, Hu B, Yamamoto M, Kanneganti TD, Bliska JB, Coers J, Brodsky IE (2017) Guanylate binding proteins regulate inflammasome activation in response to hyperinjected Yersinia translocon components. Infect Immun 85:10

    Article  Google Scholar 

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Acknowledgements

We thank Professor Bing Yang (Department of Genetics, Development, and Cell Biology, Iowa State University) for the gift of pthXo1 vector and our colleague Professor Ling Jiang (Agronomy College, Nanjing Agricultural University) for assistance in rice transformation. This work was supported by grants from China National Key Research and Development Plan (grant number 2017YFD0200901), Natural Science Foundation of China (grant number 31772247), and Talent Recruitment Funding of Shandong Agricultural University (grant number 20171226).

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  1. Department of Plant Pathology, Shandong Agricultural University, Taian, 271018, Shandong Province, China

    Liyuan Zhang & Hansong Dong

  2. Department of Plant Pathology, Nanjing Agricultural University, Nanjing, 210095, Jiangsu Province, China

    Liyuan Zhang, Yiqun Hu, Ping Li, Xiaobing Wang & Hansong Dong

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  1. Liyuan Zhang
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Correspondence to Hansong Dong.

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Zhang, L., Hu, Y., Li, P. et al. Silencing of an aquaporin gene diminishes bacterial blight disease in rice. Australasian Plant Pathol. 48, 143–158 (2019). https://doi.org/10.1007/s13313-018-0609-1

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