Interaction of Rice and Xanthomonas TAL Effectors

  • Si Nian Char
  • Sangryeol Park
  • Bing Yang


Bacterial blight of rice, caused by the bacterial pathogen Xanthomonas oryzae pv. oryzae (Xoo) in rice, represents one of the most well-studied crop diseases and is also well-known as a model for studying host/microbe interaction. TALEs (transcription activator-like effectors), as a group of pathogenesis factors and once translocated into the host cells from pathogen, recognize and activate host genes to condition disease susceptibility and also trigger host resistance responses dependent on the nature of target genes in plants. TALEs and their target genes have become the foci of the molecular battles between Xoo and rice. The continuing battles have led to incredibly diverse virulence mechanisms in pathogen and counteracting defense mechanisms in rice. Extensive efforts have been made to understand the TALE biology, identify host target genes, and elucidate their interaction and resulting physiological relevance to rice blight and other crop diseases. This review aims to summarize how much we have learned about TALEs and their role in bacterial blight of rice, as well as associated susceptibility and resistance genes in the host. The review also intends to provide a prospect of engineering genetic resistance by applying precise genome editing of TALE-associated target genes in rice.


TALE Rice Oryza Xanthomonas Bacterial blight Resistance Susceptibility Immunity SWEET gene 



The authors gratefully acknowledge grant support from the Rural Development Administration (RDA) of the Republic of Korea (PJ012098 to S.P. and B.Y.) and the Bill and Melinda Gates Foundation (Grand Challenge Program, a subaward from Carnegie Institute for Science to BY).


  1. Allen BL, Taatjes DJ (2015) The mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol 16:155–166CrossRefPubMedPubMedCentralGoogle Scholar
  2. Al-Saadi A, Reddy JD, Duan YP, Brunings AM, Yuan Q, Gabriel DW (2007) All five host-range variants of Xanthomonas citri carry one pthA homolog with 17.5 repeats that determines pathogenicity on citrus, but none determine host-range variation. Mol Plant-Microbe Interact 20:934–943CrossRefPubMedGoogle Scholar
  3. Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–3876CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bai J, Choi SH, Ponciano G, Leung H, Leach JE (2000) Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Mol Plant-Microbe Interact 13:1322–1329CrossRefPubMedGoogle Scholar
  5. Bart R, Cohn M, Kassen A, McCallum EJ, Shybut M, Petriello A, Krasileva K, Dahlbeck D, Medina C, Alicai T, Kumar L, Moreira LM, Rodrigues Neto J, Verdier V, Santana MA, Kositcharoenkul N, Vanderschuren H, Gruissem W, Bernal A, Staskawicz BJ (2012) High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proc Natl Acad Sci U S A 109:E1972–E1979CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blanvillain-Baufumé S, Reschke M, Solé M, Auguy F, Doucoure H, Szurek B, Meynard D, Portefaix M, Cunnac S, Guiderdoni E, Boch J, Koebnik R (2017) Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnol J 15:306–317CrossRefPubMedGoogle Scholar
  7. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–1512CrossRefPubMedGoogle Scholar
  8. Boch J, Bonas U, VanAlfen N, Bruening G, Leach J (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436CrossRefPubMedGoogle Scholar
  9. Bogdanove A, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394–401CrossRefPubMedGoogle Scholar
  10. Bogdanove AJ, Koebnik R, Lu H, Furutani A, Angiuoli SV, Patil PB, Van Sluys MA, Ryan RP, Meyer DF, Han SW, Aparna G, Rajaram M, Delcher AL, Phillippy AM, Puiu D, Schatz MC, Shumway M, Sommer DD, Trapnell C, Benahmed F, Dimitrov G, Madupu R, Radune D, Sullivan S, Jha G, Ishihara H, Lee SW, Pandey A, Sharma V, Sriariyanun M, Szurek B, Vera-Cruz CM, Dorman KS, Ronald PC, Verdier V, Dow JM, Sonti RV, Tsuge S, Brendel VP, Rabinowicz PD, Leach JE, White FF, Salzberg SL (2011) Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J Bacteriol 193:5450–5464CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bonas U, Schulte R, Fenselau S, Minsavage GV, Staskawicz BJ, Stall RE (1991) Isolation of a gene cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol Plant-Microbe Interact 4:81–88CrossRefGoogle Scholar
  12. Booher NJ, Carpenter SC, Sebra RP, Wang L, Salzberg SL, Leach JE, Bogdanove AJ (2015) Single molecule real-time sequencing of Xanthomonas oryzae genomes reveals a dynamic structure and complex TAL (transcription activator-like) effector gene relationships. Microb Genom 1:e000032PubMedCentralGoogle Scholar
  13. Buttner D, Bonas U (2002) Getting across – bacterial type III effector proteins on their way to the plant cell. EMBO J 21:5313–5322CrossRefPubMedPubMedCentralGoogle Scholar
  14. Castiblanco LF, Gil J, Rojas A, Osorio D, Gutiérrez S, Muñoz-Bodnar A, Perez-Quintero AL, Koebnik R, Szurek B, López C, Restrepo S, Verdier V, Bernal AJ (2013) TALE1 from Xanthomonas axonopodis pv. manihotis acts as a transcriptional activator in plant cells and is important for pathogenicity in cassava plants. Mol Plant Pathol 14:84–95CrossRefPubMedGoogle Scholar
  15. 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 468:527–532CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cohn M, Bart RS, Shybut M, Dahlbeck D, Gomez M, Morbitzer R, Hou BH, Frommer WB, Lahaye T, Staskawicz BJ (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol Plant-Microbe Interact 27:1186–1198CrossRefPubMedGoogle Scholar
  18. Cohn M, Morbitzer R, Lahaye T, Staskawicz BJ (2016) Comparison of gene activation by two TAL effectors from Xanthomonas axonopodis pv. manihotis reveals candidate host susceptibility genes in cassava. Mol Plant Pathol 17:875–889CrossRefPubMedGoogle Scholar
  19. Cox KL, Meng F, Wilkins KE, Li F, Wang P, Booher NJ, Carpenter SCD, Chen LQ, Zheng H, Gao X, Zheng Y, Fei Z, Yu JZ, Isakeit T, Wheeler T, Frommer WB, He P, Bogdanove AJ, Shan L (2017) TAL effector driven induction of a SWEET gene confers susceptibility to bacterial blight of cotton. Nat Commun 8:15588CrossRefPubMedPubMedCentralGoogle Scholar
  20. Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.) Genetics 165:759–769PubMedPubMedCentralGoogle Scholar
  21. Grau J, Reschke M, Erkes A, Streubel J, Morgan RD, Wilson GG, Koebnik R, Boch J (2016) AnnoTALE: bioinformatics tools for identification, annotation, and nomenclature of TALEs from Xanthomonas genomic sequences. Sci Rep 6:21077CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang GL, White FF, Yin Z (2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–1125CrossRefPubMedGoogle Scholar
  23. Gu K, Tian D, Qiu C, Yin Z (2009) Transcription activator-like type III effector AvrXa27 depends on OsTFIIA gamma 5 for the activation of Xa27 transcription in rice that triggers disease resistance to Xanthomonas oryzae pv. oryzae. Mol Plant Pathol 10:829–835CrossRefPubMedGoogle Scholar
  24. Hopkins CM, White FF, Choi SH, Guo A, Leach JE (1992) Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact 5:451–459CrossRefPubMedGoogle Scholar
  25. Hu Y, Zhang J, Jia H, Sosso D, Li T, Frommer WB, Yang B, White FF, Wang N, Jones JB (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci U S A 111:E521–E529CrossRefPubMedPubMedCentralGoogle Scholar
  26. Huang S, Antony G, Li T, Liu B, Obasa K, Yang B, White FF (2016) The broadly effective recessive resistance gene xa5 of rice is a virulence effector-dependent quantitative trait for bacterial blight. Plant J 86:186–194CrossRefPubMedGoogle Scholar
  27. Huguet-Tapia JC, Peng Z, Yang B, Yin Z, Liu S, White FF (2016) Complete genome sequence of the African strain AXO1947 of Xanthomonas oryzae pv. oryzae. Genome Announc 4:e01730–e01715CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hutin M, Sabot F, Ghesquière A, Koebnik R, Szurek B (2015) A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. Plant J 84:694–703CrossRefPubMedGoogle Scholar
  29. Iyer AS, McCouch SR (2004) The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol Plant-Microbe Interact 17:1348–1354CrossRefPubMedGoogle Scholar
  30. Ji Z, Ji C, Liu B, Zou L, Chen G, Yang B (2016) Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat Commun 7:13435CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jiang GH, Xia ZH, Zhou YL, Wan J, Li DY, Chen RS, Zhai WX, Zhu LH (2006) Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAgamma1. Mol Gen Genomics 275:354–366CrossRefGoogle Scholar
  32. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefPubMedGoogle Scholar
  33. Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392CrossRefPubMedGoogle Scholar
  34. Li T, Huang S, Zhou J, Yang B (2013) Designer TAL effectors induce disease susceptibility and resistance to Xanthomonas oryzae pv. oryzae in rice. Mol Plant 6:781–789CrossRefPubMedGoogle Scholar
  35. Liu Q, Yuan M, Zhou Y, Li X, Xiao J, Wang S (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ 34:1958–1969CrossRefPubMedGoogle Scholar
  36. Marois E, Van den Ackerveken G, Bonas U (2002) The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant-Microbe Interact 15:637–646CrossRefPubMedGoogle Scholar
  37. McDonald B, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379CrossRefPubMedGoogle Scholar
  38. Mew T (1987) Current status and future-prospects of research on bacterial-blight of rice. Annu Rev Phytopathol 25:359–382CrossRefGoogle Scholar
  39. Mew TW, Alvarez AM, Leach JE, Swing J (1993) Focus on bacterial blight of rice. Plant Dis 77:5–12CrossRefGoogle Scholar
  40. Minsavage GV, Dahlbeck D, Whalen MC, Kearney B, Bonas U, Staskawicz BJ, Stall RE (1990) Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatoria-pepper interactions. Mol Plant-Microbe Interact 3:41–47CrossRefGoogle Scholar
  41. Mishra D, Vishnupriya MR, Anil MG, Konda K, Raj Y, Sonti RV (2013) Pathotype and genetic diversity amongst Indian isolates of Xanthomonas oryzae pv. oryzae. PLoS One 8:e81996CrossRefPubMedPubMedCentralGoogle Scholar
  42. Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326:1501CrossRefPubMedGoogle Scholar
  43. Niño-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324CrossRefPubMedGoogle Scholar
  44. Ochiai H, Horino O, Miyajima K, Kaku H (2000) Genetic diversity of Xanthomonas oryzae pv. oryzae strains from Sri Lanka. Phytopathology 90:415–421CrossRefPubMedGoogle Scholar
  45. 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. Jpn Agric Res Q 39:275–287CrossRefGoogle Scholar
  46. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43CrossRefGoogle Scholar
  47. Quibod IL, Perez-Quintero A, Booher NJ, Dossa GS, Grande G, Szurek B, Vera Cruz C, Bogdanove AJ, Oliva R (2016) Effector diversification contributes to Xanthomonas oryzae pv. oryzae phenotypic adaptation in a semi-isolated environment. Sci Rep 6:34137CrossRefPubMedPubMedCentralGoogle Scholar
  48. Read AC, Rinaldi FC, Hutin M, He YQ, Triplett LR, Bogdanove AJ (2016) Suppression of Xo1-mediated disease resistance in rice by a truncated, non-DNA-binding TAL effector of Xanthomonas oryzae. Front Plant Sci 7:1516CrossRefPubMedPubMedCentralGoogle Scholar
  49. Römer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645–648CrossRefPubMedGoogle Scholar
  50. 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 9:204CrossRefPubMedPubMedCentralGoogle Scholar
  51. Strauss T, van Poecke RM, Strauss A, Römer P, Minsavage GV, Singh S, Wolf C, Kim S, Lee HA, Yeom SI, Parniske M, Stall RE, Jones JB, Choi D, Prins M, Lahaye T (2012) RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large-crop genome. Proc Natl Acad Sci U S A 109:19480–19485CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 200:808–819CrossRefPubMedGoogle Scholar
  53. Sugio A, Yang B, Zhu T, White F (2007) Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIA gamma 1 and OsTFX1 during bacterial blight of rice. Proc Natl Acad Sci USA 104:10720–10725CrossRefPubMedPubMedCentralGoogle Scholar
  54. Swarup S, Feyter RD, Brlansky RH, Gabriel ADW (1991) A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of X. campestris to elicit canker like lesions on citrus. Phytopathology 81:802–809CrossRefGoogle Scholar
  55. Swarup S, Yang Y, Kingsley MT, Gabriel DW (1992) An Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on nonhosts. Mol Plant-Microbe Interact 5:204–213CrossRefPubMedGoogle Scholar
  56. Szurek B, Marois E, Bones U, Van den Ackerveken G (2001) Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J 26:523–534CrossRefPubMedGoogle Scholar
  57. Szurek B, Rossier O, Hause G, Bonas U (2002) Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol Microbiol 46:13–23CrossRefPubMedGoogle Scholar
  58. Tian D, Wang J, Zeng X, Gu K, Qiu C, Yang X, Zhou Z, Goh M, Luo Y, Murata-Hori M, White F, Yin Z (2014) The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell 26:497–515CrossRefPubMedPubMedCentralGoogle Scholar
  59. Triplett L, Cohen S, Heffelfinger C, Schmidt C, Huerta A, Tekete C, Verdier V, Bogdanove A, Leach J (2016) A resistance locus in the American heirloom rice variety Carolina gold select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola. Plant J 87:472–483CrossRefPubMedPubMedCentralGoogle Scholar
  60. Van den Ackerveken G, Marois E, Bonas U (1996) Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307–1316CrossRefPubMedGoogle Scholar
  61. Vera Cruz CM, Bai J, Ona I, Leung H, Nelson RJ, Mew TW, Leach JE (2000) Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc Natl Acad Sci U S A 97:13500–13505CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wang C, Qin T, Yu H, Zhang X, Che J, Gao Y, Zheng C, Yang B, Zhao K (2014) The broad bacterial blight resistance of rice line CBB23 is triggered by a novel transcription activator-like (TAL) effector of Xanthomonas oryzae pv. oryzae. Mol Plant Pathol 15:333–341CrossRefPubMedGoogle Scholar
  63. Webb KM, Oña I, Bai J, Garrett KA, Mew T, Vera Cruz CM, Leach JE (2010) A benefit of high temperature: increased effectiveness of a rice bacterial blight disease resistance gene. New Phytol 185:568–576CrossRefPubMedGoogle Scholar
  64. Weeks D, Spalding M, Yang B (2016) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J 14:483–495CrossRefPubMedGoogle Scholar
  65. White F, Yang B (2009) Host and pathogen factors controlling the rice-Xanthomonas oryzae interaction. Plant Physiol 150:1677–1686CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wichmann G, Bergelson J (2004) Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. Genetics 166:693–706CrossRefPubMedPubMedCentralGoogle Scholar
  67. Yang Y, Gabriel D (1995) Xanthomonas avirulence/pathogenicity gene family encodes functional-plant nuclear targeting signals. Mol Plant-Microbe Interact 8:627–631CrossRefPubMedGoogle Scholar
  68. Yang B, White FF (2004) Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol Plant-Microbe Interact 17:1192–1200CrossRefPubMedGoogle Scholar
  69. Yang Y, De Feyter R, Gabriel DW (1994) Host-specific symptoms and increased release of Xanthomonas citri and X. campestris pv. malvacearum from leaves are determined by the 102-bp tandem repeats of pthA and avrb6, respectively. Mol Plant-Microbe Interac 7:345–355CrossRefGoogle Scholar
  70. Yang Y, Yuan Q, Gabriel DW (1996) Watersoaking function(s) of XcmH1005 redundantly encoded by members of the Xanthomonas avr/pth gene family. Mol Plant-Microbe Interact 9:105–112CrossRefGoogle Scholar
  71. Yang B, Zhu W, Johnson L, White F (2000) The virulence factor AvrXa7 of Xanthomonas oryzae pv, oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc Natl Acad Sci U S A 97:9807–9812CrossRefPubMedPubMedCentralGoogle Scholar
  72. Yang B, Sugio A, White F (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci U S A 103:10503–10508CrossRefPubMedPubMedCentralGoogle Scholar
  73. Yu Y, Streubel J, Balzergue S, Champion A, Boch J, Koebnik R, Feng J, Verdier V, Szurek B (2011) Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol Plant-Microbe Interact 24:1102–1113CrossRefPubMedGoogle Scholar
  74. Yu YH, Lu Y, He YQ, Huang S, Tang JL (2015) Rapid and efficient genome-wide characterization of Xanthomonas TAL effector genes. Sci Rep 5:13162CrossRefPubMedPubMedCentralGoogle Scholar
  75. Yuan M, Chu Z, Li X, Xu C, Wang S (2009) Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant Cell Physiol 50:947–955CrossRefPubMedGoogle Scholar
  76. Yuan M, Ke Y, Huang R, Ma L, Yang Z, Chu Z, Xiao J, Li X, Wang S (2016) A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria. elife 5:e19605CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom J, Huang S, Liu S, Cruz C, Frommer W, White F, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–643CrossRefPubMedGoogle Scholar
  78. Zhu W, Yang B, Chittoor JM, Johnson LB, White FF (1998) AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol Plant-Microbe Interact 11:824–832CrossRefPubMedGoogle Scholar
  79. Zhu W, Yang B, Wills N, Johnson LB, White FF (1999) The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. Plant Cell 11:1665–1674CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Genetics, Development and Cell BiologyIowa State UniversityAmesUSA
  2. 2.National Institute of Agricultural SciencesRural Development AdministrationJeonjuRepublic of Korea

Personalised recommendations