Advertisement

Interfamily transfer of Bs2 from pepper to cassava (Manihot esculenta Crantz)

  • Paula A. Díaz-Tatis
  • Juan C. Ochoa
  • Lina García
  • Paul Chavarriaga
  • Adriana J. Bernal
  • Camilo E. LópezEmail author
ORIGINAL ARTICLE
  • 33 Downloads

Abstract

Cassava (Manihot esculenta Crantz) is the principal source of calories among root and tuber crops in tropical countries. Cassava bacterial blight (CBB) caused by Xanthomonas axonopodis pv. manihotis (Xam) is the most prevalent bacterial disease in cassava. Genome and mutagenesis analysis of Xam strains has led to the identification of an effector similar to avrBs2 from Xanthomonas euvesicatoria among a core set effectors contributing to Xam virulence. Previous studies have demonstrated that transgenic tomato plants expressing Bs2, the AvrBs2 cognate resistance protein from pepper, are resistant to Xanthomonas euvesicatoria. According to avrBs2 wide distribution and important contribution to Xam virulence, we aimed at overexpressing Bs2 in cassava plants as a strategy to control CBB. The susceptible cultivar 60444 was transformed with the Bs2 gene from pepper and transgenic cassava plants that functionally express Bs2 were regenerated. Our results show that overexpression of Bs2 in a highly susceptible cultivar leads to reactive oxygen species production. However, the overexpression of Bs2 neither leads to an HR in cassava nor reduces Xam growth on in vitro plants. These results suggest that BS2 activates defense-signaling pathways in cassava such as ROS production, although this is not sufficient to restrict Xam growth.

Keywords

Cassava bacterial blight Heterologous system Nucleotide-binding leucine-rich repeats Plant immunity R gene interfamily transfer Transgenic cassava 

Notes

Acknowledgements

The authors would like to acknowledge Emily McCallum, Hervé Vanderschuren and Wilhelm Gruissem (ETH Zürich, Switzerland) for comments and support during PADT’s internship in their laboratory, and Camilo Dorado for his support on the statistical analysis. The Bs2 gene was kindly provided by Brian Staskawicz (University of California, Berkeley, USA). This research was supported by a National Science Foundation/BREAD (Basic Research to Enable Agricultural Development) grant (Award 0965418). PADT was supported with a scholarship for graduate students from Universidad Nacional de Colombia. The authors have no conflict of interest to declare.

Supplementary material

40858_2019_279_MOESM1_ESM.xlsx (56 kb)
Supplementary Table S1 - List of primers used in this study. (XLSX 55 kb)
40858_2019_279_MOESM2_ESM.xlsx (65 kb)
Supplementary Table S2 - Result of BLASTp analysis against the cassava proteome (v. 6.1) using the Bs2 sequence from pepper as a query. (XLSX 64 kb)
40858_2019_279_Fig8_ESM.png (2.1 mb)
Supplementary Figure S1

- Transient over-expression of Bs2 and Bs2(D475V) assays in N. benthamiana and N. tabacum. aN. benthamiana leaves were infiltrated with A. tumefaciens strain GV3101 (OD600nm = 0,3) transformed with the binary vectors pBAV139 containing 35S::Bs2, 35S::Bs2(D475V),35S::Pto(L205D) and an empty vector (EV). b Destained leaf shown in a. cN. tabacum leaves were infiltrated with A. tumefaciens strain GV3101 (OD600nm = 0,3) transformed with the binary vectors pBAV139 containing 35S::Bs2, 35S::Bs2(D475V),35S::Pto(L205D) and an EV. d Destained leaf shown in c. (PNG 2143 kb)

40858_2019_279_MOESM3_ESM.tif (12.3 mb)
High Resolution Image (TIF 12572 kb)
40858_2019_279_Fig9_ESM.png (615 kb)
Supplementary Figure S2

- Transient overexpression of Bs2 and Bs2(D475V) assays in cassava leaves. a Cassava leaves (cultivar SG10735) were infiltrated with A. tumefaciens strain AGL1 (OD600nm = 0,3) transformed with the binary vectors pBAV139 containing 35S::Bs2, 35S::Bs2(D475V) and an empty vector (EV). b Destained leaf shown in a. (PNG 615 kb)

40858_2019_279_MOESM4_ESM.tif (3.6 mb)
High Resolution Image (TIF 3706 kb)
40858_2019_279_Fig10_ESM.png (382 kb)
Supplementary Figure S3

- PCR analysis of Bs2 cassava transgenic plants. Genomic DNA was isolated from fresh leaves and a PCR was performed using specific primers for Bs2, Bs2_F and Bs2_R in Suppl. Table S1 (a). PP2A was used as an endogenous control; primers used are listed in Suppl. Table S1 (b). L.1-L.11, genomic DNA from the different transgenic plants obtained; M, 1 Kb plus DNA ladder; −, negative control. (PNG 382 kb)

40858_2019_279_MOESM5_ESM.tif (28.9 mb)
High Resolution Image (TIF 29564 kb)
40858_2019_279_Fig11_ESM.png (680 kb)
Supplementary Figure S4

- Southern-blot analysis of Bs2 cassava transgenic plants. Genomic DNA was isolated from fresh leaves and a southern Blot was performed using hptII as a probe. L.1-L.11, genomic DNA from the different transgenic plants obtained; WT, genomic DNA from wild-type (non-transformed) plants used as a negative control. (PNG 679 kb)

40858_2019_279_MOESM6_ESM.tif (14.2 mb)
High Resolution Image (TIF 14573 kb)
40858_2019_279_Fig12_ESM.png (2.1 mb)
Supplementary Figure S5

- Differences in the phenotype of in vitro wild-type (non-transformed; WT) plants (a), empty vector (EV) transgenic plants (b) and Bs2 transgenic plants (c). The pictures were taken to one-month-old in vitro plants. (PNG 2115 kb)

40858_2019_279_MOESM7_ESM.tif (15.3 mb)
High Resolution Image (TIF 15662 kb)

References

  1. Ade J, DeYoung BJ, Golstein C, Innes RW (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci USA 104:2531–2536Google Scholar
  2. Afroz A, Chaudhry Z, Rashid U, Ali MG, Nazir F, Iqbal J, Khan MR (2011) Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tissue and Organ Culture 104:227–237CrossRefGoogle Scholar
  3. Allem AC (1994) The origin of Manihot esculenta Crantz (Euphorbiaceae). Genetic Resources and Crop Evolution 41:133–150CrossRefGoogle Scholar
  4. Allem A (1999) The closest wild relatives of cassava (Manihot esculenta Crantz). Euphytica 107:123–133CrossRefGoogle Scholar
  5. Arrieta-Ortiz ML, Rodríguez-R LM, Pérez-Quintero ÁL, Poulin L, Díaz AC, Arias-Rojas N, Trujillo C, Restrepo-Benavides M, Bart R, Boch J, Boureau T, Darrasse A, David P, Dugé de Bernonville T, Fontanilla P, Gagnevin L, Guérin F, Jacques MA, Lauber E, Lefeuvre P, Medina C, Medina E, Montenegro N, Muñoz-Bodnar A, Noël LD, Ortiz-Quiñones JF, Osorio D, Pardo C, Patil P, Poussier S, Pruvost O, Robène-Soustrade I, Ryan RP, Tabima J, Urrego-Morales OG, Vernière C, Carrere S, Verdier V, Szurek B, Restrepo S, López C, Koebnik R, Bernal A (2013) Genomic survey of pathogenicity determinants and VNTR markers in the cassava bacterial pathogen Xanthomonas axonopodis pv. manihotis strain CIO151. PLoS One 8:e79704CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bart R, Cohn M, Kassen A, McCallum EJ, Shybut M, Petriello A, Krasileva K, Dahlbeck D, Medina C, Alicai T, Kumar L, Moreira LM, Neto JR, 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. Proceedings of the National Academy of Sciences USA 109:E1972–E1979CrossRefGoogle Scholar
  7. Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nature Reviews Genetics 8:382–393Google Scholar
  8. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biology 5:e236CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bradeen JM, Iorizzo M, Mollov DS, Raasch J, Kramer L, Millett BP, Austin-Phillips S, Jiang J, Carputo D (2009) Higher copy numbers of the potato RB transgene correspond to enhanced transcript and late blight resistance levels. Molecular Plant-Microbe Interactions 22:437–446CrossRefPubMedGoogle Scholar
  10. Bredeson JV, Lyons JB, Prochnik SE, Wu A, Ha CM, Edsinger-Gonzales E, Grimwood J, Schmutz J, Rabbi IY, Egesi C, Nauluvula P, Lebot V, Ndunguru J, Mkamilo G, Bart R, Setter TL, Gleadow RM, Kulakow P, Ferguson ME, Rounsley S, Rokhsar DS (2016) Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nature Biotechnology 34:562–570CrossRefPubMedGoogle Scholar
  11. Bull SE, Owiti JA, Niklaus M, Beeching JR, Gruissem W, Vanderschuren H (2009) Agrobacterium-mediated transformation of friable embryogenic calli and regeneration of transgenic cassava. Nature Protocols 4:1845–1854CrossRefPubMedGoogle Scholar
  12. Chung E-H, da Cunha L, Wu AJ, Gao Z, Cherkis K, Afzal AJ, Mackey D, Dangl JL (2011) Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host & Microbe 9:125–136CrossRefGoogle Scholar
  13. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death and Differentiation 18:1247–1256CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annual Review of Plant Biology 66:487–511CrossRefPubMedGoogle Scholar
  15. Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341:746–751CrossRefPubMedGoogle Scholar
  16. Feuillet C, Travella S, Stein N, Albar L (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proceedings of the National Academy of Sciences USA 100:15253–15258CrossRefGoogle Scholar
  17. Foster SJ, Park TH, Pel M, Brigneti G, Sliwka J, Jagger L, van der Vossen E, Jones JDG (2009) Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Molecular Plant-Microbe Interactions 22:589–600CrossRefPubMedGoogle Scholar
  18. Goggin FL, Jia L, Shah G, Hebert S, Williamson VM, Ullman DE (2006) Heterologous expression of the Mi-1.2 gene from tomato confers resistance against nematodes but not aphids in eggplant. Molecular Plant-Microbe Interactions 19:383–388CrossRefPubMedGoogle Scholar
  19. Gupta SK, Rai AK, Kanwar SS, Chand D, Singh NK, Sharma TR (2012) The single functional blast resistance gene Pi54 activates a complex defence mechanism in rice. Journal of Experimental Botany 63:757–772CrossRefPubMedGoogle Scholar
  20. Hajri A, Brin C, Hunault G, Lardeuex F, Lemaire C, Manceau C, Boureau T, Poussier S (2009) A “repertoire for repertoire” hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas. PLoS One 4:e6632CrossRefPubMedPubMedCentralGoogle Scholar
  21. Heath MC (2000) Hypersensitive response-related death. Plant Molecular Biology 44:321–334CrossRefPubMedGoogle Scholar
  22. Holton N, Nekrasov V, Ronald PC, Zipfel C (2015) The phylogenetically-related pattern recognition receptors EFR and Xa21 recruit similar immune signaling components in monocots and dicots. PLoS Pathogens 11:e1004602Google Scholar
  23. Horvath DM, Stall RE, Jones JB, Pauly MH, Valad GE, Dahlbeck D, Staskawicz BJ, Scott JW (2012) Transgenic resistance confers effective field level control of bacterial spot disease in tomato. PLoS One 7:e42036CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefPubMedGoogle Scholar
  25. Jorge V, Fregene MA, Duque MC, Bonierbale MW, Tohme J, Verdier V (2000) Genetic mapping of resistance to bacterial blight disease in cassava (Manihot esculenta Crantz). Theoretical and Applied Genetics 101:865–872CrossRefGoogle Scholar
  26. Kearney B, Staskawicz BJ (1990) Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346:385–386CrossRefPubMedGoogle Scholar
  27. Kpemoua K, Boher B, Nicole M, Calatayud P, Geiger JP (1996) Cytochemistry of defense responses in cassava infected by Xanthomonas campestris pv. manihotis. Canadian Journal of Microbiology 1143:1131–1143CrossRefGoogle Scholar
  28. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma BP, Staskawicz B, Jones JD, Zipfel C (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnology 28:365–369Google Scholar
  29. Li HQ, Sautter C, Potrykus I, Puonti-Kaerlas J (1996) Genetic transformation of cassava (Manihot esculenta Crantz). Nature Biotechnology 14:303–308CrossRefGoogle Scholar
  30. Li S, Wang Y, Wang S, Fang A, Wang J, Liu L, Zhang K, Mao Y, Sun W (2015) The type III effector AvrBs2 in Xanthomonas oryzae pv. oryzicola suppresses rice immunity and promotes disease development. Molecular Plant-Microbe Interactions 28:869–880CrossRefPubMedGoogle Scholar
  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  32. López CE, Bernal AJ (2012) Cassava bacterial blight: using genomics for the elucidation and management of an old problem. Tropical Plant Biology 5:117–126CrossRefGoogle Scholar
  33. Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G (2012) Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group Phureja. PLoS One 7:e34775CrossRefPubMedPubMedCentralGoogle Scholar
  34. Maekawa T, Kufer TA, Schulze-Lefert P (2011) NLR functions in plant and animal immune systems: so far and yet so close. Nature Immunology 12:817–826CrossRefPubMedGoogle Scholar
  35. Maekawa T, Kracher B, Vernaldi S, Ver Loren van Themaat E, Schulze-Lefert P (2012) Conservation of NLR-triggered immunity across plant lineages. Proceedings of the National Academy of Sciences USA 109:20119–20123CrossRefGoogle Scholar
  36. McCallum EJ, Anjanappa RB, Gruissem W (2017) Tackling agriculturally relevant diseases in the staple crop cassava (Manihot esculenta). Current Opinion in Plant Biology 38:50–58CrossRefPubMedGoogle Scholar
  37. Medina CA, Reyes PA, Trujillo CA, Gonzalez JL, Bejarano DA, Montenegro NA, Jacobs JM, Joe A, Restrepo S, Alfano JR, Bernal A (2017) The role of type three effectors from Xanthomonas axonopodis pv. manihotis in virulence and suppression of plant immunity. Molecular Plant Pathology 19:593–606CrossRefPubMedGoogle Scholar
  38. Mendes BMJ, Cardoso SC, Boscariol-Camargo RL, Cruz RB, Mourao Filho FAA, Bergamin Filho A (2010) Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathology 59:68–75Google Scholar
  39. Mukhtar MS (2013) Engineering NLR immune receptors for broad-spectrum disease resistance. Trends in Plant Science 18:469–472CrossRefPubMedGoogle Scholar
  40. Narusaka M, Hatakeyama K, Shirasu K, Narusaka Y (2014) Arabidopsis dual resistance proteins, both RPS4 and RRS1, are required for resistance to bacterial wilt in transgenic Brassica crops. Plant Signaling & Behavior 9:e29130CrossRefGoogle Scholar
  41. Newman M-A, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Frontiers in Plant Science 4:139CrossRefPubMedPubMedCentralGoogle Scholar
  42. Olsen KM, Schaal BA (1999) Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proceedings of the National Academy of Sciences USA 96:5586–5591CrossRefGoogle Scholar
  43. Qi D, Innes RW (2013) Recent advances in plant NLR structure, function, localization, and signaling. Frontiers in Immunology 4:1–10CrossRefGoogle Scholar
  44. Rathjen JP, Chang JH, Staskawicz BJ, Michelmore RW (1999) Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of avrPto. EMBO Journal 18:3232–3240CrossRefPubMedGoogle Scholar
  45. Rentel MC, Leonelli L, Dahlbeck D, Zhao B, Staskawicz BJ (2008) Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proceedings of the National Academy of Sciences USA 105:1091–1096CrossRefGoogle Scholar
  46. Restrepo S, Verdier V (1997) Geographical differentiation of the population of Xanthomonas axonopodis pv. manihotis in Colombia. Applied and Environmental Microbiology 63:4427–4434PubMedPubMedCentralGoogle Scholar
  47. Roux B, Bolot S, Guy E, Denancé N, Lautier M, Jardinaud MF, Fischer-Le Saux M, Portier P, Jacques MA, Gagnevin L, Pruvost O, Lauber E, Arlat M, Carrère S, Koebnik R, Noël LD (2015) Genomics and transcriptomics of Xanthomonas campestris species challenge the concept of core type III effectome. BMC Genomics 16:975CrossRefPubMedPubMedCentralGoogle Scholar
  48. Sandino T, López-Kleine L, López C, Marquínez X (2015) Caracterización de la respuesta morfológica de variedades susceptibles y resistentes de yuca (Manihot esculenta Crantz) a la bacteriosis vascular causada por Xanthomonas axonopodis pv. manihotis. Summa Phytopathologica 41:94–100CrossRefGoogle Scholar
  49. Schoonbeek HJ, Wang HH, Stefanato FL, Craze M, Bowden S, Wallington E, Zipfel C, Ridout CJ (2015) Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytologist 206:606–613CrossRefPubMedGoogle Scholar
  50. Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annual Review of Plant Biology 63:451–482CrossRefPubMedGoogle Scholar
  51. Sendín LN, Filippone MP, Orce IG, Enrique R, Peña L, Vojno AA, Marano MR, Castagnaro AP (2012) Transient expression of pepper Bs2 gene in Citrus limon as an approach to evaluate its utility for management of citrus canker disease. Plant Pathology 61:648–657CrossRefGoogle Scholar
  52. Soto JC, Ortiz JF, Perlaza-Jiménez L, Vásquez AX, Lopez-Lavalle LA, Mathew B, Léon J, Bernal AJ, Ballvora A, López CE (2015) A genetic map of cassava (Manihot esculenta Crantz) with integrated physical mapping of immunity-related genes. BMC Genomics 16:190CrossRefPubMedPubMedCentralGoogle Scholar
  53. Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology 12:89–100Google Scholar
  54. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proceedings of the National Academy of Sciences USA 96:14153–14158CrossRefGoogle Scholar
  55. Tao Y, Yuan F, Leister RT, Ausubel FM, Katagiri F (2000) Mutational analysis of the Arabidopsis nucleotide binding site-leucine-rich repeat resistance gene RPS2. Plant Cell 12:2541–2554Google Scholar
  56. Taylor NJ, Edwards M, Kiernan RJ, Davey CD, Blakesley D, Henshaw GG (1996) Development of friable embryogenic callus and embryogenic suspension culture systems in cassava (Manihot esculenta Crantz). Nature Biotechnology 14:303–308CrossRefGoogle Scholar
  57. Taylor N, Gaitán-Solís E, Moll T, Trauterman B, Jones T, Pranjal A, Trembley C, Abernathy V, Corbin D, Fauquet C (2012) A high-throughput platform for the production and analysis of transgenic cassava (Manihot esculenta) plants. Tropical Plant Biology 5:127–139CrossRefGoogle Scholar
  58. 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. Plant Journal 11:1187–1194CrossRefGoogle Scholar
  59. Tripathi JN, Lorenzen J, Bahar O, Ronald P, Tripathi L (2014) Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnology Journal 12:663–673CrossRefPubMedPubMedCentralGoogle Scholar
  60. Trujillo CA, Arias-Rojas N, Poulin L, Medina CA, Tapiero A, Restrepo S, Koebnik R, Bernal A (2014a) Population typing of the causal agent of cassava bacterial blight in the Eastern Plains of Colombia using two types of molecular markers. BMC Microbiology 14:161CrossRefPubMedPubMedCentralGoogle Scholar
  61. Trujillo CA, Ochoa JC, Mideros MF, Restrepo S, López C, Bernal A (2014b) A complex population structure of the cassava pathogen Xanthomonas axonopodis pv. manihotis in recent years in the caribbean region of Colombia. Microbiology Ecology 68:155–167Google Scholar
  62. Wu Y, Zhou JM (2013) Receptor-like kinases in plant innate immunity. Journal of Integrative Plant Biology 55:1271–1286CrossRefPubMedGoogle Scholar
  63. Wydra K, Zinsou V, Jorge V, Verdier V (2004) Identification of pathotypes of Xanthomonas axonopodis pv. manihotis in Africa and detection of quantitative trait loci and markers for resistance to bacterial blight of cassava. Phytopathology 94:1084–1093CrossRefPubMedGoogle Scholar
  64. Zhang Y, Dorey S, Swiderski M, Jones JDG (2004) Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant Journal 40:213–224CrossRefPubMedGoogle Scholar
  65. Zhao B, Lin X, Poland J, Trick H, Leach J, Hulbert S (2005) A maize resistance gene functions against bacterial streak disease in rice. Proceedings of the National Academy of Sciences USA 102:15383–15388CrossRefGoogle Scholar
  66. Zhao C, Escalante LN, Chen H, Benatti TR, Qu J, Chellapilla S, Waterhouse RM, Wheeler D, Andersson MN, Bao R, Batterton M, Behura SK, Blankenburg KP, Caragea D, Carolan JC, Coyle M, El-Bouhssini M, Francisco L, Friedrich M, Gill N, Grace T, Grimmelikhuijzen CJ, Han Y, Hauser F, Herndon N, Holder M, Ioannidis P, Jackson L, Javaid M, Jhangiani SN, Johnson AJ, Kalra D, Korchina V, Kovar CL, Lara F, Lee SL, Liu X, Löfstedt C, Mata R, Mathew T, Muzny DM, Nagar S, Nazareth LV, Okwuonu G, Ongeri F, Perales L, Peterson BF, Pu LL, Robertson HM, Schemerhorn BJ, Scherer SE, Shreve JT, Simmons D, Subramanyam S, Thornton RL, Xue K, Weissenberger GM, Williams CE, Worley KC, Zhu D, Zhu Y, Harris MO, Shukle RH, Werren JH, Zdobnov EM, Chen MS, Brown SJ, Stuart JJ, Richards S (2015) A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Current Biology 25:613–620Google Scholar
  67. Zipfel C (2014) Plant pattern-recognition receptors. Trends in Immunology 35:345–351CrossRefPubMedGoogle Scholar
  68. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760CrossRefPubMedGoogle Scholar

Copyright information

© Sociedade Brasileira de Fitopatologia 2019

Authors and Affiliations

  • Paula A. Díaz-Tatis
    • 1
    • 2
  • Juan C. Ochoa
    • 1
    • 3
  • Lina García
    • 1
  • Paul Chavarriaga
    • 4
  • Adriana J. Bernal
    • 5
  • Camilo E. López
    • 1
    Email author
  1. 1.Manihot Biotec, Departamento de BiologíaUniversidad Nacional de ColombiaBogotá D.C.Colombia
  2. 2.Grupo de Ciencias Biológicas y Químicas, Departamento de BiologíaUniversidad Antonio NariñoBogotáColombia
  3. 3.Institute of Plant Genetics, Department of Integrative BiologyPolish Academy of SciencesPoznanPoland
  4. 4.Transformation PlatformCentro Internacional de Agricultura Tropical (CIAT)PalmiraColombia
  5. 5.Laboratorio de Interacciones Moleculares de Microorganismos Agrícolas (LIMMA), Departamento de Ciencias BiológicasUniversidad de los AndesBogotá D.C.Colombia

Personalised recommendations