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Cassava Bacterial Blight: Using Genomics for the Elucidation and Management of an Old Problem

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Abstract

Bacterial Blight is an important disease of cassava, causing losses that have resulted in historical famines in certain growing zones. The disease is caused by Xanthomonas axonopodis pv. manihotis, a gram-negative rod that belongs to the gammaproteobacteria. In this review, we describe the pathosystem and the recent studies that have been undertaken to elucidate both susceptibility and resistance mechanisms in cassava, with the hope of generating resistant plants using biotechnology. We first describe studies of the pathogen, including pathogen population changes through time as well as genomic tools that have recently been generated to determine pathogenicity factors. Secondly, we discuss mechanisms of disease resistance that have been elucidated in recent years and how these mechanisms could be used for the generation of improved plants resistant to CBB.

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Abbreviations

CBB:

Cassava bacterial blight

Xam :

Xanthomonas axonopodis pv. manihotis

RFLP:

Restriction fragment length polymorphism

AFLP:

Amplified fragment length polymorphisms

RAPD:

Random amplified polymorphic DNA

TTSS:

Type III secretion system

TAL:

Transcriptional activator-like

QTL:

Quantitative trait loci

MAMP:

Microbe-associated molecular pattern

MTI:

MAMP-triggered immunity

ETI:

Effector-triggered immunity

NBS:

Nucleotide binding site

TIR:

Toll/interleukin receptor

CC:

Coiled coil

LRR:

Leucine-rich repeat

HR:

Hypersensitive response

GST:

Glutathione S-transferase

IRP:

Immunity-related protein

IRG:

Immunity-related gene

PR:

Pathogenesis-related proteins

References

  • AGI Arabidopsis Genome Initiative (2000) Analyses of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:769–815

    Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Berthier Y, Verdier V, Guesdon JL, Chevrier D, Denis JB, Decoux G, Lemattre M (1993) Characterization of Xanthomonas campestris pathovars by rRNA gene restriction patterns. Appl Environ Microbiol 59:851–859

    PubMed  CAS  Google Scholar 

  • 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 326:1509–1512

    Article  PubMed  CAS  Google Scholar 

  • Bogdanove AJ et al (2011) Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J Bacteriol 193(19):5450–64

    Article  PubMed  CAS  Google Scholar 

  • Boher B, Verdier V (1995) Cassava bacterial blight in Africa: the state of knowledge and implications for designing control strategies. Afr Crop Sci J 2:1–5

    Google Scholar 

  • Boher B, Kpemoua K, Nicole M, Luisetti J, Geiger JP (1995) Ultrastructure of interactions between cassava and Xanthomonas campestris pv. manihotis cytochemistry of cellulose and pectin degradation in a susceptible cultivar. Phytopathology 85:777–788

    Article  Google Scholar 

  • Boher B, Nicole M, Potin M, Geiger JP (1997) Extracellular polysaccharides from Xanthomonas axonopodis pv. manihotis interact with cassava cell walls during pathogenesis. Mol Plant Microbe Interact 10:803–811

    Article  PubMed  CAS  Google Scholar 

  • Bonas U, Stall RE, Staskawicz B (1989) Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet 218:127–136

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Voinnet O (2009) Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 10:141–148

    Article  PubMed  CAS  Google Scholar 

  • Chan AP, Crabtree J, Zhao Q, Lorenzi H, Orvis J, Puiu D, Melake-Berhan A, Jones KM, Redman J, Chen G, Cahoon EB, Gedil M, Stanke M, Haas BJ, Wortman JR, Fraser-Liggett CM, Ravel J, Rabinowicz PD (2010) Draft genome sequence of the oilseed species Ricinus communis. Nat Biotechnol 28:951–956

    Article  PubMed  CAS  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  PubMed  CAS  Google Scholar 

  • CIAT (1980) Cassava Program. Annual Report 1979. (Cali, Colombia), pp. 156p.

  • Da Silva RAC et al (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host speci cities. Nature 417:459–463

    Article  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548

    Article  PubMed  CAS  Google Scholar 

  • Elango F, Lozano JC (1981) Pathogenic variability of Xanthomonas manihotis, the causal agent of cassava bacterial blight. Fitopatologia Brasilia 6:57–63

    Google Scholar 

  • Fessehaie A (1997) Biochemical/physiological characterization and detection methods of Xanthomonas campestris pv. manihotis (Berthet-Bondar) Dye 1978, the causal organism of cassava bacterial blight (Germany.: University of Göttingen)

  • Fregene M, Angel F, Gomez R, Rodriguez F, Chavarriaga P, Roca W, Tohme J, Bonierbale M (1997) A molecular genetic map of cassava (Manihot esculenta Crantz). Theor Appl Genet 95:431–441

    Article  CAS  Google Scholar 

  • Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen X, Sela H, Fahima T, Dubcovsky J (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360

    Article  PubMed  CAS  Google Scholar 

  • Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, Ebana K, Hayashi N, Takahashi A, Hirochika H, Okuno K, Yano M (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • 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). Theor Appl Genet 101:865–872

    Article  CAS  Google Scholar 

  • Jorge V, Fregene M, Vélez CM, Duque MC, Tohme J, Verdier V (2001) QTL analysis of field resistance to Xanthomonas axonopodis pv. manihotis in cassava. 102:564–571

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

    Article  PubMed  CAS  Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463

    Article  PubMed  CAS  Google Scholar 

  • Kemp BP, Horne J, Bryant A, Cooper RM (2004) Xanthomonas axonopodis gumD gene is essential for EPS production and pathogenicity and enhances epiphytic survival on cassava (Manihot esculenta). Physiol Mol Plant Pathol 64:209–218

    Article  CAS  Google Scholar 

  • Kemp BP, Beeching JR, Cooper RM (2005) cDNA-AFLP reveals genes differentially expressed during the hypersensitive response of cassava. Mol Plant Pathol 6:113–123

    Article  PubMed  CAS  Google Scholar 

  • Kpémoua K, Boher B, Nicole M, Calatayud P, Geiger JP (1996) Cytochemistry of defense responses in cassava infected by Xanthomonas campestris pv. manihotis. Can J Microbiol 42:1131–1143

    Article  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  PubMed  CAS  Google Scholar 

  • 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. Nat Biotechnol 28(4):365–9

    Article  PubMed  CAS  Google Scholar 

  • Lee BM, Park YJ, Park DS, Kang HW, Kim JG, Song ES, Park IC, Yoon UH (2005) The genome sequence of Xanthomonas oryzae pv. oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33:577–586

    Article  PubMed  CAS  Google Scholar 

  • Lopez CE, Zuluaga AP, Cooke R, Delseny M, Tohme J, Verdier V (2003) Isolation of Resistance Gene Candidates (RGCs) and characterization of an RGC cluster in cassava. Mol Genet Genom 269:658–671

    Article  CAS  Google Scholar 

  • Lopez C, Jorge V, Piegu B, Mba C, Cortes D, Restrepo S, Soto M, Laudie M, Berger C, Cooke R, Delseny M, Tohme J, Verdier V (2004) A unigene catalogue of 5700 expressed genes in cassava. Plant Mol Biol 56:541–554

    Article  PubMed  Google Scholar 

  • Lopez C, Soto M, Restrepo S, Piegu B, Cooke R, Delseny M, Tohme J, Verdier V (2005) Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray. Plant Mol Biol 57:393–410

    Article  PubMed  CAS  Google Scholar 

  • Lopez CE, Quesada-Ocampo LM, Bohorquez A, Duque MC, Vargas J, Tohme J, Verdier V (2007) Mapping EST-derived SSRs and ESTs involved in resistance to bacterial blight in Manihot esculenta. Genome 50:1078–1088

    Article  PubMed  CAS  Google Scholar 

  • Louws FJ, Rademaker JLW, de Bruijn FJ (1999) The three Ds of PCR-based genomic analysis of phytobacteria: diversity, detection, and disease diagnosis. Ann Rev Phytopathol 37:81–125

    Article  CAS  Google Scholar 

  • Lozano JC (1975) Bacterial blight of cassava. PANS 21:38–43

    Google Scholar 

  • Lozano JC (1986) Cassava bacterial blight: a manageable disease. Plant Dis 70:1089–1093

    Article  Google Scholar 

  • Lozano JC, Sequeira L (1974) Bacterial blight of cassava in Colombia: epidemiology and control. Phytopathology 64:83–88

    Article  Google Scholar 

  • Malone JH, Oliver B (2011) Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol 9:34

    Article  PubMed  CAS  Google Scholar 

  • Marguerat S, Bahler J (2009) RNA-seq: from technology to biology. Cell Mol Life Sci 67:569–579

    Article  PubMed  Google Scholar 

  • Mendes BMJ, Cardoso SC, Boscariol-Camargo RL, Cruz RB, Mourão Filho FAA, Bergamin Filho A (2010) Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol 59:68–75

    Article  CAS  Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    Article  PubMed  CAS  Google Scholar 

  • Ming R et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996

    Article  PubMed  CAS  Google Scholar 

  • Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science (New York, NY) 326:1501

    Article  CAS  Google Scholar 

  • Mukhtar MS et al (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601

    Article  PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    Article  PubMed  CAS  Google Scholar 

  • Navarro L, Jay F, Nomura K, He SY, Voinnet O (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–967

    Article  PubMed  CAS  Google Scholar 

  • Nicaise V, Roux M, Zipfel C (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150:1638–1647

    Article  PubMed  CAS  Google Scholar 

  • Ogunjobi AA, Dixon A (2006) Molecular variation in population structure of Xanthomonas axonopodis pv. manihotis in the southeastern Nigeria. Afr J Biotechnol 5:1868–1872

    CAS  Google Scholar 

  • Ogunjobi AA, Dixon AGO, Fagade OE (2007) Molecular genetic study of cassava bacterial blight causal agent in Nigeria using Random Amplified Polymorphic DNA. Elecron J Environ Agr Food Chem 6:2364–2376

    CAS  Google Scholar 

  • Ogunjobi AA, Fagade OE, Dixon A (2010) Physiological studies on Xanthomonas axonopodis pv. manihotis (Xam) strains isolated in Nigeria. Eur J Biol Sci 2:84–90

    Google Scholar 

  • Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Cociancich S, Couloux A, Darrasse A, Gouzy J, Jacques M-A, Lauber E, Manceau C, Mangenot S, Poussier S, Segurens B, Szurek B, Verdier V, Arlat M, Rott P (2009) The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genom 10:616

    Article  Google Scholar 

  • Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ (2009) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genom 281:609–626

    Article  CAS  Google Scholar 

  • Potnis N, Krasileva K, Chow V, Almeida NF, Patil PB, Ryan RP, Sharlach M, Behlau F, Dow JM, Momol M, White FF, Preston JF, Vinatzer BA, Koebnik R, Setubal JC, Norman DJ, Staskawicz BJ, Jones JB (2011) Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genom 12:146

    Article  CAS  Google Scholar 

  • Qian W et al (2005) Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res 15:757–767

    Article  PubMed  CAS  Google Scholar 

  • Restrepo S (1999) Etude de la structure des populations de Xanthomonas axonopodis pv. manihotis en Colombie. Paris VI, Pierre et Marie Curie, Paris, p 136

    Google Scholar 

  • Restrepo S, Verdier V (1997) Geographical differentiation of the population of Xanthomonas axonopodis pv. manihotis in Colombia. Appl Environ Microbiol 63:4427–2234

    PubMed  CAS  Google Scholar 

  • Restrepo S, Duque MC, Tohme J, Verdier V (1999a) AFLP fingerprinting: an efficient technique for detecting genetic variation of Xanthomonas axonopodis pv. manihotis. Microbiology 145:107–114

    Article  PubMed  CAS  Google Scholar 

  • Restrepo S, Valle T, Duque MC, Verdier V (1999b) Assessing genetic variability among Brazilian strains of Xanthomonas axonopodis pv. manihotis through RFLP and AFLP analyses. Can J Microbiol

  • Restrepo S, Duque MC, Verdier V (2000a) Characterization of pathotypes among isolates of Xanthomonas axonopodis pv. manihotis in Colombia. Plant Pathol 49:680–687

    Article  Google Scholar 

  • Restrepo S, Velez CM, Verdier V (2000b) Measuring the genetic diversity of Xanthomonas axonopodis pv. manihotis within different fields in Colombia. Phytopathology 90:683–690

    Article  PubMed  CAS  Google Scholar 

  • Restrepo S, Velez CM, Duque MC, Verdier V (2004) Genetic structure and population dynamics of Xanthomonas axonopodis pv. manihotis in Colombia from 1995 to 1999. Appl Environ Microbiol 70:255–261

    Article  PubMed  CAS  Google Scholar 

  • Ronaghi M (2001) Pyrosequencing sheds light on DNA sequencing. Genome Res 11:3–11

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    Article  PubMed  CAS  Google Scholar 

  • Ryan RP, Vorhölter F-J, Potnis N, Jones JB, Van Sluys M-A, Bogdanove AJ, Dow JM (2011) Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 9:344–355

    Article  PubMed  CAS  Google Scholar 

  • Salzberg SL et al (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genom 9:204

    Article  Google Scholar 

  • Santaella M, Suarez E, Lopez C, Gonzalez C, Mosquera G, Restrepo S, Tohme J, Verdier V (2004) Identification of genes in cassava that are differentially expressed during infection with Xanthomonas axonopodis pv. manihotis. Mol Plant Pathol 5:549–558

    Article  PubMed  CAS  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD (1995) Molecular genetics of plant disease resistance. Science 268:661–667

    Article  PubMed  CAS  Google Scholar 

  • Studholme DJ, Kemen E, MacLean D, Schornack S, Aritua V, Thwaites R, Grant M, Smith J, Jones JDG (2010) Genome-wide sequencing data reveals virulence factors implicated in banana Xanthomonas wilt. FEMS Microbiol Lett 310:182–192

    Article  PubMed  CAS  Google Scholar 

  • Swings RJ, Civerolo E, Swings JG (1993) Xanthomonas. Chapman and Hall, London

    Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  PubMed  CAS  Google Scholar 

  • Thieme F, Koebnik R, Bekel T, Berger C, Boch J, Bu D, Caldana C, Gaigalat L, Goesmann A, Kay S, Kirchner O, Lanz C (2005) Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv.vesicatoria. J Bacteriol 187:7254–7266

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Verdier V, Dongo P, Boher B (1993) Assessment of genetic diversity among strains of Xanthomonas campestris pv. manihotis. J Gen Microbiol 139:2591–2601

    CAS  Google Scholar 

  • Verdier V, Boher B, Maraite H, Geiger JP (1994) Pathological and molecular characterization of Xanthomonas campestris strains causing diseases of cassava (Manihot esculenta). Appl Environ Microbiol 60:4478–4486

    PubMed  CAS  Google Scholar 

  • Verdier V, Restrepo S, Mosquera G, Duque MC, Gerstl A, Laberry R (1998) Genetic and pathogenic variation of Xanthomonas axonopodis pv. manihotis in Venezuela. Plant Pathol 47:601–608

    Article  Google Scholar 

  • Verdier V, Restrepo S, Mosquera G, Jorge V, Lopez C (2004) Recent progress in the characterization of molecular determinants in the Xanthomonas axonopodis pv. manihotis-cassava interaction. Plant Mol Biol 56:573–584

    Article  PubMed  CAS  Google Scholar 

  • Vorhölter F-J, Schneiker S, Goesmann A, Krause L, Bekel T, Kaiser O, Linke B, Patschkowski T, Rückert C, Schmid J, Sidhu VK, Sieber V, Tauch A, Watt SA, Weisshaar B, Becker A, Niehaus K, Pühler A (2008) The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis. J Biotechnol 134:33–45

    Article  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  PubMed  CAS  Google Scholar 

  • Wydra K, Verdier V (2002) Occurrence of cassava diseases in relation to environmental, agronomic and plant characteristics. Agric Ecosyst Environ 93:211–226

    Article  Google Scholar 

  • 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 94:1084–1093

    Article  PubMed  CAS  Google Scholar 

  • Xu X et al (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  PubMed  CAS  Google Scholar 

  • Zeng C, Wang W, Zheng Y, Chen X, Bo W, Song S, Zhang W, Peng M (2010) Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants. Nucleic Acids Res 38:981–995

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The work of CEL and AJB is funded by the Colombian Ministry of Agriculture, ICGEB, The Colombian Administrative Department of Science, Technology and Innovation and the International Foundation for Science.

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Authors and Affiliations

  1. Manihot Biotech. Departamento de Biología, Universidad Nacional de Colombia, Cra 30 No 45-03, Bogota, Colombia

    Camilo E. López

  2. Laboratory of Mycology and Plant Pathology, Universidad de los Andes, Carrera 1 # 18A-10, Bogota, Colombia

    Adriana J. Bernal

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  1. Camilo E. López
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  2. Adriana J. Bernal
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Correspondence to Adriana J. Bernal.

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Communicated by: Nigel Taylor

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López, C.E., Bernal, A.J. Cassava Bacterial Blight: Using Genomics for the Elucidation and Management of an Old Problem. Tropical Plant Biol. 5, 117–126 (2012). https://doi.org/10.1007/s12042-011-9092-3

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