Area Under Curve; Disease Progression; Genome, Bacterial; Genomics; Geography; Immunity, Innate; Manihot/metabolism/microbiology; Models, Genetic; Molecular Sequence Data; Phylogeny; Plant Diseases/genetics/microbiology; Polymorphism, Genetic; Polymorphism, Single Nucleotide; Sequence Analysis, DNA/methods; Time Factors; Xanthomonas axonopodis/metabolism
Abstract :
[en] Cassava bacterial blight (CBB), incited by Xanthomonas axonopodis pv. manihotis (Xam), is the most important bacterial disease of cassava, a staple food source for millions of people in developing countries. Here we present a widely applicable strategy for elucidating the virulence components of a pathogen population. We report Illumina-based draft genomes for 65 Xam strains and deduce the phylogenetic relatedness of Xam across the areas where cassava is grown. Using an extensive database of effector proteins from animal and plant pathogens, we identify the effector repertoire for each sequenced strain and use a comparative sequence analysis to deduce the least polymorphic of the conserved effectors. These highly conserved effectors have been maintained over 11 countries, three continents, and 70 y of evolution and as such represent ideal targets for developing resistance strategies.
Fu D, et al. (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357-1360.
Kunkeaw S, Tan S, Coaker G (2010) Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Mol Plant Microbe Interact 23:415-424.
Lieberman TD, et al. (2011) Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43:1275-1280.
Harris SR, et al. (2012) Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat Genet 44:413-419, S1.
Lee S-W, et al. (2009) A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326:850-853.
Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and effectors: The blurred PTI-ETI dichotomy. Plant Cell 23:4-15.
Cunnac S, et al. (2011) Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc Natl Acad Sci USA 108:2975-2980.
Zhao B, Dahlbeck D, Krasileva KV, Fong RW, Staskawicz BJ (2011) Computational and biochemical analysis of the Xanthomonas effector AvrBs2 and its role in the modulation of Xanthomonas type three effector delivery. PLoS Pathog 7(12): e1002408.
Metz M, et al. (2005) The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. Plant J 41:801-814. (Pubitemid 40398711)
Kim J-G, et al. (2009) Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21:1305-1323.
Underwood W, Zhang S, He SY (2007) The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana. Plant J 52:658-672. (Pubitemid 350060587)
Kay S, Bonas U (2009) How Xanthomonas type III effectors manipulate the host plant. Curr Opin Microbiol 12:37-43.
Food and Agriculture Organization (2008) Cassava [Food and Agriculture Organization of the United Nations (FAO), Rome].
Lozano JCS, L. (1974) Bacterial blight of cassava in Colombia: Epidemiology and control. Phytopathology 64:83-88.
Hillocks RJ, Thresh JM, Bellotti AC (2002) Cassava: Biology, Production and Utilization (CABI, New York).
Potnis N, et al. (2011) Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 12:146.
Verdiera V, Restrepob S, Mosquerab G (1998) Genetic and pathogenic variation of Xanthomonas axonopodis pv. manihotis in Venezuela. Plant Pathol 47:601-608.
Williams RJ, Agboola SD (1973) Bacterial wilt of cassava in Nigeria. Plant Dis Reporter 57:824-827.
Verdier V, Dongo P, Boher B (1993) Assessment of genetic diversity among strains of Xanthomonas campestris pv. manihotis. Microbiology 139:2591-2601.
Sundin GW, Demezas DH, Bender CL (1994) Genetic and plasmid diversity within natural populations of Pseudomonas syringae with various exposures to copper and streptomycin bactericides. Appl Environ Microbiol 60:4421-4431. (Pubitemid 24370811)
Darling AE, Mau B, Perna NT (2010) ProgressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE, 10.1371/journal. pone.0011147.
Parkinson N, Cowie C, Heeney J, Stead D (2009) Phylogenetic structure of Xanthomonas determined by comparison of gyrB sequences. Int J Syst Evol Microbiol 59:264-274.
Han SW, et al. (2011) Small protein-mediated quorum sensing in a Gram-negative bacterium. PLoS ONE 6:e29192.
Lee SW, Han SW, Bartley LE, Ronald PC (2006) From the Academy: Colloquium review. Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proc Natl Acad Sci USA 103:18395-18400. (Pubitemid 44913421)
Cai R, et al. (2011) The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog, 10.1371/journal.ppat.1002130.
White FF, Potnis N, Jones JB, Koebnik R (2009) The type III effectors of Xanthomonas. Mol Plant Pathol 10:749-766.
Dean P (2011) Functional domains and motifs of bacterial type III effector proteins and their roles in infection. FEMS Microbiol Rev 35:1100-1125.
Koebnik R (2011) The Xanthomonas Resource. Available at http://xanthomonas.org/.
Bull SE, et al. (2009) Agrobacterium-mediated transformation of friable embryogenic calli and regeneration of transgenic cassava. Nat Protoc 4:1845-1854.
Restrepo S, Duque M, Verdier V (2000) Characterization of pathotypes among isolates of Xanthomonas axonopodis pv. manihotis in Colombia. Plant Pathol 49:680-687. (Pubitemid 32035556)
Lu H, et al. (2008) Acquisition and evolution of plant pathogenesis-associated gene clusters and candidate determinants of tissue-specificity in xanthomonas. PLoS ONE, 10.1371/journal.pone.0003828.
Li YR, et al. (2011) Hpa2 required by HrpF to translocate Xanthomonas oryzae transcriptional activator-like effectors into rice for pathogenicity. Appl Environ Microbiol 77:3809-3818.
Lorenz C, et al. (2008) HpaA from Xanthomonas is a regulator of type III secretion. Mol Microbiol 69:344-360. (Pubitemid 351988010)
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. (Pubitemid 34311130)
Kim JG, et al. (2003) Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J Bacteriol 185:3155-3166.
Jiang W, et al. (2009) Identification of six type III effector genes with the PIP box in Xanthomonas campestris pv. campestris and five of them contribute individually to full pathogenicity. Mol Plant Microbe Interact 22:1401-1411.
Furutani A, et al. (2009) Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 22:96-106.
Kim JG, et al. (2009) Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21:1305-1323.
Mackey D, Holt BF, 3rd, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-754. (Pubitemid 34327527)
Tang XY, et al. (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-2063.
Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7:601-611. (Pubitemid 44325351)
Nei M, Jin L (1989) Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol 6:290-300.
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.
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 15:637-646. (Pubitemid 34780473)
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 17:1192-1200. (Pubitemid 39428876)
Shiotani H, Fujikawa T, Ishihara H, Tsuyumu S, Ozaki K (2007) A pthA homolog from Xanthomonas axonopodis pv. citri responsible for host-specific suppression of virulence. J Bacteriol 189:3271-3279. (Pubitemid 46697417)
Antony G, et al. (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864-3876.
Al-Saadi A, et al. (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 20:934-943. (Pubitemid 47105726)
Flor HH (1955) Host-parasite interaction in flax rust- its genetics and other implications. Phytopathology 45:680-685.
Zhao B, et al. (2004) The avrRxo1 gene from the rice pathogen Xanthomonas oryzae pv. oryzicola confers a nonhost defense reaction on maize with resistance gene Rxo1. Mol Plant Microbe Interact 17:771-779. (Pubitemid 38774164)
Bart RS, Chern M, Vega-Sánchez ME, Canlas P, Ronald PC (2010) Rice Snl6, a cinnamoyl-CoA reductase-like gene family member, is required for NH1-mediated immunity to Xanthomonas oryzae pv. oryzae. PLoS Genet, 6:pii:e1001123.
Römer P, et al. (2010) Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae. New Phytol 187:1048-1057.
Restrepo S, Verdier V (1997) Geographical differentiation of the population of Xanthomonas axonopodis pv. manihotis in Colombia. Appl Environ Microbiol 63: 4427-4434. (Pubitemid 27485771)
Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: Finding plant genes for disease and defense. Curr Opin Plant Biol 13:394-401.
Zhu S, Li Y, Vossen JH, Visser RG, Jacobsen E (2012) Functional stacking of three resistance genes against Phytophthora infestans in potato. Transgenic Res 21:89-99.
Verdier V, Mosquera G, Assigbétsé K (1998) Detection of the cassava bacterial blight pathogen, Xanthomonas axonopodis pv. manihotis, by polymerase chain reaction. Plant Dis 82:79-83.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697-703.
