Origin and diversification of Xanthomonas citri subsp. citri pathotypes revealed by inclusive phylogenomic, dating, and biogeographic analyses

Civerolo EL. Bacterial canker disease of citrus [Xanthomonas campestris]. Journal of the Rio Grande Valley Horticultural Society. 1984;37:127–45. Brunings AM, Gabriel DW. Xanthomonas citri: breaking the surface. Mol Plant Pathol. 2003;4(3):141–57. Graham JH, Gottwald TR, Cubero J, Achor DS. Xanthomonas axonopodis pv. Citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol. 2004;5(1):1–15. Lee HA. Further data on the susceptibility of rutaceous plants to citrus-canker. J Agric Res. 1918;15:661–5. Bitancourt AA. O Cancro Cítrico. Biológico. 1957;23:101–11. Schubert TS, Miller JW: Bacterial citrus canker. Fla Department Agric \& Consumer Services, Division of Plant Industry 1996. Raychaudhuri SP, Verma JP, Nariani TK, Sen B. The history of plant pathology in India. Annu Rev Phytopathol. 1972;10(1):21–36. Malavolta VA Jr, Yamashiro T, Nogueira EMC, Feichtenberger E. Distribuição do tipo C de Xanthomonas campestris pv. citri no Estado de São Paulo. Summa Phytopathol. 1984;10(11). da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM, et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature. 2002;417(6887):459–63. Verniere C, Hartung JS, Pruvost OP, Civerolo EL, Alvarez AM, Maestri P, Luisetti J. Characterization of phenotypically distinct strains of Xanthomonas axonopodis pv. Citri from Southwest Asia. Eur J Plant Pathol. 1998;104(5):477–87. Derso E, Vernière C, Pruvost OP. First Report of Xanthomonas citri pv. citri-A* Causing Citrus Canker on Lime in Ethiopia. Plant Dis. 2009;93:203. Sun XA, Stall RE, Jones JB, Cubero J, Gottwald TR, Graham JH, Dixon WN, Schubert TS, Chaloux PH, Stromberg VK, et al. Detection and characterization of a new strain of citrus canker bacteria from key Mexican lime and Alemow in South Florida. Plant Dis. 2004;88(11):1179–88. Zhang Y, Jalan N, Zhou X, Goss E, Jones JB, Setubal JC, Deng X, Wang N. Positive selection is the main driving force for evolution of citrus canker-causing Xanthomonas. ISME J. 2015;9:2128–38. Gordon JL, Lefeuvre P, Escalon A, Barbe V, Cruveiller S, Gagnevin L, Pruvost O. Comparative genomics of 43 strains of Xanthomonas citri pv. citri reveals the evolutionary events giving rise to pathotypes with different host ranges. BMC Genomics. 2015;16:1098. Bui Thi Ngoc L, Vernière C, Jouen E, Ah-You N, Lefeuvre P, Chiroleu F, Gagnevin L, Pruvost O. Amplified fragment length polymorphism and multilocus sequence analysis-based genotypic relatedness among pathogenic variants of Xanthomonas citri pv. Citri and Xanthomonas campestris pv. Bilvae. Int J Syst Evol Microbiol. 2010;60(3):515–25. Pruvost O, Magne M, Boyer K, Leduc A, Tourterel C, Drevet C, Ravigne V, Gagnevin L, Guerin F, Chiroleu F, et al. A MLVA genotyping scheme for global surveillance of the citrus pathogen Xanthomonas citri pv. citri suggests a worldwide geographical expansion of a single genetic lineage. PLoS One. 2014;9(6):e98129. Nixon KC, Carpenter JM. On Outgroups. Cladistics. 1993;9:413–26. Smith AB. Rooting molecular trees: problems and strategies. Biol J Linn Soc. 1994;51(3):279–92. Lyons-Weiler J, Hoelzer GA, Tausch RJ. Optimal outgroup analysis. Biol J Linn Soc. 1998;64(4):493–511. Bergsten J. A review of long-branch attraction. Cladistics. 2005;21(2):163–93. Bansal K, Midha S, Kumar S, Patil PB. Ecological and evolutionary insights into Xanthomonas citri pathovar diversity. Appl Env Microbiol. 2017;83(9):e02993–16. Parkinson N, Cowie C, Heeney J, Stead D. Phylogenetic structure of Xanthomonas determined by comparison of gyrB sequences. Int J Syst Evol Microbiol. 2009;59(2):264–74. Darrasse A, Bolot S, Serres-Giardi L, Charbit E, Boureau T, Fisher-Le Saux M, Briand M, Arlat M, Gagnevin L, Koebnik R. High-quality draft genome sequences of Xanthomonas axonopodis pv. Glycines strains CFBP 2526 and CFBP 7119. Genome Announc. 2013;1(6):e01036–13. Cunnac S, Bolot S, Serna NF, Ortiz E, Szurek B, Noël LD, Arlat M, Jacques M-A, Gagnevin L, Carrere S. High-quality draft genome sequences of two Xanthomonas citri pv. Malvacearum strains. Genome Announc. 2013;1(4):e00674–13. Midha S, Ranjan M, Sharma V, Pinnaka AK, Patil PB. Genome sequence of Xanthomonas citri pv. mangiferaeindicae strain LMG 941. In: Am Soc Microbiol; 2012. Gochez AM, Huguet-Tapia JC, Minsavage GV, Shantaraj D, Jalan N, Strauß A, Lahaye T, Wang N, Canteros BI, Jones JB: Pacbio sequencing of copper-tolerant Xanthomonas citri reveals presence of a chimeric plasmid structure and provides insights into reassortment and shuffling of transcription activator-like effectors among X. citri strains. BMC genomics 2018, 19(1):16. Jalan N, Kumar D, Yu F, Jones JB, Graham JH, Wang N. Complete genome sequence of Xanthomonas citri subsp. citri strain AW12879, a restricted-host-range citrus canker-causing bacterium. Genome Announc. 2013;1(3):e00235–13. Richard D, Tribot N, Boyer C, Terville M, Boyer K, Javegny S, Roux-Cuvelier M, Pruvost O, Moreau A, Chabirand A: First report of copper-resistant Xanthomonas citri pv. citri pathotype A causing Asiatic citrus canker in Réunion, France. Plant Disease 2017, 101(3):503. Jalali A, Alavi SM, Sangtarash MH. Comparative genomic analysis of wide and narrow host range strains of Xanthomonas citri subsp. citri, showing differences in the genetic content of their pathogenicity and virulence factors. Australas Plant Pathol. 2017;46(1):49–61. Jalali A, Alavi SM, Sangtarash MH: Genomic characterization and phylogenetic analysis of a narrow host-range Iranian strain of Xanthmonas citri sub. citri, NIGEB-88. 2018. Bodnar AM, Santillana G, Mavrodieva V, Liu Z, Nakhla M, Gabriel DW. Complete genome sequences of three Xanthomonas citri strains from Texas. Genome Announc. 2017;5(28):e00609–17. Mhedbi-Hajri N, Hajri A, Boureau T, Darrasse A, Durand K, Brin C, Fischer-Le Saux M, Manceau C, Poussier S, Pruvost OP, et al. Evolutionary history of the plant pathogenic bacterium Xanthomonas axonopodis. PLoS One. 2013;8:e58474. Laia ML, Moreira LM, Dezajacomo J, Brigati JB, Ferreira CB, Ferro MI, Silva AC, Ferro JA, Oliveira JC. New genes of Xanthomonas citri subsp citri involved in pathogenesis and adaptation revealed by a transposon-based mutant library. BMC Microbiol. 2009;9:12. Li J, Wang N. The gpsX gene encoding a glycosyltransferase is important for polysaccharide production and required for full virulence in Xanthomonas citri subsp. citri. BMC Microbiol. 2012;12(1):31. Yan Q, Wang N. High-throughput screening and analysis of genes of Xanthomonas citri subsp. citri involved in citrus canker symptom development. Mol Plant-Microbe Interact. 2012;25(1):69–84. Zhou X, Hu X, Li J, Wang N. A novel periplasmic protein, VrpA, contributes to efficient protein secretion by the type III secretion system in Xanthomonas spp. Mol Plant-Microbe Interact. 2015;28(2):143–53. Ferreira CB, Moreira LM, Brigati JB, Lima LLD, Ferro JA, Ferro MIT, Oliveira JCF. Identification of new genes related to virulence of Xanthomonas axonopodis pv. Citri during citrus host interactions. Advances in Microbiology. 2017;7:22–46. Vieira FCF, Gonçalves AM, Mendoza EFR, Ferreira RM, Costa MLM, Balbuena TS, Sebinelli HG, Ciancaglini P, Pizauro JM Jr, Ferro JA. A Xanthomonas citri subsp citri hypothetical protein related to virulence contains a non-functional HD domain and is implicated in flagellar motility. Genet Mol Res. 2017:16(3). Larsson A. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics. 2014;30:3276–8. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One. 2010;5(6):e11147. Müller K. SeqState - primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinform. 2005;4(1):65–9. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:94. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol. 2015;11(2):e1004041. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–4. Revell LJ. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012;3(2):217–23. Volz EM, SDW F. Scalable relaxed clock phylogenetic dating. Virus Evol. 2017:3(2). Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016;2(1):vew007. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;4(1):vey016. Raftery AE, Newton MA, Satagopan JM, Krivitsky PN: Estimating the integrated likelihood via posterior simulation using the harmonic mean identity. In: Bayesian Statistics 8. Edited by Bernardo JM, Bayarri MJ, Berger JO, Dawid AP, Heckerman D, Smith AFM, West M: Oxford University Press; 2007: 1–45. Corander J, Waldmann P, Marttinen P, Sillanpaa MJ. BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics. 2004;20(15):2363–9. Vos M, Didelot X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 2009;3(2):199–208. Goss EM, Kreitman M, Bergelson J. Genetic diversity, recombination and cryptic clades in Pseudomonas viridiflava infecting natural populations of Arabidopsis thaliana. Genetics. 2005;169(1):21–35. Sarkar SF, Guttman DS. Evolution of the core genome of pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol. 2004;70(4):1999–2012. Huang CL, Pu PH, Huang HJ, Sung HM, Liaw HJ, Chen YM, Chen CM, Huang MB, Osada N, Gojobori T, et al. Ecological genomics in Xanthomonas: the nature of genetic adaptation with homologous recombination and host shifts. BMC Genomics. 2015;16:188. Srinivasan MC, Patel MK. Two new Phytopathogenic bacteria on verbenacious hosts. Curr Sci. 1957;26:90–1. Schenk JJ, Hufford L. Effects of substitution models on divergence time estimates: simulations and an empirical study of model uncertainty using Cornales. Syst Bot. 2010;35(3):578–92. Burnham KP, Anderson DR. Mode selection and inference: a practical information-theoretical approach. New York: Springer-Verlag; 2002. Duchene S, Holt KE, Weill FX, Le Hello S, Hawkey J, Edwards DJ, Fourment M, Holmes EC. Genome-scale rates of evolutionary change in bacteria. Microb Genomics. 2016;2(11). Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 2005;22(5):1185–92. Ritchie AM, Lo N, Ho SYW. Examining the sensitivity of molecular species delimitations to the choice of mitochondrial marker. Org Divers Evol. 2016;16(3):467–80. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7. Rademaker JL, Hoste B, Louws FJ, Kersters K, Swings J, Vauterin L, Vauterin P, de Bruijn FJ. Comparison of AFLP and rep-PCR genomic fingerprinting with DNA-DNA homology studies: Xanthomonas as a model system. Int J Syst Evol Microbiol. 2000;50(Pt 2):665–77. Lapierre M, Blin C, Lambert A, Achaz G, Rocha EP. The impact of selection, gene conversion, and biased sampling on the assessment of microbial demography. Mol Biol Evol. 2016;33(7):1711–25. Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM. The last glacial maximum. Science. 2009;325(5941):710–4. Fuller DQ, Castillo C, Kingwell-Banham E, Qin L, Weisskopf A. Charred pummelo peel, historical linguistics and other tree crops: Approaches to framing the historical context of early Citrus cultivation in East, South and Southeast Asia. In: Fiorentino G, Zech-Matterne V, editors. AGRUMED: Archaeology and history of citrus fruit in the mediterranean. Naples: Publications du Centre Jean Bérard; 2018. p. 31–50. Carbonell-Caballero J, Alonso R, Ibanez V, Terol J, Talon M, Dopazo J. A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus citrus. Mol Biol Evol. 2015;32(8):2015–35. Wu GA, Terol J, Ibanez V, Lopez-Garcia A, Perez-Roman E, Borreda C, Domingo C, Tadeo FR, Carbonell-Caballero J, Alonso R, et al. Genomics of the origin and evolution of citrus. Nature. 2018;554(7692):311–6. Bock CH, Cook AZ, Parker PE, Gottwald TR, Graham JH. Short-distance dispersal of splashed bacteria of Xanthomonas citri subsp. citri from canker-infected grapefruit tree canopies in turbulent wind. Plant Pathol. 2012;61(5):829–36. Barak JD, Vancheva T, Lefeuvre P, Jones JB, Timilsina S, Minsavage GV, Vallad GE, Koebnik R. Whole-genome sequences of Xanthomonas euvesicatoria strains clarify taxonomy and reveal a stepwise erosion of type 3 effectors. Front Plant Sci. 2016;7:1805. Furutani A, Takaoka M, Sanada H, Noguchi Y, Oku T, Tsuno K, Ochiai H, Tsuge S. Identification of novel type III secretion effectors in Xanthomonas oryzae pv. Oryzae. Mol Plant-Microbe Interact. 2009;22(1):96–106. Rybak M, Minsavage GV, Stall RE, Jones JB. Identification of Xanthomonas citri ssp. citri host specificity genes in a heterologous expression host. Mol Plant Pathol. 2009;10(2):249–62. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77. Antipov D, Hartwick N, Shen M, Raiko M, Lapidus A, Pevzner PA. plasmidSPAdes: assembling plasmids from whole genome sequencing data. Bioinformatics. 2016;32(22):3380–7. Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics. 2018;34(6):1037–9. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44(14):6614–24. Contreras-Moreira B, Vinuesa P. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol. 2013;79(24):7696–701. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402. Li L, Stoeckert CJ Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178–89. Comas I, Moya A, Gonzalez-Candelas F: Phylogenetic signal and functional categories in Proteobacteria genomes. Bmc Evol Biol 2007, 7 Suppl 1:S7. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. Kück P, Meusemann K. FASconCAT: convenient handling of data matrices. Mol Phylogenet Evol. 2010;56(3):1115–8. Felsenstein J. Distance methods for inferring phylogenies: a justification. Evolution. 1984;38(1):16–24. Xia X, Xie Z. DAMBE: software package for data analysis in molecular biology and evolution. J Hered. 2001;92(4):371–3. Philippe H, Brinkmann H, Lavrov DV, Littlewood DT, Manuel M, Worheide G, Baurain D. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 2011;9(3):e1000602. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2017;35(2):518–22. Hoang DT, Vinh LS, Flouri T, Stamatakis A, von Haeseler A, Minh BQ. MPBoot: fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evol Biol. 2018;18(1):11. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23(2):254–67. Davidson R, Vachaspati P, Mirarab S, Warnow T: Phylogenomic species tree estimation in the presence of incomplete lineage sorting and horizontal gene transfer. BMC Genomics 2015, 16 Suppl 10:S1. Zhang C, Rabiee M, Sayyari E, Mirarab S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics. 2018;19(Suppl 6):153. Gupta RS. The branching order and phylogenetic placement of species from completed bacterial genomes, based on conserved indels found in various proteins. Int Microbiol. 2001;4(4):187–202. Lewis PO. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol. 2001;50(6):913–25. Tria FDK, Landan G, Dagan T. Phylogenetic rooting using minimal ancestor deviation. Nature Ecol Evol. 2017;1:0193. Jombart T. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–5. Bruen TC, Philippe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics. 2006;172(4):2665–81. Bouckaert R, Vaughan TG, Barido-Sottani J, Duchene S, Fourment M, Gavryushkina A, Heled J, Jones G, Kuhnert D, De Maio N et al: BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. Plos Comput Biol 2019, 15(4):e1006650. Hasse CH. Pseudomonas citri, the cause of citrus canker - a preliminary report. J Agric Res. 1915;4:97–100. Drake JW. Spontaneous mutation. Annu Rev Genet. 1991;25:125–46. Ochman H, Elwyn S, Moran NA. Calibrating bacterial evolution. Proc Natl Acad Sci U S A. 1999;96(22):12638–43. Kuo CH, Ochman H. Inferring clocks when lacking rocks: the variable rates of molecular evolution in bacteria. Biol Direct. 2009;4(1):35. Gibson B, Wilson DJ, Feil E, Eyre-Walker A. The distribution of bacterial doubling times in the wild. Proc Biol Sci. 2018:285(1880). Xie W, Lewis PO, Fan Y, Kuo L, Chen MH. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol. 2011;60(2):150–60. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol. 2012;29(9):2157–67. Baele G, Li WL, Drummond AJ, Suchard MA, Lemey P. Accurate model selection of relaxed molecular clocks in bayesian phylogenetics. Mol Biol Evol. 2013;30(2):239–43. Zarza E, O'Hara RB, Kolb A, Pfenninger M. A prior-based approach for hypothesis comparison and its utility to discern among temporal scenarios of divergence. bioRxiv. 2018;302539. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian Phylogenetics using tracer 1.7. Syst Biol. 2018;67(5):901–4. Yu Y, Harris AJ, Blair C, He X. RASP (reconstruct ancestral state in phylogenies): a tool for historical biogeography. Mol Phylogenet Evol. 2015;87:46–9. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421.