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Genetic patterns reveal historical and contemporary dispersal of a tree pathogen

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Abstract

Sphaerulina musiva (Peck) Verkley, Quaedvlieg and Crous (syn = Septoria musiva Peck, Mycosphaerella populorum Thompson) is a pathogen of poplar that causes two distinct diseases, leaf spots and cankers. This pathogen co-evolved with Populus deltoides but recent reports have linked it to infections in planted stands of P. trichocarpa, P. balsamifera and their hybrids. Reports of S. musiva have mainly come from central and eastern US and eastern Canada, the assumed endemic range of the pathogen. S. musiva was detected for the first time in the Canadian provinces of British Columbia in 2006 and in Alberta in 2009. Our objectives were to determine the source of S. musiva in British Columbia and Alberta and examine the dispersal pathways of this pathogen across North America. For this task we sequenced eight genes and extracted single nucleotide polymorphisms on a geographically diverse set of 73 strains of S. musiva. Population structure and Approximate Bayesian Computation (ABC) analyses eliminated eastern Canada as a source for these introductions. Genetic diversity estimates and ABC analyses support an eastern US centre of origin for S. musiva and two waves of dispersal into Canada. The recently detected west Canadian populations appear to have received contributions from Saskatchewan (a western Canadian population) and also, in the case of British Columbia from the mid-west US populations. These results also reveal distinct eastern and western Canadian populations. Our analyses suggest that dissemination of the pathogen appears to be associated with the natural distribution of wild P. deltoides and more recently linked to anthropogenic activities. The most parsimonious explanation for the contemporary spread of S. musiva across the landscape is via infected plant material. Our analysis of the tree disease caused by S. musiva demonstrates that a population genetics approach is essential to reveal potential sources and patterns of spread of a pathogen.

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References

  • Agapow P-M, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102. doi:10.1046/j.1471-8278.2000.00014.x

    Article  CAS  Google Scholar 

  • Barrès B, Carlier J, Seguin M, Fenouillet C, Cilas C, Ravigné V (2012) Understanding the recent colonization history of a plant pathogenic fungus using population genetic tools and Approximate Bayesian Computation. Heredity 109:269–279. doi:10.1038/hdy.2012.37

    Article  PubMed  PubMed Central  Google Scholar 

  • Bier JE (1939) Septoria canker of introduced and native hybrid poplars. Can J Res 17:195–204

    Article  Google Scholar 

  • Callan B, Leal I, Foord BM, Dennis JJ, van Oosten C (2007) Septoria musiva isolated from cankered stems in hybrid poplar stool beds, Fraser Valley, British Columbia. North Am Fungi 2:1–9. doi:10.2509/pnwf.2007.002.007

    Article  Google Scholar 

  • Carnegie AJ, Cooper K (2011) Emergency response to the incursion of an exotic myrtaceous rust in Australia. Australas Plant Pathol 40:346–359. doi:10.1007/s13313-011-0066-6

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Snell Q, Walke P et al (2002) TCS: estimating gene genealogies. Proceedings of the 16th international parallel and distributed processing symposium, p 184

  • Comes HPC, Kadereit JW (1998) The effect of quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438

    Article  Google Scholar 

  • Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIYABC: a user-friendly approach to Approximate Bayesian Computation. Bioinformatics 24:2713–2719. doi:10.1093/bioinformatics/btn514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornuet J-M, Ravigné V, Estoup A (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinformatics 11:401. doi:10.1186/1471-2105-11-401

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin J-M, Estoup A (2014) DIYABC v2.0: a software to make Approximate Bayesian Computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189. doi:10.1093/bioinformatics/btt763

    Article  CAS  Google Scholar 

  • Derbowka DR, Andersen S, Lee-Andersen S, Stenberg C (2012) Poplar and willow cultivation and utilization in Canada. 2008–2011 Canadian Country Progress Report. Canadian Report to the 24th IPC Session, Dehradun, India—International Poplar Commis

  • Dhillon B, Feau N, Aerts AL, Beauseigle S, Bernier L, Copeland A, Foster A, Gill N, Henrissat B, Herath P et al (2015) Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen. Proc Natl Acad Sci USA 112:3451–3456. doi:10.1073/pnas.1424293112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dlugosch KMM, Parker IMM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. doi:10.1111/j.1365-294X.2007.03538.x

    Article  CAS  PubMed  Google Scholar 

  • dos Santos ÁF, Machado EB, Stanosz GR, Smith DR (2010) First report of Septoria musiva in poplar in Brazil. Trop Plant Pathol 35:52–53. doi:10.1590/S1982-56762010000100009

    Article  Google Scholar 

  • Dutech C, Barrès B, Bridier J, Robin C, Milgroom MG, Ravigné V (2012) The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen. Mol Ecol 21:3931–3946. doi:10.1111/j.1365-294X.2012.05575.x

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, VonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  • Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501. doi:10.1146/annurev.ecolsys.39.110707.173414

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. doi:10.1111/j.1471-8286.2007.01758.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2012) Improving lives with poplars and willows. Synthesis of Country Progress Reports. 24th Session of the International Poplar Commission, Dehradun, India, 30 Oct–2 Nov 2012. Working Paper IPC/12. Forest Assessment, Management and Conservation Division, FAO. Rome

  • Feau N, Bernier L (2004) First report of shining willow as a host plant for Septoria musiva. Plant Dis 88:770

    Article  Google Scholar 

  • Feau N, Hamelin RC, Vandecasteele C, Bernier L (2005) Genetic structure of Mycosphaerella populorum (anamorph Septoria musiva) populations in north-central and northeastern North America. Phytopathology 95:608–616. doi:10.1094/PHYTO-95-0608

    Article  CAS  PubMed  Google Scholar 

  • Feau N, Mottet M-J, Périnet P, Hamelin RC, Bernier L (2010) Recent advances related to poplar leaf spot and canker caused by Septoria musiva. Can J Plant Pathol 32:122–134. doi:10.1080/07060661003740009

    Article  Google Scholar 

  • Geils BW, Hummer KE, Hunt RS (2010) White pines, Ribes, and blister rust: a review and synthesis. For Pathol 40:147–185. doi:10.1111/j.1439-0329.2010.00654.x

    Google Scholar 

  • Gladieux P, Zhang X-G, Róldan-Ruiz I, Caffier V, Leroy T, Devaux M, Van Glabeke S, Coart E, Le Cam B (2010) Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Mol Ecol 19:658–674. doi:10.1111/j.1365-294X.2009.04498.x

    Article  PubMed  Google Scholar 

  • Good IJ (1953) On the population frequency of species and the estimation of population parameters. Biometrika 40:237–264. doi:10.2307/2333344

    Article  Google Scholar 

  • Goss EM, Larsen M, Chastagner GA, Givens DR, Grünwald NJ (2009) Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLoS Pathog 5:e1000583. doi:10.1371/journal.ppat.1000583

    Article  PubMed  PubMed Central  Google Scholar 

  • Government of British Columbia (2004) Invasive alien species framework for British Columbia: identifying and addressing threats to biodiversity. Victoria, BC. Available: http://www.for.gov.bc.ca/hra/invasive631species/Publications/MoE_alien_species_framework_BC_2004.pdf. Accessed 29 Sept 2014

  • Government of Canada (2004) An invasive alien species strategy for Canada. Ottawa, ON. Available: http://publications.gc.ca/collections/collection_2014/ec/CW66-394-2004-eng.pdf. Accessed 29 Sept 2014

  • Hamelin RC, Hunt RS, Geils BW, Jensen GD, Jacobi V, Lecours N (2000) Barrier to gene flow between eastern and western populations of Cronartium ribicola in North America. Phytopathology 90:1073–1078. doi:10.1094/PHYTO.2000.90.10.1073

    Article  CAS  PubMed  Google Scholar 

  • Hansen EA, Ostry ME, Johnson WD et al (1994) Field performance of Populus in short-rotation intensive culture plantations in the north-central U.S. USDA For Ser Res pap NC-320

  • Herath P, Beauseigle S, Dhillon B, Ojeda DI, Bilodeau G, Isabel N, Gros-Louis M-C, Kope H, Zeglen S, Hamelin RC, Feau N (2016) Anthropogenic signature in the incidence and distribution of an emerging pathogen of poplars. Biol Invasions 18:1147–1161. doi:10.1007/s10530-015-1051-8

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. doi:10.1111/j.1755-0998.2009.02591.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J, Pyšek P, Roques A, Sol D, Solarz W, Vilà M (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414. doi:10.1111/j.1365-2664.2007.01442.x

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr : an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. doi:10.7717/peerj.281

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamvar ZN, Brooks JC, Grünwald NJ (2015) Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front Genet 6:1664–8021. doi:10.3389/fgene.2015.00208

    Article  Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. doi:10.1111/2041-210X.12067

    Article  Google Scholar 

  • Lande R (1996) Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76:5–13. doi:10.2307/3545743

    Article  Google Scholar 

  • LeBoldus JM, Blenis PV, Thomas BR, Feau N, Bernier L (2009) Susceptibility of Populus balsamifera to Septoria musiva: a field study and greenhouse experiment. Plant Dis 93:1146–1150. doi:10.1094/PDIS-93-11-1146

    Article  Google Scholar 

  • Ludwig JA, Reynolds JF (1988) Statistical ecology: a primer on methods and computing. Wiley, New York

    Google Scholar 

  • Maxwell DL, Kruger EL, Stanosz GR (1997) Effects of water stress on colonization of Poplar stems and excised leaf disks by Septoria musiva. Phytopathology 87:381–388. doi:10.1094/PHYTO.1997.87.4.381

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith J, Smith NH, O’Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90:4384–4388

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Boston

    Book  Google Scholar 

  • Meirmans P, Van Tienderen P (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. doi:10.1111/j.1471-8286.2004.00770.x

    Article  Google Scholar 

  • Milgroom MG, Wang K, Zhou Y et al (1996) Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88:179–190

    Article  Google Scholar 

  • Mottet MJ, Lamontagne D, Caron F, Fauchon A, Perinet P (2007) Risk management of Septoria canker in Quebec hybrid poplar plantation. Conf. Handb.—2007 Annual Meeting Poplar Council Canada, Rivière-du-Loup et Québec, Canada, p 59

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1978) Estimate of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, p 512

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273. doi:10.1073/pnas.76.10.5269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Newcombe G (1998) A review of exapted resistance to diseases of Populus. Eur J For Pathol 28:209–216

    Article  Google Scholar 

  • Newcombe G, Bradshaw HDJ (1996) Quantative trait loci conferring resistance in hybrid poplar to Septoria populicola, the cause of leaf spot. Can J For Res 26:1943–1950

    Article  Google Scholar 

  • Newcombe G, Ostry M (2001) Recessive resistance to Septoria stem canker of hybrid Poplar. Phytopathology 91:1081–1084. doi:10.1094/PHYTO.2001.91.11.1081

    Article  CAS  PubMed  Google Scholar 

  • Newcombe G, Ostry ME, Hubbes M, Perinet P, Mottet MJ (2001) Poplar diseases. In: Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture North America. National Research Council of Canada Press, Ottawa, pp 249–276

    Google Scholar 

  • Ostry ME (1987) Biology of Septoria musiva and Marssonina brunnea in hybrid Populus plantations and control of Septoria canker in nurseries. For Pathol 17:158–165. doi:10.1111/j.1439-0329.1987.tb00741.x

    Google Scholar 

  • Ostry M, McNabb H (1983) Diseases of intensively cultured hybrid poplars: a summary of recent research in the north central region. In: Hansen, Edward A (eds) Intensive planting culture 12 years research general technologies. U.S. Department of Agriculture, Forest Service, North Central Forest Experiment Station, St. Paul, MN, pp 102–109

  • Peck CH (1881) Report of the botanist. Annual report of the New York State Museum of Natural History, 35th edn. Regents of the University of the State of New York, Albany, p 138

  • Petit RJ, Aguinagalde I, de Beaulieu J-L et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565. doi:10.1126/science.1083264

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571

    Article  PubMed  Google Scholar 

  • Robert S, Ravigne V, Zapater M-F, Abadie C, Carlier J (2012) Contrasting introduction scenarios among continents in the worldwide invasion of the banana fungal pathogen Mycosphaerella fijiensis. Mol Ecol 21:1098–1114. doi:10.1111/j.1365-294X.2011.05432.x

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Sakalidis ML, Slippers B, Wingfield BD, Hardy GSJ, Burgess TI (2013) The challenge of understanding the origin, pathways and extent of fungal invasions: global populations of the Neofusicoccum parvum-N. ribis species complex. Divers Distrib 19:873–883. doi:10.1111/ddi.12030

    Article  Google Scholar 

  • Sarasola AA (1944) Dos septorios is de las alamedas Argentinas. Rev Argent Agron 11:20–43

    Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688. doi:10.1038/163688a0

    Article  Google Scholar 

  • Sivanesan A (1990) Mycosphaerella populorum. CMI descriptions of pathogenic fungi and bacteria. No. 988. Mycopathologia 109:57–58

    Article  Google Scholar 

  • Stanton BJ, Serapiglia MJ, Smart LB (2014) Domestication and conservation of genetic resources. In: Isebrands JG, Richardson J (eds) Poplars willows trees society environment. CAB International, Wallingford, pp 124–199

    Chapter  Google Scholar 

  • Strobl S, Fraser K (1989) Incidence of Septoria canker of hybrid poplars in eastern Ontario. Can Plant Dis Surv 69:109–112

    Google Scholar 

  • Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA (2007) Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 24:398–411. doi:10.1093/molbev/msl169

    Article  CAS  PubMed  Google Scholar 

  • Stukenbrock EH, Jørgensen FG, Zala M, Hansen TT, McDonald BA, Schierup MH (2010) Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet 6:e1001189. doi:10.1371/journal.pgen.1001189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tay WT, Soria MF, Walsh T et al (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8:e80134. doi:10.1371/journal.pone.0080134

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson GE (1941) Leaf-spot diseases of poplars caused by Septoria musiva and S. populicola. Phytopathology 31:241–254

    Google Scholar 

  • Thomas B, Richardson J (2006) Poplar genomics to Poplar production: bridging the gap for best use of our resources and knowledge. Poplar Council of Canada. Available: www.poplar.ca/upload/documents/g2ppaper.pdf. Accessed 29 Sept 2014

  • Tsui CKM, Roe AD, El-Kassaby YA, Rice AV, Alamouti SM, Sperling FA, Cooke JE, Bohlmann J, Hamelin RC (2012) Population structure and migration pattern of a conifer pathogen, Grosmannia clavigera, as influenced by its symbiont, the mountain pine beetle. Mol Ecol 21:71–86. doi:10.1111/j.1365-294X.2011.05366.x

    Article  PubMed  Google Scholar 

  • Vercken E, Fontaine MC, Gladieux P, Hood ME, Jonot O, Giraud T (2010) Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathog 6:e1001229. doi:10.1371/journal.ppat.1001229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waterman AM, Aldrich KF (1952) Surface sterilization of poplar cuttings. Plant Dis Rep 36:203–207

    CAS  Google Scholar 

  • Waterman AM, Aldrich KF (1954) Additional information on the surface sterilization of poplar cuttings. Plant Dis Rep 38:96–100

    CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358. doi:10.2307/2408641

    Article  Google Scholar 

  • Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Zalasky H (1978) Stem and leaf spot infections caused by Septoria musiva and Septoria populicola on poplar seedlings. Phytoprotection 59:43–50

    Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the reviewers whose valuable comments helped improve this manuscript. We would like to thank Harry Kope, Stephan Zeglan and Cees van Oosten for their advice on the history of poplar material imports into British Columbia. Also Dr. Cyril Dutech (INRA de Bordeaux, France) for his excellent advice regarding the findings of this manuscript. We appreciate the assistance Kevin Keenan (Queen’s University, Belfast, Northern Ireland, United Kingdom) provided in modifying his R package diveRsity for haploid organism analysis. Thank you to Dr. Glen Stanoz (University of Wisconsin-Madison, WI, USA), Dr. Jared Leboldus (North Dakota State University, ND, USA) and Dr. Louis Bernier (Laval University, QC, Canada) for providing us with some cultures. This work would not have been possible without members of the TAIGA team who assisted with the lab work. This work was supported by grants from Genome Canada and Genome British Columbia (Large Scale Applied Research Program, Grant #164) to the TAIGA project (www.taigaforesthealth.com) of the University of British Columbia.

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Sakalidis, M.L., Feau, N., Dhillon, B. et al. Genetic patterns reveal historical and contemporary dispersal of a tree pathogen. Biol Invasions 18, 1781–1799 (2016). https://doi.org/10.1007/s10530-016-1120-7

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