Reconstructing the history of Maize streak virus 1 strain-A dispersal to reveal diversification 2 hotspots and its origin in southern Africa 3 4

64 65 Maize streak virus (MSV) strain A, the causal agent of Maize streak disease is 66 today one of the most serious biotic threats to African food security. Determining 67 where MSV-A originated and how it spread trans-continentally could yield 68 valuable insights into its historical emergence as a crop pathogen. Similarly, 69 determining where the major extant MSV-A lineages arose could identify 70 geographical hotspots of MSV evolution. Here, we use model-based 71 phylogeographic analyses of 353 fully-sequenced MSV-A isolates to reconstruct 72 a plausible history of MSV-A movements over the past 150 years. We show that 73 since the probable emergence of MSV-A in southern Africa around 1863, the 74 virus spread trans-continentally at an average rate of 32.5 km/yr (95% highest 75 probability density intervals 15.6-51.6 km/yr). Using distinctive patterns of 76 nucleotide variation caused by 20 unique intra-MSV-A recombination events we 77 tentatively classified the MSV-A isolates into 24 easily discernable lineages. 78 Despite many of these lineages displaying distinct geographical distributions, it is 79 apparent that almost all have emerged within the past four decades from either 80 southern or eastern-central Africa. Collectively, our results suggest that regular 81 analysis of MSV-A genomes within these diversification hotspots could be used 82 to monitor the emergence of future MSV-A lineages that could affect maize 83 cultivation in Africa. 84 85 on O cber 2, 2017 by gest http/jvi.asm .rg/ D ow nladed fom

[1]  M. Suchard,et al.  Phylodynamics and Human-Mediated Dispersal of a Zoonotic Virus , 2010, PLoS pathogens.

[2]  Vincent Moulton,et al.  RDP3: a flexible and fast computer program for analyzing recombination , 2010, Bioinform..

[3]  M. Suchard,et al.  Phylogeography takes a relaxed random walk in continuous space and time. , 2010, Molecular biology and evolution.

[4]  H. Jeske,et al.  Replicative intermediates of maize streak virus found during leaf development. , 2010, The Journal of general virology.

[5]  S. Duffy,et al.  Dating the origins of the maize-adapted strain of maize streak virus, MSV-A , 2009, The Journal of general virology.

[6]  E. Rybicki,et al.  Comparative analysis of Panicum streak virus and Maize streak virus diversity, recombination patterns and phylogeography , 2009, Virology Journal.

[7]  E. Holmes,et al.  Insights into the Evolutionary History of an Emerging Livestock Pathogen: Porcine Circovirus 2 , 2009, Journal of Virology.

[8]  R. Lawry,et al.  A novel sugarcane-infecting mastrevirus from South Africa , 2009, Archives of Virology.

[9]  Alexei J. Drummond,et al.  Bayesian Phylogeography Finds Its Roots , 2009, PLoS Comput. Biol..

[10]  O. Pybus,et al.  Phylogeography and molecular epidemiology of hepatitis C virus genotype 2 in Africa. , 2009, The Journal of general virology.

[11]  Gavin J. D. Smith,et al.  Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic , 2009, Nature.

[12]  D. Shepherd,et al.  The epidemiology, economic impact and control of maize streak disease , 2009, Food Security.

[13]  Oliver P. F. Windram,et al.  Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen , 2008, The Journal of general virology.

[14]  Sergei L. Kosakovsky Pond,et al.  Evolutionary and Transmission Dynamics of Reassortant H5N1 Influenza Virus in Indonesia , 2008, PLoS pathogens.

[15]  E. Rybicki,et al.  A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. , 2008, Journal of virological methods.

[16]  J. Brown,et al.  Geminivirus strain demarcation and nomenclature , 2008, Archives of Virology.

[17]  E. Rybicki,et al.  Genetic analysis of maize streak virus isolates from Uganda reveals widespread distribution of a recombinant variant. , 2007, The Journal of general virology.

[18]  Darren P Martin,et al.  Avoidance of Protein Fold Disruption in Natural Virus Recombinants , 2007, PLoS pathogens.

[19]  H. Prasanna,et al.  Detection and frequency of recombination in tomato-infecting begomoviruses of South and Southeast Asia , 2007, Virology Journal.

[20]  David Posada,et al.  An Exact Nonparametric Method for Inferring Mosaic Structure in Sequence Triplets , 2007, Genetics.

[21]  N. Taylor,et al.  Successful application of FTA Classic Card technology and use of bacteriophage phi29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. , 2007, Journal of virological methods.

[22]  K. Hefferon,et al.  Multi‐tasking of nonstructural gene products is required for bean yellow dwarf geminivirus transcriptional regulation , 2006, The FEBS journal.

[23]  D. Bryant,et al.  A Simple and Robust Statistical Test for Detecting the Presence of Recombination , 2006, Genetics.

[24]  K. Crandall,et al.  A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. , 2005, AIDS research and human retroviruses.

[25]  Christopher J. Lee,et al.  Combining partial order alignment and progressive multiple sequence alignment increases alignment speed and scalability to very large alignment problems , 2004, Bioinform..

[26]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[27]  D. Martin,et al.  Investigation of Maize streak virus pathogenicity determinants using chimaeric genomes. , 2002, Virology.

[28]  K. Crandall,et al.  Evaluation of methods for detecting recombination from DNA sequences: Computer simulations , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  H. Jeske,et al.  DNA forms indicate rolling circle and recombination‐dependent replication of Abutilon mosaic virus , 2001, The EMBO journal.

[30]  D. Martin,et al.  Sequence diversity and virulence in Zea mays of Maize streak virus isolates. , 2001, Virology.

[31]  M. Suchard,et al.  Bayesian selection of continuous-time Markov chain evolutionary models. , 2001, Molecular biology and evolution.

[32]  E. Rybicki,et al.  Analysis of the diversity of African streak mastreviruses using PCR-generated RFLPs and partial sequence data. , 2001, Journal of virological methods.

[33]  J. Mccann Maize and Grace: History, Corn, and Africa's New Landscapes, 1500–1999 , 2001, Comparative Studies in Society and History.

[34]  N. Bosque-pérez,et al.  Eight decades of maize streak virus research. , 2000, Virus research.

[35]  Mark J. Gibbs,et al.  Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences , 2000, Bioinform..

[36]  Darren Martin,et al.  RDP: detection of recombination amongst aligned sequences , 2000, Bioinform..

[37]  S. Sawyer,et al.  Possible emergence of new geminiviruses by frequent recombination. , 1999, Virology.

[38]  P. Mullineaux,et al.  The two nonstructural proteins from wheat dwarf virus involved in viral gene expression and replication are retinoblastoma-binding proteins. , 1996, Virology.

[39]  L. Nault,et al.  Movement of Cicadulina Storeyi (Homoptera: Cicadellidae) in Maize Fields and Its Behaviour in Relation to Maize Growth Stage , 1995 .

[40]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[41]  R. Briddon,et al.  Analysis of the genetic variability of maize streak virus , 1994, Virus Genes.

[42]  A. Lucy,et al.  RNA-primed complementary-sense DNA synthesis of the geminivirus African cassava mosaic virus. , 1992, Nucleic acids research.

[43]  John Maynard Smith,et al.  Analyzing the mosaic structure of genes , 1992, Journal of Molecular Evolution.

[44]  J. Hofer,et al.  Coordinate regulation of replication and virion sense gene expression in wheat dwarf virus. , 1992, The Plant cell.

[45]  P. Mullineaux,et al.  Replication of wheat dwarf virus DNA in protoplasts and analysis of coat protein mutants in protoplasts and plants. , 1989, Nucleic acids research.

[46]  S. G. Rogers,et al.  Maize streak virus genes essential for systemic spread and symptom development , 1989, The EMBO journal.

[47]  Z. Dąbrowski,et al.  Population density, species composition and infectivity with maize streak virus (MSV) of Cicadulina spp. leafhoppers in some ecological zones in Nigeria , 1987 .

[48]  Z. Dąbrowski Two new species of Cicadulina China (Hemiptera: Euscelidae) from West Africa , 1987 .

[49]  D. Rose Times and sizes of dispersal flights by Cicadulina species (Homoptera: Cicadellidae), vectors of maize streak disease. , 1972 .

[50]  M. Jeffreys How Ancient is West African Maize? , 1963, Africa.

[51]  R. G. Fennah A new species of Cicadulina (Homoptera : Cicadellidae) from East Africa , 1959 .

[52]  Darren P Martin,et al.  Maize streak virus: an old and complex 'emerging' pathogen. , 2010, Molecular plant pathology.

[53]  Graziano Pesole,et al.  BMC Evolutionary Biology BioMed Central , 2007 .

[54]  M. Nei,et al.  Molecular Evolutionary Genetics Analysis , 2007 .

[55]  R. Frutos,et al.  Infectivity and complete nucleotide sequence of the genome of a genetically distinct strain of maize streak virus from Reunion Island , 2005, Archives of Virology.

[56]  W. G. Buchholz,et al.  Specificity of Agrobacterium-mediated delivery of maize streak virus DNA to members of the Gramineae , 2004, Plant Molecular Biology.

[57]  D. Martin,et al.  The relative infectivities and genomic characterisation of three distinct mastreviruses from South Africa , 2001, Archives of Virology.

[58]  A. Raftery,et al.  Bayes factors , 1995 .

[59]  B. Reynaud Transmission des virus de la striure, du stripe et de la mosai͏̈que du mai͏̈s par leurs vecteurs Cicadulina Mbila (Naude, 1924) et Peregrinus maidis (Ashmead, 1890) (Homoptera) : approches biologique, génétique et épidémiologique de la relation vecteur-virus-plante , 1988 .

[60]  A. Kopp Les maladies des plantes à la Réunion. , 1930 .