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The Phylogeography, Epidemiology and Determinants of Maize Streak Virus Dispersal Across Africa and the Adjacent Indian Ocean Islands

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The Phylogeography, Epidemiology and Determinants of Maize Streak Virus Dispersal Across Africa and the Adjacent Indian Ocean Islands The Phylogeography, Epidemiology and Determinants of Maize streak virus dispersal across Africa and the adjacent Indian Ocean Islands Eugene. T. Madzokere A thesis submitted in partial fulfilment of the requirements for the degree of MAGISTER SCIENTIAE (M.Sc.) South African National Bioinformatics Institute (SANBI) University of the Western Cape Supervisors: Dr. Gordon W. Harkins and Professor Darren P. Martin December 2015 KEYWORDS Maize streak virus Maize streak disease Phylogeography Epidemiology Source-sink dynamics i ABBREVIATIONS AFTZ African Free Trade Zone AICc corrected Akaike Information Criterion AN Anjouan BEAST Bayesian Evolutionary Analysis by Sampling Trees BF Bayes Factor BF Burkina Faso BJ Benin BSSVS Bayesian Stochastic Search Variable Selection CABI Commonwealth Agricultural Beaurex International CBIO Computational Biology Unit CF Central African Republic CIMMYT International Maize and Wheat Improvement Center CIRAD French Agricultural Research Center for International Development CM Cameroon CMG Cassava mosaic geminiviruses COMESA Common Market for Eastern and Southern Africa CP Coat Protein CRI Crop Research Institute CSIR Centre for Scientific and Industrial Research CTMC Continuous time Markov chain DNA Deoxyribonucleic Acid EAC East African Community EPPO European and Mediterranean Plant Protection Organization ERS Export Retention Scheme ii ESS Effective Sample Size ET Ethiopia FAO Food and Agricultural Organization FAOSTAT Food and Agriculture Organization Corporate Statistical Database FICA Farm Inputs Care Centre Limited FUBAR Fast Unbiased Bayesian Approximation FG Full Genome GARD Genetic Algorithm for Recombination Detection GDP Gross Domestic Product GH Ghana GLM Generalized Linear Model GMRF Gaussian Markov random field GTR+G+I General Time Reversible + Gamma + Invariant sites HKY Hasegawa Kishino Yano HME Harmonic mean estimate HPD Highest Posterior Density HyPhy Hypothesis testing using Phylogenies IITA International Institute of Tropical Agriculture IMPALE Improved Alignment Editor IOC Indian Ocean Commission IR Intergenic Region IRAT Institute of Agronomic and Tropical Research JIC John Innes Centre KARI Kenyan Agricultural Research Institute KE Kenya iii KH Kishino-Hasegawa KML key markup language LIR Long Intergenic Region LS Lesotho MBYMIV Mung bean yellow mosaic India virus MCB Molecular and Cell Biology MCC Maximum Clade Credibility MCMC Metropolis-Hastings Markov chain Monte Carlo MD Madagascar MEGA Molecular Evolutionary Genetics Analysis MH Moheli ML Maximum Likelihood MP Movement Protein MP Maximum Parsimony MPCP Movement Protein-Coat Protein MRCA Most Recent Common Ancestor MSD Maize streak disease MSV Maize streak virus MSV-A Maize streak virus subtype strain A MZ Mozambique NASECO Nalweyo Seed Company Limited NRF National Research Foundation NCBI National Center for Biotechnology Information OECD Organization for Economic Cooperation and Development iv PARRIS Partitioning approach for Robust Inference of Selection PRF Poliomyelitis Research Foundation PS Path Sampling RCR Rolling Circle Replication RDP Recombination Detection Program RDR Recombination Dependent Replication RTC Regional Trade Communities SADC Southern African Development Community SANBI South African National Bioinformatics Institute SARI Savanna Agricultural Research Institute SCRI Scottish Crop Research Institute SDT Sequence Demarcation Tool SIR Short Intergenic Region SPREAD Spatial Reconstruction of Evolutionary Dynamics SS Stepping stone ssDNA single-stranded Deoxyribonucleic Acid TD Chad tMRCA Time to the Most Recent Common Ancestor TYLCV Tomato yellow leaf curl virus UCT University of Cape Town UG Uganda US/ USA United States of America USAID United States Agency for International Development USP Uganda Seed Project UWC University of the Western Cape v WAEMU West African Economic and Monetary Union WNV West Nile virus ZM Zambia ZW Zimbabwe vi ABSTRACT The Phylogeography, Epidemiology and determinants of Maize streak virus dispersal across Africa and the adjacent Indian Ocean Islands E. T. Madzokere Master of Science Thesis, South African National Bioinformatics Institute, University of the Western Cape Maize streak disease (MSD), caused by variants of the Maize streak virus (MSV) A strain, is the world's third and Africa’s most important maize foliar disease. Outbreaks of the disease occur frequently and in an erratic fashion across Africa and Islands in the Indian Ocean causing devastating yield losses such that the emergence, resurgence and rapid diffusion of MSV-A variants in this region presents a serious threat to maize production, farmer livelihoods and food security. To compliment current MSD management systems, a total of 689 MSV-A full genomes sampled over a 32 year period (1979-2011) from 20 countries across Africa and the adjacent Indian Ocean Islands, 286 of which were novel, were used to estimate: (i) the levels of genetic diversity using MEGA and the Sequence Demarcation Tool v1.2 (SDT); (ii) the times of occurrence and distribution of recombination using the recombination detection program (RDP v.4) and the genetic algorithm for recombination detection (GARD); (iii) selection pressure on codon positions using PARRIS and FUBAR methods implemented on the DATAMONKEY web server; (iv) reconstruct the history of spatio-temporal diffusion for MSV-A using the discrete phylogeographic models implemented in BEAST v1.8.1; (v) characterize source-sink dynamics and identify predictor variables driving MSV-A dispersal using the generalized linear models, again implemented in BEAST v1.8.1. Isolates used displayed low levels of genetic diversity (0.017 mean pairwise distance and ≥ 98% nucleotide sequence identities), and a well-structured geographical distribution where all of the 233 novel isolates clustered together with the -A1 strains. A total of 34 MSV inter-strain recombination events and 33 MSV-A intra-strain recombination events, 15 of which have not been reported in previous analyses (Owor et al., 2007, Varsani et al., 2008 and Monjane et al., 2011), were detected. The majority of intra-strain MSV-A recombination events detected were inferred to have vii occurred within the last six decades, the oldest and most conserved of these being events 19, 26 and 28 whereas the most recent events were 8, 16, 17, 21, 23, and 29. Intra-strain recombination events 20, 25 and 33, were widely distributed amongst East African MSV-A samples, whereas events 16, 21 and 23, occurred more frequently within West African MSV-A samples. Events 1, 4, 8, 10, 14, 17, 19, 22, 24, 25, 26, 28, and 29 were more widely distributed across East, West and Southern Africa and the adjacent Indian Ocean Islands. Whereas codon positions 12 and 19 within motif I in the coat protein transcript, and four out of the seven codon positions (147, 166, 195, 203, 242, 262, 267) in the Rep transcript (codons 195 and 203 in the Rb motif and codons 262 and 267 in site B of motif IV), evolved under strong positive selection pressure, those in the movement protein (MP) and RepA protein encoding genes evolved neutrally and under negative selection pressure respectively. Phylogeographic analyses revealed that MSV-A first emerged in Zimbabwe around 1938 (95% HPD 1904 - 1956), and its dispersal across Africa and the adjacent Indian Ocean Islands was achieved through approximately 34 migration events, 19 of which were statistically supported using Bayes factor (BF) tests. The higher than previously reported mean nucleotide substitution rate [9.922 × 10-4 (95% HPD 8.54 × 10-4 to 1.1317 × 10-3) substitutions per site per year)] for the full genome recombination-free MSV-A dataset H estimated was possibly a result of high nucleotide substitution rates being conserved among geminiviruses such as MSV as previously suggested. Persistence of MSV-A was highest in source locations that include Zimbabwe, followed by South Africa, Uganda, and Kenya. These locations were characterized by high average annual precipitation; moderately high average annual temperatures; high seasonal changes; high maize yield; high prevalence of undernourishment; low trade imports and exports; high GDP per capita; low vector control pesticide usage; high percentage forest land area; low percentage arable land; high population densities, and were in close proximity to sink locations. Dispersal of MSV-A was frequent between locations that received high average annual rainfall, had high percentage forest land area, occupied high latitudes and experienced similar climatic seasons, had high GDP per capita and had balanced maize import to export ratios, and were in close geographical proximity. December 2015 viii DECLARATION I declare that, The Phylogeography, Epidemiology, and Determinants of Maize streak virus dispersal across Africa and the adjacent Indian Ocean Islands, is my own work, that it has not been submitted for any degree or examination in any other university, and that all the sources I have used or quoted have been indicated and acknowledged by complete references. Eugene. T. Madzokere December 2015 Signed:........................ ix ACKNOWLEDGEMENTS I would like to acknowledge my supervisors Dr. Gordon William Harkins and Professor Darren Martin for their patience, exceptional guidance and support during the study period. I would also like to thank Dr. Arvind Varsani for sequencing and providing data on both novel and publicly available samples used in the study. The financial assistance of the National Research Foundation (NRF), the Poliomyelitis Research Foundation
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