Testing for host adaptive evolution using the maize streak virus model

Doctoral Thesis


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Maize streak virus (MSV; Genus: Mastrevirus; Family: Geminiviridae) causes maize streak disease (MSD); a major biotic threat to maize farming especially in sub-Saharan Africa, and it neighbouring Indian and Atlantic Ocean Islands, where its insect vectors in the genus Cicadulina thrive. Of the eleven known MSV strains (called A through K), only MSV-A is economically significant as it is the only one that causes severe disease in maize. MSV is a single stranded DNA (ssDNA) virus which, like RNA viruses, has high mutation and recombination rates. Given that these processes can sometimes promote viral diversity and result in the rapid evolution of new, fitter MSV variants, continuous genomic surveillance of MSV is therefore important. Based on analyses of full genome sequences, MSV-A has been classified into five subtypes (-A1, -A2, -A3, -A4, and -A6) and more than 20 recombinant lineages. Here, I showed using laboratory-based experiments that maize infecting mastreviruses such as Maize streak Reunion virus (MSRV) and MSV-C which have been found maize plants displaying severe streak symptoms do not in fact cause severe streak symptoms in maize when used to infect maize on their own. Although a mixed infection involving MSRV and MSV-B resulted in slight changes in symptom phenotypes it is unlikely that MSRV and MSV-C are responsible for emerging maize diseases. I carried out model-based phylogenetic and phylogeographic analyses of MSV-A movement dynamics in and out of Madagascar, Ethiopia and Rwanda using newly determined MSV-A genome sequences (Madagascar: n = 56; Ethiopia: n = 84) together with other sequences from GenBank. I showed that most movements of MSV-A into Madagascar have been from East Africa between the early 1990s and 2000s. My inferences show that MSV-A1 variants currently found in Ethiopia likely arrived there from Uganda or Kenya between 1985 and 1988. Similarly the MSV-A1 variants found in Rwanda likely also moved there from Ethiopia, Kenya or Uganda between 2007 and 2011. The time periods over which inferred movements of MSV-A1 into Madagascar, Rwanda and Ethiopia occurred all correspond with the period during which trade between these and other East African nations was being liberalized. Although these temporally-scaled phylogeographic analyses indicated that human activities are likely responsible for some of the long-range movements of MSV-A1 variants (such as movements from East Africa to Madagascar), leafhopper-mediated dissemination of these variants also likely played a major role in long and short distance movements of these variants within both Madagascar and between East African countries. Over 90 years of evolution that yielded MSV-A-ZW-MatA_1994 in the MSV-A1 lineage, produced symptoms that have varied in a less concerted ways, or largely remained unchanged. Major harms (intensity of chlorosis, leaf deformation and stunting) have decreased while the amount of colonized cells (chlorotic areas) that determine onward transmission have increased. These data suggest MSV-A has evolved to optimize the number of cells it infects for effective onward transmission, while reducing excessive harm to its hosts. Altogether, these results suggest (1) synergism potentially plays a role in some instances of severe streak disease and (2) the movement of MSV-A1 within the East African region and Madagascar emphasizes the importance of this MSV-A subtype as a major ongoing threat to maize production within these regions; and (3) over the last 90 years, the MSV-A1 subtype has evolved to produce greater chlorotic areas on the leaves of infected maize plants while at the same time either not increasing or reducing the degrees of chloroplast destruction, stunting and deformation caused by infections: characteristics that may have enhanced the transmissibility of this variant and therefore played an important role in the present rise to dominance of this subtype throughout East Africa and Madagascar.