Maize streak virus (MSV; family Geminiviridae, genus Mastrevirus), the causal agent of maize streak disease, ranks amongst the most serious biological threats to food security in subSaharan Africa. Although five distinct MSV strains have been currently described, only one of these – MSV-A – causes severe disease in maize. Due primarily to their not being an obvious threat to agriculture, very little is known about the ‘grass-adapted’ MSV strains, MSV-B, -C, -D and -E. Since comparing the genetic diversities, geographical distributions and natural host ranges of MSV-A with the other MSV strains could provide valuable information on the epidemiology, evolution and emergence of MSV-A, we carried out a phylogeographical analysis of MSVs found in uncultivated indigenous African grasses. Amongst the 83 new MSV genomes presented here, we report the discovery of six new MSV strains (MSV-F to -K). The non-random recombination breakpoint distributions detectable with these and other available mastrevirus sequences partially mirror those seen in begomoviruses, implying that the forces shaping these breakpoint patterns have been largely conserved since the earliest geminivirus ancestors. We present evidence that the ancestor of all MSV-A variants was the recombinant progeny of ancestral MSV-B and MSV-G/-F variants. While it remains unknown whether recombination influenced the emergence of MSV-A in maize, our discovery that MSV-A variants may both move between and become established in different regions of Africa with greater ease, and infect more grass species than other MSV strains, goes some way towards explaining why MSV-A is such a successful maize pathogen.
Maize streak virus strain A (MSV-A), the causal agent of maize streak disease, is today one of the most serious biotic threats to African food security. Determining where MSV-A originated and how it spread transcontinentally could yield valuable insights into its historical emergence as a crop pathogen. Similarly, determining where the major extant MSV-A lineages arose could identify geographical hot spots of MSV evolution. Here, we use model-based phylogeographic analyses of 353 fully sequenced MSV-A isolates to reconstruct a plausible history of MSV-A movements over the past 150 years. We show that since the probable emergence of MSV-A in southern Africa around 1863, the virus spread transcontinentally at an average rate of 32.5 km/year (95% highest probability density interval, 15.6 to 51.6 km/year). Using distinctive patterns of nucleotide variation caused by 20 unique intra-MSV-A recombination events, we tentatively classified the MSV-A isolates into 24 easily discernible lineages. Despite many of these lineages displaying distinct geographical distributions, it is apparent that almost all have emerged within the past 4 decades from either southern or east-central Africa. Collectively, our results suggest that regular analysis of MSV-A genomes within these diversification hot spots could be used to monitor the emergence of future MSV-A lineages that could affect maize cultivation in Africa.
The chemical ecology of the leafhopper, Cicadulina storeyi China (Homoptera: Cicadellidae), an important vector of Maize Streak Virus (MSV), was studied with a view to developing novel leafhopper control strategies in sub-Saharan Africa. Choice tests using a Y-tube olfactometer revealed that odors from uninfested maize seedlings (Zea mays cv. Delprim) were significantly more attractive to C. storeyi than odors from C. storeyi-infested seedlings. Headspace samples of volatile organic compounds (VOCs) collected from 10 to 12 day-old uninfested seedlings were more attractive than those collected from infested seedlings. While VOCs collected from uninfested maize seedlings were attractive, VOCs collected from C. storeyi-infested seedlings were significantly repellent. Analysis of the collected VOCs by gas chromatography (GC) and coupled GC-mass spectrometry (GC-MS) led to the identification of myrcene, linalool, (E)-2-decen-1-ol, and decanal from uninfested seedlings, and (Z)-3-hexenyl acetate, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), methyl salicylate, benzyl acetate, indole, geranyl acetate, (E)-caryophyllene, α-bergamotene, (E)-β-farnesene, β-sesquiphellandrene, and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT) from infested seedlings. Of these, methyl salicylate, (E)-caryophyllene, (E)-β-farnesene, and TMTT were identified previously as volatile semiochemicals involved in plant defense against other sucking insect pests. When tested individually for behavioral activity, all compounds were repellent for C. storeyi. Moreover, when these induced VOCs were added to the blend of VOCs from uninfested maize seedlings, a shift from attraction to repellency was observed. Addition of methyl salicylate, (E)-β-farnesene, or TMTT resulted in a choice for the solvent control (i.e., repulsion), whereas addition of (E)-caryophyllene resulted in no reduction in host VOC attractiveness. These results show that VOCs induced in maize have the potential to be exploited in the control of viruliferous leafhoppers in sub-Saharan Africa.
cis-Jasmone (CJ) is a natural plant product that activates defence against herbivores in model and crop plants. In this study, we investigated whether CJ could prime defence in maize, Zea mays, against the leafhopper, Cicadulina storeyi, responsible for the transmission of maize streak virus (MSV). Priming occurs when a pre-treatment, in this case CJ, increases the potency and speed of a defence response upon subsequent attack on the plant. Here, we tested insect responses to plant volatile organic compounds (VOCs) using a Y-tube olfactometer bioassay. Our initial experiments showed that, in this system, there was no significant response of the herbivore to CJ itself and no difference in response to VOCs collected from unexposed plants compared to CJ exposed plants, both without insects. VOCs were then collected from C. storeyi-infested maize seedlings with and without CJ pre-treatment. The bioassay revealed a significant preference by this pest for VOCs from infested seedlings without the CJ pre-treatment. A timed series of VOC collections and bioassays showed that the effect was strongest in the first 22 h of insect infestation, i.e. before the insects had themselves induced a change in VOC emission. Chemical analysis showed that treatment of maize seedlings with CJ, followed by exposure to C. storeyi, led to a significant increase in emission of the defensive sesquiterpenes (E)-(1R,9S)-caryophyllene, (E)-α-bergamotene, (E)-β-farnesene and (E)-4,8-dimethyl-1,3,7-nonatriene, known to act as herbivore repellents. The chemical analysis explains the behavioural effects observed in the olfactometer, as the CJ treatment caused plants to emit a blend of VOCs comprising more of the repellent components in the first 22 h of insect infestation than control plants. The speed and potency of VOC emission was increased by the CJ pre-treatment. This is the first indication that CJ can prime plants for enhanced production of defensive VOCs antagonist towards herbivores.
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