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Dawit Kidanemariam Thesis Viruses of taro and other edible aroids in East Africa by Dawit Beyene KIDANEMARIAM Bachelor of Education (Biology) Master of Science (Botany) Centre for Tropical Crops and Biocommodities School of Earth, Environmental and Biological Sciences Science and Engineering Faculty A thesis submitted in fulfilment of the requirement for the degree of Doctor of Philosophy Queensland University of Technology Brisbane, Australia 2018 “The end of a journey is the beginning of another….” Abstract Edible aroids such as taro and tannia are important root crops in most parts of East Africa and cultivated mainly by small-holder farmers. Taro is the most preferred aroid in the region where it plays significant nutritional, economic and social roles. Viruses are among the most important constraints for the production of edible aroids worldwide. To date, no comprehensive study has been carried out to determine the status of viruses infecting taro and other edible aroids in East Africa. This PhD project, therefore, aimed to investigate the incidence, distribution and possible origin of viruses infecting taro and other edible aroids in the region. During 2014/15, a survey was carried out in the major growing areas in Ethiopia, Kenya, Tanzania and Uganda. A total of 25 districts were visited in the four countries and a total of 392 leaf samples were collected. Based on the availability of reliable diagnostic molecular tests, the samples were tested for the presence of badnaviruses, potyviruses and cucumber mosaic virus. Additional screening was also carried out for the presence of rhabdoviruses known to infect taro. When the 392 samples were tested by PCR using degenerate badnavirus primers, between 58-74 % of the samples from the four countries were positive. BLAST analysis of the core RT/RNase H-coding sequences revealed the presence of both taro bacilliform virus (TaBV) and taro bacilliform CH virus (TaBCHV) with TaBCHV identified in all four countries and TaBV identified in all countries except Ethiopia. Full-length genome sequences of representative TaBV and TaBCHV isolates infecting both taro and tannia from East Africa were generated by rolling circle amplification (RCA) and outward-facing PCR, respectively. The genome of TaBV isolates from East Africa ranged between 7,796-7,805 nucleotides and contained four open reading frames consistent with that of a previously reported isolate from Papua New Guinea. The genome of TaBCHV isolates from East Africa ranged from 7,389-7,654 nucleotides. Unlike previous reports of TaBCHV isolates from China and Hawaii which possessed six and five ORFs, respectively, the TaBCHV isolates from East Africa contained only four ORFs. No obvious symptoms were associated with TaBV and i TaBCHV infection in East Africa, with a number of asymptomatic plants also testing positive. Phylogenetic analysis showed that all East African TaBV isolates form a single subgroup together with a known TaBV isolate from New Caledonia. However, TaBCHV isolates formed several distinct subgroups in the phylogenetic tree. Due to quarantine restrictions, an Australian TaBV isolate was used as a model to generate a TaBV infectious clone. A terminally redundant cloned copy of the TaBV genome was generated and was shown to be infectious when inoculated into taro plants by agrobacterium-mediated inoculation. TaBV genomic DNA was amplified from inoculated plants using rolling circle amplification at 12 weeks post-inoculation confirms the presence of episomal TaBV DNA. At 20 weeks post-inoculation, some plants developed symptoms including downward-curling of the leaf margins, similar to that observed in some TaBV-infected taro plants in the field. This was the first report describing the development of an infectious clone of TaBV and may serve as an important tool to facilitate further investigation into the virus host range, symptoms and yield loss. The incidence and distribution in East Africa of four RNA viruses known to infect taro, namely cucumber mosaic virus (CMV), dasheen mosaic virus (DsMV), taro vein chlorosis virus (TaVCV) and colocasia bobone disease-associated virus (CBDaV), was also investigated by RT-PCR using degenerate and/or virus-specific primers. No samples tested positive for TaVCV or CBDaV. Further, CMV was only detected in three tannia plants with mosaic, mottling and vein chlorosis symptoms from Buikwe district in Uganda. Next generation sequencing of total RNA extracted from these samples confirmed the presence of CMV in all three plants, the nucleotide sequences of which showed 99.5-99.8 % identity. One isolate, designated CMV-Xa, was characterised further. Pairwise sequence comparison, BLAST search and phylogenetic analysis based on full-length RNA 1, 2 and 3 sequences showed that CMV-Xa belonged to subgroup-IB of CMV isolates. The genome organisation of RNA 1 and 3 of CMV-Xa was similar to previously reported CMV isolates. However, RNA 2 contained an additional, non-AUG initiated putative ORF, referred to as ORF 2c, in addition to ORF 2a and 2b. This was the first report of a complete genome sequence of a subgroup IB ii CMV isolate from sub-Saharan Africa and was also the first report of CMV infecting Xanthosoma sp. DsMV was detected in 40 samples, including 36 out of 171 from Ethiopia, 1 out of 94 from Uganda and 3 out of 41 from Tanzania, while no samples from Kenya tested positive. The complete genomes of nine DsMV isolates from East Africa were cloned and sequenced. Phylogenetic analyses based on the amino acid sequence of the CP-coding region revealed two distinct clades, which is consistent with previous reports. Interestingly, samples from Ethiopia were distributed across several subgroups in both clades, while samples from Uganda and Tanzania belonged to different clades. During preliminary RT-PCR assay development for potyviruses at QUT, an aroid (Alocasia sp.) showing a mosaic and feathery-mottle symptom typical of DsMV infection was identified growing near Brisbane. The plant tested positive for potyvirus infection by RT-PCR using degenerate primers and subsequent cloning and sequence analysis revealed the presence of the potyvirus, Zantedeschia mild mosaic virus (ZaMMV). The complete genome of ZaMMV from Australia (ZaMMV-AU) was obtained and was found to be closely related to a previously reported ZaMMV isolate from Taiwan (ZaMMV-TW). This was the first report of ZaMMV from Australia and from an Alocasia sp. To our knowledge, this is the first study describing the occurrence, distribution and genome organisation of viruses infecting aroids in East Africa and it will contribute to ongoing surveillance and to disease management activities throughout the region. Aroids are considered an ‘orphan-crop’ in East Africa and, as a result, are receiving less attention from national and regional research agencies. The findings from this study will hopefully raise awareness of the status of viral diseases of aroids in the region and may be the catalyst for attracting much needed funding for research and development activities in the future. iii Keywords Colocasia esculenta, CMV, DsMV, East Africa, Ethiopia, Infectious clone, Kenya, RCA, taro, tannia, TaBCHV, TaBV, Tanzania, Uganda, Xanthosoma sp., ZaMMV iv Publications Peer reviewed publications related to this PhD thesis 1. Kidanemariam, D.B., Abraham, A.D., Sukal, A.C., Holton, T.A., Dale, J.L., James, A.P. and Harding, R.M. (2016). Complete genome sequence of a novel zantedeschia mild mosaic virus isolate: the first report from Australia and from Alocasia sp. Archives of Virology 161:1079–1082. 2. Kidanemariam, D.B., Sukal, A.C., Abraham, A.D., Stomeo, F., Dale, J.L., James, A.P. and Harding, R.M. Identification and molecular characterisation of taro bacilliform virus and taro bacilliform CH virus from East Africa. Submitted to Plant Pathology https://doi.org/10.1111/ppa.12921. 3. Kidanemariam, D.B., Sukal, A.C., Crew, K., Jackson, G.V.H., Abraham, A.D., Stomeo, F., Dale, J.L., James, A.P. and Harding, R.M. (2018). Characterization of an Australian isolate of Taro bacilliform virus and development of an infectious clone. Archives of Virology 163:1677–1681. 4. Kidanemariam, D.B., Sukal, A.C., Abraham, A.D., Njuguna, J.N., Mware, B.O., Stomeo, F., Dale, J.L., James, A.P. and Harding, R.M. Characterisation of a subgroup IB isolate of Cucumber mosaic virus from Xanthosoma sp. in sub- Saharan Africa. Submitted to Virus Genes. 5. Kidanemariam, D.B., Sukal, A.C., Abraham, A.D., Njuguna, J.N., Stomeo, F., Dale, J.L., James, A.P. and Harding, R.M. Incidence and distribution of four RNA viruses infecting taro and tannia in East Africa and molecular characterisation of Dasheen mosaic virus isolates. Formatted for submission to Annals of Applied Biology. v Table of Contents Abstract .......................................................................................................................................... i Publications ....................................................................................................................................v Table of Contents .......................................................................................................................... vi List of Figures ............................................................................................................................... viii List of Tables ................................................................................................................................... x List of Abbreviations .....................................................................................................................
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