Molecular and Cytogenetic Analyses of the Integration Events of Badnavirus Endogenous Pararetrovirus Sequences in Yam (Dioscorea species)
Abstract
Yam (Dioscorea spp.) is an important staple food crop in Sub-Saharan Africa and is vegetatively-propagated. This had led to the accumulation of viruses and their integrated sequences leading to decreased yam production and hindering international movement of selected germplasm. It is unclear if badna virus sequences are integrated in the genomes of West African yam breeding lines. This study was aimed to determine that. DNAs were extracted from leaf samples of Nigerian yam breed using an optimised CTAB-extraction method and then screened by PCR using degenerate badnavirus primers targeting a 579 bp RT-RNaseH region and Rolling cycle amplification. Diversity of the RT-RNaseH region sequence was determined using Denaturing Gradient Gel Electrophoresis (DGGE). All the yam samples tested badnavirus PCR-positive (100%). Probes for the Southern Band Fluorescent in situ hybridisation (FISH) results were designed using individual DGGE partial RT-RNaseH band sequences (NGb4_Dr, NGb5_Dr and NGb6_Dr), badnavirus complete genome and partial genome cloned. The FISH result was inconclusive to suggests integration of badnavirus sequences in genomes of D. rotundata breeding lines. The consequences of the integrated and episomal badnavirus sequences for yam improvement programmes in West Africa are discussed
Downloads
References
Aighewi B .A., Maroya, N. G. and Asiedu, R. (2014). Seed yam production from minisetts: A training manual. YIIFSWA International Institute of Tropical Agriculture (IITA).
Alangar, I. B., Thomas, H. and Ramasamy, S. (2016). Badnaviruses: The Current Global Scenario. Viruses 8(6):177; doi:10.3390/v8060177
Bömer, M., Rathnayake, A. I., Visendi, P., Silva, G. and Seal, S. E. (2017). Complete genome sequence of a new member of the genus Badnavirus, Dioscorea bacilliform RT virus 3, reveals the first evidence of recombination in yam badnaviruses. Archive of Virology 163(2):533–538.
Bömer, M., Turaki, A. A., Silva, G., Kumar, P. L. and Seal, S. E. (2016). A sequence-independent strategy for amplification and characterisation of episomal badnavirus sequences reveals three previously uncharacterised yam badnaviruses. Viruses 8(7):188-209.
Bousalem, M., Durand, O., Scarcelli, N., Lebas, B.S.M., Kenyon, L., Marchand, J.L., Lefort, F. and Seal, E.S. (2009). Dilemmas caused by endogenous pararetrovirus regarding the taxonomy and diagnosis of yam (Dioscorea spp.) badnaviruses: analyses to support safe movement. Archives of Virology 154 (2):297-314.
Briddon, R. W., Phillips, S., Brunt A. and Hull R. (1999). Analysis of the sequence of Dioscorea alata bacilliform virus; comparison to other members of the badnavirus group. Virus Genes 183: 277-283.
Campbell, A (2003). The future of bacteriophage biology. Nature Review Genetics 4:471-477.
Chabannes, M. and Iskra-Caruana M. L. (2013). Endogenous pararetroviruses-a reservoir of virus infection in plants. Current Opinion Virology 3: 615-620.
Chabannes, M., Baurens, F. C., Duroy, P. O., Bocs, S., Vernerey, M. S., Rodier-Goud, M., Barbe, V., Gayral, P. and Iskra-Caruana, M. L. (2013) Three infectious viral species lying in wait in the banana genome. Journal of Virology 87: 8624-8637.
Dallot S., Acuña P., Rivera C., Ramírez P., Côte F., Lockhart, B. E. L. and Iskra-Caruana, M. L. (2001). Evidence that the proliferation stage of micropropagation procedure is determinant in the expression of Banana streak virus integrated in to genome of the FHIA21 hybrid (Musa AAAB). Archives of Virology 146: 2179-2190.
Eni, A. O., Hughes, J. d’A., Asiedu, R. and Rey M. E. C. (2008). Sequence diversity among badnavirus isolates infecting yam (Dioscorea spp.) in Ghana, Togo, Benin and Nigeria. Archives of Virology 153: 2263-2272.
Fang, G., Hammar, S. and Grumet, R. (1992). A quick and inexpensive method for removing polysaccharides from plant genomic DNA. Biotechniques 13:52.
Feschotte, C. and Gilbert, C. (2012). Endogenous viruses: insights into viral evolution and impact on host biology. Nature Review Genetics 13:283-296.
Gayral, P., Noa-Carrazana, J. C., Lescot, M., Lheureux, F., Lockhart, B. E. L., Matsumoto, T., Piffanelli, P. and Iskra-Caruana, M. L. (2008). A single Banana streak virus integration event in the banana genome as the origin of infectious endogenous pararetrovirus. Journal of Virology 82: 6697-6710.
Geering, A. D. W., Olszewski, N. E., Dahal, G., Thomas, J. E. and Lockhart, B. E. L. (2001). Analysis of the distribution and structure of integrated Banana streak virus DNA in a range of Musa cultivars. Molecular Plant Pathology 2: 207-213.
Geering, A. D. W., Olszewski, N. E., Harper, G., Lockhart, B. E. L., Hull, R. and Thomas, J. E. (2005a). Banana contains a diverse array of endogenous badnaviruses. Journal of General Virology 86:511-520.
Geering A. D. W., Pooggin, M. M., Olszewski, N. E., Lockhart, B. E. L. and Thomas, J. E. (2005b). Characterisation of Banana streak Mysore virus and evidence that its DNA is integrated in the B
genome of the cultivated Musa sp. Archives of Virology 150:787-796.
Geering, A. D. W., Tanya, S. and Teycheney, P. Y. (2010). The classification and nomenclature of endogenous viruses of the family Caulimoviridae. Archives of Virology 155:123-131.
Gerlach, W. L. and Bedbrook, J. R. (1979). Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Research 7:1869-1885.
Gerlach, W. L. and Dyer, T. A. (1980). Sequence organization of the repeating units in the nucleus of wheat which contain 5S rRNA genes. Nucleic Acids Research 8:4851-4865.
Ghaffari, S., Hasnaoui, N. and Ferchichi, A. (2011). Rapid, high quality DNA isolation from Tunisian Grapevine (Vitis vinifera L.) cultivars and optimization of the RAPD Marker Technique. Romanian Biotechnological Letters 16:2881-2890.
Hansen, C. N., Harper, G. and Heslop-Harrison, J. S. (2005). Characterisation of pararetrovirus-like sequences in the genome of potato (Solanum tuberosum). Cytogenetic and Genome Research 110:559-565.
Harper, G., Hull, R., Lockhart, B. E. L. and Olszewski, N. E. (2002). Viral sequences integrated into plant genomes. Annual Review of Phytopathology 140:119-136.
Harper, G., Osuji, O. J., Heslop-Harrison, J. S. and Hull, R. (1999). Integration of banana streak badnavirus into the Musa genome: molecular and cytogenetic evidence. Virology 255:207-213.
Heslop-Harrison, J. S. P, Brandes, A., Taketa, S., Schmidt, T., Vershinin, A. V., Alkhimova, E. G., Kamm, A., Doudrick, R. L., Schwarzacher, T., Katsiotis, A., Kubis, S., Kumar, A., Pearce, S. R., Flavell, A. J., Harrison, G. E. and Capy, P. (1997). The chromosomal distributions of Ty1-copia group retrotransposable elements in higher plants and their implications for genome evolution. Genetica 100:197-204.
Hohn, T., Richert-Pӧggeler, K. R., Harper, G., Schwarzacher, T., Teo, C. H., Techeney, P. Y., Iskra-Caruana, M. L. and Hull, R. (2008). Evolution of integrated plant viruses. In: M. Roossinck (ed.), Plant virus evolution. Springer, Heidelberg, Germany, pp. 58–81.
Iskra-Caruana, M. L., Baurens, F. C., Gayral, P. and Chabannes, M. (2010). A four-partner plant-virus interaction: enemies can also come from within. The American Phytopathological Society 23:1394-1402.
Iskra-Caruana, M. L., Chabannes, M. and Duroy, P. O. (2014b). A possible scenario for the evolution of Banana streak virus in banana Virus Research http://dx.doi.org/10.1016/j.virusres.2014.01.005.
Iskra-Caruana, M. L., Duroy, P. O., Chabannes, M. and Muller, E. (2014a). The common evolutionary history of badnaviruses and banana. Infectious Genetic Evolution 21:83-89.
Jakowitsch J., Mette, M. F., Van der Winden, G., Matzke, M. A. and Matzke, A. J. M. (1999). Integrated pararetroviral sequences define a unique class of dispersed repetitive DNA in plants. Evolution 96:13241-13246.
Katzourakis, A., Vini Pereira, V. and Tristem, M. (2007). Effects of recombination rate on human endogenous retrovirus fixation and persistence. Journal of Virology 81: 10712-10717.
Kenyon, L., Lebas, B. S. M. and Seal, S. E. (2008). Yams (Dioscorea spp.) from the South Pacific Islands contain many novel badnaviruses: implications for international movement of yam germplasm. Archives of Virology 153:877-889.
Kunii, M., Kanda, M., Nagano, H., Uyeda, I., Kishima, Y. and Sano, Y. (2004). Reconstruction of putative DNA virus from endogenous Rice tungro bacilliform virus-like sequences in the rice genome: implications for integration and evolution. BMC Genomics 5:80.
Le Provost, G., Iskra-Caruana, M. L., Acina, I. and Teycheney, P. Y. (2006). Improved detection of episomal banana streak viruses by multiplex immunocapture PCR. Journal of Virological Methods 137:7-13.
Lefeuvre, P., Harkins, G. W., Lett, J. M., Briddon, R. W., Chase, M. W., Benoit, M. and Darren, P. M. (2011). Evolutionary time-scale of the Begomoviruses: evidence from integrated sequences in the Nicotiana genome. PLoS ONE, 6:e19193.
Lheureux F., Carreel, F., Jenny, C., Lockhart, B. E. L. and Iskra-Caruana, M. L. (2003). Identification of genetic makers linked to banana streak disease expression in inter-specific Musa hybrids. Theoretical Applied Genetics 106: 594-598.
Lockhart. B. E. L., Menke, J., Dahal, G. and Olszewski, N. E. (2000). Characterisation and genome analysis of Tobacco vein clearing virus: a plant pararetrovirus that is transmitted vertically and related to sequences integrated in the host genome. Journal of General Virology 81:1579-1585.
Mette, M. F., Kanno, T., Aufsatz, W., Jakowitsch, J., Van der Winden, J., Matzke, M. A. and Matzke, A. J. M. (2002). Endogenous viral sequences and their potential contribution to heritable virus resistance in plants. The EMBO Journal 21:461-469.
Tamiru, M., Satoshi, N., Hiroki, T., Benjamen, W., Hiroki, Y., Motoki, S., Kentaro, Y., Aiko, U., Kaori, O., Akira, A., Naoya, U., Hideo, M., Pachakkil, B., Shinsuke, Y., Ryo, M., Satoru, M., Gezahegn, G., Antonio, L. M., Melaku, G., Ranjana, B., Michael, A., Lava, K. P., Ismail, R., Mai, T., Toru, T., Wilfried, H., Manuel, C., Sophien, K., Günter, K., Hiroko, T., Robert, A. and Ryohei, T. (2017). Genome sequencing of the staple food crop white Guinea yam enables the development of a molecular marker for sex determination. BMC Biology 15:86 DOI 10.1186/s12915-017-0419-x
Ndowora, T. C., Dahal, G., LaFleur, D., Harper, G., Hull, R., Olszewski, N. E. and Lockhart, B. E. L. (1999). Evidence that badnavirus infection in Musa can originate from integrated pararetroviral sequences. Virology 225:214-220.
Pahalawatta, V., Druffel, K. and Pappu, H. (2008). A new and distinct species in the genus Caulimovirus exists as an endogenous plant pararetroviral sequence in its host, Dahlia variabilis. Virology 376:253-257.
Phillips, S., Briddon, R. W., Brunt, A. A. and Hull, R. (1999). The partial characterisation of a badnavirus infecting the greater Asiatic or water yam (Dioscorea alata). Journal of Phytopathology 147:265-26. Pistello, M. and Antonelli, G. (2016). Integration of the viral genome into the host cell genome: a double-edged sword. Clinical Microbiology and Infection 22(4):296-298.
Richert-Pöggeler, K. R., Noreen, F., Schwarzacher, T., Harper, G. and Hohn, T. (2003) Induction of infectious petunia vein clearing (pararetro) virus from endogenous provirus in petunia. The EMBO Journal 22:4836-4845.
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular cloning: a laboratory manual, 2rd edition Cold Spring Harbor Laboratory Press, Cold Spring Harbour, New York, USA. pp. 931-957.
Seal, S. E., Turaki, A., Muller, E., Kumar, P. L., Kenyon, L., Filloux, D., Galzi, S., Lopez-Montes, A. and Iskra-Caruana, M. L. (2014). The prevalence of badnaviruses in West African yams (Dioscorea cayenensis-rotundata) and evidence of endogenous pararetrovirus sequences in their genomes. Virus Research 186:144-154.
Seal, S. E. and Muller, E. (2007). Molecular analysis of a full-length sequence of a new yam badnavirus from Dioscorea sansibarensis. Archives of Virology 7:1-7.
Sharma, A. D., Gill, P. K. and Singh, P. (2002). DNA isolation from dry and fresh samples of polysaccharide-rich plants. Plant Molecular Biology Reporter 20:415-419.
Staginnus, C. and Richert-Pöggeler, K. R. (2006). Endogenous pararetroviruses: two-faced travellers in the plant genome. Trends in Plant Science 11:485-491.
Staginnus, C., Gregor, W., Mette, M. F., Teo, C. H., Borroto-fernàndez, E. G., Machado, M. L., Matzke, M. and Schwarzacher, T. (2007). Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species. BMC Plant Biology 7:24-32.
Staginnus, C., Iskra-Caruana, M. L., Lockhart, B. E. L., Hohn, T. and Richert-Poggeler, K. R. (2009). Suggestions for nomenclature of endogenous pararetroviral (EPRV) sequences in plants. Archives of Virology 154:1189-1193.
Tamiru, M., Natsume, S., Takagi, H., Babil, P., Yamanaka, S., Lopez-Montes, A., Gedil, M., Bhattacharjee, R., Takagi, H., Asiedu, R. and Terauchi, R. (2013). Whole genome sequencing of Guinea yam (Dioscorea rotundata). In: Book of abstracts for Yams-2013, First global conference on Yam, 3–6 October 2013, Accra, Ghana, pp. 20.
Turaki,, A. A., Bömer, M., Silva, G., Kumar, P. L. and Seal, S. E. (2017a). PCR-DGGE analysis: Unravelling complex mixtures of Badnavirus sequences present in yam germplasm. Viruses 9(7);181; doi:10.3390/v9070181
Turaki A. A., Ahmad, B., Magaji, U. F., Abdulrazak U. K., Yusuf, B. A. and Hamza, A. B. (2017b). Optimised cetyltrimethylammonium bromide (CTAB) DNA extraction method of plant leaf with high polysaccharide and polyphenolic compounds for downstream reliable molecular analyses African Journal of Biotechnology 16(24):1354-1365.
Umber, M., Filloux, D., Muller, E., Laboureau, N., Galzi, S., Roumagnac, P., Iskra-Caruana, M. L., Pavis, C., Teycheney, P. Y. and Seal, S. E. (2014). The genome of African yam (Dioscorea cayenensis-rotundata complex) hosts endogenous sequences from four distinct badnavirus species. Molecular Plant Pathology 1-12 DOI: 10.1111/mpp.12137
Additional Files
Published
Issue
Section
Categories
License
Copyright (c) 2023 Turaki, A. A., Abdulrazak, U. K.
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
