A new full-length circular DNA sequencing method for viral-sized genomes reveals that RNAi transgenic plants provoke a shift in geminivirus populations in the field.
[en] We present a new method, CIDER-Seq (Circular DNA Enrichment sequencing) for the unbiased enrichment and long-read sequencing of viral-sized circular DNA molecules. We used CIDER-Seq to produce single-read full-length virus genomes for the first time. CIDER-Seq combines PCR-free virus enrichment with Single Molecule Real Time sequencing and a new sequence de-concatenation algorithm. We apply our technique to produce >1200 full-length, highly accurate geminivirus genomes from RNAi-transgenic and control plants in a field trial in Kenya. Using CIDER-Seq we can demonstrate for the first time that the expression of antiviral double-stranded RNA (dsRNA) in transgenic plants causes a consistent shift in virus populations towards species sharing low homology to the transgene derived dsRNA. Our method and its application in an economically important crop plant opens new possibilities in periodic virus sequence surveillance and accurate profiling of diverse circular DNA elements.
Vanderschuren, Hervé ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions végétales et valorisation
Language :
English
Title :
A new full-length circular DNA sequencing method for viral-sized genomes reveals that RNAi transgenic plants provoke a shift in geminivirus populations in the field.
Simmonds, P., Adams, M.J., Benko, M., Breitbart, M., Brister, J.R., Carstens, E.B., Davison, A.J., Delwart, E., Gorbalenya, A.E., Harrach, B. et al. (2017) Consensus statement: Virus taxonomy in the age of metagenomics. Nat. Rev. Microbiol., 15, 161-168.
Massart, S., Candresse, T., Gil, J., Lacomme, C., Predajna, L., Ravnikar, M., Reynard, J.S., Rumbou, A., Saldarelli, P., Skoric, D. et al. (2017) A framework for the evaluation of biosecurity, commercial, regulatory, and scientifc impacts of plant viruses and viroids identifed by NGS technologies. Front. Microbiol., 8, 45.
Wu, Q., Ding, S., Zhang, Y. and Zhu, S. (2015) Identifcation of viruses and viroids by Next-Generation sequencing and homology-dependent and homology-independent algorithms. Annu. Rev. Phytopathol., 53, 425-444.
Mavromatis, K., Ivanova, N., Barry, K., Shapiro, H., Goltsman, E., McHardy, A.C., Rigoutsos, I., Salamov, A., Korzeniewski, F., Land, M. et al. (2007) Use of simulated data sets to evaluate the fdelity of metagenomic processing methods. Nat. Methods, 4, 495-500.
Mende, D.R., Waller, A.S., Sunagawa, S., Järvelin, A.I., Chan, M.M., Arumugam, M., Raes, J. and Bork, P. (2012) Assessment of metagenomic assembly using simulated next generation sequencing data. PLoS One, 7, e31386.
Pignatelli, M. and Moya, A. (2011) Evaluating the fdelity of De Novo short read metagenomic assembly using simulated data. PLoS One, 6, e19984.
Dean, F., Nelson, J., Giesler, T. and Lasken, R. (2001) Rapid amplifcation of plasmid and phage DNA using Phi29 polymerase and a multiply-pimed rolling circle amplifcation. Genome Res., 11, 1095-1099.
Sipos, R., Szekely, A., Revesz, S. and Marialigeti, K. (2010) Addressing PCR biases in environmental microbiology studies. In: Cummings, SP (ed). Methods in Molecular Biology: Bioremediation. Humana Press, NY, Vol. 599, pp. 37-58.
Lasken, R.S. and Stockwell, T.B. (2007) Mechanism of chimera formation during the Multiple Displacement Amplifcation reaction. BMC Biotechnol., 7, 19.
Inoue-Nagata, A.K., Albuquerque, L.C., Rocha, W.B. and Nagata, T. (2004) A simple method for cloning the complete begomovirus genome using the bacteriophage Phi29 DNA polymerase. J. Virol. Methods, 116, 209-211.
Zhang, K., Martiny, A.C., Reppas, N.B., Barry, K.W., Malek, J., Chisholm, S.W. and Church, G.M. (2006) Sequencing genomes from single cells by polymerase cloning. Nat. Biotechnol., 24, 680-686.
Acevedo, A. and Andino, R. (2014) Library preparation for highly accurate population sequencing of RNA viruses. Nat. Protoc., 9, 1760-1769.
Acevedo, A., Brodsky, L. and Andino, R. (2014) Mutational and ftness landscapes of an RNA virus revealed through population sequencing. Nature, 505, 686-690.
Lou, D.I., Hussmann, J.A., Mcbee, R.M., Acevedo, A., Andino, R. and Press, W.H. (2013) High-throughput DNA sequencing errors are reduced by orders of magnitude using circle sequencing. Proc. Natl. Acad. Sci. U.S.A., 110, 19872-19877.
Teng, J.L.L., Yeung, M.L., Chan, E., Jia, L., Lin, C.H., Huang, Y., Tse, H., Wong, S.S.Y., Sham, P.C., Lau, S.K.P. et al. (2017) PacBio but not illumina technology can achieve fast, accurate and complete closure of the high GC, complex Burkholderia pseudomallei two-chromosome genome. Front. Microbiol., 8, 1-15.
Ardui, S., Ameur, A., Vermeesch, J.R. and Hestand, M.S. (2018) Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res., 46, 2159-2168.
Rey, C. and Vanderschuren, H. (2017) Cassava mosaic and brown streak diseases: current perspectives and beyond. Annu. Rev. Virol., 4, 429-452.
Pooggin, M.M. (2017) RNAi-mediated resistance to viruses: a critical assessment of methodologies. Curr. Opin. Virol., 26, 28-35.
Aragão, F.J.L. and Faria, J.C. (2009) First transgenic geminivirus-resistant plant in the feld. Nat. Biotechnol., 27, 1086-1088.
Fuentes, A., Carlos, N., Ruiz, Y., Callard, D., Sánchez, Y., Ochagav´ia, M., Seguin, J., Malpica-López, N., Hohn, T., Lecca, M. et al. (2016) Field trial and molecular characterization of RNAi-transgenic tomato plants that exhibit resistance to tomato yellow leaf curl geminivirus. Mol. Plant-Microbe Interact., 29, 197-209.
Ogbe, F.O., Atiri, G.I., Dixon, A.G.O. and Thottappilly, G. (2003) Symptom severity of cassava mosaic disease in relation to concentration of African cassava mosaic virus in different cassava genotypes. Plant Pathol., 52, 84-91.
Chang, S., Puryear, J. and Cairney, J. (1993) A simple and effcient method for isolating RNA from pine trees. Plant Mol. Biol. Report., 11, 113-116.
Pacific Biosciences Inc (2015) Pacific Biosciences Glossary of Terms. https://www.pacb.com/wp-content/uploads/2015/09/Pacific-Biosciences-Glossary-of-Terms.pdf.
Edgar, R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
Laehnemann, D., Borkhardt, A. and Mchardy, A.C. (2016) Denoising DNA deep sequencing data-high-throughput sequencing errors and their correction. Brief. Bioinform., 17, 154-179.
International Committee on Taxonomy of Viruses (2016) ICTV Master Species Listv1.3. https://talk.ictvonline.org/fles/master-species-lists/.
Vanderschuren, H., Alder, A., Zhang, P. and Gruissem, W. (2009) Dose-dependent RNAi-mediated geminivirus resistance in the tropical root crop cassava. Plant Mol. Biol., 70, 265-272
Jiao, X., Zheng, X., Ma, L., Kutty, G., Gogineni, E., Sun, Q., Sherman, B.T., Hu, X., Jones, K., Raley, C. et al. (2013) A benchmark study on error assessment and quality control of CCS reads derived from the PacBio RS. J. Data Min. Genomics Proteomics, 424, 1-9.
Du, N. and Sun, Y. (2016) Improve homology search sensitivity of PacBio data by correcting frameshifts. Bioinformatics, 32, i529-i537.
Eren, K. and Murrell, B. (2018) RIFRAF: a frame-resolving consensus algorithm. Bioinformatics, bty426.
Ssemadaali, M.A., Effertz, K., Singh, P., Kolyvushko, O. and Ramamoorthy, S. (2016) Identifcation of heterologous Torque Teno Viruses in humans and swine. Sci. Rep., 6, 26655.
