Abstract
Maize Iranian mosaic virus (MIMV) is a distinct member of the genus Nucleorhabdovirus. In this study, expression of all MIMV genes in maize for four weeks after inoculation and in inoculative planthoppers was examined using a quantitative RT-PCR (RT-qPCR) assay. Accumulation of MIMV P, gene 3, M, G and L transcripts relative to N transcripts was measured and normalized to 18S rRNA in maize plants and to the ribosomal protein S13 gene (RPS13) in planthoppers using the comparative CT method. In plants, higher levels of MIMV N transcripts were found relative to other transcripts, while MIMV L transcripts were at the lowest levels. The highest accumulation of MIMV transcripts was found at 14 days postinoculation (dpi). At 21 dpi, we found the lowest transcript levels for all genes, which increased again at 28 dpi, although in lower amounts than at 14 dpi. In Laodelphax striatellus, MIMV M, G and L transcripts accumulated at lower levels than other transcripts. The gene 3 transcript level was high in both plants and planthoppers. Our results showed that transcript accumulation for the MIMV genes was similar in both hosts and followed the pattern of sequential transcriptional attenuation from the 3ˊ to the 5ˊ end of the genome, similar to vertebrate rhabdoviruses. These results indicate that the regulation of virus gene transcription for this plant-infecting rhabdovirus is similar to that of some vertebrate-infecting rhabdoviruses.
Similar content being viewed by others
References
Abernathy E, Glaunsinger B (2015) Emerging roles for RNA degradation in viral replication and antiviral defense. Virology 479–480:600–608
Abraham G, Banerjee AK (1976) Sequential transcription of the genes of vesicular stomatitis virus. Proc Natl Acad Sci USA 73:1504–1508
Albertini AAV (2011) Rabies virus transcription and replication. Adv Virus Res 79:1–22
Assenberg R, Delmas O, Morin B, Graham SC, De Lamballerie X, Laubert C, Coutard B, Grimes JM, Neyts J, Owens RJ, Brandt BW, Gorbalenya A, Tucker P, Stuart DI, Canard B, Bourhy H (2010) Genomics and structure/function studies of Rhabdoviridae proteins involved in replication and transcription. Antivir Res 87:149–161
Ball LA, White CN (1976) Order of transcription of genes of vesicular stomatitis virus. Proc Natl Acad Sci USA 73:442–446
Banerjee AK (1987) Transcription and replication of rhabdoviruses. Microbiol Rev 51:66–87
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622
Channuntapipat C, Sedgley M, Collins G (2001) Sequences of the cDNAs and genomic DNAs encoding the S1, S7, S8, and Sf alleles from almond, Prunus dulcis. Theor Appl Genet 103:1115–1122
Cisneros Delgadillo FM (2013) Maize fine streak virus (MFSV) Gene Expression and Protein Interaction. Dissertation, The Ohio State University.
Collins PL, Hightower LE, Ball LA (1980) Transcriptional map for Newcastle disease virus. J Virol 35:682–693
Dickens LE, Collins PL, Wertz GW (1984) Transcriptional mapping of human respiratory syncytial virus. J Virol 52:364–369
Dietzgen RG, Calisher CH, Kurath G, Kuzmin IV, Rodriguez LL, Stone DM, Tesh RB, Tordo N, Walker PJ, Wetzel T, Whitfield AE (2011) Family Rhabdoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus Taxonomy—Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Oxford, pp 686–714
Flamand A, Delagneau JF (1978) Transcriptional mapping of rabies virus in vivo. J Virol 28:518–523
Glazier K, Raghow R, Kingsbury DW (1977) Regulation of Sendai virus transcription: evidence for a single promoter in vivo. J Virol 21:863–871
Guo H, Song X, Xie C, Huo Y, Zhang F, Chen X, Geng Y, Fang R (2013) Rice yellow stunt rhabdovirus protein 6 suppresses systemic RNA silencing by blocking RDR6-mediated secondary siRNA synthesis. Mol Plant Microbe Interact 26:927–936
Holmes EC, Woelk CH, Kassis R, Bourhy H (2002) Genetic constraints and the adaptive evolution of rabies virus in nature. Virology 292:247–257
Huang YW, Geng YF, Ying XB, Chen XY, Fang RX (2005) Identification of a movement protein of rice yellow stunt Rhabdovirus. J Virol 79:2108–2114
Ivanov I, Yabukarski F, Ruigrok RW, Jamin M (2011) Structural insights into the rhabdovirus transcription/replication complex. Virus Res 162:126–137
Iverson LE, Rose JK (1981) Localized attenuation and discontinuous synthesis during vesicular stomatitis-virus transcription. Cell 23:477–484
Izadpanah K (1989) Purification and serology of the Iranian maize mosaic rhabdovirus. J Phytopathol 126:43–50
Izadpanah K, Ahmadi A, Parvin S, Jafari SA (1983) Transmission, particle size and additional hosts of the rhabdovirus causing maize mosaic in Shiraz, Iran. Phytopathol Z 107:283–288
Izadpanah K, Parvin S (1979) Occurrence of maize mosaic virus in corn fields around Shiraz. Iran. J Plant Pathol 15:78–82
Jackson AO, Dietzgen RG, Goodin MM, Bragg JN, Deng M (2005) Biology of plant rhabdoviruses. Annu Rev Phytopathol 43:623–660
Lacerda AL, Fonseca LN, Blawid R, Boiteux LS, Ribeiro SG, Brasileiro AC (2015) Reference gene selection for qPCR analysis in tomato-bipartite Begomovirus interaction and validation in additional tomato-virus pathosystems. PLoS One 10:e0136820
Lilly ST, Drummond RS, Pearson MN, MacDiarmid RM (2011) Identification and validation of reference genes for normalization of transcripts from virus-infected Arabidopsis thaliana. Mol Plant Microbe Interact 24:294–304
Mann KS, Bejerman N, Johnson KN, Dietzgen RG (2016) Cytorhabdovirus P3 genes encode 30K-like cell-to-cell movement proteins. Virology 489:20–33
Mann KS, Johnson KN, Carroll BJ, Dietzgen RG (2016) Cytorhabdovirus P protein suppresses RISC-mediated cleavage and RNA silencing amplification in planta. Virology 490:27–40
Mann KS, Johnson KN, Dietzgen RG (2015) Cytorhabdovirus phosphoprotein shows RNA silencing suppressor activity in plants, but not in insect cells. Virology 476:413–418
Massah A, Izadpanah K, Afsharifar AR, Winter S (2008) Analysis of nucleotide sequence of Iranian maize mosaic virus confirms its identity as a distinct nucleorhabdovirus. Arch Virol 153:1041–1047
Massah A, Izadpanah K, Lesemann DE (2005) Relationship of Iranian Maize mosaic virus with insect vector and plant cells. Iran J Plant Path 41:151–159
Melcher U (2000) The ‘30K’ superfamily of viral movement proteins. J Gen Virol 81:257–266
Nault LR (1997) Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Amer 90:521–541
Noton SL, Fearns R (2015) Initiation and regulation of paramyxovirus transcription and replication. Virology 479–480:545–554
Oksayan S, Ito N, Moseley G, Blondel D (2012) Subcellular trafficking in rhabdovirus infection and immune evasion: a novel target for therapeutics. Infect Disord Drug Targets 12:38–58
Pennica D, Lyncht KR, Cohen PS, Ennis HL (1979) Decay of vesicular stomatitis virus mRNAs in Vivo. Virol 94:484–487
Pfaffl MW (2004) Quantification strategies in real-time PCR. In: Bustin SA (ed) A–Z of quantitative PCR. International University Line, La Jolla, pp 89–113
von Kobbe C, van Deursen JM, Rodrigues JP, Sitterlin D, Bachi A (2000) Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol Cell 6:1243–1252
Wang Q, Ma X, Qian S, Zhou X, Sun K, Chen X (2015) Rescue of a plant negative-strand RNA virus from cloned cdna: insights into enveloped plant virus movement and morphogenesis. PLoS Pathog 11:e1005223
Wertz GW, Davies NL, Patton J (1987) The role of proteins in vesicular stomatitis virus RNA replication. In: Wagner RR (ed) The rhabdoviruses. Plenum Press, New York, pp 271–296
Whelan SP, Barr JN, Wertz GW (2004) Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol 283:61–119
Zhang L, Liu S, Zhang L, You H, Huang R, Sun L, He P, Chen S, Zhang H, Xie P (2014) Real-time qPCR identifies suitable reference genes for Borna disease virus-infected rat cortical neurons. Int J Mol Sci 15:21825–21839
Funding
This study was supported by Research and Technology Affairs of Isfahan University of Technology.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.
Additional information
Handling Editor: Ralf Georg Dietzgen.
Rights and permissions
About this article
Cite this article
Hortamani, M., Massah, A. & Izadpanah, K. Maize Iranian mosaic virus shows a descending transcript accumulation order in plant and insect hosts. Arch Virol 163, 887–893 (2018). https://doi.org/10.1007/s00705-017-3680-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-017-3680-y