Abstract
Macroptilium atropurpureum (siratro) samples from Queensland, Australia were collected as part of virus surveys and screened using tissue blot immunoassays for the presence of luteoviridae viruses. Sequencing of a reverse transcription polymerase chain reaction (RT-PCR) product, generated with degenerate primers for poleroviruses, revealed the non-symptomatic virus in siratro was a novel polerovirus, given the proposed name siratro latent polerovirus (SLPV). SLPV-specific RT-PCR showed that SLPV was widely distributed in siratro throughout Queensland. SLPV was transmitted via Aphis craccivora (cowpea aphids) to siratro and Pisum sativum (field pea). The complete genome of one isolate of SLPV was found to be 6090 nucleotides in length and shared only 69% nucleotide identity with its closest match, phasey bean mild yellows virus. Poleroviruses contain six major open reading frames (ORFs) labelled ORF 0–5. The SLPV genome has a similar arrangement. However, the region that should encode for ORF 0 is missing an AUG start codon. Sequencing of this region, from eight SLPV isolates, from different geographic regions, showed all lacked the ORF 0 AUG site and some isolates contained point mutations and deletions in this region, thus inhibiting translation of ORF 0. These results suggest that SLPV does not have a functional ORF 0 which may affect viral pathogenicity and restrict host range. This is the first report, to date, of a polerovirus with an apparently non-functional ORF 0 region.
References
Abraham AD, Menzel W, Lesemann DE, Varrelmann M, Vetten HJ (2006) Chickpea chlorotic stunt virus: a new Polerovirus infecting cool-season food legumes in Ethiopia. Phytopathology 96(5):437–446. https://doi.org/10.1094/PHYTO-96-0437
Abraham AD, Varrelmann M, Vetten HJ (2008) Molecular evidence for the occurrence of two new luteoviruses in cool season food legumes in Northeast Africa. Afr J Biotechnol 7:414–420
Asaad NY, Kumari SG, Haj-Kassem AA, Shalaby A-BA, Al-Shaabi S, Malhotra RS (2009) Detection and characterization of chickpea chlorotic stunt virus in Syria. J Phytopathol 157(11–12):756–761. https://doi.org/10.1111/j.1439-0434.2009.01574.x
Asif MH, Dhawan P, Nath P (2000) A simple procedure for the isolation of high quality RNA from ripening banana fruit. Plant Mol Biol Report 18(2):109–115. https://doi.org/10.1007/bf02824018
Baumberger N, Tsai C-H, Lie M, Havecker E, Baulcombe David C (2007) The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol 17(18):1609–1614. https://doi.org/10.1016/j.cub.2007.08.039
Bortolamiol D, Pazhouhandeh M, Marrocco K, Genschik P, Ziegler-Graff V (2007) The polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr Biol 17(18):1615–1621. https://doi.org/10.1016/j.cub.2007.07.061
Brault V, van den Heuvel JF, Verbeek M, Ziegler-Graff V, Reutenauer A, Herrbach E, Garaud JC, Guilley H, Richards K, Jonard G (1995) Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J 14(4):650–659
Brault V, Périgon S, Reinbold C, Erdinger M, Scheidecker D, Herrbach E, Richards K, Ziegler-Graff V (2005) The Polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid. J Virol 79(15):9685–9693. https://doi.org/10.1128/jvi.79.15.9685-9693.2005
Bray RA (1988) Inheritance of rust resistance in Macroptilium atropurpureum. Plant Pathol 37(1):88–95. https://doi.org/10.1111/j.1365-3059.1988.tb02199.x
Bushnell B (2016) BBTools: a suit of bioinformatic tools used for DNA and RNA sequence data analysis. [WWW document] URL http://jgi.doe.gov/data-and-tools/bbtools/. Accessed May 2016
Congdon BS, Kehoe MA, Filardo FF, Coutts BA (2019) In-field capable loop-mediated isothermal amplification detection of turnip yellows virus in plants and its principal aphid vector Myzus persicae. J Virol Methods 265:15–21. https://doi.org/10.1016/j.jviromet.2018.12.014
Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. P Natl Acad Sci 109(39):15942–15946. https://doi.org/10.1073/pnas.1209487109
Díaz-Pendón JA, Ding S-W (2008) Direct and indirect roles of viral suppressors of RNA silencing in pathogenesis. Annu Rev Phytopathol 46(1):303–326. https://doi.org/10.1146/annurev.phyto.46.081407.104746
Filardo FF, Thomas JE, Webb M, Sharman M (2019) Faba bean polerovirus 1 (FBPV-1); a new polerovirus infecting legume crops in Australia. Arch Virol 164 (7):1915-1921. https://doi.org/10.1007/s00705-019-04233-w
Firth AE, Brierley I (2012) Non-canonical translation in RNA viruses. J Gen Virol 93(7):1385–1409. https://doi.org/10.1099/vir.0.042499-0
Freeman A, Aftab M (2011) Effective management of viruses in pulse crops in south eastern Australia should include management of weeds. Australas Plant Path 40(4):430–441. https://doi.org/10.1007/s13313-011-0058-6
Fusaro AF, Barton DA, Nakasugi K, Jackson C, Kalischuk ML, Kawchuk LM, Vaslin MFS, Correa RL, Waterhouse PM (2017) The Luteovirus P4 movement protein is a suppressor of systemic RNA silencing. Viruses 9(10):294
Garnsey SM, Permar TA, Cambra M (1993) Direct tissue blot immunoassay (DTBIA) for detection of Citrus Tristeza virus (CTV). International Organization of Citrus Virologists Conference Proceedings 12:39–50
Gibbs A, Mackenzie A (1997) A primer pair for amplifying part of the genome of all potyvirids by RT-PCR. J Virol Methods 63:9–16
Herrbach E (1999) Vector-virus interaction. In: Smith HG, Barker H (eds) The Luteoviridae. CAB international, UK, pp 85–146
Jaag HM, Kawchuk L, Rohde W, Fischer R, Emans N, Prüfer D (2003) An unusual internal ribosomal entry site of inverted symmetry directs expression of a potato leafroll polerovirus replication-associated protein. P Natl Acad Sci 100(15):8939–8944. https://doi.org/10.1073/pnas.1332697100
Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36(Web Server):W5–W9. https://doi.org/10.1093/nar/gkn201
Katul L (1992) Characterization by serology and molecular biology of bean leaf roll virus and faba bean necrotic yellows virus. PhD, PhD thesis, University of Göttingen, Göttingen, Germany,
Kearse MG, Wilusz JE (2017) Non-AUG translation: a new start for protein synthesis in eukaryotes. Genes Dev 31(17):1717–1731. https://doi.org/10.1101/gad.305250.117
King AM, Lefkowitz E, Adams MJ, Carstens EB (2011) Virus taxonomy: ninth report of the international committee on taxonomy of viruses. Elsevier
Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44(2):283–292. https://doi.org/10.1016/0092-8674(86)90762-2
Krueger EN, Beckett RJ, Gray SM, Miller WA (2013) The complete nucleotide sequence of the genome of barley yellow dwarf virus-RMV reveals it to be a new Polerovirus distantly related to other yellow dwarf viruses. Front Microbiol 4:205. https://doi.org/10.3389/fmicb.2013.00205
Makkouk KM, Comeau A (1994) Evaluation of various methods for the detection of barley yellow dwarf virus by the tissue-blot immunoassay and its use for virus detection in cereals inoculated at different growth stages. Eur J Plant Pathol 100:71–80. https://doi.org/10.1007/bf01871967
Mayo MA, D'Arcy CJ (1999) Family Luteoviridae: a reclassification of Luteoviruses. The Luteoviridae. CABI publishing, Wallingford, UK
Mayo MA, Miller WA (1999) The structure and expression of luteovirus genomes. In: Smith HG, Barker H (eds) The Luteoviridae. CAB international, Wallingford, pp 23–42
Mayo MA, Ziegler-Graff V (1996) Molecular biology of Luteoviruses. Adv Virus Res 46:413–460
Najar A, Kumari SG, Attar N, Lababidi S (2011) Present status of some virus diseases affecting legume crops in Tunisia, and partial characterization of chickpea chlorotic stunt virus. Phytopathol Mediterr 50 (2):310-315. https://doi.org/10.14601/Phytopathol_Mediterr-9043
Pazhouhandeh M, Dieterle M, Marrocco K, Lechner E, Berry B, Brault V, xe r, Hemmer O, Kretsch T, Richard KE, Genschik P, Ziegler-Graff V, xe r (2006) F-box-like domain in the Polerovirus protein P0 is required for silencing suppressor function. Proc Natl Acad Sci U S A 103(6):1994–1999
Peter KA, Liang D, Palukaitis P, Gray SM (2008) Small deletions in the potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation. J Gen Virol 89(8):2037–2045. https://doi.org/10.1099/vir.0.83625-0
Peter KA, Gildow F, Palukaitis P, Gray SM (2009) The C terminus of the Polerovirus P5 Readthrough domain limits virus infection to the phloem. J Virol 83(11):5419–5429. https://doi.org/10.1128/jvi.02312-08
Ray JD, Sharman M, Quintao V, Rossel B, Westaway J, Gambley C (2016) Cotton leafroll dwarf virus detected in Timor-Leste. Australas Plant Dis Notes 11(1):29. https://doi.org/10.1007/s13314-016-0217-2
Risseeuw EP, Daskalchuk TE, Banks TW, Liu E, Cotelesage J, Hellmann H, Estelle M, Somers DE, Crosby WL (2003) Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J 34(6):753–767. https://doi.org/10.1046/j.1365-313X.2003.01768.x
Sadowy E, Maasen A, Juszczuk M, David C, Zagórski-Ostoja W, Gronenborn B, Hulanicka MD (2001) The ORF0 product of potato leafroll virus is indispensable for virus accumulation. J Gen Virol 82(6):1529–1532. https://doi.org/10.1099/0022-1317-82-6-1529
Schmitz J, Stussi-Garaud C, Tacke E, Prüfer D, Rohde W, Rohfritsch O (1997) In SituLocalization of the putative movement protein (pr17) from potato Leafroll Luteovirus (PLRV) in infected and transgenic potato plants. Virology 235(2):311–322. https://doi.org/10.1006/viro.1997.8679
Sharman M, Thomas JE (2013) Genetic diversity of subgroup 1 ilarviruses from eastern Australia. Arch Virol 158(8):1637–1647. https://doi.org/10.1007/s00705-013-1628-4
Sharman M, Lapbanjob S, Sebunruang P, Belot JL, Galbieri R, Giband M, Suassuna N (2015a) First report of cotton leafroll dwarf virus in Thailand using a species-specific PCR validated with isolates from Brazil. Australas Plant Dis Notes 10(1):1–4. https://doi.org/10.1007/s13314-015-0174-1
Sharman M, Thomas JE, Persley DM (2015b) Natural host range, thrips and seed transmission of distinct tobacco streak virus strains in Queensland, Australia. Ann Appl Biol 167(2):197–207. https://doi.org/10.1111/aab.12218
Sharman M, Kehoe M, Coutts B, van Leur J, Filardo F, Thomas J (2016) Two complete genome sequences of Phasey bean mild yellows virus, a novel member of the Luteoviridae from Australia. Genome Announc 4(1). https://doi.org/10.1128/genomeA.01569-15
Smirnova E, Firth AE, Miller WA, Scheidecker D, Brault V, Reinbold C, Rakotondrafara AM, Chung BYW, Ziegler-Graff V (2015) Discovery of a small non-AUG-initiated ORF in Poleroviruses and Luteoviruses that is required for long-distance movement. PLoS Pathog 11(5):e1004868. https://doi.org/10.1371/journal.ppat.1004868
van den Heuvel JF, Bruyère A, Hogenhout SA, Ziegler-Graff V, Brault V, Verbeek M, van der Wilk F, Richards K (1997) The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J Virol 71(10):7258–7265
van der Wilk F, Verbeek M, Dullemans AM, van den Heuvel JFJM (1997) The genome-linked protein of potato Leafroll virus is located downstream of the putative protease domain of the ORF1 product. Virology 234(2):300–303. https://doi.org/10.1006/viro.1997.8654
Wang K-D, Empleo R, Nguyen TTV, Moffett P, Sacco MA (2015) Elicitation of hypersensitive responses in Nicotiana glutinosa by the suppressor of RNA silencing protein P0 from poleroviruses. Mol Plant Pathol 16(5):435–448. https://doi.org/10.1111/mpp.12201
Ziegler-Graff V, Brault V, Mutterer JD, Simonis MT, Herrbach E, Guilley H, Richards KE, Jonard G (1996) The coat protein of beet western yellows luteovirus is essential for systemic infection but the viral gene products P29 and P19 are dispensable for systemic infection and aphid transmission. Mol Plant Microbe In 1996 v.9 no.6 (no. 6):pp. 501–510. https://doi.org/10.1094/mpmi-9-0501
Acknowledgements
This study was funded by the Australian Grains Research and Development Corporation projects DAQ00154, DAQ00186 and DAN00202.
Author information
Authors and Affiliations
Corresponding author
Additional information
Nucleotide sequence data reported are available in the GenBank database under the accession number MK482114
Electronic supplementary material
ESM 1
(PDF 366 kb)
Rights and permissions
About this article
Cite this article
Filardo, F.F., Sharman, M. Siratro latent polerovirus (SLPV): a new polerovirus from Australia with a non-functional open reading frame 0. Australasian Plant Pathol. 48, 491–501 (2019). https://doi.org/10.1007/s13313-019-00650-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13313-019-00650-2