Skip to main content
Top
Published in: Archives of Virology 3/2017

01-03-2017 | Annotated Sequence Record

Molecular characterization of a novel ssRNA ourmia-like virus from the rice blast fungus Magnaporthe oryzae

Authors: Adriana Illana, Marco Marconi, Julio Rodríguez-Romero, Ping Xu, Tamas Dalmay, Mark D. Wilkinson, Maria Ángeles Ayllón, Ane Sesma

Published in: Archives of Virology | Issue 3/2017

Login to get access

Abstract

In this study we characterize a novel positive and single stranded RNA (ssRNA) mycovirus isolated from the rice field isolate of Magnaporthe oryzae Guy11. The ssRNA contains a single open reading frame (ORF) of 2,373 nucleotides in length and encodes an RNA-dependent RNA polymerase (RdRp) closely related to ourmiaviruses (plant viruses) and ourmia-like mycoviruses. Accordingly, we name this virus Magnaporthe oryzae ourmia-like virus 1 (MOLV1). Although phylogenetic analysis suggests that MOLV1 is closely related to ourmia and ourmia-like viruses, it has some features never reported before within the Ourmiavirus genus. 3’ RLM-RACE (RNA ligase-mediated rapid amplification of cDNA ends) and extension poly(A) tests (ePAT) suggest that the MOLV1 genome contains a poly(A) tail whereas the three cytosine and the three guanine residues present in 5’ and 3’ untranslated regions (UTRs) of ourmia viruses are not observed in the MOLV1 sequence. The discovery of this novel viral genome supports the hypothesis that plant pathogenic fungi may have acquired this type of viruses from their host plants.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ai Y-P, Zhong J, Chen C-Y, Zhu H-J, Gao B-D (2016) A novel single-stranded RNA virus isolated from the rice-pathogenic fungus Magnaporthe oryzae with similarity to members of the family Tombusviridae. Arch Virol 161:725–729CrossRefPubMed Ai Y-P, Zhong J, Chen C-Y, Zhu H-J, Gao B-D (2016) A novel single-stranded RNA virus isolated from the rice-pathogenic fungus Magnaporthe oryzae with similarity to members of the family Tombusviridae. Arch Virol 161:725–729CrossRefPubMed
2.
go back to reference Andrew King EL, Michael J. Adams and Eric B. Carstens (2012) Virus taxonomy, 1st edn. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier, p 1344 Andrew King EL, Michael J. Adams and Eric B. Carstens (2012) Virus taxonomy, 1st edn. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier, p 1344
3.
go back to reference Cai G, Krychiw JF, Myers K, Fry WE, Hillman BI (2013) A new virus from the plant pathogenic oomycete Phytophthora infestans with an 8 kb dsRNA genome: The sixth member of a proposed new virus genus. Virology 435:341–349CrossRefPubMed Cai G, Krychiw JF, Myers K, Fry WE, Hillman BI (2013) A new virus from the plant pathogenic oomycete Phytophthora infestans with an 8 kb dsRNA genome: The sixth member of a proposed new virus genus. Virology 435:341–349CrossRefPubMed
4.
go back to reference Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421CrossRef Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421CrossRef
5.
go back to reference Chao CCT, Ellingboe AH (1991) Selection for mating competence in Magnaporthe grisea pathogenic to rice. Can J Bot 69:130–134CrossRef Chao CCT, Ellingboe AH (1991) Selection for mating competence in Magnaporthe grisea pathogenic to rice. Can J Bot 69:130–134CrossRef
6.
go back to reference Donaire L, Rozas J, Ayllón MA (2016) Molecular characterization of Botrytis ourmia-like virus, a mycovirus close to the plant pathogenic genus Ourmiavirus. Virology 489:158–164CrossRefPubMed Donaire L, Rozas J, Ayllón MA (2016) Molecular characterization of Botrytis ourmia-like virus, a mycovirus close to the plant pathogenic genus Ourmiavirus. Virology 489:158–164CrossRefPubMed
8.
go back to reference Ghabrial SA (1998) Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes 16(1):119–131CrossRefPubMed Ghabrial SA (1998) Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes 16(1):119–131CrossRefPubMed
9.
10.
go back to reference Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368CrossRefPubMed Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368CrossRefPubMed
11.
go back to reference Hillman BI, Cai G (2013) The family Narnaviridae: simplest of RNA viruses, chapter 6. In: Said AG (ed) Advances in virus research. Academic Press, pp 149–176 Hillman BI, Cai G (2013) The family Narnaviridae: simplest of RNA viruses, chapter 6. In: Said AG (ed) Advances in virus research. Academic Press, pp 149–176
12.
go back to reference Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW (1999) Multiple mitochondrial viruses in an isolate of the Dutch elm disease fungus Ophiostoma novo-ulmi. Virology 258:118–127CrossRefPubMed Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW (1999) Multiple mitochondrial viruses in an isolate of the Dutch elm disease fungus Ophiostoma novo-ulmi. Virology 258:118–127CrossRefPubMed
14.
go back to reference Hunst PLLHF, Rossi AE (1986) Variation in a double-stranded RNA from isolates of Pyricularia oryzae. Phytopathology 76:674–678CrossRef Hunst PLLHF, Rossi AE (1986) Variation in a double-stranded RNA from isolates of Pyricularia oryzae. Phytopathology 76:674–678CrossRef
15.
go back to reference Jänicke A, Vancuylenberg J, Boag PR, Traven A, Beilharz TH (2012) ePAT: A simple method to tag adenylated RNA to measure poly(A)-tail length and other 3 ‘ RACE applications. RNA 18:1289–1295CrossRefPubMedPubMedCentral Jänicke A, Vancuylenberg J, Boag PR, Traven A, Beilharz TH (2012) ePAT: A simple method to tag adenylated RNA to measure poly(A)-tail length and other 3 ‘ RACE applications. RNA 18:1289–1295CrossRefPubMedPubMedCentral
16.
go back to reference Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72:2197–2206CrossRefPubMed Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72:2197–2206CrossRefPubMed
17.
go back to reference Leung H, Borromeo E, Bernardo M, Notteghem JL (1988) Genetic analysis of virulence in the rice blast fungus Magnaporthe grisea. Phytopathology 78:1227–1233CrossRef Leung H, Borromeo E, Bernardo M, Notteghem JL (1988) Genetic analysis of virulence in the rice blast fungus Magnaporthe grisea. Phytopathology 78:1227–1233CrossRef
18.
go back to reference Li W, Zhang Y, Zhang C, Pei X, Wang Z, Jia S (2014) Presence of poly(A) and poly(A)-rich tails in a positive-strand RNA virus known to lack 3′ poly(A) tails. Virology 454–455:1–10CrossRefPubMed Li W, Zhang Y, Zhang C, Pei X, Wang Z, Jia S (2014) Presence of poly(A) and poly(A)-rich tails in a positive-strand RNA virus known to lack 3′ poly(A) tails. Virology 454–455:1–10CrossRefPubMed
19.
go back to reference Liu L, Xie J, Cheng J, Fu Y, Li G, Yi X, Jiang D (2014) Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci USA 111:12205–12210CrossRefPubMedPubMedCentral Liu L, Xie J, Cheng J, Fu Y, Li G, Yi X, Jiang D (2014) Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci USA 111:12205–12210CrossRefPubMedPubMedCentral
20.
go back to reference Maejima K, Himeno M, Komatsu K, Kakizawa S, Yamaji Y, Hamamoto H, Namba S (2008) Complete nucleotide sequence of a new double-stranded RNA virus from the rice blast fungus, Magnaporthe oryzae. Arch Virol 153:389–391CrossRefPubMed Maejima K, Himeno M, Komatsu K, Kakizawa S, Yamaji Y, Hamamoto H, Namba S (2008) Complete nucleotide sequence of a new double-stranded RNA virus from the rice blast fungus, Magnaporthe oryzae. Arch Virol 153:389–391CrossRefPubMed
21.
go back to reference Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515CrossRefPubMed Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515CrossRefPubMed
22.
go back to reference Marzano S-YL, Domier LL (2016) Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213:332–342CrossRefPubMed Marzano S-YL, Domier LL (2016) Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213:332–342CrossRefPubMed
23.
go back to reference Marzano S-YL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ, Hartman GL, Eastburn DM, Domier LL (2016) Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J Virol 90:6846–6863. doi:10.1128/JVI.00357-16 CrossRefPubMedPubMedCentral Marzano S-YL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ, Hartman GL, Eastburn DM, Domier LL (2016) Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J Virol 90:6846–6863. doi:10.​1128/​JVI.​00357-16 CrossRefPubMedPubMedCentral
24.
go back to reference Nuss DL (2005) Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol 3:632–642CrossRefPubMed Nuss DL (2005) Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol 3:632–642CrossRefPubMed
25.
go back to reference Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–D504CrossRefPubMed Pruitt KD, Tatusova T, Maglott DR (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33:D501–D504CrossRefPubMed
26.
go back to reference Raju R, Hajjou M, Hill KR, Botta V, Botta S (1999) In vivo addition of poly(A) tail and AU-rich sequences to the 3′ terminus of the Sindbis virus RNA genome: a novel 3′-end repair pathway. J Virol 73:2410–2419PubMedPubMedCentral Raju R, Hajjou M, Hill KR, Botta V, Botta S (1999) In vivo addition of poly(A) tail and AU-rich sequences to the 3′ terminus of the Sindbis virus RNA genome: a novel 3′-end repair pathway. J Virol 73:2410–2419PubMedPubMedCentral
27.
go back to reference Rastgou M, Habibi MK, Izadpanah K, Masenga V, Milne RG, Wolf YI, Koonin EV, Turina M (2009) Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J Gen Virol 90:2525–2535CrossRefPubMedPubMedCentral Rastgou M, Habibi MK, Izadpanah K, Masenga V, Milne RG, Wolf YI, Koonin EV, Turina M (2009) Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J Gen Virol 90:2525–2535CrossRefPubMedPubMedCentral
28.
go back to reference Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genetics 16:276–277CrossRef Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genetics 16:276–277CrossRef
29.
go back to reference Skamnioti P, Gurr SJ (2009) Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol 27:141–150CrossRefPubMed Skamnioti P, Gurr SJ (2009) Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol 27:141–150CrossRefPubMed
30.
31.
go back to reference Tang L, Hu Y, Liu L, Wu S, Xie J, Cheng J, Fu Y, Zhang G, Ma J, Wang Y, Zhang L (2015) Genomic organization of a novel victorivirus from the rice blast fungus Magnaporthe oryzae. Arch Virol 160(11):2907–2910CrossRefPubMed Tang L, Hu Y, Liu L, Wu S, Xie J, Cheng J, Fu Y, Zhang G, Ma J, Wang Y, Zhang L (2015) Genomic organization of a novel victorivirus from the rice blast fungus Magnaporthe oryzae. Arch Virol 160(11):2907–2910CrossRefPubMed
32.
go back to reference Urayama S, Kato S, Suzuki Y, Aoki N, Le MT, Arie T, Teraoka T, Fukuhara T, Moriyama H (2010) Mycoviruses related to chrysovirus affect vegetative growth in the rice blast fungus Magnaporthe oryzae. J Gen Virol 91:3085–3094CrossRefPubMed Urayama S, Kato S, Suzuki Y, Aoki N, Le MT, Arie T, Teraoka T, Fukuhara T, Moriyama H (2010) Mycoviruses related to chrysovirus affect vegetative growth in the rice blast fungus Magnaporthe oryzae. J Gen Virol 91:3085–3094CrossRefPubMed
33.
go back to reference Urayama S, Ohta T, Onozuka N, Sakoda H, Fukuhara T, Arie T, Teraoka T, Moriyama H (2012) Characterization of Magnaporthe oryzae chrysovirus 1 structural proteins and their expression in Saccharomyces cerevisiae. J Virol 86:8287–8295CrossRefPubMedPubMedCentral Urayama S, Ohta T, Onozuka N, Sakoda H, Fukuhara T, Arie T, Teraoka T, Moriyama H (2012) Characterization of Magnaporthe oryzae chrysovirus 1 structural proteins and their expression in Saccharomyces cerevisiae. J Virol 86:8287–8295CrossRefPubMedPubMedCentral
34.
go back to reference Urayama S, Sakoda H, Takai R, Katoh Y, Le Minh T, Fukuhara T, Arie T, Teraoka T, Moriyama H (2014) A dsRNA mycovirus, Magnaporthe oryzae chrysovirus 1-B, suppresses vegetative growth and development of the rice blast fungus. Virology 448:265–273CrossRefPubMed Urayama S, Sakoda H, Takai R, Katoh Y, Le Minh T, Fukuhara T, Arie T, Teraoka T, Moriyama H (2014) A dsRNA mycovirus, Magnaporthe oryzae chrysovirus 1-B, suppresses vegetative growth and development of the rice blast fungus. Virology 448:265–273CrossRefPubMed
35.
go back to reference Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699CrossRefPubMed Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699CrossRefPubMed
36.
go back to reference Xie J, Ghabrial SA (2012) Molecular characterizations of two mitoviruses co-infecting a hyovirulent isolate of the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 428:77–85CrossRefPubMed Xie J, Ghabrial SA (2012) Molecular characterizations of two mitoviruses co-infecting a hyovirulent isolate of the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 428:77–85CrossRefPubMed
37.
go back to reference Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68CrossRefPubMed Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68CrossRefPubMed
38.
go back to reference Yamashita S, Doi Y, Yora K (1971) A polyhedral virus found in rice blast fungus, Pyricularia oryzae Cavara. Jpn J Phytopathol 37:356–359CrossRef Yamashita S, Doi Y, Yora K (1971) A polyhedral virus found in rice blast fungus, Pyricularia oryzae Cavara. Jpn J Phytopathol 37:356–359CrossRef
39.
go back to reference Yokoi T, Yamashita S, Hibi T (2007) The nucleotide sequence and genome organization of Magnaporthe oryzae virus 1. Arch Virol 152:2265–2269CrossRefPubMed Yokoi T, Yamashita S, Hibi T (2007) The nucleotide sequence and genome organization of Magnaporthe oryzae virus 1. Arch Virol 152:2265–2269CrossRefPubMed
Metadata
Title
Molecular characterization of a novel ssRNA ourmia-like virus from the rice blast fungus Magnaporthe oryzae
Authors
Adriana Illana
Marco Marconi
Julio Rodríguez-Romero
Ping Xu
Tamas Dalmay
Mark D. Wilkinson
Maria Ángeles Ayllón
Ane Sesma
Publication date
01-03-2017
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 3/2017
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-016-3144-9

Other articles of this Issue 3/2017

Archives of Virology 3/2017 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.