Skip to main content
Top
Published in: Archives of Virology 9/2013

01-09-2013 | Brief Report

Large-scale codon de-optimisation of the p29 replicase gene by synonymous substitutions causes a loss of infectivity of melon necrotic spot virus

Authors: Atsushi Usami, Tomofumi Mochizuki, Shinya Tsuda, Satoshi T. Ohki

Published in: Archives of Virology | Issue 9/2013

Login to get access

Abstract

The effect of synonymous substitutions in the melon necrotic spot virus p29 replicase gene on viral pathogenicity was investigated. The codons in the p29 gene were replaced by the least frequently used synonymous codons in Arabidopsis thaliana or melons. Mechanical inoculation of melon with p29 variants resulted in a loss of viral infectivity when all, one-half, or one-quarter of the gene was de-optimised. The effect of the de-optimisation in one-sixth of the gene was different depending on the de-optimised region. These results demonstrate that large-scale codon bias de-optimisation without amino acid substitutions of the p29 gene alter viral infectivity.
Appendix
Available only for authorised users
Literature
1.
go back to reference Adams MJ, Antoniw JF (2004) Codon usage bias amongst plant viruses. Arch Virol 149:113–135PubMed Adams MJ, Antoniw JF (2004) Codon usage bias amongst plant viruses. Arch Virol 149:113–135PubMed
2.
go back to reference Avgelis A (1989) Watermelon necrosis caused by a strain of Melon necrotic spot virus. Plant Pathol 38:618–622CrossRef Avgelis A (1989) Watermelon necrosis caused by a strain of Melon necrotic spot virus. Plant Pathol 38:618–622CrossRef
3.
go back to reference Bos L, Van Dorst HJM, Huttinga H, Maat DZ (1984) Further characterization of melon necrotic spot virus causing severe disease in glasshouse cucumbers in the Netherlands and its control. Neth J Plant Pathol 90:55–69CrossRef Bos L, Van Dorst HJM, Huttinga H, Maat DZ (1984) Further characterization of melon necrotic spot virus causing severe disease in glasshouse cucumbers in the Netherlands and its control. Neth J Plant Pathol 90:55–69CrossRef
4.
go back to reference Campbell RN, Wipf-Scheibel C, Lecoq H (1996) Vector-assisted seed transmission of melon necrotic spot virus in melon. Phytopathology 86:1294–1298CrossRef Campbell RN, Wipf-Scheibel C, Lecoq H (1996) Vector-assisted seed transmission of melon necrotic spot virus in melon. Phytopathology 86:1294–1298CrossRef
5.
go back to reference Cardinale DJ, Derosa K, Duffy S (2013) Base composition and translational selection are insufficient to explain codon usage bias in plant viruses. Viruses 15:162–181CrossRef Cardinale DJ, Derosa K, Duffy S (2013) Base composition and translational selection are insufficient to explain codon usage bias in plant viruses. Viruses 15:162–181CrossRef
6.
go back to reference Cheng XF, Wu XY, Wang HZ, Sun YQ, Qian YS, Luo L (2012) High codon adaptation in citrus tristeza virus to its citrus host. Virol J 9:113PubMedCrossRef Cheng XF, Wu XY, Wang HZ, Sun YQ, Qian YS, Luo L (2012) High codon adaptation in citrus tristeza virus to its citrus host. Virol J 9:113PubMedCrossRef
7.
go back to reference Cimino PA, Nicholson BL, Wu B, Xu W, White KA (2011) Multifaceted regulation of translational readthrough by RNA replication elements in a tombusvirus. PLoS Pathog 7:e1002423PubMedCrossRef Cimino PA, Nicholson BL, Wu B, Xu W, White KA (2011) Multifaceted regulation of translational readthrough by RNA replication elements in a tombusvirus. PLoS Pathog 7:e1002423PubMedCrossRef
8.
go back to reference Clepet C, Joobeur T, Zheng Y, Jublot D, Huang M, Truniger V, Boualem A, Hernandez-Gonzalez ME, Dolcet-Sanjuan R, Portnoy V, Mascarell-Creus A, Caño-Delgado AI, Katzir N, Bendahmane A, Giovannoni JJ, Aranda MA, Garcia-Mas J, Fei Z (2011) Analysis of expressed sequence tags generated from full-length enriched cDNA libraries of melon. BMC Genomics 12:252PubMedCrossRef Clepet C, Joobeur T, Zheng Y, Jublot D, Huang M, Truniger V, Boualem A, Hernandez-Gonzalez ME, Dolcet-Sanjuan R, Portnoy V, Mascarell-Creus A, Caño-Delgado AI, Katzir N, Bendahmane A, Giovannoni JJ, Aranda MA, Garcia-Mas J, Fei Z (2011) Analysis of expressed sequence tags generated from full-length enriched cDNA libraries of melon. BMC Genomics 12:252PubMedCrossRef
9.
go back to reference Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S (2008) Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784–1787PubMedCrossRef Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S (2008) Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784–1787PubMedCrossRef
10.
go back to reference Furuki I (1981) Epidemiological studies on melon necrotic spot. Shizuoka (Japan) Agr Exp Sta Tech Bull 14 Furuki I (1981) Epidemiological studies on melon necrotic spot. Shizuoka (Japan) Agr Exp Sta Tech Bull 14
11.
go back to reference Kido K, Tanaka C, Mochizuki T, Kubota K, Ohki T, Ohnishi J, Knight LM, Tsuda S (2008) High temperatures activate local viral multiplication and cell-to-cell movement of Melon necrotic spot virus but restrict expression of systemic symptoms. Phytopathology 98:181–186PubMedCrossRef Kido K, Tanaka C, Mochizuki T, Kubota K, Ohki T, Ohnishi J, Knight LM, Tsuda S (2008) High temperatures activate local viral multiplication and cell-to-cell movement of Melon necrotic spot virus but restrict expression of systemic symptoms. Phytopathology 98:181–186PubMedCrossRef
12.
go back to reference Kishi K (1966) Necrotic spot of melon, a new virus disease. Ann Phytopathol Soc Jpn 32:138–144CrossRef Kishi K (1966) Necrotic spot of melon, a new virus disease. Ann Phytopathol Soc Jpn 32:138–144CrossRef
13.
go back to reference Kubota K, Tsuda S, Tamai A, Meshi T (2003) Tomato mosaic virus replication protein suppresses virus targeted posttranscriptional gene silencing. J Virol 77:11016–11026PubMedCrossRef Kubota K, Tsuda S, Tamai A, Meshi T (2003) Tomato mosaic virus replication protein suppresses virus targeted posttranscriptional gene silencing. J Virol 77:11016–11026PubMedCrossRef
14.
go back to reference Mochizuki T, Ohnishi J, Ohki T, Kanda A, Tsuda S (2008) Amino acid substitution in the coat protein of Melon necrotic spot virus causes loss of binding to the surface of Olpidium bornovanus zoospores. J Gen Plant Pathol 74:176–181CrossRef Mochizuki T, Ohnishi J, Ohki T, Kanda A, Tsuda S (2008) Amino acid substitution in the coat protein of Melon necrotic spot virus causes loss of binding to the surface of Olpidium bornovanus zoospores. J Gen Plant Pathol 74:176–181CrossRef
15.
go back to reference Mochizuki T, Hirai K, Kanda A, Ohnishi J, Ohki T, Tsuda S (2009) Induction of necrosis via mitochondrial targeting of Melon necrotic spot virus replication protein p29 by its second transmembrane domain. Virology 390:239–249PubMedCrossRef Mochizuki T, Hirai K, Kanda A, Ohnishi J, Ohki T, Tsuda S (2009) Induction of necrosis via mitochondrial targeting of Melon necrotic spot virus replication protein p29 by its second transmembrane domain. Virology 390:239–249PubMedCrossRef
16.
go back to reference Monkewich S, Lin HX, Fabian MR, Xu W, Na H, Ray D, Chernysheva OA, Nagy PD, White KA (2005) The p92 polymerase coding region contains an internal RNA element required at an early step in tombusvirus genome replication. J Virol 79:4848–4858PubMedCrossRef Monkewich S, Lin HX, Fabian MR, Xu W, Na H, Ray D, Chernysheva OA, Nagy PD, White KA (2005) The p92 polymerase coding region contains an internal RNA element required at an early step in tombusvirus genome replication. J Virol 79:4848–4858PubMedCrossRef
17.
go back to reference Mueller S, Coleman JR, Papamichail D, Ward CB, Nimnual A, Futcher B, Skiena S, Wimmer E (2010) Live attenuated influenza virus vaccines by computer-aided rational design. Nat Biotechnol 28:723–726PubMedCrossRef Mueller S, Coleman JR, Papamichail D, Ward CB, Nimnual A, Futcher B, Skiena S, Wimmer E (2010) Live attenuated influenza virus vaccines by computer-aided rational design. Nat Biotechnol 28:723–726PubMedCrossRef
18.
go back to reference Mueller S, Papamichail D, Coleman JR, Skiena S, Wimmer E (2006) Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J Virol 80:9687–9696PubMedCrossRef Mueller S, Papamichail D, Coleman JR, Skiena S, Wimmer E (2006) Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J Virol 80:9687–9696PubMedCrossRef
19.
go back to reference Nishiguchi M, Kobayashi K (2011) Attenuated plant viruses: preventing virus diseases and understanding the molecular mechanism. J Gen Plant Pathol 77:221–229CrossRef Nishiguchi M, Kobayashi K (2011) Attenuated plant viruses: preventing virus diseases and understanding the molecular mechanism. J Gen Plant Pathol 77:221–229CrossRef
20.
go back to reference Novoa EM, Ribas de Pouplana L (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet 28:574–581PubMedCrossRef Novoa EM, Ribas de Pouplana L (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet 28:574–581PubMedCrossRef
21.
go back to reference Plotkin JB, Kudla G (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12:32–42PubMedCrossRef Plotkin JB, Kudla G (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12:32–42PubMedCrossRef
22.
go back to reference Pogany J, White KA, Nagy PD (2005) Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J Virol 79:4859–4869PubMedCrossRef Pogany J, White KA, Nagy PD (2005) Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J Virol 79:4859–4869PubMedCrossRef
23.
go back to reference Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I (1999) Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J Virol 73:4972–4982PubMed Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I (1999) Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J Virol 73:4972–4982PubMed
24.
go back to reference Zhou H, Wang H, Huang LF, Naylor M, Clifford P (2005) Heterogeneity in codon usages of sobemovirus genes. Arch Virol 150:1591–1605PubMedCrossRef Zhou H, Wang H, Huang LF, Naylor M, Clifford P (2005) Heterogeneity in codon usages of sobemovirus genes. Arch Virol 150:1591–1605PubMedCrossRef
Metadata
Title
Large-scale codon de-optimisation of the p29 replicase gene by synonymous substitutions causes a loss of infectivity of melon necrotic spot virus
Authors
Atsushi Usami
Tomofumi Mochizuki
Shinya Tsuda
Satoshi T. Ohki
Publication date
01-09-2013
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 9/2013
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-013-1683-x

Other articles of this Issue 9/2013

Archives of Virology 9/2013 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 discuss last year's major advances in heart failure and cardiomyopathies.