Skip to main content
Top
Published in: Virology Journal 1/2023

Open Access 01-12-2023 | Research

MRF: a tool to overcome the barrier of inconsistent genome annotations and perform comparative genomics studies for the largest animal DNA virus

Authors: Karthic Krishnan, Vinaya Kumar Katneni, Sudheesh K. Prabhudas, Nimisha Kaikkolante, Ashok Kumar Jangam, Upendra Kumar Katneni, Chris Hauton, Luca Peruzza, Shashi Shekhar Mudagandur, Vijayan K. Koyadan, Jithendran Karingalakkandy Poochirian, Joykrushna Jena

Published in: Virology Journal | Issue 1/2023

Login to get access

Abstract

Background

The genome of the largest known animal virus, the white spot syndrome virus (WSSV) responsible for huge economic losses and loss of employment in aquaculture, suffers from inconsistent annotation nomenclature. Novel genome sequence, circular genome and variable genome length led to nomenclature inconsistencies. Since vast knowledge has already accumulated in the past two decades with inconsistent nomenclature, the insights gained on a genome could not be easily extendable to other genomes. Therefore, the present study aims to perform comparative genomics studies in WSSV on uniform nomenclature.

Methods

We have combined the standard mummer tool with custom scripts to develop missing regions finder (MRF) that documents the missing genome regions and coding sequences in virus genomes in comparison to a reference genome and in its annotation nomenclature. The procedure was implemented as web tool and in command-line interface. Using MRF, we have documented the missing coding sequences in WSSV and explored their role in virulence through application of phylogenomics, machine learning models and homologous genes.

Results

We have tabulated and depicted the missing genome regions, missing coding sequences and deletion hotspots in WSSV on a common annotation nomenclature and attempted to link them to virus virulence. It was observed that the ubiquitination, transcription regulation and nucleotide metabolism might be essentially required for WSSV pathogenesis; and the structural proteins, VP19, VP26 and VP28 are essential for virus assembly. Few minor structural proteins in WSSV would act as envelope glycoproteins. We have also demonstrated the advantage of MRF in providing detailed graphic/tabular output in less time and also in handling of low-complexity, repeat-rich and highly similar regions of the genomes using other virus cases.

Conclusions

Pathogenic virus research benefits from tools that could directly indicate the missing genomic regions and coding sequences between isolates/strains. In virus research, the analyses performed in this study provides an advancement to find the differences between genomes and to quickly identify the important coding sequences/genomes that require early attention from researchers. To conclude, the approach implemented in MRF complements similarity-based tools in comparative genomics involving large, highly-similar, length-varying and/or inconsistently annotated viral genomes.
Appendix
Available only for authorised users
Literature
1.
go back to reference Pradeep B, Rai P, Mohan SA, Shekhar MS, Karunasagar I. Biology, host range, pathogenesis and diagnosis of white spot syndrome virus. Indian J Virol. 2012;23(2):161–74.PubMedPubMedCentralCrossRef Pradeep B, Rai P, Mohan SA, Shekhar MS, Karunasagar I. Biology, host range, pathogenesis and diagnosis of white spot syndrome virus. Indian J Virol. 2012;23(2):161–74.PubMedPubMedCentralCrossRef
2.
go back to reference FAO. Globefish highlights—a quarterly update on world seafood markets. Food Agric Organ U N. 2020;2:37–42. FAO. Globefish highlights—a quarterly update on world seafood markets. Food Agric Organ U N. 2020;2:37–42.
3.
go back to reference Briggs M, Funge-Smith S, Subasinghe RP, Phillips M. Introductions and movement of two penaeid shrimp species in Asia and the Pacific. FAO Fisheries Technical Paper 476. Rome: Food & Agriculture Org.; 2005. Briggs M, Funge-Smith S, Subasinghe RP, Phillips M. Introductions and movement of two penaeid shrimp species in Asia and the Pacific. FAO Fisheries Technical Paper 476. Rome: Food & Agriculture Org.; 2005.
4.
go back to reference Flegel TW, Lightner DV, Lo CF, Owens L. Shrimp disease control: past, present and future. In: Bondad-Reantaso MG, Mohan CV, Crumlish M, Subasinghe RP, editors. Diseases in Asian aquaculture VI. Fish heal section. Philippines: Asian Fisheries Society; 2008. p. 355–78. Flegel TW, Lightner DV, Lo CF, Owens L. Shrimp disease control: past, present and future. In: Bondad-Reantaso MG, Mohan CV, Crumlish M, Subasinghe RP, editors. Diseases in Asian aquaculture VI. Fish heal section. Philippines: Asian Fisheries Society; 2008. p. 355–78.
5.
go back to reference Lightner DV, Redman RM, Pantoja CR, Tang KFJ, Noble BL, Schofield P, et al. Historic emergence, impact and current status of shrimp pathogens in the Americas. J Invertebr Pathol. 2012;110(2):174–83.PubMedCrossRef Lightner DV, Redman RM, Pantoja CR, Tang KFJ, Noble BL, Schofield P, et al. Historic emergence, impact and current status of shrimp pathogens in the Americas. J Invertebr Pathol. 2012;110(2):174–83.PubMedCrossRef
6.
go back to reference Stentiford GD, Neil DM, Peeler EJ, Shields JD, Small HJ, Flegel TW, et al. Disease will limit future food supply from the global crustacean fishery and aquaculture sectors. J Invertebr Pathol. 2012;110(2):141–57.PubMedCrossRef Stentiford GD, Neil DM, Peeler EJ, Shields JD, Small HJ, Flegel TW, et al. Disease will limit future food supply from the global crustacean fishery and aquaculture sectors. J Invertebr Pathol. 2012;110(2):141–57.PubMedCrossRef
7.
go back to reference Shinn AP, Pratoomyot J, Griffiths D, Trong TQ, Vu NT, Jiravanichpaisal P, et al. Asian shrimp production and the economic costs of disease. Asian Fish Sci S. 2018;31:29–58. Shinn AP, Pratoomyot J, Griffiths D, Trong TQ, Vu NT, Jiravanichpaisal P, et al. Asian shrimp production and the economic costs of disease. Asian Fish Sci S. 2018;31:29–58.
8.
go back to reference Patil PK, Geetha R, Ravisankar T, Avunje S, Solanki HG, Abraham TJ, et al. Economic loss due to diseases in Indian shrimp farming with special reference to Enterocytozoon hepatopenaei (EHP) and white spot syndrome virus (WSSV). Aquaculture. 2021;533:736231.CrossRef Patil PK, Geetha R, Ravisankar T, Avunje S, Solanki HG, Abraham TJ, et al. Economic loss due to diseases in Indian shrimp farming with special reference to Enterocytozoon hepatopenaei (EHP) and white spot syndrome virus (WSSV). Aquaculture. 2021;533:736231.CrossRef
9.
go back to reference Lightner DV. A handbook of shrimp pathology and diagnostic procedures for diseases of cultured penaeid shrimp. Louisiana: World Aquaculture Society; 1996. Lightner DV. A handbook of shrimp pathology and diagnostic procedures for diseases of cultured penaeid shrimp. Louisiana: World Aquaculture Society; 1996.
10.
go back to reference Cavalli LS, Marins LFF, Netto SA, de Abreu PCOV. Evaluation of white spot syndrome virus (WSSV) in wild shrimp after a major outbreak in shrimp farms at Laguna, Southern Brazil. Atlantica. 2008;30(1):45–52. Cavalli LS, Marins LFF, Netto SA, de Abreu PCOV. Evaluation of white spot syndrome virus (WSSV) in wild shrimp after a major outbreak in shrimp farms at Laguna, Southern Brazil. Atlantica. 2008;30(1):45–52.
11.
go back to reference Yang F, He J, Lin X, Li Q, Pan D, Zhang X, et al. Complete genome sequence of the shrimp white spot bacilliform virus. J Virol. 2001;75(23):11811–20.PubMedPubMedCentralCrossRef Yang F, He J, Lin X, Li Q, Pan D, Zhang X, et al. Complete genome sequence of the shrimp white spot bacilliform virus. J Virol. 2001;75(23):11811–20.PubMedPubMedCentralCrossRef
12.
go back to reference Wang H-C, Hirono I, Maningas MBB, Somboonwiwat K, Stentiford G. ICTV report consortium. ICTV virus taxonomy profile: Nimaviridae. J Gen Virol. 2019;100(7):1053–4.PubMedCrossRef Wang H-C, Hirono I, Maningas MBB, Somboonwiwat K, Stentiford G. ICTV report consortium. ICTV virus taxonomy profile: Nimaviridae. J Gen Virol. 2019;100(7):1053–4.PubMedCrossRef
13.
go back to reference Vinaya Kumar K, Shekhar MS, Otta SK, Karthic K, Ashok Kumar J, Gopikrishna G, et al. First report of a complete genome sequence of White spot syndrome virus from India. Genome Announc. 2018;6(8):1–2.CrossRef Vinaya Kumar K, Shekhar MS, Otta SK, Karthic K, Ashok Kumar J, Gopikrishna G, et al. First report of a complete genome sequence of White spot syndrome virus from India. Genome Announc. 2018;6(8):1–2.CrossRef
14.
go back to reference Li F, Gao M, Xu L, Yang F. Comparative genomic analysis of three white spot syndrome virus isolates of different virulence. Virus Genes. 2017;53(2):249–58.PubMedCrossRef Li F, Gao M, Xu L, Yang F. Comparative genomic analysis of three white spot syndrome virus isolates of different virulence. Virus Genes. 2017;53(2):249–58.PubMedCrossRef
15.
go back to reference Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinforma. 2003;1:10–3. Delcher AL, Salzberg SL, Phillippy AM. Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinforma. 2003;1:10–3.
16.
go back to reference Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–45.PubMedPubMedCentralCrossRef Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–45.PubMedPubMedCentralCrossRef
17.
go back to reference Gao M, Li F, Xu L, Zhu X. White spot syndrome virus strains of different virulence induce distinct immune response in Cherax quadricarinatus. Fish Shellfish Immunol. 2014;39(1):17–23.PubMedCrossRef Gao M, Li F, Xu L, Zhu X. White spot syndrome virus strains of different virulence induce distinct immune response in Cherax quadricarinatus. Fish Shellfish Immunol. 2014;39(1):17–23.PubMedCrossRef
18.
go back to reference Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80.PubMedPubMedCentralCrossRef Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80.PubMedPubMedCentralCrossRef
19.
20.
go back to reference Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42.PubMedPubMedCentralCrossRef Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539–42.PubMedPubMedCentralCrossRef
21.
go back to reference Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674–6.PubMedCrossRef Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674–6.PubMedCrossRef
22.
go back to reference Chapman DAG, Tcherepanov V, Upton C, Dixon LK. Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. J Gen Virol. 2008;89(2):397–408.PubMedCrossRef Chapman DAG, Tcherepanov V, Upton C, Dixon LK. Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. J Gen Virol. 2008;89(2):397–408.PubMedCrossRef
25.
go back to reference Gorry PR, McPhee DA, Verity E, Dyer WB, Wesselingh SL, Learmont J, et al. Pathogenicity and immunogenicity of attenuated, nef-deleted HIV-1 strains in vivo. Retrovirology. 2007;4(1):66.PubMedPubMedCentralCrossRef Gorry PR, McPhee DA, Verity E, Dyer WB, Wesselingh SL, Learmont J, et al. Pathogenicity and immunogenicity of attenuated, nef-deleted HIV-1 strains in vivo. Retrovirology. 2007;4(1):66.PubMedPubMedCentralCrossRef
26.
go back to reference Schindler M, Münch J, Kutsch O, Li H, Santiago ML, Bibollet-Ruche F, et al. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell. 2006;125(6):1055–67.PubMedCrossRef Schindler M, Münch J, Kutsch O, Li H, Santiago ML, Bibollet-Ruche F, et al. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell. 2006;125(6):1055–67.PubMedCrossRef
28.
go back to reference Spatz SJ, Zhao Y, Petherbridge L, Smith LP, Baigent SJ, Nair V. Comparative sequence analysis of a highly oncogenic but horizontal spread-defective clone of Marek’s disease virus. Virus Genes. 2007;35(3):753–66.PubMedCrossRef Spatz SJ, Zhao Y, Petherbridge L, Smith LP, Baigent SJ, Nair V. Comparative sequence analysis of a highly oncogenic but horizontal spread-defective clone of Marek’s disease virus. Virus Genes. 2007;35(3):753–66.PubMedCrossRef
29.
go back to reference Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.PubMedCrossRef Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.PubMedCrossRef
30.
go back to reference Tsai J-M, Wang H-C, Leu J-H, Wang AH-J, Zhuang Y, Walker PJ, et al. Identification of the nucleocapsid, tegument, and envelope proteins of the shrimp white spot syndrome virus virion. J Virol. 2006;80(6):3021–9.PubMedPubMedCentralCrossRef Tsai J-M, Wang H-C, Leu J-H, Wang AH-J, Zhuang Y, Walker PJ, et al. Identification of the nucleocapsid, tegument, and envelope proteins of the shrimp white spot syndrome virus virion. J Virol. 2006;80(6):3021–9.PubMedPubMedCentralCrossRef
31.
go back to reference Akhila DS, Mani MK, Rai P, Condon K, Owens L, Karunasagar I. Antisense RNA mediated protection from white spot syndrome virus (WSSV) infection in Pacific white shrimp Litopenaeus vannamei. Aquaculture. 2015;435:306–9.CrossRef Akhila DS, Mani MK, Rai P, Condon K, Owens L, Karunasagar I. Antisense RNA mediated protection from white spot syndrome virus (WSSV) infection in Pacific white shrimp Litopenaeus vannamei. Aquaculture. 2015;435:306–9.CrossRef
32.
go back to reference Agüero M, Blasco R, Wilkinson P, Vinuela E. Analysis of naturally occurring deletion variants of African swine fever virus: multigene family 110 is not essential for infectivity or virulence in pigs. Virology. 1990;176(1):195–204.PubMedCrossRef Agüero M, Blasco R, Wilkinson P, Vinuela E. Analysis of naturally occurring deletion variants of African swine fever virus: multigene family 110 is not essential for infectivity or virulence in pigs. Virology. 1990;176(1):195–204.PubMedCrossRef
33.
go back to reference Marks H, van Duijse JJA, Zuidema D, van Hulten MCW, Vlak JM. Fitness and virulence of an ancestral white spot syndrome virus isolate from shrimp. Virus Res. 2005;110(1–2):9–20.PubMedCrossRef Marks H, van Duijse JJA, Zuidema D, van Hulten MCW, Vlak JM. Fitness and virulence of an ancestral white spot syndrome virus isolate from shrimp. Virus Res. 2005;110(1–2):9–20.PubMedCrossRef
34.
go back to reference Laramore SE, Scarpa J, Laramore CR, Lin J. Virulence variation of white spot syndrome virus in Pacific white shrimp Litopenaeus vannamei. J Aquat Anim Health. 2009;21(2):82–90.PubMedCrossRef Laramore SE, Scarpa J, Laramore CR, Lin J. Virulence variation of white spot syndrome virus in Pacific white shrimp Litopenaeus vannamei. J Aquat Anim Health. 2009;21(2):82–90.PubMedCrossRef
35.
go back to reference Marks H, Goldbach RW, Vlak JM, Van Hulten MCW. Genetic variation among isolates of white spot syndrome virus. Arch Virol. 2004;149(4):673–97.PubMedCrossRef Marks H, Goldbach RW, Vlak JM, Van Hulten MCW. Genetic variation among isolates of white spot syndrome virus. Arch Virol. 2004;149(4):673–97.PubMedCrossRef
36.
go back to reference Tan Y, Xing Y, Zhang H, Feng Y, Zhou Y, Shi Z-L. Molecular detection of three shrimp viruses and genetic variation of white spot syndrome virus in Hainan Province, China, in 2007. J Fish Dis. 2009;32(9):777–84.PubMedCrossRef Tan Y, Xing Y, Zhang H, Feng Y, Zhou Y, Shi Z-L. Molecular detection of three shrimp viruses and genetic variation of white spot syndrome virus in Hainan Province, China, in 2007. J Fish Dis. 2009;32(9):777–84.PubMedCrossRef
37.
38.
go back to reference Wang Y, Bininda-Emonds ORP, van Oers MM, Vlak JM, Jehle JA. The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes. 2011;42(3):444–56.PubMedCrossRef Wang Y, Bininda-Emonds ORP, van Oers MM, Vlak JM, Jehle JA. The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes. 2011;42(3):444–56.PubMedCrossRef
40.
go back to reference Wang Z, Chua HK, Gusti AARA, He F, Fenner B, Manopo I, et al. RING-H2 protein WSSV249 from white spot syndrome virus sequesters a shrimp ubiquitin-conjugating enzyme, PvUbc, for viral pathogenesis. J Virol. 2005;79(14):8764–72.PubMedPubMedCentralCrossRef Wang Z, Chua HK, Gusti AARA, He F, Fenner B, Manopo I, et al. RING-H2 protein WSSV249 from white spot syndrome virus sequesters a shrimp ubiquitin-conjugating enzyme, PvUbc, for viral pathogenesis. J Virol. 2005;79(14):8764–72.PubMedPubMedCentralCrossRef
41.
go back to reference He F, Fenner BJ, Godwin AK, Kwang J. White spot syndrome virus open reading frame 222 encodes a viral E3 ligase and mediates degradation of a host tumor suppressor via ubiquitination. J Virol. 2006;80(8):3884–92.PubMedPubMedCentralCrossRef He F, Fenner BJ, Godwin AK, Kwang J. White spot syndrome virus open reading frame 222 encodes a viral E3 ligase and mediates degradation of a host tumor suppressor via ubiquitination. J Virol. 2006;80(8):3884–92.PubMedPubMedCentralCrossRef
42.
go back to reference He F, Kwang J. Identification and characterization of a new E3 ubiquitin ligase in white spot syndrome virus involved in virus latency. Virol J. 2008;5(1):151.PubMedPubMedCentralCrossRef He F, Kwang J. Identification and characterization of a new E3 ubiquitin ligase in white spot syndrome virus involved in virus latency. Virol J. 2008;5(1):151.PubMedPubMedCentralCrossRef
43.
go back to reference Jeena K, Prasad KP, Pathan MK, Babu PG. Expression profiling of WSSV ORF 199 and shrimp ubiquitin conjugating enzyme in WSSV Infected Penaeus monodon. Asian-Australas J Anim Sci. 2012;25(8):1184.PubMedPubMedCentralCrossRef Jeena K, Prasad KP, Pathan MK, Babu PG. Expression profiling of WSSV ORF 199 and shrimp ubiquitin conjugating enzyme in WSSV Infected Penaeus monodon. Asian-Australas J Anim Sci. 2012;25(8):1184.PubMedPubMedCentralCrossRef
44.
go back to reference Liu Y, Wu J, Song J, Sivaraman J, Hew CL. Identification of a novel nonstructural protein, VP9, from white spot syndrome virus: its structure reveals a ferredoxin fold with specific metal binding sites. J Virol. 2006;80(21):10419–27.PubMedPubMedCentralCrossRef Liu Y, Wu J, Song J, Sivaraman J, Hew CL. Identification of a novel nonstructural protein, VP9, from white spot syndrome virus: its structure reveals a ferredoxin fold with specific metal binding sites. J Virol. 2006;80(21):10419–27.PubMedPubMedCentralCrossRef
45.
go back to reference Kawato S, Shitara A, Wang Y, Nozaki R, Kondo H, Hirono I. Crustacean genome exploration reveals the evolutionary origin of white spot syndrome virus. J Virol. 2019;93(3):e01144-e1218.PubMedPubMedCentralCrossRef Kawato S, Shitara A, Wang Y, Nozaki R, Kondo H, Hirono I. Crustacean genome exploration reveals the evolutionary origin of white spot syndrome virus. J Virol. 2019;93(3):e01144-e1218.PubMedPubMedCentralCrossRef
46.
go back to reference Liu W-J, Chang Y-S, Wang C-H, Kou G-H, Lo C-F. Microarray and RT-PCR screening for white spot syndrome virus immediate-early genes in cycloheximide-treated shrimp. Virology. 2005;334(2):327–41.PubMedCrossRef Liu W-J, Chang Y-S, Wang C-H, Kou G-H, Lo C-F. Microarray and RT-PCR screening for white spot syndrome virus immediate-early genes in cycloheximide-treated shrimp. Virology. 2005;334(2):327–41.PubMedCrossRef
47.
go back to reference Li F, Li M, Ke W, Ji Y, Bian X, Yan X. Identification of the immediate-early genes of white spot syndrome virus. Virology. 2009;385(1):267–74.PubMedCrossRef Li F, Li M, Ke W, Ji Y, Bian X, Yan X. Identification of the immediate-early genes of white spot syndrome virus. Virology. 2009;385(1):267–74.PubMedCrossRef
48.
go back to reference Zuo H, Chen C, Gao Y, Lin J, Jin C, Wang W. Regulation of shrimp PjCaspase promoter activity by WSSV VP38 and VP41B. Fish Shellfish Immunol. 2011;30(4–5):1188–91.PubMedCrossRef Zuo H, Chen C, Gao Y, Lin J, Jin C, Wang W. Regulation of shrimp PjCaspase promoter activity by WSSV VP38 and VP41B. Fish Shellfish Immunol. 2011;30(4–5):1188–91.PubMedCrossRef
49.
go back to reference Wang L, Zhi B, Wu W, Zhang X. Requirement for shrimp caspase in apoptosis against virus infection. Dev Comp Immunol. 2008;32(6):706–15.PubMedCrossRef Wang L, Zhi B, Wu W, Zhang X. Requirement for shrimp caspase in apoptosis against virus infection. Dev Comp Immunol. 2008;32(6):706–15.PubMedCrossRef
50.
go back to reference Van Hulten MCW, Reijns M, Vermeesch AMG, Zandbergen F, Vlak JM. Identification of VP19 and VP15 of white spot syndrome virus (WSSV) and glycosylation status of the WSSV major structural proteins. J Gen Virol. 2002;83(1):257–65.PubMedCrossRef Van Hulten MCW, Reijns M, Vermeesch AMG, Zandbergen F, Vlak JM. Identification of VP19 and VP15 of white spot syndrome virus (WSSV) and glycosylation status of the WSSV major structural proteins. J Gen Virol. 2002;83(1):257–65.PubMedCrossRef
51.
go back to reference Del Val M, Carrascosa JL, Vinuela E. Glycosylated components of African swine fever virus particles. Virology. 1986;152(1):39–49.PubMedCrossRef Del Val M, Carrascosa JL, Vinuela E. Glycosylated components of African swine fever virus particles. Virology. 1986;152(1):39–49.PubMedCrossRef
52.
go back to reference Julenius K, Mølgaard A, Gupta R, Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology. 2005;15(2):153–64.PubMedCrossRef Julenius K, Mølgaard A, Gupta R, Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology. 2005;15(2):153–64.PubMedCrossRef
54.
go back to reference van Hulten MCW, Goldbach RW, Vlak JM. Three functionally diverged major structural proteins of white spot syndrome virus evolved by gene duplication. J Gen Virol. 2000;81(10):2525–9.PubMedCrossRef van Hulten MCW, Goldbach RW, Vlak JM. Three functionally diverged major structural proteins of white spot syndrome virus evolved by gene duplication. J Gen Virol. 2000;81(10):2525–9.PubMedCrossRef
56.
go back to reference Le Francois BG, Maroun JA, Birnboim HC. Expression of thymidylate synthase in human cells is an early G 1 event regulated by CDK4 and p16INK4A but not E2F. Br J Cancer. 2007;97(9):1242.PubMedPubMedCentralCrossRef Le Francois BG, Maroun JA, Birnboim HC. Expression of thymidylate synthase in human cells is an early G 1 event regulated by CDK4 and p16INK4A but not E2F. Br J Cancer. 2007;97(9):1242.PubMedPubMedCentralCrossRef
57.
go back to reference Islam Z, Gurevic I, Strutzenberg TS, Ghosh AK, Iqbal T, Kohen A. Bacterial versus human thymidylate synthase: kinetics and functionality. PLoS ONE. 2018;13(5):e0196506.PubMedPubMedCentralCrossRef Islam Z, Gurevic I, Strutzenberg TS, Ghosh AK, Iqbal T, Kohen A. Bacterial versus human thymidylate synthase: kinetics and functionality. PLoS ONE. 2018;13(5):e0196506.PubMedPubMedCentralCrossRef
58.
go back to reference Carreras CW, Santi DV. The catalytic mechanism and structure of thymidylate synthase. Annu Rev Biochem. 1995;64(1):721–62.PubMedCrossRef Carreras CW, Santi DV. The catalytic mechanism and structure of thymidylate synthase. Annu Rev Biochem. 1995;64(1):721–62.PubMedCrossRef
59.
go back to reference Mu K, Tidona CA, Bahr U, Darai G, et al. Identification of a thymidylate synthase gene within the genome of Chilo iridescent virus. Virus Genes. 1998;17(3):243–58.CrossRef Mu K, Tidona CA, Bahr U, Darai G, et al. Identification of a thymidylate synthase gene within the genome of Chilo iridescent virus. Virus Genes. 1998;17(3):243–58.CrossRef
60.
go back to reference Jiang L, Xiao J, Liu L, Pan Y, Yan S, Wang Y. Characterization and prevalence of a novel white spot syndrome viral genotype in naturally infected wild crayfish, Procambarus clarkii, in Shanghai, China. Virusdisease. 2017;28(3):250–61.PubMedPubMedCentralCrossRef Jiang L, Xiao J, Liu L, Pan Y, Yan S, Wang Y. Characterization and prevalence of a novel white spot syndrome viral genotype in naturally infected wild crayfish, Procambarus clarkii, in Shanghai, China. Virusdisease. 2017;28(3):250–61.PubMedPubMedCentralCrossRef
61.
go back to reference Oakey HJ, Smith CS. Complete genome sequence of a white spot syndrome virus associated with a disease incursion in Australia. Aquaculture. 2018;484:152–9.CrossRef Oakey HJ, Smith CS. Complete genome sequence of a white spot syndrome virus associated with a disease incursion in Australia. Aquaculture. 2018;484:152–9.CrossRef
62.
go back to reference Rodriguez-Anaya LZ, Gonzalez-Galaviz JR, Casillas-Hernandez R, Lares-Villa F, Estrada K, Ibarra-Gamez JC, et al. Draft genome sequence of white spot syndrome virus isolated from cultured Litopenaeus vannamei in Mexico. Genome Announc. 2016;4(2):e01674-e1715.PubMedPubMedCentralCrossRef Rodriguez-Anaya LZ, Gonzalez-Galaviz JR, Casillas-Hernandez R, Lares-Villa F, Estrada K, Ibarra-Gamez JC, et al. Draft genome sequence of white spot syndrome virus isolated from cultured Litopenaeus vannamei in Mexico. Genome Announc. 2016;4(2):e01674-e1715.PubMedPubMedCentralCrossRef
63.
go back to reference Wang CH, Lo CF, Leu J-H, Chou C-M, Yeh PY, Chou HY, et al. Purification and genomic analysis of baculovirus associated with white spot syndrome (WSBV) of Penaeus monodon. Dis Aquat Organ. 1995;23(3):239–42.CrossRef Wang CH, Lo CF, Leu J-H, Chou C-M, Yeh PY, Chou HY, et al. Purification and genomic analysis of baculovirus associated with white spot syndrome (WSBV) of Penaeus monodon. Dis Aquat Organ. 1995;23(3):239–42.CrossRef
64.
go back to reference Kumar KV, Shekhar MS, Otta SK, Karthic K, Kumar JA, Gopikrishna G, et al. First report of a complete genome sequence of white spot syndrome virus from India. Genome Announc. 2018;6(8):e00055-18.CrossRef Kumar KV, Shekhar MS, Otta SK, Karthic K, Kumar JA, Gopikrishna G, et al. First report of a complete genome sequence of white spot syndrome virus from India. Genome Announc. 2018;6(8):e00055-18.CrossRef
65.
go back to reference Chai CY, Yoon J, Lee YS, Kim YB, Choi T-J. Analysis of the complete nucleotide sequence of a white spot syndrome virus isolated from Pacific white shrimp. J Microbiol. 2013;51(5):695–9.PubMedCrossRef Chai CY, Yoon J, Lee YS, Kim YB, Choi T-J. Analysis of the complete nucleotide sequence of a white spot syndrome virus isolated from Pacific white shrimp. J Microbiol. 2013;51(5):695–9.PubMedCrossRef
66.
go back to reference Restrepo L, Reyes A, Bajaña L, Betancourt I, Bayot B. Draft genome sequence of a white spot syndrome virus isolate obtained in Ecuador. Genome Announc. 2018;6(26):e00605-e618.PubMedPubMedCentralCrossRef Restrepo L, Reyes A, Bajaña L, Betancourt I, Bayot B. Draft genome sequence of a white spot syndrome virus isolate obtained in Ecuador. Genome Announc. 2018;6(26):e00605-e618.PubMedPubMedCentralCrossRef
Metadata
Title
MRF: a tool to overcome the barrier of inconsistent genome annotations and perform comparative genomics studies for the largest animal DNA virus
Authors
Karthic Krishnan
Vinaya Kumar Katneni
Sudheesh K. Prabhudas
Nimisha Kaikkolante
Ashok Kumar Jangam
Upendra Kumar Katneni
Chris Hauton
Luca Peruzza
Shashi Shekhar Mudagandur
Vijayan K. Koyadan
Jithendran Karingalakkandy Poochirian
Joykrushna Jena
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2023
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-023-02035-w

Other articles of this Issue 1/2023

Virology Journal 1/2023 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
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.