Skip to main content

Advertisement

Springer Nature Link
Log in

Genome recoding: a review of basic concepts, current research and future prospects of virus attenuation for controlling plant viral diseases

  • Review Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Plants are very susceptible to pathogens and every year, 25% of crop loss is caused by various types of pathogens including viruses. Many different strategies are being used for developing resistance against virus infection, including RNA silencing, and the genome editing including CRISPR-Cas-9 but these may produce variants/recombinants and could cause the problems for future crops. Another promising approach named as genome recoding or rewriting would be a better potential tool for controlling viral infections in plants. It relies on the concepts of replacement of synonymous codons, change in codon bias, codon pair bias and dinucleotide content. Recoding of the genome does not alter the amino acid sequences but it affects the expression level and translation efficiency. In the present report, the concept of synonymous codons, the basics of genome recoding and the possible strategies to generate genome recoded organisms are provided in details. Viral attenuation has been achieved by consideration of dinucleotide bias and codon pair bias manipulations and used in the synthesis of vaccines against various types of pathogenic bacteria and viruses. The idea of the future scope of genome recoding for developing virus-resistant plants and their challenges for the same are also comprehensively discussed. Although genome recoding is not yet tested on plants, however it could be very helpful in controlling plant viral diseases. So, it is a novel emerging area of research for developing viral resistant plants and thus would help in minimizing the agricultural losses in the near future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

CAI:

Codon adaptation index

CPS:

Codon pair score

CPB:

Codon pair bias

MAGE:

Multiplex automated genome engineering

CAGE:

Conjugative assembly genome engineering

CRISPR:

Clustered regularly interspaced short palindromic repeats

Cas9:

CRISPR associated protein9

GRO:

Genome recoded organisms

References

  • Agrawal N, Dasaradhi PVN, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK (2003) RNA interference: biology, mechanism and applications. Microbial Mol Biol Rev 67:657–685

    CAS  Google Scholar 

  • Ali Z, Abulfaraj A, Idris A et al (2015) CRISPR/Cas9 mediated viral interference in plants. Genome Biol 16:238

    PubMed  PubMed Central  Google Scholar 

  • Ali Z, Ali S, Tashkandi M (2016) CRISPR/Cas9-mediated immunity to geminiviruses: differential interference and evasion. Sci Rep 6:26912

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asano M, Satoh R, Mochizuki A et al (2005) Tobamovirus-resistant tobacco generated by RNA interference directed against host genes. FEBS Lett 579:4479–4484

    CAS  PubMed  Google Scholar 

  • Atkinson NJ, Witteveldt J, Evans DJ, Simmonds P (2014) The influence of CpG and UpA dinucleotide frequencies on RNA virus replication and characterization of the innate cellular pathways underlying virus attenuation and enhanced replication. Nucleic Acids Res 42:4527–4545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bacher JM, Waas WF, Metzgar D, Crécy-Lagard V, Schimmel P (2007) Genetic code ambiguity confers a selective advantage on Acinetobacter baylyi. J Bacteriol 189:6494–6496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baulcombe DC (1996) Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 18:1833–1844

    Google Scholar 

  • Bazzini AA, Asurmendi S, Hopp HE, Beachy RN (2006) Tobacco mosaic virus (TMV) and potato virus X (PVX) coat proteins confer heterologous interference to PVX and TMV infection, respectively. J Gen Virol 87:1005–1012

    CAS  PubMed  Google Scholar 

  • Bendahmane M, Chen I, Asurmendi S et al (2007) Coat protein-mediated resistance to TMV infection of Nicotiana tabacum involves multiple modes of interference by coat protein. Virology 366:107–116

    CAS  PubMed  Google Scholar 

  • Botzman M, Margalit H (2011) Variation in global codon usuage bias among prokaryotic organisms is assocaited with their lifestyles. Genome Biol 12:R1–9

    Google Scholar 

  • Brule CE, Grayhack EJ (2017) Synonymous codons: choose wisely for expression. Trends Genet 33:283–297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burns CC, Campagnoli R, Shaw J et al (2009) Genetic inactivation of poliovirus infectivity by increasing the frequencies of CpG and UpA dinucleotides within and across synonymous capsid region codons. J Virol 83:9957–9969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burns CC, Shaw J, Campagnoli R et al (2006) Modulation of poliovirus replicative fitness in HeLa cells by deoptimization of synonymous codon usage in the capsid region. J Virol 80:3259–3272

    CAS  PubMed  PubMed Central  Google Scholar 

  • Camiolo S, Farina L, Porceddu A (2012) The relation of codon bias to tissue-specific gene expression in Arabidopsis thaliana. Genetics 192:641–649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cannarozzi G, Schraudolph NN, Faty M et al (2010) A role for codon order in translation dynamics. Cell 141:355–357

    PubMed  Google Scholar 

  • Cardinale DJ, DeRosa K, Duffy S (2013) Base composition and translational selection are insufficient to explain codon usage bias in plant viruses. Viruses 5:162–181

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carrau L, Rezelj VV, Noval MG et al (2019) Chikungunya virus vaccine candidates with decreased mutational robustness are attenuated in vivo and have compromised transmissibility. J Virol 93(18):e00775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chewachong GM, Miller SA, Blakeslee JJ et al (2015) Generation of an attenuated, cross-protective Pepino mosaic virus variant through alignment-guided mutagenesis of the viral capsid protein. Phytopathol 105:126–134

    CAS  Google Scholar 

  • Coleman JR, Papamichail D, Skiena S et al (2008) Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784–1787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crick FH (1966) Codon-anticodon pairing: the wobble hypothesis. J Mol Biol 19:548–555

    CAS  PubMed  Google Scholar 

  • Diaz-San Segundo F, Medina GN, Ramirez-Medina E et al (2016) Synonymous deoptimization of foot-and-mouth disease virus causes attenuation in vivo while inducing a strong neutralizing antibody response. J Virol 90:1298–1310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eschke K, Trimpert J, Osterrieder N, Kunec D (2018) Attenuation of a very virulent marek's disease herpervirus (MDV) by codon pair bias deoptimization. Plos Pathog 14:e1006857

    PubMed  PubMed Central  Google Scholar 

  • Flanagan EB, Zamparo JM, Ball LA et al (2001) Rearrangement of the genes of vesicular stomatitis virus eliminates clinical disease in the natural host: new strategy for vaccine development. J Virol 75:6107–6114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs M, Gonsalves D (2007) Safety of virus-resistant transgenic plants two decades after their introduction: lessons from realistic field risk assessment studies. Annu Rev Phytopathol 45:173–202

    CAS  PubMed  Google Scholar 

  • Gingold H, Pilpel Y (2011) Determinants of translation efficiency and accuracy. Mol Syst Biol 7:481

    PubMed  PubMed Central  Google Scholar 

  • Goto T, Iizuka N, Komochi S (1984) Selection and utilization of an attenuated isolate of pepper strain of tobacco mosaic virus. Jpn J Phytopathol 50:221–228

    Google Scholar 

  • Greenbaum BD, Rabadan R, Levine AJ (2009) Patterns of oligonucleotide sequences in viral and host cell RNA identify mediators of the host innate immune system. PLoS ONE 4:e5969

    PubMed  PubMed Central  Google Scholar 

  • Hodgkinson A, Eyre-Walker A (2011) Variation in the mutation rate across mammalian genomes. Nat Rev Genet 12:756

    CAS  PubMed  Google Scholar 

  • Holmes FO (1934) A masked strain of tobacco-mosaic virus. Phytopathol 24:845–873

    Google Scholar 

  • Huang XD, Fang L, Gu QS, Tian YP, Geng C, Li XD (2019) Cross protection against the watermelon strain of Papaya ringspot virus through modification of viral RNA silencing suppressor. Virus Res 265:166–171

    CAS  PubMed  Google Scholar 

  • Hutchison CA, Chuang RY, Noskov VN et al (2016) Design and synthesis of a minimal bacterial genome. Science 351:6280

    Google Scholar 

  • Isaacs FJ, Carr PA, Wang HH et al (2011) Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333:348–353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ji X, Zhang H, Zhang Y, Wang Y, Gao C (2015) Establishing a CRISPR–Cas-like immune system conferring DNA virus resistance in plants. Nat Plant 1:15144

    CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323

    CAS  PubMed  Google Scholar 

  • Karlin S, Ladunga I (1994) Comparisons of eukaryotic genomic sequences. Proc Natl Acad Sci USA 91:12832–12836

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kosaka Y, Fukunishi T (1993) Attenuated isolates of soybean mosaic virus derived at a low temperature. Plant Dis 77:882–886

    Google Scholar 

  • Kosaka Y, Ryang BS, Kobori T, Shiomi H et al (2006) Effectiveness of an attenuated Zucchini yellow mosaic virus isolate for cross-protecting cucumber. Plant Dis 90:67–72

    CAS  PubMed  Google Scholar 

  • Kumagai Y, Takeuchi O, Akira S (2008) TLR9 as a key receptor for the recognition of DNA. Adv Drug Deliver Rev 60:795–804

    CAS  Google Scholar 

  • Kunec D, Osterrieder N (2016) Codon pair bias is a direct consequence of dinucleotide bias. Cell Rep 14:55–67

    CAS  PubMed  Google Scholar 

  • Kuo J, Stirling F, Lau YH, Shulgina Y, Way JC, Silver PA (2018) Synthetic genome recoding: new genetic codes for new features. Curr Genet 64:327–333

    CAS  PubMed  Google Scholar 

  • Lajoie MJ, Kosuri S, Mosberg JA, Gregg CJ, Zhang D, Church GM (2013a) Probing the limits of genetic recoding in essential genes. Science 342:361–363

    CAS  PubMed  Google Scholar 

  • Lajoie MJ, Rovner AJ, Goodman DB et al (2013b) Genomically recoded organisms expand biological functions. Science 342:357–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lau YH, Stirling F, Kuo J et al (2017) Large-scale recoding of a bacterial genome by iterative recombineering of synthetic DNA. Nucleic Acids Res 45:6971–6980

    CAS  PubMed  PubMed Central  Google Scholar 

  • Le Nouën C, Brock LG, Luongo C et al (2014) Attenuation of human respiratory syncytial virus by genome-scale codon-pair deoptimization. Proc Nat Acad Sci 111:13169–13174

    PubMed  PubMed Central  Google Scholar 

  • Li J, Zhou J, Wu Y, Yang S, Tian D (2015) GC-content of synonymous codons profoundly influences amino acid usage. G3-Genes Genom Genet 5:2017–3026

    Google Scholar 

  • Li P, Ke X, Wang T, Tan Z, Luo D, Miao Y et al (2018) Zika virus attenuation by codon pair deoptimization induces sterilizing immunity in mouse models. J Virol 92:e00701–e718

    PubMed  PubMed Central  Google Scholar 

  • Lin SS, Henriques R, Wu HW, Niu QW, Yeh SD, Chua NH (2007) Strategies and mechanisms of plant virus resistance. Plant Biotechnol Rep 1:125–134

    Google Scholar 

  • Liu CC, Schultz PG (2010) Adding new chemistries to the genetic code. Annu Rev Biochem 79:413–444

    CAS  PubMed  Google Scholar 

  • Ma JN, Isaacs FJ (2016) Genomic recoding broadly obstructs the propagation of horizontally transferred genetic elements. Cell Syst 3:199–207

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez MA, Jordan-Paiz A, Franco S, Nevot M (2016) Synonymous virus genome recoding as a tool to impact viral fitness. Trends Microbiol 24:134–147

    PubMed  Google Scholar 

  • Martrus G, Nevot M, Andres C, Clotet B, Martinez MA (2013) Changes in codon-pair bias of human immunodeficiency virus type 1 have profound effects on virus replication in cell culture. Retrovirology 10:78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Motoyoshi F, Nishiguchi M (1988) Control of virus diseases by attenuated virus strains: comparison between attenuated strains of cucumber green mottle mosaic virus and tobacco mosaic virus. Gamma Field Symp Inst Radiat Breed Natl Inst Agrobiol Resour 27:91–109

    Google Scholar 

  • 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 80:9687–9696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Murray EE, Lotzer J, Eberle M (1989) Codon usage in plant genes. Nucleic Acid Res 17:477–498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakazono-Nagaoka E, Takahashi T, Shimizu T, Kosaka Y et al (2009) Cross-protection against bean yellow mosaic virus (BYMV) and clover yellow vein virus by attenuated BYMV isolate M11. Phytopathol 99:251–257

    CAS  Google Scholar 

  • Nishiguchi M, Kobayashi K (2011) Attenuated plant viruses: preventing virus diseases and understanding the molecular mechanism. J Gen Plant Pathol 77:221–229

    Google Scholar 

  • Nogales A, Baker SF, Ortiz-Riaño E, Dewhurst S, Topham DJ, Martínez-Sobrido L (2014) Influenza A virus attenuation by codon deoptimization of the NS gene for vaccine development. J Virol 88:10525–10540

    PubMed  PubMed Central  Google Scholar 

  • Nougairede A, De Fabritus L, Aubry F, Gould EA, Holmes EC, de Lamballerie X (2013) Random codon re-encoding induces stable reduction of replicative fitness of Chikungunya virus in primate and mosquito cells. Plos Pathog 9:e1003172

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ostrov N, Landon M, Guell M et al (2016) Design, synthesis, and testing toward a 57-codon genome. Science 353:819–822

    CAS  PubMed  Google Scholar 

  • Paul P, Malakar AK, Chakraborty S (2018) Compositional bias coupled with selection and mutation pressure drives codon usage in Brassica compestris genes. Food Sci Biotechnol 27:725–733

    CAS  PubMed  Google Scholar 

  • Pechmann S, Frydman J (2013) Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat Struct Mol Biol 20:237

    CAS  PubMed  Google Scholar 

  • Pixley KV, Falck-Zepeda JB, Giller KE et al (2019) Genome editing, gene drives, and synthetic biology: will they contribute to disease-resistant crops, and who will benefit. Ann Rev Phytopathol 57:165–188

    CAS  Google Scholar 

  • Prabha R, Singh DP, Sinha S, Ahmad K, Rai A (2017) Genome-wide comparative analysis of codon usage bias and codon context patterns among cyanobacterial genomes. Mar Genomics 32:31–39

    PubMed  Google Scholar 

  • Prins M, Laimer M, Noris E et al (2008) Strategies for antiviral resistance in transgenic plants. Mol Plant Pathol 9:73–83

    CAS  PubMed  Google Scholar 

  • Quax TEF, Claassens NJ, Söll D, Oost JVD (2015) Codon bias as a means to fine-tune gene expression. Mol Cell 59:149–161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ratcliff FG, MacFarlane SA, Baulcombe DC (1999) Gene silencing without DNA: RNA-mediated cross-protection between viruses. Plant Cell 11:1207–1215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha EP (2004) Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14:2279–2286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Samson JE, Moineau S (2013) Bacteriophages in food fermentations: new frontiers in a continuous arms race. Annu Rev Food Sci Technol 4:347–368

    CAS  PubMed  Google Scholar 

  • Sayama H, Sato T, Kominato M, Natsuaki T, Kaper JM (1993) Field testing of a satellite-containing attenuated strain of cucumber mosaic virus for tomato protection in Japan. Phytopathol 83:405–410

    CAS  Google Scholar 

  • Scholthof KBG, Adkins S, Czosnek H et al (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp PM, Li WH (1987) The codon Adaptation Index–a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen SH, Stauft CB, Gorbatsevych O et al (2015) Large-scale recoding of an arbovirus genome to rebalance its insect versus mammalian preference. Proc Natl Acad Sci USA 112:4749–4754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takata MA, Goncalves-Carbeiro D, Zang TM, Soll SJ et al (2017) CG dinucleotide suppression enables antiviral defense targeting non-self RNA. Nature 550:124–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tulloch F, Atkinson NJ, Evans DJ, Ryan MD, Simmonds P (2014) RNA virus attenuation by codon pair deoptimization is an artefact of increases in CpG/UpA dinucleotide frequencies. Elife 3:e04531

    PubMed  PubMed Central  Google Scholar 

  • Tuorto F, Lyko F (2016) Genome recoding by tRNA modifications. Open Biol 6:160287

    PubMed  PubMed Central  Google Scholar 

  • Uniyal AP, Mansotra K, Yadav SK, Kumar V (2019a) An overview of designing and selection of sgRNAs for precise genome editing by the CRISPR-Cas9 system in plants. 3 Biotech 9:223

    PubMed  PubMed Central  Google Scholar 

  • Uniyal AP, Yadav SK, Kumar V (2019b) The CRISPR-Cas9, Genome editing approach: a promising tool for drafting defense strategy against begomoviruses including cototn leaf curl viruses. J Plant Biochem Biotechnol 28:121–132

    CAS  Google Scholar 

  • Varsani A, Lefeuvre P, Roumagnac P, Martin D (2018) Notes on recombination and reassortment in multipartite/segmented viruses. Curr Opin Virol 33:156–166

    CAS  PubMed  Google Scholar 

  • Velazquez-Salinas L, Risatti GR, Holinka LG et al (2016) Recoding structural glycoprotein E2 in classical swine fever virus (CSFV) produces complete virus attenuation in swine and protects infected animals against disease. Virol 494:178–189

    CAS  Google Scholar 

  • Wang B, Yang C, Tekes G, Mueller S, Paul A, Whelan SP, Wimmer E (2015) Recoding of the vesicular stomatitis virus L gene by computer-aided design provides a live, attenuated vaccine candidate. MBio 6:e00237–e315

    PubMed  PubMed Central  Google Scholar 

  • Wang L, Huixian X, Yancho Y et al (2018) Genome-wide analysis of codon usage bias in four sequenced cotton species. PLoS ONE 13:e0194372

    PubMed  PubMed Central  Google Scholar 

  • Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87:23–29

    CAS  PubMed  Google Scholar 

  • Xiao H, Nasertorabi F, Choi SH, Han GW, Reed SA, Stevens RC, Schultz PG (2015) Exploring the potential impact of an expanded genetic code on protein function. Proc Natl Acad Sci USA 112:6961–6966

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XZ, Liu QP, Fan LJ, Cui XF, Zhou XP (2008) Analysis of synonymous codon usage and evolution of begomoviruses. J Zhejiang Uni Sci B 9:667–674

    CAS  Google Scholar 

  • Yang G, Qiu BS, Liu XG, Li Y, Wang XF (2002) Nonsense mutations of replicase and movement protein genes contribute to the attenuation of an avirulent tomato mosaic virus. Virus Res 87:119–128

    CAS  PubMed  Google Scholar 

  • Yeh SD, Gonsalves D (1984) Evaluation of induced mutants of papaya ringspot virus for control by cross protection. Phytopathol 74:1086–1091

    Google Scholar 

  • Zhang T, Zheng Q, Yi X, An H, Zhao Y, Ma S, Zhou G (2018) Establishing RNA virus resistance in plants by harnessing CRISPR immune system. Plant Biotechnol J 16:1415–1423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XH, Tee LY, Wang XG, Huang QS, Yang SH (2015) Off-target effects in CRISPR/Cas9-mediated genome engineering. Mol Ther Nucleic Acids 4:e264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YM, Shao ZQ, Yang LT et al (2013) Non-random arrangement of synonymous codons in archaea coding sequences. Genomics 101:362–367

    CAS  PubMed  Google Scholar 

  • Zhao Y, Zheng H, Xu A et al (2016) Analysis of codon usage bias of envelope glycoprotein genes in nuclear polyhedrosis virus (NPV) and its relation to evolution. BMC Genomics 17:677

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors express gratitude to Vice Chancellor of Central University of Punjab, India for providing necessary support for present work. “UGC-BSR start up grant” sanctioned to Vinay Kumar, who sponsors this research.

Author information

Authors and Affiliations

  1. Department of Botany, School of Basic and Applied Sciences, Central University of Punjab, Bathinda, 151001, India

    Vinay Kumar & Tanya Singh

Authors
  1. Vinay Kumar
    View author publications

    Search author on:PubMed Google Scholar

  2. Tanya Singh
    View author publications

    Search author on:PubMed Google Scholar

Contributions

VK conceived and designed the present research. VK conducted the experiments. VK analyzed the data. VK and TS wrote the manuscript. All the authors read and approved the manuscript.

Corresponding author

Correspondence to Vinay Kumar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, V., Singh, T. Genome recoding: a review of basic concepts, current research and future prospects of virus attenuation for controlling plant viral diseases. J. Plant Biochem. Biotechnol. 30, 221–232 (2021). https://doi.org/10.1007/s13562-020-00583-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-020-00583-8

Keywords

Profiles

  1. Vinay Kumar View author profile