An Evolutionary Perspective of Codon Usage Pattern, Dinucleotide Composition and Codon Pair Bias in Prunus Necrotic Ringspot Virus

Prunus necrotic ringspot virus (PNRSV) is a significant virus of ornamental plants and fruit trees. It is essential to study this virus due to its impact on the horticultural industry. Several studies on PNRSV diversity and phytosanitary detection technology were reported, but the content on the codon usage bias (CUB), dinucleotide preference and codon pair bias (CPB) of PNRSV is still uncertain. We performed comprehensive analyses on a dataset consisting of 359 coat protein (CP) gene sequences in PNRSV to examine the characteristics of CUB, dinucleotide composition, and CPB. The CUB analysis of PNRSV CP sequences showed that it was not only affected by natural selection, but also affected by mutations, and natural selection played a more significant role compared to mutations as the driving force. The dinucleotide composition analysis showed an over-expression of the CpC/GpA dinucleotides and an under-expression of the UpA/GpC dinucleotides. The dinucleotide composition of the PNRSV CP gene showed a weak association with the viral lineages and hosts, but a strong association with viral codon positions. Furthermore, the CPB of PNRSV CP gene is low and is related to dinucleotide preference and codon usage patterns. This research provides reference for future research on PNRSV genetic diversity and gene evolution mechanism.

[1]  Zhen He,et al.  Compositional biases and evolution of the largest plant RNA virus order Patatavirales. , 2023, International journal of biological macromolecules.

[2]  Zhen He,et al.  Evolution and host adaptability of plant RNA viruses: Research insights on compositional biases , 2022, Computational and structural biotechnology journal.

[3]  Xiaowei Xu,et al.  Synonymous Codon Usage Analysis of Three Narcissus Potyviruses , 2022, Viruses.

[4]  V. Bhadana,et al.  Codon usage bias , 2021, Molecular Biology Reports.

[5]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation , 2021, Nucleic Acids Res..

[6]  Haifeng Gan,et al.  Phylodynamics and Codon Usage Pattern Analysis of Broad Bean Wilt Virus 2 , 2021, Viruses.

[7]  Haifeng Gan,et al.  Comprehensive codon usage analysis of rice black-streaked dwarf virus based on P8 and P10 protein coding sequences. , 2020, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[8]  N. Habili,et al.  Molecular characterization and pathogenicity analysis of prunus necrotic ringspot virus isolates from China rose (Rosa chinensis Jacq.) , 2020, Archives of Virology.

[9]  Haifeng Gan,et al.  Genetic changes and host adaptability in sugarcane mosaic virus based on complete genome sequences. , 2020, Molecular phylogenetics and evolution.

[10]  P. Simmonds,et al.  Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection , 2020, mBio.

[11]  Olga Chernomor,et al.  IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era , 2019, bioRxiv.

[12]  Q. Ma,et al.  Complete genome sequences of five prunus necrotic ringspot virus isolates from Inner Mongolia of China and comparison to other PNRSV isolates around the world , 2019, Journal of Plant Pathology.

[13]  G. Franzo,et al.  Genetic Analysis and Evolutionary Changes of Porcine Circovirus 2. , 2019, Molecular phylogenetics and evolution.

[14]  Haifeng Gan,et al.  Analysis of Synonymous Codon Usage Bias in Potato Virus M and Its Adaption to Hosts , 2019, Viruses.

[15]  G. Ebel,et al.  Effects of Arbovirus Multi-Host Life Cycles on Dinucleotide and Codon Usage Patterns , 2019, Viruses.

[16]  L. Poon,et al.  Dinucleotide evolutionary dynamics in influenza A virus , 2019, Virus evolution.

[17]  Richard F. Lee,et al.  Codon Usage Bias Analysis of Citrus tristeza virus: Higher Codon Adaptation to Citrus reticulata Host , 2019, Viruses.

[18]  M. Veit,et al.  Genetic Evolution and Molecular Selection of the HE Gene of Influenza C Virus , 2019, Viruses.

[19]  Shuo Su,et al.  Evolutionary changes of the novel Influenza D virus hemagglutinin-esterase fusion gene revealed by the codon usage pattern , 2018, Virulence.

[20]  Jiyong Zhou,et al.  Insights into the genetic and host adaptability of emerging porcine circovirus 3 , 2018, Virulence.

[21]  Cheng-qiang He,et al.  Evolution of rice stripe virus. , 2017, Molecular phylogenetics and evolution.

[22]  M. Shi,et al.  Dinucleotide Composition in Animal RNA Viruses Is Shaped More by Virus Family than by Host Species , 2017, Journal of Virology.

[23]  A. Anyamba,et al.  Rift Valley Fever: An Emerging Mosquito-Borne Disease. , 2016, Annual review of entomology.

[24]  W. Chen,et al.  COMPLETE GENOMIC SEQUENCE OF A SWEET CHERRY ISOLATE OF PRUNUS NECROTIC RINGSPOT VIRUS FROM CHINA , 2016 .

[25]  Nikolaus Osterrieder,et al.  Codon Pair Bias Is a Direct Consequence of Dinucleotide Bias. , 2016, Cell reports.

[26]  A. Butt,et al.  Evolution of codon usage in Zika virus genomes is host and vector specific , 2016, Emerging microbes & infections.

[27]  Gongwei Wang,et al.  Genetic diversity of Prunus necrotic ringspot virus infecting stone fruit trees grown at seven regions in China and differentiation of three phylogroups by multiplex RT-PCR , 2015 .

[28]  A. Saha,et al.  Phylogeny and synonymous codon usage pattern of Papaya ringspot virus coat protein gene in the sub-Himalayan region of north-east India. , 2015, Canadian journal of microbiology.

[29]  Charles B. Ward,et al.  Large-scale recoding of an arbovirus genome to rebalance its insect versus mammalian preference , 2015, Proceedings of the National Academy of Sciences.

[30]  B. Murrell,et al.  RDP4: Detection and analysis of recombination patterns in virus genomes , 2015, Virus evolution.

[31]  S. Behura,et al.  Antagonistic relationships between intron content and codon usage bias of genes in three mosquito species: functional and evolutionary implications , 2013, Evolutionary applications.

[32]  I. Belalov,et al.  Causes and Implications of Codon Usage Bias in RNA Viruses , 2013, PloS one.

[33]  M. Sánchez-Pina,et al.  Ilarviruses of Prunus spp.: a continued concern for fruit trees. , 2012, Phytopathology.

[34]  Raul Rabadan,et al.  Codon usage bias and the evolution of influenza A viruses. Codon Usage Biases of Influenza Virus , 2010, BMC Evolutionary Biology.

[35]  S. Garcia-Vallvé,et al.  RCDI/eRCDI: a web-server to estimate codon usage deoptimization , 2010, BMC Research Notes.

[36]  V. Pallás,et al.  Implication of the C terminus of the Prunus necrotic ringspot virus movement protein in cell-to-cell transport and in its interaction with the coat protein. , 2010, The Journal of general virology.

[37]  Andreas Tauch,et al.  Virus-Host Coevolution: Common Patterns of Nucleotide Motif Usage in Flaviviridae and Their Hosts , 2009, PloS one.

[38]  D. Willner,et al.  Metagenomic signatures of 86 microbial and viral metagenomes. , 2009, Environmental microbiology.

[39]  J. R. Coleman,et al.  Virus Attenuation by Genome-Scale Changes in Codon Pair Bias , 2008, Science.

[40]  V. Hallan,et al.  Incidence of Prunus necrotic ring spot virus on Malus domestica in India , 2008 .

[41]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[42]  Joel Arrais,et al.  Large Scale Comparative Codon-Pair Context Analysis Unveils General Rules that Fine-Tune Evolution of mRNA Primary Structure , 2007, PloS one.

[43]  David Posada,et al.  An Exact Nonparametric Method for Inferring Mosaic Structure in Sequence Triplets , 2007, Genetics.

[44]  Ian Stansfield,et al.  tRNA properties help shape codon pair preferences in open reading frames , 2006, Nucleic acids research.

[45]  Manuel A. S. Santos,et al.  Comparative context analysis of codon pairs on an ORFeome scale , 2005, Genome Biology.

[46]  J. Novembre.  Accounting for background nucleotide composition when measuring codon usage bias. , 2002, Molecular biology and evolution.

[47]  M. Glasa,et al.  Biological and molecular characterisation of Prunus necrotic ringspot virus isolates and possible approaches to their phylogenetic typing , 2002 .

[48]  K. Crandall,et al.  Evaluation of methods for detecting recombination from DNA sequences: Computer simulations , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Mark J. Gibbs,et al.  Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences , 2000, Bioinform..

[50]  H. Romero,et al.  Codon usage in Chlamydia trachomatis is the result of strand-specific mutational biases and a complex pattern of selective forces. , 2000, Nucleic acids research.

[51]  V. Pallás,et al.  Molecular Variability Among Isolates of Prunus Necrotic Ringspot Virus from Different Prunus spp. , 1999, Phytopathology.

[52]  N. Sueoka,et al.  Translation-coupled violation of Parity Rule 2 in human genes is not the cause of heterogeneity of the DNA G+C content of third codon position. , 1999, Gene.

[53]  J. Bol.  Alfalfa mosaic virus and ilarviruses: involvement of coat protein in multiple steps of the replication cycle. , 1999, The Journal of general virology.

[54]  L. Duret,et al.  Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Etsuko N. Moriyama,et al.  Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli , 1998, Nucleic Acids Res..

[56]  N. Mcferran,et al.  Dinucleotide and stop codon frequencies in single-stranded RNA viruses. , 1997, The Journal of general virology.

[57]  S Karlin,et al.  Compositional differences within and between eukaryotic genomes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  D. Burke,et al.  Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. , 1995, AIDS research and human retroviruses.

[59]  G. W. Hatfield,et al.  Codon Pair Utilization Biases Influence Translational Elongation Step Times (*) , 1995, The Journal of Biological Chemistry.

[60]  S. Karlin,et al.  Dinucleotide relative abundance extremes: a genomic signature. , 1995, Trends in genetics : TIG.

[61]  John Maynard Smith,et al.  Analyzing the mosaic structure of genes , 1992, Journal of Molecular Evolution.

[62]  G. W. Hatfield,et al.  Nonrandom utilization of codon pairs in Escherichia coli. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[63]  T. Miyata,et al.  Secondary structure of MS2 phage RNA and bias in code word usage. , 1979, Nucleic acids research.

[64]  K. R. Bock.  Strains of Prunus necrotic ringspot virus in hop (Humulus lupulus L.) , 1967 .

[65]  F. Supek.  The Code of Silence: Widespread Associations Between Synonymous Codon Biases and Gene Function , 2015, Journal of Molecular Evolution.

[66]  V. Pallás,et al.  Evolutionary relationships in the ilarviruses: nucleotide sequence of prunus necrotic ringspot virus RNA 3. , 1997, Archives of virology.

[67]  S. Scott,et al.  Important Diseases of Prunus Caused by Viruses and Other Graft-Transmissible Pathogens in California and South Carolina , 1992 .

[68]  J A Koziol,et al.  Evolution of the genome and the genetic code: selection at the dinucleotide level by methylation and polyribonucleotide cleavage. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Wen-Hsiung Li,et al.  An evolutionary perspective on synonymous codon usage in unicellular organisms , 1986, Journal of Molecular Evolution.

[70]  J. Grainger.  Plant Viruses , 1946, Nature.