-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability
The evolutionary benefit of viral genome segmentation is a classical, yet unsolved question in evolutionary biology and RNA genetics. Theoretical studies anticipated that replication of shorter RNA segments could provide a replicative advantage over standard size genomes. However, this question has remained elusive to experimentalists because of the lack of a proper viral model system. Here we present a study with a stable segmented bipartite RNA virus and its ancestor non-segmented counterpart, in an identical genomic nucleotide sequence context. Results of RNA replication, protein expression, competition experiments, and inactivation of infectious particles point to a non-replicative trait, the particle stability, as the main driver of fitness gain of segmented genomes. Accordingly, measurements of the volume occupation of the genome inside viral capsids indicate that packaging shorter genomes involves a relaxation of the packaging density that is energetically favourable. The empirical observations are used to design a computational model that predicts the existence of a critical multiplicity of infection for domination of segmented over standard types. Our experiments suggest that viral segmented genomes may have arisen as a molecular solution for the trade-off between genome length and particle stability. Genome segmentation allows maximizing the genetic content without the detrimental effect in stability derived from incresing genome length.
Vyšlo v časopise: Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001344
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001344Souhrn
The evolutionary benefit of viral genome segmentation is a classical, yet unsolved question in evolutionary biology and RNA genetics. Theoretical studies anticipated that replication of shorter RNA segments could provide a replicative advantage over standard size genomes. However, this question has remained elusive to experimentalists because of the lack of a proper viral model system. Here we present a study with a stable segmented bipartite RNA virus and its ancestor non-segmented counterpart, in an identical genomic nucleotide sequence context. Results of RNA replication, protein expression, competition experiments, and inactivation of infectious particles point to a non-replicative trait, the particle stability, as the main driver of fitness gain of segmented genomes. Accordingly, measurements of the volume occupation of the genome inside viral capsids indicate that packaging shorter genomes involves a relaxation of the packaging density that is energetically favourable. The empirical observations are used to design a computational model that predicts the existence of a critical multiplicity of infection for domination of segmented over standard types. Our experiments suggest that viral segmented genomes may have arisen as a molecular solution for the trade-off between genome length and particle stability. Genome segmentation allows maximizing the genetic content without the detrimental effect in stability derived from incresing genome length.
Zdroje
1. Garcia-ArriazaJ
ManrubiaSC
TojaM
DomingoE
EscarmisC
2004 Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol 78 11678 11685
2. Garcia-ArriazaJ
OjosnegrosS
DavilaM
DomingoE
EscarmisC
2006 Dynamics of mutation and recombination in a replicating population of complementing, defective viral genomes. J Mol Biol 360 558 572
3. NeeS
1987 The evolution of multicompartmental genomes in viruses. J Mol Evol 25 277 281
4. SzathmaryE
1992 Natural selection and dynamical coexistence of defective and complementing virus segments. J Theor Biol 157 383 406
5. ChaoL
1988 Evolution of sex in RNA viruses. J Theor Biol 133 99 112
6. HolmesEC
2009 The Evolution and Emergence of RNA Viruses;
HarveyPM
MayRM
Oxford Oxford University Press
7. EscarmisC
CarrilloEC
FerrerM
ArriazaJF
LopezN
1998 Rapid selection in modified BHK-21 cells of a foot-and-mouth disease virus variant showing alterations in cell tropism. J Virol 72 10171 10179
8. BarclayW
LiQ
HutchinsonG
MoonD
RichardsonA
1998 Encapsidation studies of poliovirus subgenomic replicons. J Gen Virol 79 Pt 7 1725 1734
9. MateoR
LunaE
RinconV
MateuMG
2008 Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J Virol 82 12232 12240
10. SzathmaryE
1992 Viral sex, levels of selection, and the origin of life. J Theor Biol 159 99 109
11. MillsDR
PetersonRL
SpiegelmanS
1967 An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc Natl Acad Sci USA 58 217 224
12. SaboDL
DomingoE
BandleEF
FlavellRA
WeissmannC
1977 A guanosine to adenosine transition in the 3′ terminal extracistronic region of bacteriophage Qβ RNA leading to loss of infectivity. J Mol Biol 112 235 252
13. ColeCN
BaltimoreD
1973 Defective interfering particles of poliovirus. IV. Mechanisms of enrichment. J Virol 12 1414 1426
14. LundquistRE
SullivanM
MaizelJVJr
1979 Characterization of a new isolate of poliovirus defective interfering particles. Cell 18 759 769
15. NowakMA
MayRM
2000 Virus Dynamics. Mathematical Principles of Immunology and Virology New York Oxford University Press Inc
16. MatthewsBW
1968 Solvent content of protein crystals. J Mol Biol 33 491 497
17. JohnsonJE
RueckertRR
1997 Packaging and release of the viral genome.
ChiuW
BurnettRM
GarceaRL
Structural Biology of Viruses New York Oxford University Press 269 287
18. EscarmisC
DavilaM
CharpentierN
BrachoA
MoyaA
1996 Genetic lesions associated with Muller's ratchet in an RNA virus. J Mol Biol 264 255 267
19. DiezJ
DavilaM
EscarmisC
MateuMG
DominguezJ
1990 Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J Virol 64 5519 5528
20. BettAJ
PrevecL
GrahamFL
1993 Packaging capacity and stability of human adenovirus type 5 vectors. J Virol 67 5911 5921
21. GelbartWM
KnoblerCM
2009 Virology. Pressurized viruses. Science 323 1682 1683
22. De PaepeM
TaddeiF
2006 Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol 4 e193 doi:10.1371/journal.pbio.0040193
23. ChiricoN
VianelliA
Belshaw R Why genes overlap in viruses. Proc Biol Sci 277 3809 3817
24. SobrinoF
DavilaM
OrtinJ
DomingoE
1983 Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128 310 318
25. EscarmisC
DavilaM
DomingoE
1999 Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J Mol Biol 285 495 505
26. ManrubiaSC
Garcia-ArriazaJ
EscarmísC
DomingoE
2006 Long-range transport and universality classes in in vitro viral infection spread. Europhysics Letters 74 547 553
27. PeralesC
AgudoR
TejeroH
ManrubiaSC
DomingoE
2009 Potential benefits of sequential inhibitor-mutagen treatments of RNA virus infections. PLoS Pathog 5 e1000658 doi:10.1371/journal.ppat.1000658
28. PeralesC
MateoR
MateuMG
DomingoE
2007 Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J Mol Biol 369 985 1000
29. MateuMG
MartinezMA
CapucciL
AndreuD
GiraltE
1990 A single amino acid substitution affects multiple overlapping epitopes in the major antigenic site of foot-and-mouth disease virus of serotype C. J Gen Virol 71 Pt 3 629 637
30. EscarmisC
PeralesC
DomingoE
2009 Biological effect of Muller's Ratchet: distant capsid site can affect picornavirus protein processing. J Virol 83 6748 6756
31. MareeAF
KeulenW
BoucherCA
De BoerRJ
2000 Estimating relative fitness in viral competition experiments. J Virol 74 11067 11072
32. HollandJJ
de la TorreJC
ClarkeDK
DuarteE
1991 Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65 2960 2967
33. MateoR
LunaE
MateuMG
2007 Thermostable variants are not generally represented in foot-and-mouth disease virus quasispecies. J Gen Virol 88 859 864
Štítky
Genetika Reprodukčná medicína
Článek Genetic Regulation by NLA and MicroRNA827 for Maintaining Nitrate-Dependent Phosphate Homeostasis inČlánek c-di-GMP Turn-Over in Is Controlled by a Plethora of Diguanylate Cyclases and Phosphodiesterases
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2011 Číslo 3- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- Whole-Exome Re-Sequencing in a Family Quartet Identifies Mutations As the Cause of a Novel Skeletal Dysplasia
- Origin-Dependent Inverted-Repeat Amplification: A Replication-Based Model for Generating Palindromic Amplicons
- Testing for an Unusual Distribution of Rare Variants
- Limited dCTP Availability Accounts for Mitochondrial DNA Depletion in Mitochondrial Neurogastrointestinal Encephalomyopathy (MNGIE)
- FUS Transgenic Rats Develop the Phenotypes of Amyotrophic Lateral Sclerosis and Frontotemporal Lobar Degeneration
- Repeat Associated Non-ATG Translation Initiation: One DNA, Two Transcripts, Seven Reading Frames, Potentially Nine Toxic Entities!
- Initial Mutations Direct Alternative Pathways of Protein Evolution
- Dopamine Signalling in Mushroom Bodies Regulates Temperature-Preference Behaviour in
- Sensing of Replication Stress and Mec1 Activation Act through Two Independent Pathways Involving the 9-1-1 Complex and DNA Polymerase ε
- Genetic Regulation by NLA and MicroRNA827 for Maintaining Nitrate-Dependent Phosphate Homeostasis in
- Identification of a Novel Type of Spacer Element Required for Imprinting in Fission Yeast
- Chiasmata Promote Monopolar Attachment of Sister Chromatids and Their Co-Segregation toward the Proper Pole during Meiosis I
- Global Analysis of the Relationship between JIL-1 Kinase and Transcription
- H3K9me2/3 Binding of the MBT Domain Protein LIN-61 Is Essential for Vulva Development
- REVEILLE8 and PSEUDO-REPONSE REGULATOR5 Form a Negative Feedback Loop within the Arabidopsis Circadian Clock
- A Novel Unstable Duplication Upstream of Predisposes to a Breed-Defining Skin Phenotype and a Periodic Fever Syndrome in Chinese Shar-Pei Dogs
- Polycomb Repressive Complex 2 Controls the Embryo-to-Seedling Phase Transition
- A Role for Set1/MLL-Related Components in Epigenetic Regulation of the Germ Line
- Genome-Wide Association Analysis Identifies Variants Associated with Nonalcoholic Fatty Liver Disease That Have Distinct Effects on Metabolic Traits
- A Genome-Wide Association Study of Upper Aerodigestive Tract Cancers Conducted within the INHANCE Consortium
- Ancestral Mutation in Telomerase Causes Defects in Repeat Addition Processivity and Manifests As Familial Pulmonary Fibrosis
- Ultra-Deep Sequencing of Mouse Mitochondrial DNA: Mutational Patterns and Their Origins
- Phenotype Restricted Genome-Wide Association Study Using a Gene-Centric Approach Identifies Three Low-Risk Neuroblastoma Susceptibility Loci
- The Toll-Like Receptor Gene Family Is Integrated into Human DNA Damage and p53 Networks
- Polycomb Targets Seek Closest Neighbours
- Widespread Hypomethylation Occurs Early and Synergizes with Gene Amplification during Esophageal Carcinogenesis
- c-di-GMP Turn-Over in Is Controlled by a Plethora of Diguanylate Cyclases and Phosphodiesterases
- Estimating Divergence Time and Ancestral Effective Population Size of Bornean and Sumatran Orangutan Subspecies Using a Coalescent Hidden Markov Model
- Rif1 Supports the Function of the CST Complex in Yeast Telomere Capping
- A Tradeoff Drives the Evolution of Reduced Metal Resistance in Natural Populations of Yeast
- Quantifying the Underestimation of Relative Risks from Genome-Wide Association Studies
- Population-Based Resequencing of Experimentally Evolved Populations Reveals the Genetic Basis of Body Size Variation in
- Triplet Repeat–Derived siRNAs Enhance RNA–Mediated Toxicity in a Drosophila Model for Myotonic Dystrophy
- The FUN30 Chromatin Remodeler, Fft3, Protects Centromeric and Subtelomeric Domains from Euchromatin Formation
- Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability
- Environmental Sex Determination in the Branchiopod Crustacean : Deep Conservation of a Gene in the Sex-Determining Pathway
- Systematic Detection of Polygenic Regulatory Evolution
- The SUMO Isopeptidase Ulp2p Is Required to Prevent Recombination-Induced Chromosome Segregation Lethality following DNA Replication Stress
- Uncoupling Antisense-Mediated Silencing and DNA Methylation in the Imprinted Cluster
- Role of the Drosophila Non-Visual ß-Arrestin Kurtz in Hedgehog Signalling
- Differential Genetic Associations for Systemic Lupus Erythematosus Based on Anti–dsDNA Autoantibody Production
- COMPASS-Like Complexes Mediate Histone H3 Lysine-4 Trimethylation to Control Floral Transition and Plant Development
- H3 Lysine 4 Is Acetylated at Active Gene Promoters and Is Regulated by H3 Lysine 4 Methylation
- Diverse Roles and Interactions of the SWI/SNF Chromatin Remodeling Complex Revealed Using Global Approaches
- A Bow-Tie Genetic Architecture for Morphogenesis Suggested by a Genome-Wide RNAi Screen in
- Roles of () in Oocyte Nuclear Architecture, Gametogenesis, Gonad Tumors, and Genome Stability in Zebrafish
- A Molecular Phylogeny of Living Primates
- Roles of the Espin Actin-Bundling Proteins in the Morphogenesis and Stabilization of Hair Cell Stereocilia Revealed in CBA/CaJ Congenic Jerker Mice
- A Cholinergic-Regulated Circuit Coordinates the Maintenance and Bi-Stable States of a Sensory-Motor Behavior during Male Copulation
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Whole-Exome Re-Sequencing in a Family Quartet Identifies Mutations As the Cause of a Novel Skeletal Dysplasia
- Origin-Dependent Inverted-Repeat Amplification: A Replication-Based Model for Generating Palindromic Amplicons
- FUS Transgenic Rats Develop the Phenotypes of Amyotrophic Lateral Sclerosis and Frontotemporal Lobar Degeneration
- Limited dCTP Availability Accounts for Mitochondrial DNA Depletion in Mitochondrial Neurogastrointestinal Encephalomyopathy (MNGIE)
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy