Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject ha...
Saved in:
| Published in: | PLoS pathogens Vol. 7; no. 5; p. e1002028 |
|---|---|
| Main Authors: | , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Public Library of Science
01.05.2011
Public Library of Science (PLoS) |
| Subjects: | |
| ISSN: | 1553-7374, 1553-7366, 1553-7374 |
| Online Access: | Get full text |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling-a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of "mosaic" virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses. |
|---|---|
| AbstractList |
Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling--a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of "mosaic" virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses. Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling-a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of "mosaic" virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses. Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling-a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of "mosaic" virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses.Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling-a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of "mosaic" virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses. Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling-a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of "mosaic" virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses. Recombination creates new genome combinations by joining genome fragments of distinct "parental" origin. This phenomenon, frequent in viral populations, combines mutations originally present on distinct parental genomes, increasing genetic diversity and creating "offspring" with altered biological properties. Consistently, recombination is often associated with the emergence of economically important viruses, with modified host range and virulence. In fact, recombination events can be lethal, deleterious or beneficial, but the respective frequency of these phenotypic effects is unknown and unpredictable. A generally accepted view, which we formally challenge in the present paper, is that most viral recombination events are deleterious or lethal when the parental sequences diverge by more than 10%. However, at present, no dedicated data set supports this supposition. We generated hundreds of "mosaic" genomes randomly from two plant virus species diverging by 18%, and tested a subset of 47 of these recombinants for viability and within-host accumulation. Surprisingly, all were viable, replicated, and accumulated at a pace comparable to that of the parents. Our results are in striking contrast to the current view, and show that viral recombination can have little phenotypic effect, at least in some cases, even when the parental sequences diverge by far more than 10%. Author Summary : Recombination creates new genome combinations by joining genome fragments of distinct “parental” origin. This phenomenon, frequent in viral populations, combines mutations originally present on distinct parental genomes, increasing genetic diversity and creating “offspring” with altered biological properties. Consistently, recombination is often associated with the emergence of economically important viruses, with modified host range and virulence. In fact, recombination events can be lethal, deleterious or beneficial, but the respective frequency of these phenotypic effects is unknown and unpredictable. A generally accepted view, which we formally challenge in the present paper, is that most viral recombination events are deleterious or lethal when the parental sequences diverge by more than 10%. However, at present, no dedicated data set supports this supposition. We generated hundreds of “mosaic” genomes randomly from two plant virus species diverging by 18%, and tested a subset of 47 of these recombinants for viability and within-host accumulation. Surprisingly, all were viable, replicated, and accumulated at a pace comparable to that of the parents. Our results are in striking contrast to the current view, and show that viral recombination can have little phenotypic effect, at least in some cases, even when the parental sequences diverge by far more than 10%. |
| Audience | Academic |
| Author | Urbino, Cica Peterschmitt, Michel Froissart, Rémy Vuillaume, Florence Forfert, Nadège Thébaud, Gaël Blanc, Stéphane Granier, Martine |
| AuthorAffiliation | 2 Laboratoire Maladies Infectieuses & Vecteurs: Écologie, Génétique, Évolution & Contrôle (MIVEGEC), CNRS-IRD-Université de Montpellier I, Agropolis, Montpellier, France 1 CIRAD, INRA, CNRS – Unité mixte de recherche Biologie & génétique des interactions plante-parasite (BGPI), Montpellier, France Cornell University, United States of America |
| AuthorAffiliation_xml | – name: Cornell University, United States of America – name: 1 CIRAD, INRA, CNRS – Unité mixte de recherche Biologie & génétique des interactions plante-parasite (BGPI), Montpellier, France – name: 2 Laboratoire Maladies Infectieuses & Vecteurs: Écologie, Génétique, Évolution & Contrôle (MIVEGEC), CNRS-IRD-Université de Montpellier I, Agropolis, Montpellier, France |
| Author_xml | – sequence: 1 givenname: Florence surname: Vuillaume fullname: Vuillaume, Florence – sequence: 2 givenname: Gaël surname: Thébaud fullname: Thébaud, Gaël – sequence: 3 givenname: Cica surname: Urbino fullname: Urbino, Cica – sequence: 4 givenname: Nadège surname: Forfert fullname: Forfert, Nadège – sequence: 5 givenname: Martine surname: Granier fullname: Granier, Martine – sequence: 6 givenname: Rémy surname: Froissart fullname: Froissart, Rémy – sequence: 7 givenname: Stéphane surname: Blanc fullname: Blanc, Stéphane – sequence: 8 givenname: Michel surname: Peterschmitt fullname: Peterschmitt, Michel |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21573141$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-02647631$$DView record in HAL |
| BookMark | eNqVk99v0zAQxyM0xH7Af4AgEg9oDy3-kTjJHpCqMWilClA3eLVs59J6SuwQOxv773HbbFqrCYTyEOvu873zne-OowNjDUTRa4zGmGb4w7XtOyPqcdsKP8YIEUTyZ9ERTlM6ymiWHDw6H0bHzl0jlGCK2YvokOA0ozjBR5H6pJ3vtOy9tia2VexXEH9fgbH-rtUqvqgqUN6tPQthStvEU9vY2i5t7-IFKNtIbcRGLMHfApj46tbGP3UX_JctKA3uZfS8ErWDV8P_JPrx-eLqfDqaf_syO5_MRyojzI8UkoliBAqksMxJlctQUThIyiTBIq8oEyWWSgJQlBcSUpJlSBGUMkErnNCT6O02bltbx4f-OI5JXmCEU0YCMdsSpRXXvO10I7o7boXmG4Ptllx0XqsaOMvSHCTkUhGWMIxEkhKqgIkcSkZlEWJ9HLL1soFSgfGdqHeC7nqMXvGlveHh8nlGaAhwug2w2pNNJ3O-tqGQOWMU3-DAvh-SdfZXD87zRjsFdS0MhJfgBSKUEZTQf5I5yyhJkhQF8t0e-XTLBmopQle0qWwoRq1j8glJA8ZwkQVq_AQVvhIarcLgVjrYdwSnO4LAePjtl6J3js8uF__Bft1l3zx-lYe-3k98AJItoDrrXAfVA4IRXy_WfRf4erH4sFhBdrYnU9pv5j4Uquu_i_8AfIIoeg |
| CitedBy_id | crossref_primary_10_1111_eva_12157 crossref_primary_10_3390_agronomy15051006 crossref_primary_10_1016_j_coviro_2014_12_005 crossref_primary_10_1007_s13595_015_0487_4 crossref_primary_10_1371_journal_pone_0174651 crossref_primary_10_1099_jgv_0_000633 crossref_primary_10_1016_j_virol_2020_01_002 crossref_primary_10_3390_v3091699 crossref_primary_10_1016_j_coviro_2018_08_013 crossref_primary_10_24072_pcjournal_379 crossref_primary_10_1186_1743_422X_11_66 crossref_primary_10_7717_peerj_1320 crossref_primary_10_1016_j_virol_2015_06_019 crossref_primary_10_1038_srep08153 crossref_primary_10_1128_JVI_00541_21 crossref_primary_10_1371_journal_pone_0058375 |
| Cites_doi | 10.1099/vir.0.83077-0 10.1073/pnas.91.22.10747 10.1128/JVI.02152-08 10.1016/j.virol.2006.02.028 10.1099/0022-1317-81-7-1839 10.1128/JVI.74.9.4214-4219.2000 10.1099/vir.0.18894-0 10.1371/journal.ppat.0030181 10.1016/j.jviromet.2007.09.015 10.1146/annurev.genet.36.040202.111115 10.1186/1743-422X-5-61 10.1371/journal.pgen.0010051 10.1063/1.3449300 10.1110/ps.0306603 10.1186/1743-422X-5-135 10.1016/j.virol.2003.10.002 10.1006/viro.2002.1633 10.1094/PDIS.1999.83.3.303B 10.1016/j.virol.2004.11.017 10.1093/nar/29.9.e45 10.1128/JVI.00524-07 10.1534/genetics.105.051136 10.1128/JVI.00337-08 10.1094/PDIS.1999.83.11.1006 10.1099/0022-1317-78-8-2101 10.1098/rstb.2010.0068 10.1073/pnas.0500729102 10.1099/vir.0.83252-0 10.1038/nrg2323 10.1073/pnas.0400146101 10.1016/j.meegid.2008.07.010 10.1016/0042-6822(91)90795-D 10.1371/journal.pcbi.1000178 10.1099/vir.0.80805-0 10.1371/journal.pbio.0030089 10.1128/JVI.79.9.5732-5742.2005 10.1006/viro.1999.0056 10.1371/journal.ppat.0030008 |
| ContentType | Journal Article |
| Copyright | COPYRIGHT 2011 Public Library of Science 2011 Vuillaume et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Vuillaume F, Thébaud G, Urbino C, Forfert N, Granier M, et al. (2011) Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species. PLoS Pathog 7(5): e1002028. doi:10.1371/journal.ppat.1002028 Attribution Vuillaume et al. 2011 |
| Copyright_xml | – notice: COPYRIGHT 2011 Public Library of Science – notice: 2011 Vuillaume et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Vuillaume F, Thébaud G, Urbino C, Forfert N, Granier M, et al. (2011) Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species. PLoS Pathog 7(5): e1002028. doi:10.1371/journal.ppat.1002028 – notice: Attribution – notice: Vuillaume et al. 2011 |
| DBID | AAYXX CITATION CGR CUY CVF ECM EIF NPM ISN ISR 3V. 7QL 7U9 7X7 7XB 88E 8FE 8FH 8FI 8FJ 8FK ABUWG AEUYN AFKRA AZQEC BBNVY BENPR BHPHI C1K CCPQU COVID DWQXO FYUFA GHDGH GNUQQ H94 HCIFZ K9. LK8 M0S M1P M7P PHGZM PHGZT PIMPY PJZUB PKEHL PPXIY PQEST PQGLB PQQKQ PQUKI PRINS 7X8 1XC VOOES 5PM DOA |
| DOI | 10.1371/journal.ppat.1002028 |
| DatabaseName | CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Gale In Context: Canada Gale In Context: Science ProQuest Central (Corporate) Bacteriology Abstracts (Microbiology B) Virology and AIDS Abstracts Health & Medical Collection ProQuest Central (purchase pre-March 2016) Medical Database (Alumni Edition) ProQuest SciTech Collection ProQuest Natural Science Collection ProQuest Hospital Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest One Sustainability ProQuest Central UK/Ireland ProQuest Central Essentials Biological Science Collection ProQuest Central Natural Science Collection Environmental Sciences and Pollution Management ProQuest One Coronavirus Research Database ProQuest Central Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student AIDS and Cancer Research Abstracts SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) Biological Sciences ProQuest Health & Medical Collection Medical Database Biological Science Database ProQuest Central Premium ProQuest One Academic (New) Publicly Available Content Database ProQuest Health & Medical Research Collection ProQuest One Academic Middle East (New) ProQuest One Health & Nursing ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Applied & Life Sciences ProQuest One Academic (retired) ProQuest One Academic UKI Edition ProQuest Central China MEDLINE - Academic Hyper Article en Ligne (HAL) Hyper Article en Ligne (HAL) (Open Access) PubMed Central (Full Participant titles) DOAJ Open Access Full Text |
| DatabaseTitle | CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) Publicly Available Content Database ProQuest Central Student ProQuest One Academic Middle East (New) ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest One Health & Nursing ProQuest Natural Science Collection ProQuest Central China Environmental Sciences and Pollution Management ProQuest Central ProQuest One Applied & Life Sciences ProQuest One Sustainability ProQuest Health & Medical Research Collection Health Research Premium Collection Health and Medicine Complete (Alumni Edition) Natural Science Collection ProQuest Central Korea Bacteriology Abstracts (Microbiology B) Health & Medical Research Collection Biological Science Collection AIDS and Cancer Research Abstracts ProQuest Central (New) ProQuest Medical Library (Alumni) Virology and AIDS Abstracts ProQuest Biological Science Collection ProQuest One Academic Eastern Edition Coronavirus Research Database ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database ProQuest SciTech Collection ProQuest Hospital Collection (Alumni) ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ProQuest One Academic ProQuest One Academic (New) ProQuest Central (Alumni) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE MEDLINE - Academic AIDS and Cancer Research Abstracts Publicly Available Content Database |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 3 dbid: PIMPY name: Publicly Available Content Database url: http://search.proquest.com/publiccontent sourceTypes: Aggregation Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology |
| DocumentTitleAlternate | Phenotypic Effects of Random Recombination |
| EISSN | 1553-7374 |
| ExternalDocumentID | 1289101562 oai_doaj_org_article_6758ebe8bc264610a4523ce6a8ed63b9 PMC3088723 oai:HAL:hal-02647631v1 2896597821 A258916197 21573141 10_1371_journal_ppat_1002028 |
| Genre | Research Support, Non-U.S. Gov't Journal Article |
| GeographicLocations | France |
| GeographicLocations_xml | – name: France |
| GroupedDBID | --- 123 29O 2WC 53G 5VS 7X7 88E 8FE 8FH 8FI 8FJ AAFWJ AAUCC AAWOE AAYXX ABDBF ABUWG ACCTH ACGFO ACIHN ACPRK ACUHS ADBBV ADRAZ AEAQA AENEX AEUYN AFFHD AFKRA AFPKN AFRAH AHMBA ALMA_UNASSIGNED_HOLDINGS AOIJS B0M BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI BWKFM CCPQU CITATION CS3 DIK DU5 E3Z EAP EAS EBD EMK EMOBN ESX F5P FPL FYUFA GROUPED_DOAJ GX1 HCIFZ HMCUK HYE IAO IHR INH INR ISN ISR ITC KQ8 LK8 M1P M48 M7P MM. O5R O5S OK1 OVT P2P PGMZT PHGZM PHGZT PIMPY PJZUB PPXIY PQGLB PQQKQ PROAC PSQYO QN7 RNS RPM SV3 TR2 TUS UKHRP WOW ~8M 3V. CGR CUY CVF ECM EIF H13 IPNFZ M~E NPM PV9 QF4 RIG RZL WOQ 7QL 7U9 7XB 8FK AZQEC C1K COVID DWQXO GNUQQ H94 K9. PKEHL PQEST PQUKI PRINS 7X8 PUEGO 1XC VOOES 5PM AAPBV ABPTK |
| ID | FETCH-LOGICAL-c726t-c0b4c62e90c1b82f8b028b82b36b21a8f36ad1bcbee3089be52770c2056a3f143 |
| IEDL.DBID | DOA |
| ISICitedReferencesCount | 18 |
| ISICitedReferencesURI | http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000291014000014&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| ISSN | 1553-7374 1553-7366 |
| IngestDate | Sun Oct 01 00:11:19 EDT 2023 Tue Oct 14 19:06:43 EDT 2025 Tue Nov 04 01:57:57 EST 2025 Tue Oct 14 20:43:05 EDT 2025 Fri Sep 05 10:32:01 EDT 2025 Thu Oct 02 09:40:28 EDT 2025 Sat Nov 29 14:37:51 EST 2025 Tue Nov 11 10:30:01 EST 2025 Tue Nov 04 17:57:55 EST 2025 Thu Nov 13 14:47:33 EST 2025 Thu Nov 13 14:22:39 EST 2025 Wed Feb 19 02:05:04 EST 2025 Sat Nov 29 04:10:11 EST 2025 Tue Nov 18 22:28:03 EST 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 5 |
| Keywords | VIROLOGIE BEGOMOVIRUS |
| Language | English |
| License | Attribution: http://creativecommons.org/licenses/by This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. Creative Commons Attribution License |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c726t-c0b4c62e90c1b82f8b028b82b36b21a8f36ad1bcbee3089be52770c2056a3f143 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 ObjectType-Article-2 ObjectType-Feature-1 Conceived and designed the experiments: SB MP. Performed the experiments: FV CU NF MG MP. Analyzed the data: FV GT SB MP. Wrote the paper: FV GT RF SB MP. |
| ORCID | 0000-0002-3412-0989 0000-0001-8234-1308 0000-0002-2987-4997 0000-0002-6215-9389 |
| OpenAccessLink | https://doaj.org/article/6758ebe8bc264610a4523ce6a8ed63b9 |
| PMID | 21573141 |
| PQID | 1289101562 |
| PQPubID | 1436335 |
| ParticipantIDs | plos_journals_1289101562 doaj_primary_oai_doaj_org_article_6758ebe8bc264610a4523ce6a8ed63b9 pubmedcentral_primary_oai_pubmedcentral_nih_gov_3088723 hal_primary_oai_HAL_hal_02647631v1 proquest_miscellaneous_902362043 proquest_miscellaneous_867324450 proquest_journals_1289101562 gale_infotracmisc_A258916197 gale_infotracacademiconefile_A258916197 gale_incontextgauss_ISR_A258916197 gale_incontextgauss_ISN_A258916197 pubmed_primary_21573141 crossref_primary_10_1371_journal_ppat_1002028 crossref_citationtrail_10_1371_journal_ppat_1002028 |
| PublicationCentury | 2000 |
| PublicationDate | 2011-05-01 |
| PublicationDateYYYYMMDD | 2011-05-01 |
| PublicationDate_xml | – month: 05 year: 2011 text: 2011-05-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: San Francisco – name: San Francisco, USA |
| PublicationTitle | PLoS pathogens |
| PublicationTitleAlternate | PLoS Pathog |
| PublicationYear | 2011 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
| Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
| References | R Froissart (ref34) 2010; 365 WPC Stemmer (ref27) 1994; 91 (ref39) 2010 S Wain-Hobson (ref5) 2003; 84 C Urbino (ref35) 2008; 5 S De Rozieres (ref9) 2008; 82 A Bruyere (ref14) 2000; 74 J Bonnet (ref13) 2005; 332 MW Pfaffl (ref38) 2001; 29 LR Banner (ref20) 1991; 185 S Duffy (ref1) 2008; 9 D Posada (ref19) 2002; 36 DA Drummond (ref6) 2005; 102 P Carrasco (ref8) 2007; 81 IM Moreno (ref16) 2004; 318 B Pico (ref36) 1999; 83 X Zhou (ref26) 1997; 78 O Pierrugues (ref12) 2007; 88 M Padidam (ref22) 1999; 265 P Lefeuvre (ref28) 2007; 88 F Escriu (ref15) 2007; 3 DP Martin (ref10) 2005; 1 P Agudelo-Romero (ref29) 2008; 8 P Lefeuvre (ref21) 2007; 3 P Lefeuvre (ref18) 2009; 83 SF Elena (ref2) 2010; 20 S Duffy (ref30) 2006; 172 G Mason (ref37) 2008; 147 A Urbanowicz (ref4) 2005; 79 F Monci (ref24) 2002; 303 AI Sanz (ref25) 2000; 81 MM Meyer (ref31) 2003; 12 M Peterschmitt (ref33) 1999; 83 H Delatte (ref32) 2005; 86 R Sanjuan (ref7) 2004; 101 J Archer (ref17) 2008; 4 S Garcia-Andres (ref23) 2006; 350 R Froissart (ref3) 2005; 3 E van der Walt (ref11) 2008; 5 |
| References_xml | – volume: 88 start-page: 2852 year: 2007 ident: ref12 article-title: Biological properties and relative fitness of inter-subgroup Cucumber mosaic virus RNA 3 recombinants produced in vitro. publication-title: J Gen Virol doi: 10.1099/vir.0.83077-0 – volume: 91 start-page: 10747 year: 1994 ident: ref27 article-title: DNA Shuffling by Random Fragmentation and Reassembly - in-Vitro Recombination for Molecular Evolution. publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.91.22.10747 – volume: 83 start-page: 2697 year: 2009 ident: ref18 article-title: Widely Conserved Recombination Patterns among Single-Stranded DNA Viruses. publication-title: J Virol doi: 10.1128/JVI.02152-08 – volume: 350 start-page: 433 year: 2006 ident: ref23 article-title: Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: Evidence for the presence of a new virus species of recombinant nature. publication-title: Virology doi: 10.1016/j.virol.2006.02.028 – volume: 81 start-page: 1839 year: 2000 ident: ref25 article-title: Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. publication-title: J Gen Virol doi: 10.1099/0022-1317-81-7-1839 – volume: 74 start-page: 4214 year: 2000 ident: ref14 article-title: Frequent homologous recombination events between molecules of one RNA component in a multipartite RNA virus. publication-title: J Virol doi: 10.1128/JVI.74.9.4214-4219.2000 – volume: 84 start-page: 885 year: 2003 ident: ref5 article-title: Network analysis of human and simian immunodeficiency virus sequence sets reveals massive recombination resulting in shorter pathways. publication-title: J Gen Virol doi: 10.1099/vir.0.18894-0 – volume: 3 start-page: 1782 year: 2007 ident: ref21 article-title: Avoidance of protein fold disruption in natural virus recombinants. publication-title: Plos Pathog doi: 10.1371/journal.ppat.0030181 – volume: 147 start-page: 282 year: 2008 ident: ref37 article-title: Real-time PCR for the quantitation of Tomato yellow leaf curl Sardinia virus in tomato plants and in Bemisia tabaci. publication-title: J Virol Methods doi: 10.1016/j.jviromet.2007.09.015 – volume: 36 start-page: 75 year: 2002 ident: ref19 article-title: Recombination in evolutionary genomics. publication-title: Annu Rev Genet doi: 10.1146/annurev.genet.36.040202.111115 – volume: 5 start-page: 11 year: 2008 ident: ref11 article-title: Viable chimaeric viruses confirm the biological importance of sequence specific Maize streak virus movement protein and coat protein interactions. publication-title: Virol J doi: 10.1186/1743-422X-5-61 – volume: 1 start-page: 475 year: 2005 ident: ref10 article-title: The evolutionary value of recombination is constrained by genome modularity. publication-title: Plos Genet doi: 10.1371/journal.pgen.0010051 – year: 2010 ident: ref39 article-title: R: A Language and Environment for Statistical Computing. – volume: 20 start-page: 12 year: 2010 ident: ref2 article-title: Simple genomes, complex interactions: Epistasis in RNA virus. publication-title: Chaos doi: 10.1063/1.3449300 – volume: 12 start-page: 1686 year: 2003 ident: ref31 article-title: Library analysis of SCHEMA-guided protein recombination. publication-title: Protein Sci doi: 10.1110/ps.0306603 – volume: 5 start-page: 10 year: 2008 ident: ref35 article-title: A novel cloning strategy for isolating, genotyping and phenotyping genetic variants of geminiviruses. publication-title: Virol J doi: 10.1186/1743-422X-5-135 – volume: 318 start-page: 451 year: 2004 ident: ref16 article-title: Variability and genetic structure of the population of Watermelon mosaic virus infecting melon in Spain. publication-title: Virology doi: 10.1016/j.virol.2003.10.002 – volume: 303 start-page: 317 year: 2002 ident: ref24 article-title: A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. publication-title: Virology doi: 10.1006/viro.2002.1633 – volume: 83 start-page: 303 year: 1999 ident: ref33 article-title: First report of Tomato yellow leaf curl virus in Réunion Island. publication-title: Plant Dis doi: 10.1094/PDIS.1999.83.3.303B – volume: 332 start-page: 359 year: 2005 ident: ref13 article-title: Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. publication-title: Virology doi: 10.1016/j.virol.2004.11.017 – volume: 29 start-page: 2002 year: 2001 ident: ref38 article-title: A new mathematical model for relative quantification in real-time RT-PCR. publication-title: Nucleic Acids Res doi: 10.1093/nar/29.9.e45 – volume: 81 start-page: 12979 year: 2007 ident: ref8 article-title: Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. publication-title: J Virol doi: 10.1128/JVI.00524-07 – volume: 172 start-page: 751 year: 2006 ident: ref30 article-title: Pleiotropic costs of niche expansion in the RNA bacteriophage Phi 6. publication-title: Genetics doi: 10.1534/genetics.105.051136 – volume: 82 start-page: 7953 year: 2008 ident: ref9 article-title: Replication properties of clade a/c chimeric feline immunodeficiency viruses and evaluation of infection kinetics in the domestic cat. publication-title: J Virol doi: 10.1128/JVI.00337-08 – volume: 83 start-page: 1006 year: 1999 ident: ref36 article-title: Improved diagnostic techniques for Tomato yellow leaf curl virus in tomato breeding programs. publication-title: Plant Dis doi: 10.1094/PDIS.1999.83.11.1006 – volume: 78 start-page: 2101 year: 1997 ident: ref26 article-title: Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. publication-title: J Gen Virol doi: 10.1099/0022-1317-78-8-2101 – volume: 365 start-page: 1907 year: 2010 ident: ref34 article-title: The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-) existing studies. publication-title: Philos Trans R Soc B Biol Sci doi: 10.1098/rstb.2010.0068 – volume: 102 start-page: 5380 year: 2005 ident: ref6 article-title: On the conservative nature of intragenic recombination. publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.0500729102 – volume: 88 start-page: 3458 year: 2007 ident: ref28 article-title: Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. publication-title: J Gen Virol doi: 10.1099/vir.0.83252-0 – volume: 9 start-page: 267 year: 2008 ident: ref1 article-title: Rates of evolutionary change in viruses: patterns and determinants. publication-title: Nat Rev Genet doi: 10.1038/nrg2323 – volume: 101 start-page: 8396 year: 2004 ident: ref7 article-title: The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.0400146101 – volume: 8 start-page: 806 year: 2008 ident: ref29 article-title: The pleiotropic cost of host-specialization in Tobacco etch potyvirus. publication-title: Infection Genetics and Evolution doi: 10.1016/j.meegid.2008.07.010 – volume: 185 start-page: 441 year: 1991 ident: ref20 article-title: Random nature of Coronavirus RNA Recombination in the absence of selection pressure. publication-title: Virology doi: 10.1016/0042-6822(91)90795-D – volume: 4 start-page: 7 year: 2008 ident: ref17 article-title: Identifying the important HIV-1 recombination breakpoints. publication-title: Plos Comput Biol doi: 10.1371/journal.pcbi.1000178 – volume: 86 start-page: 1533 year: 2005 ident: ref32 article-title: South West Indian Ocean islands tomato begomovirus populations represent a new major monopartite begomovirus group. publication-title: J Gen Virol doi: 10.1099/vir.0.80805-0 – volume: 3 start-page: 389 year: 2005 ident: ref3 article-title: Recombination every day: Abundant recombination in a virus during a single multi-cellular host infection. publication-title: Plos Biol doi: 10.1371/journal.pbio.0030089 – volume: 79 start-page: 5732 year: 2005 ident: ref4 article-title: Homologous crossovers among molecules of Brome mosaic bromovirus RNA1 or RNA2 segments in vivo. publication-title: J Virol doi: 10.1128/JVI.79.9.5732-5742.2005 – volume: 265 start-page: 218 year: 1999 ident: ref22 article-title: Possible emergence of new geminiviruses by frequent recombination. publication-title: Virology doi: 10.1006/viro.1999.0056 – volume: 3 start-page: 67 year: 2007 ident: ref15 article-title: Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. publication-title: Plos Pathog doi: 10.1371/journal.ppat.0030008 |
| SSID | ssj0041316 |
| Score | 2.0904553 |
| Snippet | Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of... Author Summary : Recombination creates new genome combinations by joining genome fragments of distinct “parental” origin. This phenomenon, frequent in viral... Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of... |
| SourceID | plos doaj pubmedcentral hal proquest gale pubmed crossref |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source |
| StartPage | e1002028 |
| SubjectTerms | Agrobacterium tumefaciens - genetics Begomovirus Begomovirus - classification Begomovirus - genetics Biology Cloning Cloning, Molecular DNA, Viral - genetics Escherichia coli - genetics Experiments Geminiviridae Geminivirus Gene Targeting Genetic Association Studies Genetic diversity Genetic recombination Genome, Viral Genomes Genomics Life Sciences Lycopersicon esculentum Mutagenesis Mutation Phenotype Phylogeny Plasmids Reassortant Viruses - classification Reassortant Viruses - genetics Recombination, Genetic Sequence Analysis, DNA Solanum lycopersicum - virology Tomatoes Viral genetics Viruses |
| SummonAdditionalLinks | – databaseName: Biological Science Database dbid: M7P link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3db9MwELdYAYkXvscKA1kIiaewxE7t5AmVj2lIqKq2gfZm2a6zVlrj0LRD---5S9zSoA0eeKviS-OP8_nOPv9-hLzJwAVxea4jU-BuleAiMszZaJAhgUiexYUuGrIJORplZ2f5OGy41SGtcm0TG0M98Rb3yA_AjsLKBtEGe1_9iJA1Ck9XA4XGDrmNKAmsSd0bry0x2OeG-hSpcSLJhQhX57hMDsJIvasqvWxgSGPkY99amhoE_42d3plimmSvuvD1da7onxmVW0vU4YP_bdxDcj84p3TYatMjcsuVj8ndlq7y6gmxnxBlNxBkUV9QcB7peOpKv7yqZpa2SMg1lhzrcuLn9MjP8V2_qinGuXMIwxtNoCE9jJ7-9PT7bAHlJ5UDM1M_Jd8OP59-PIoCSUNkJRPLyMYmtYK5PLaJyViRGehJ-GG4MCzRWcGFniTGGud4nOXGDZiUsWXgeGlegLe2S3qlL90eoYOBNhwcTJ06mxrJjBSFyDX4iC6xNo37hK_HR9mAYI5EGheqOZaTEMm0_aRwVFUY1T6JNm9VLYLHP-Q_4NBvZBF_u3ngF-cqTGeFYRaof2YsOJTggeoUAnrrhM7cRHCT98lrVByFCBslpvCc61Vdqy8nIzVkSOQIcau8Uei4I_Q2CBUeGmt1uDYBXYbIXR3J_Y4k2Anb_doUm7rVrKPhV4XPIA5PYZ1JLpM-2UMdX3dMrX5rJvz9WnevL6abYvwy5u6VDvRLZUKC154O4ptFcuQxwFvaffKsnUibesK0ljxJoWayM8U6DemWlLNpg5POcQVl_PnfK_6C3GvPCTCJdZ_0louVe0nu2MvlrF68agzKL8tRfcI priority: 102 providerName: ProQuest – databaseName: Public Library of Science (PLoS) Journals Open Access dbid: FPL link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3db9MwELdYAYkXvmGFgSyExFMgsVPbeSwfVZGmqhoD7c2yXWettCZR0w7tv-cuccsyrUK8Rblz4juf7d8l5ztC3iuAID7LTGRz_FoluIgs8y4aKCwgkqk4N3lTbEJOJursLJv-dRRv_MHnMvkUdPqxqsy6SRgKO-IBucu4EOhsjabH25UX1uNEhONx-1p2tp8mS_9uLT6YYyhkr7oo69vg5s2oyWvb0OjR_wrwmDwMgJMOWwt5Qu744im535agvHpG3FfMnBuKXtEypwAI6XTui3J9VS0cbbMb10g5McWsXNJxucS25aam6LsuwbVuRpeGkC96-rukvxYroDfF7X39nPwcfTv9Mo5C4YXISSbWkYtt6gTzWewSq1iuLHQZLiwXliVG5VyYWWKd9Z7HKrN-wKSMHQMwZXgOCOwF6RVl4Q8JHQyM5QAaTepdaiWzUuQiM4D7fOJcGvcJ346HdiErORbHuNDNrzYJ3kmrJ43q00F9fRLtWlVtVo5_8H_God7xYk7t5gaMkw5TVKPrBCatrAOQCKjSpOCkOy-M8jPBbdYn79BQNGbNKDAs59xs6lp__zHRQ4bFGcEXlXuZTjpMHwJTXoKwzoSjEKAyzMbV4TzqcMLcd923zVHUa2KNh8ca74FvncLekVwmfXKINr1VTK0BkgBIBMedweO3dn47me7I-GaMxys82JdWQgISTwfxfpYMaxPgyes-edlOnF0_AWZKnqTQM9mZUh1BupRiMW9yn3PcFRl_tV-m1-RB-90fg1KPSG-92vg35J67XC_q1dtmwfgDPJVqMA priority: 102 providerName: Public Library of Science |
| Title | Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/21573141 https://www.proquest.com/docview/1289101562 https://www.proquest.com/docview/867324450 https://www.proquest.com/docview/902362043 https://hal.inrae.fr/hal-02647631 https://pubmed.ncbi.nlm.nih.gov/PMC3088723 https://doaj.org/article/6758ebe8bc264610a4523ce6a8ed63b9 http://dx.doi.org/10.1371/journal.ppat.1002028 |
| Volume | 7 |
| WOSCitedRecordID | wos000291014000014&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| journalDatabaseRights | – providerCode: PRVAON databaseName: DOAJ Directory of Open Access Journals customDbUrl: eissn: 1553-7374 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0041316 issn: 1553-7374 databaseCode: DOA dateStart: 20050101 isFulltext: true titleUrlDefault: https://www.doaj.org/ providerName: Directory of Open Access Journals – providerCode: PRVPQU databaseName: Biological Science Database customDbUrl: eissn: 1553-7374 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0041316 issn: 1553-7374 databaseCode: M7P dateStart: 20050901 isFulltext: true titleUrlDefault: http://search.proquest.com/biologicalscijournals providerName: ProQuest – providerCode: PRVPQU databaseName: Health & Medical Collection customDbUrl: eissn: 1553-7374 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0041316 issn: 1553-7374 databaseCode: 7X7 dateStart: 20050901 isFulltext: true titleUrlDefault: https://search.proquest.com/healthcomplete providerName: ProQuest – providerCode: PRVPQU databaseName: ProQuest Central customDbUrl: eissn: 1553-7374 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0041316 issn: 1553-7374 databaseCode: BENPR dateStart: 20050901 isFulltext: true titleUrlDefault: https://www.proquest.com/central providerName: ProQuest – providerCode: PRVPQU databaseName: Publicly Available Content Database customDbUrl: eissn: 1553-7374 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0041316 issn: 1553-7374 databaseCode: PIMPY dateStart: 20050901 isFulltext: true titleUrlDefault: http://search.proquest.com/publiccontent providerName: ProQuest – providerCode: PRVATS databaseName: Public Library of Science (PLoS) : Open Access Journals [open access] customDbUrl: eissn: 1553-7374 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0041316 issn: 1553-7374 databaseCode: FPL dateStart: 20050101 isFulltext: true titleUrlDefault: http://www.plos.org/publications/ providerName: Public Library of Science |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3db9MwELdYAYkXxPcKo7IQEk9hSZzazmMHqzZpVNEAqTxZtufQSmtSNWnR_nvuErdq0Ka98BJVuUsd3118v0vOd4R8lABBXJrqwOT4toozHpjY2WAosYFIKsNc502zCTGZyOk0zfZafWFOWFseuBXcMQJaGEgaC64bfL1OIHSyjmvprjgzzda9UKTbYKpdg2FlbpqeYlOcQDDO_aY5JqJjr6PPy6WumwKkIXZi33NKTe3-3Qp9MMMEyd7yuqxuA6H_5lLuOafxM_LUo0o6amfznDxwxQvyuO0zefOS2K9YHtd3tqJlTgH1UUzuKuub5dxSn9SBFHBdV-WCzsoFXluuK4oh8wLi50aF1Od10fpPSTfzFdBxryaE26_Iz_Hpjy9nge-uEFgR8zqwoUksj10a2sjIOJcGBAE_DOMmjrTMGddXkbHGORbK1LhhLERoY0BMmuUAs16TXlEW7pDQ4VAbBshQJ84mRsRG8JynGsCdi6xNwj5hW_Eq60uPYweMa9V8TxMQgrRyUqgU5ZXSJ8HuqmVbeuMe_hPU3I4XC2c3J8CclDcndZ859ckH1LvC0hgF5t781uuqUuffJ2oUYwdGCDjFnUyXHaZPnikvYbJW-_0OIDIsudXhPOpwwgNuu6PNcKp70zobXSg8BwF0Ag4i2kR9cogmuhVMpQB3ABKE6DyGv9-a7e1kuiPjyJh0VziwLyW5ALidDMO7WVJsQIDbq_vkTfsc7O4TsKRgUQJ3JjpPSGciXUoxnzUFzhm6vpi9_R8KfUeetJ8BMEf1iPTq1dq9J4_spp5XqwE5EFPRHOWAPDw5nWSXg2YlgeM4uxhgKnAGlOz8W_brL50NeAA |
| linkProvider | Directory of Open Access Journals |
| linkToHtml | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V3Nb9MwFLe2DgQXvmGFARYCcQpL7DRODggNxtRqW1VtA42TsV1nrbQmoek29Z_ib-S9fJQGbXDagVsVvyR-7vt0nt-PkNchhCA2ipSjY9ytCnjgaGaN0wkRQCQK3VjFBdiE6PfD4-NosEJ-1mdhsKyytomFoR6mBvfIN8GOgmeDbIN9yH44iBqFX1drCI1SLHbt_AJStvx9bxv-3zeM7Xw--tR1KlQBxwgWzBzjat8EzEau8XTI4lCDi4UfmgeaeSqMeaCGnjbaWu6GkbYdJoRrGEQKiscQXsBzV8maj8LeImuD3v7gW237wSMUYKsIxuMIHgTVYT0uvM1KNt5lmZoVjU9dRIBfcoYFZsDCM6yOsDCzlZ2m-WXB7581nEtOcefu_7ac98idKvymW6W-3CcrNnlAbpaAnPOHxGxjH-EKAoymMYXwmA5GNkln82xsaNnrOceRA5UM0wntphO8Nz3LKWbyEz0ut1dpVQBHjy5S-nU8hfHDzIIhzR-RL9fC4WPSStLErhPa6SjNIYRWvjW-FkyLIA4iBVGw9Yzx3TbhtTxIU_VoR6iQU1l8eBSQq5XrJFGKZCVFbeIs7srKHiX_oP-IoragxQ7jxYV0eiIrgyUxkQQFD7WBkBlibOV3GDc2UKEdBlxHbfIKBVViD5EEi5RO1Fmey95hX24xhKqEzFxcSXTQIHpbEcUpMGtUdTAElgx7kzUoNxqUYAlN820jZHWJre7WnsRrLjABntQ799pkHXWqXphc_tYEeHytK5cP08UwvhmrExML8iXDQEBe4nfcq0kiRGrAc-ht8qRU3MU8IegW3PNhZqKh0g1GmiPJeFR0gucYIzD-9O8Tf0ludY_29-Rer7_7jNwuv4pgye4Gac2mZ_Y5uWHOZ-N8-qIyZ5R8v26V_wWgONwc |
| linkToPdf | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1Lb9QwELbaLSAuvKELBSIE4hSa2Fk7OSBUKFVXLatVW6pyMrbX6a7UJmGzbdW_xq9jJnGWBrVw6oHbKp487J3HN8l4PkJexwBBbJIoX6f4tooz7mtqjd-LkUAkiYNUpRXZhBgM4oODZLhAfjZ7YbCssvGJlaMe5Qbfka-CH4XIBtkGXU1dWcRwfeND8cNHBin80trQadQqsmXPzyB9K9_31-G_fkPpxue9T5u-YxjwjaB85ptAR4ZTmwQm1DFNYw3hFn5oxjUNVZwyrkahNtpaFsSJtj0qRGAooAbFUoAacN1FsgSQPKIdsjTsfxl-a-IARIeKeBWJeXzBOHcb95gIV52evCsKNauaoAbIBn8hMFb8AfMosTjGIs1OcZSXlwHhP-s5LwTIjbv_89LeI3ccLPfWaju6TxZs9oDcrIk6zx8Ss479hR01mJenHsBmbzi2WT47LybGq3tAlziyo7JRfuxt5sd4bn5SepjhH-tJ_drVc4Vx3t5Z7u1PpjC-W1hwsOUj8vVaZviYdLI8s8vE6_WUZgCtVWRNpAXVgqc8UYCObWhMFHQJa3RDGte7HSlEjmT1QVJADlevk0SNkk6jusSfn1XUvUv-If8R1W4ui53HqwP59FA6RyYxwQTDj7UBKA3YW0U9yozlKrYjznTSJa9QaSX2FslQlQ7VSVnK_u5ArlGksISMXVwptNMSeuuE0hwma5TbMAJLhj3LWpIrLUnwkKZ9tzFO9cK0Nte2JR4LYBIQYcPTsEuW0b6ahSnlb6uAyzd2c_mwNx_GO2PVYmZBv2TMBeQrUS-4WiRBBgfcn94lT2ojnj8ngHHBwgieTLTMuzWR9kg2GVcd4hliB8qe_v3BX5JbYOdyuz_YekZu1x9LsJJ3hXRm0xP7nNwwp7NJOX3hPJtHvl-3xf8CpmPk3A |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Distribution+of+the+phenotypic+effects+of+random+homologous+recombination+between+two+virus+species&rft.jtitle=PLoS+pathogens&rft.au=Florence+Vuillaume&rft.au=Ga%C3%ABl+Th%C3%A9baud&rft.au=Cica+Urbino&rft.au=Nad%C3%A8ge+Forfert&rft.date=2011-05-01&rft.pub=Public+Library+of+Science+%28PLoS%29&rft.issn=1553-7366&rft.eissn=1553-7374&rft.volume=7&rft.issue=5&rft.spage=e1002028&rft_id=info:doi/10.1371%2Fjournal.ppat.1002028&rft.externalDBID=DOA&rft.externalDocID=oai_doaj_org_article_6758ebe8bc264610a4523ce6a8ed63b9 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7374&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7374&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7374&client=summon |