Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome interaction networks

Darren P. Martin, Pierre Lefeuvre, Arvind Varsani, Murielle Hoareau, Jean Yves Semegni, Betty Dijoux, Claire Vincent, Bernard Reynaud, Jean Michel Lett

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Genetic recombination is an important process during the evolution of many virus species and occurs particularly frequently amongst begomoviruses in the single stranded DNA virus family, Geminiviridae. As in many other recombining viruses it is apparent that non-random recombination breakpoint distributions observable within begomovirus genomes sampled from nature are the product of variations both in basal recombination rates across genomes and in the over-all viability of different recombinant genomes. Whereas factors influencing basal recombination rates might include local degrees of sequence similarity between recombining genomes, nucleic acid secondary structures and genomic sensitivity to nuclease attack or breakage, the viability of recombinant genomes could be influenced by the degree to which their co-evolved protein-protein and protein-nucleotide and nucleotide-nucleotide interactions are disreputable by recombination. Here we investigate patterns of recombination that occur over 120 day long experimental infections of tomato plants with the begomoviruses Tomato yellow leaf curl virus and Tomato leaf curl Comoros virus. We show that patterns of sequence exchange between these viruses can be extraordinarily complex and present clear evidence that factors such as local degrees of sequence similarity but not genomic secondary structure strongly influence where recombination breakpoints occur. It is also apparent from our experiment that over-all patterns of recombination are strongly influenced by selection against individual recombinants displaying disrupted intra-genomic interactions such as those required for proper protein and nucleic acid folding. Crucially, we find that selection favoring the preservation of co-evolved longer-range protein-protein and protein DNA interactions is so strong that its imprint can even be used to identify the exact sequence tracts involved in these interactions.

Original languageEnglish (US)
Article numbere1002203
JournalPLoS Pathogens
Volume7
Issue number9
DOIs
StatePublished - Sep 2011
Externally publishedYes

Fingerprint

Geminiviridae
Coinfection
Genetic Recombination
Genome
Begomovirus
Viruses
Lycopersicon esculentum
Proteins
Nucleotides
Nucleic Acids
Comoros
DNA Viruses
Single-Stranded DNA

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

Cite this

Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome interaction networks. / Martin, Darren P.; Lefeuvre, Pierre; Varsani, Arvind; Hoareau, Murielle; Semegni, Jean Yves; Dijoux, Betty; Vincent, Claire; Reynaud, Bernard; Lett, Jean Michel.

In: PLoS Pathogens, Vol. 7, No. 9, e1002203, 09.2011.

Research output: Contribution to journalArticle

Martin, Darren P. ; Lefeuvre, Pierre ; Varsani, Arvind ; Hoareau, Murielle ; Semegni, Jean Yves ; Dijoux, Betty ; Vincent, Claire ; Reynaud, Bernard ; Lett, Jean Michel. / Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome interaction networks. In: PLoS Pathogens. 2011 ; Vol. 7, No. 9.
@article{b26169cf2ecd4e7fa9f7b905426cd37f,
title = "Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome interaction networks",
abstract = "Genetic recombination is an important process during the evolution of many virus species and occurs particularly frequently amongst begomoviruses in the single stranded DNA virus family, Geminiviridae. As in many other recombining viruses it is apparent that non-random recombination breakpoint distributions observable within begomovirus genomes sampled from nature are the product of variations both in basal recombination rates across genomes and in the over-all viability of different recombinant genomes. Whereas factors influencing basal recombination rates might include local degrees of sequence similarity between recombining genomes, nucleic acid secondary structures and genomic sensitivity to nuclease attack or breakage, the viability of recombinant genomes could be influenced by the degree to which their co-evolved protein-protein and protein-nucleotide and nucleotide-nucleotide interactions are disreputable by recombination. Here we investigate patterns of recombination that occur over 120 day long experimental infections of tomato plants with the begomoviruses Tomato yellow leaf curl virus and Tomato leaf curl Comoros virus. We show that patterns of sequence exchange between these viruses can be extraordinarily complex and present clear evidence that factors such as local degrees of sequence similarity but not genomic secondary structure strongly influence where recombination breakpoints occur. It is also apparent from our experiment that over-all patterns of recombination are strongly influenced by selection against individual recombinants displaying disrupted intra-genomic interactions such as those required for proper protein and nucleic acid folding. Crucially, we find that selection favoring the preservation of co-evolved longer-range protein-protein and protein DNA interactions is so strong that its imprint can even be used to identify the exact sequence tracts involved in these interactions.",
author = "Martin, {Darren P.} and Pierre Lefeuvre and Arvind Varsani and Murielle Hoareau and Semegni, {Jean Yves} and Betty Dijoux and Claire Vincent and Bernard Reynaud and Lett, {Jean Michel}",
year = "2011",
month = "9",
doi = "10.1371/journal.ppat.1002203",
language = "English (US)",
volume = "7",
journal = "PLoS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science",
number = "9",

}

TY - JOUR

T1 - Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome interaction networks

AU - Martin, Darren P.

AU - Lefeuvre, Pierre

AU - Varsani, Arvind

AU - Hoareau, Murielle

AU - Semegni, Jean Yves

AU - Dijoux, Betty

AU - Vincent, Claire

AU - Reynaud, Bernard

AU - Lett, Jean Michel

PY - 2011/9

Y1 - 2011/9

N2 - Genetic recombination is an important process during the evolution of many virus species and occurs particularly frequently amongst begomoviruses in the single stranded DNA virus family, Geminiviridae. As in many other recombining viruses it is apparent that non-random recombination breakpoint distributions observable within begomovirus genomes sampled from nature are the product of variations both in basal recombination rates across genomes and in the over-all viability of different recombinant genomes. Whereas factors influencing basal recombination rates might include local degrees of sequence similarity between recombining genomes, nucleic acid secondary structures and genomic sensitivity to nuclease attack or breakage, the viability of recombinant genomes could be influenced by the degree to which their co-evolved protein-protein and protein-nucleotide and nucleotide-nucleotide interactions are disreputable by recombination. Here we investigate patterns of recombination that occur over 120 day long experimental infections of tomato plants with the begomoviruses Tomato yellow leaf curl virus and Tomato leaf curl Comoros virus. We show that patterns of sequence exchange between these viruses can be extraordinarily complex and present clear evidence that factors such as local degrees of sequence similarity but not genomic secondary structure strongly influence where recombination breakpoints occur. It is also apparent from our experiment that over-all patterns of recombination are strongly influenced by selection against individual recombinants displaying disrupted intra-genomic interactions such as those required for proper protein and nucleic acid folding. Crucially, we find that selection favoring the preservation of co-evolved longer-range protein-protein and protein DNA interactions is so strong that its imprint can even be used to identify the exact sequence tracts involved in these interactions.

AB - Genetic recombination is an important process during the evolution of many virus species and occurs particularly frequently amongst begomoviruses in the single stranded DNA virus family, Geminiviridae. As in many other recombining viruses it is apparent that non-random recombination breakpoint distributions observable within begomovirus genomes sampled from nature are the product of variations both in basal recombination rates across genomes and in the over-all viability of different recombinant genomes. Whereas factors influencing basal recombination rates might include local degrees of sequence similarity between recombining genomes, nucleic acid secondary structures and genomic sensitivity to nuclease attack or breakage, the viability of recombinant genomes could be influenced by the degree to which their co-evolved protein-protein and protein-nucleotide and nucleotide-nucleotide interactions are disreputable by recombination. Here we investigate patterns of recombination that occur over 120 day long experimental infections of tomato plants with the begomoviruses Tomato yellow leaf curl virus and Tomato leaf curl Comoros virus. We show that patterns of sequence exchange between these viruses can be extraordinarily complex and present clear evidence that factors such as local degrees of sequence similarity but not genomic secondary structure strongly influence where recombination breakpoints occur. It is also apparent from our experiment that over-all patterns of recombination are strongly influenced by selection against individual recombinants displaying disrupted intra-genomic interactions such as those required for proper protein and nucleic acid folding. Crucially, we find that selection favoring the preservation of co-evolved longer-range protein-protein and protein DNA interactions is so strong that its imprint can even be used to identify the exact sequence tracts involved in these interactions.

UR - http://www.scopus.com/inward/record.url?scp=80053371350&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80053371350&partnerID=8YFLogxK

U2 - 10.1371/journal.ppat.1002203

DO - 10.1371/journal.ppat.1002203

M3 - Article

C2 - 21949649

AN - SCOPUS:80053371350

VL - 7

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 9

M1 - e1002203

ER -