Long-Term Cocirculation of Two Strains of Pepino Mosaic Virus in Tomato Crops and Its Effect on Population Genetic Variability

Mixed viral infections are common in plants, and the evolutionary dynamics of viral populations may differ depending on whether the infection is caused by single or multiple viral strains. However, comparative studies of single and mixed infections using viral populations in comparable agricultural and geographical locations are lacking. Here, we monitored the occurrence of pepino mosaic virus (PepMV) in tomato crops in two major tomato-producing areas in Murcia (southeastern Spain), supporting evidence showing that PepMV disease-affected plants had single infections of the Chilean 2 (CH2) strain in one area and the other area exhibited long-term (13 years) coexistence of the CH2 and European (EU) strains. We hypothesized that circulating strains of PepMV might be modulating the differentiation between them and shaping the evolutionary dynamics of PepMV populations. Our phylogenetic analysis of 106 CH2 isolates randomly selected from both areas showed a remarkable divergence between the CH2 isolates, with increased nucleotide variability in the geographical area where both strains cocirculate. Furthermore, the potential virus–virus interaction was studied further by constructing six full-length infectious CH2 clones from both areas, and assessing their viral fitness in the presence and absence of an EU-type isolate. All CH2 clones showed decreased fitness in mixed infections and although complete genome sequencing indicated a nucleotide divergence of those CH2 clones by area, the magnitude of the fitness response was irrespective of the CH2 origin. Overall, these results suggest that although agroecological cropping practices may be particularly important for explaining the evolutionary dynamics of PepMV in tomato crops, the cocirculation of both strains may have implications on the genetic variability of PepMV populations.

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Mixed Infections of Pepino Mosaic Virus Strains Modulate the Evolutionary Dynamics of this Emergent Virus

Journal of Virology ◽

10.1128/jvi.01486-09 ◽

2009 ◽

Vol 83 (23) ◽

pp. 12378-12387 ◽

Cited By ~ 72

Author(s):

P. Gómez ◽

R. N. Sempere ◽

S. F. Elena ◽

M. A. Aranda

Keyword(s):

Mosaic Virus ◽

Evolutionary Dynamics ◽

Economic Losses ◽

Mixed Infections ◽

In Planta ◽

Tomato Production ◽

Pepino Mosaic Virus ◽

Epidemiological Pattern ◽

Virus Emergence ◽

Virus Strains

ABSTRACT Pepino mosaic virus (PepMV) is an emerging pathogen that causes severe economic losses in tomato crops (Solanum lycopersicum L.) in the Northern hemisphere, despite persistent attempts of control. In fact, it is considered one of the most significant viral diseases for tomato production worldwide, and it may constitute a good model for the analysis of virus emergence in crops. We have combined a population genetics approach with an analysis of in planta properties of virus strains to explain an observed epidemiological pattern. Hybridization analysis showed that PepMV populations are composed of isolates of two types (PepMV-CH2 and PepMV-EU) that cocirculate. The CH2 type isolates are predominant; however, EU isolates have not been displaced but persist mainly in mixed infections. Two molecularly cloned isolates belonging to each type have been used to examine the dynamics of in planta single infections and coinfection, revealing that the CH2 type has a higher fitness than the EU type. Coinfections expand the range of susceptible hosts, and coinfected plants remain symptomless several weeks after infection, so a potentially important problem for disease prevention and management. These results provide an explanation of the observed epidemiological pattern in terms of genetic and ecological interactions among the different viral strains. Thus, mixed infections appear to be contributing to shaping the genetic structure and dynamics of PepMV populations.

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In situ hybridization for the localization of two pepino mosaic virus isolates in mixed infections

Journal of Virological Methods ◽

10.1016/j.jviromet.2019.02.003 ◽

2019 ◽

Vol 267 ◽

pp. 42-47 ◽

Cited By ~ 1

Author(s):

C. Gómez-Aix ◽

C. Alcaide ◽

P. Gómez ◽

M.A. Aranda ◽

M.A. Sánchez-Pina

Keyword(s):

In Situ Hybridization ◽

Mosaic Virus ◽

Mixed Infections ◽

Pepino Mosaic Virus ◽

Virus Isolates

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Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants

Viruses ◽

10.3390/v12080879 ◽

2020 ◽

Vol 12 (8) ◽

pp. 879 ◽

Cited By ~ 1

Author(s):

Chen Klap ◽

Neta Luria ◽

Elisheva Smith ◽

Lior Hadad ◽

Elena Bakelman ◽

...

Keyword(s):

Mosaic Virus ◽

High Throughput Sequencing ◽

Amino Acid Position ◽

Viral Disease ◽

Mixed Infections ◽

Rt Pcr ◽

Tomato Production ◽

Pepino Mosaic Virus ◽

Disease Symptoms ◽

Tomato Plants

The tobamovirus tomato brown rugose fruit virus (ToBRFV), a major threat to tomato production worldwide, has recently been documented in mixed infections with the potexvirus pepino mosaic virus (PepMV) CH2 strain in traded tomatoes in Israel. A study of greenhouse tomato plants in Israel revealed severe new viral disease symptoms including open unripe fruits and yellow patched leaves. PepMV was only detected in mixed infections with ToBRFV in all 104 tested sites, using serological and molecular analyses. Six PepMV isolates were identified, all had predicted amino acids characteristic of CH2 mild strains excluding an isoleucine at amino acid position 995 of the replicase. High-throughput sequencing of viral RNA extracted from four selected symptomatic plants showed solely the ToBRFV and PepMV, with total aligned read ratios of 40.61% and 11.73%, respectively, indicating prevalence of the viruses. Analyses of interactions between the co-infecting viruses by sequential and mixed viral inoculations of tomato plants, at various temperatures, showed a prominent increase in PepMV titers in ToBRFV pre-inoculated plants and in mixed-infected plants at 18–25 °C, compared to PepMV-single inoculations, as analyzed by Western blot and quantitative RT-PCR tests. These results suggest that Israeli mild PepMV isolate infections, preceded by ToBRFV, could induce symptoms characteristic of PepMV aggressive strains.

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Rapid evolutionary dynamics of the Pepino mosaic virus – status and future perspectives

Journal of Plant Protection Research ◽

10.1515/jppr-2016-0054 ◽

2016 ◽

Vol 56 (4) ◽

pp. 337-345 ◽

Cited By ~ 3

Author(s):

Julia Minicka ◽

Beata Hasiów-Jaroszewska ◽

Natasza Borodynko-Filas ◽

Henryk Pospieszny ◽

Inge Maria Hanssen

Keyword(s):

Mosaic Virus ◽

Evolutionary Dynamics ◽

Current Knowledge ◽

Plant Protection ◽

Diagnostic Tools ◽

Nucleotide Substitutions ◽

Single Nucleotide ◽

Pepino Mosaic Virus ◽

Worldwide Population ◽

Protection Strategies

AbstractPepino mosaic virus (PepMV) has emerged as an important pathogen of greenhouse tomato crops and is currently distributed worldwide. Population genetic studies have revealed a shift in the dominant PepMV genotype from European (EU) to Chilean 2 (CH2) in North America and several European countries. New genetic variants are constantly being created by mutation and recombination events. Single nucleotide substitutions in different parts of the genome were found to affect on development of symptoms resulting in new pathotypes and accumulation of viral RNA. The variability of the PepMV population has a great impact on designing specific diagnostic tools and developing efficient and durable strategies of disease control. In this paper we review the current knowledge about the PepMV population, the evolutionary dynamics of this highly infective virus, methods for its detection and plant protection strategies.

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Life-history specialization was not an evolutionary dead-end in Pyrenean cave beetles

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.2978 ◽

2014 ◽

Vol 281 (1781) ◽

pp. 20132978 ◽

Cited By ~ 36

Author(s):

Alexandra Cieslak ◽

Javier Fresneda ◽

Ignacio Ribera

Keyword(s):

Life History ◽

Evolutionary Dynamics ◽

Geographical Area ◽

Phenotypic Changes ◽

Dead End ◽

Single Transition ◽

Colonization Process ◽

Phylogenetic Framework ◽

Complex Characters

Research on subterranean organisms has focused on the colonization process and some of the associated phenotypic changes, but little is known on the long-term evolutionary dynamics of subterranean lineages and the origin of some highly specialized complex characters. One of the most extreme modifications is the reduction of the number of larval instars in some Leptodirini beetles from the ancestral 3 to 2 and ultimately a single instar. This reduction is usually assumed to have occurred independently multiple times within the same lineage and geographical area, but its evolution has never been studied in a phylogenetic framework. Using a comprehensive molecular phylogeny, we found a low number of independent origins of the reduction in the number of instars, with a single transition, dated to the Oligocene–Miocene, from 3 to 2 and then 1 instar in the Pyrenees, the best-studied area. In the Pyrenees, the 1-instar lineage had a diversification rate (0.22 diversification events per lineage per million years) significantly higher than that of 3- or 2-instar lineages (0.10), and similar to that seen in other Coleopteran radiations. Far from being evolutionary dead-ends, ancient lineages fully adapted to subterranean life seem able to persist and diversify over long evolutionary periods.

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Determinants of Persistent Patterns of Pepino Mosaic Virus Mixed Infections

Frontiers in Microbiology ◽

10.3389/fmicb.2021.694492 ◽

2021 ◽

Vol 12 ◽

Author(s):

Cristina Alcaide ◽

Miguel A. Aranda

Keyword(s):

Mosaic Virus ◽

Economic Losses ◽

Mixed Infections ◽

Strong Positive Correlation ◽

In Planta ◽

Nucleotide Substitutions ◽

Challenge Inoculation ◽

Pepino Mosaic Virus ◽

Time Lagged ◽

Viral Accumulation

Pepino mosaic virus (PepMV) has become a pandemic virus in tomato crops, causing important economic losses worldwide. In Spain, isolates of the EU and CH2 strains co-circulate, with PepMV-EU predominantly found in mixed infections. Simultaneous in planta mixed infections result in an asymmetric antagonism against PepMV-CH2, but the outcome of over-infections has never been tested. PepMV-EU and PepMV-CH2 time-lagged inoculations were performed, and viral accumulation was measured 10 days after challenge inoculation. PepMV-EU had a protective effect over PepMV-CH2; in contrast, the accumulation of PepMV-EU increased in plants pre-inoculated with PepMV-CH2 as compared to single infections. We also studied the effect of the type of infection on viral transmission. Independently of the nature of the infection (single or mixed), we observed a strong positive correlation between virus accumulation in the source plant and transmission, excluding mixed infection effects different than modulating viral accumulation. Finally, in order to determine the genetic variability of PepMV strains in single and mixed infections, a 430 nucleotide region was RT-PCR amplified from samples from a serial passages experiment and deep-sequenced. No significant differences were found in the number of nucleotide substitutions between single and mixed infections for PepMV-EU; in contrast, significant differences were found for PepMV-CH2, which was more variable in single than in mixed infections. Comparing PepMV-EU with PepMV-CH2, a higher nucleotide diversity was found for PepMV-CH2. Collectively, our data strongly suggest that PepMV mixed infections can impact the virus epidemiology by modulating in planta virus strain accumulation and diversification.

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