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

Full description

Bibliographic Details
Main Authors: Chen Klap, Neta Luria, Elisheva Smith, Lior Hadad, Elena Bakelman, Noa Sela, Eduard Belausov, Oded Lachman, Diana Leibman, Aviv Dombrovsky
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/12/8/879
_version_ 1797558783474401280
author Chen Klap
Neta Luria
Elisheva Smith
Lior Hadad
Elena Bakelman
Noa Sela
Eduard Belausov
Oded Lachman
Diana Leibman
Aviv Dombrovsky
author_facet Chen Klap
Neta Luria
Elisheva Smith
Lior Hadad
Elena Bakelman
Noa Sela
Eduard Belausov
Oded Lachman
Diana Leibman
Aviv Dombrovsky
author_sort Chen Klap
collection DOAJ
description 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.
first_indexed 2024-03-10T17:36:16Z
format Article
id doaj.art-227e2135ac1241b9b8dbdb83c2fc35e0
institution Directory Open Access Journal
issn 1999-4915
language English
last_indexed 2024-03-10T17:36:16Z
publishDate 2020-08-01
publisher MDPI AG
record_format Article
series Viruses
spelling doaj.art-227e2135ac1241b9b8dbdb83c2fc35e02023-11-20T09:50:45ZengMDPI AGViruses1999-49152020-08-0112887910.3390/v12080879Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato PlantsChen Klap0Neta Luria1Elisheva Smith2Lior Hadad3Elena Bakelman4Noa Sela5Eduard Belausov6Oded Lachman7Diana Leibman8Aviv Dombrovsky9Department of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Ornamental Plants and Agricultural Biotechnology, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelThe 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.https://www.mdpi.com/1999-4915/12/8/879synergismin situ immunofluorescencemixed infections
spellingShingle Chen Klap
Neta Luria
Elisheva Smith
Lior Hadad
Elena Bakelman
Noa Sela
Eduard Belausov
Oded Lachman
Diana Leibman
Aviv Dombrovsky
Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants
Viruses
synergism
in situ immunofluorescence
mixed infections
title Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants
title_full Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants
title_fullStr Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants
title_full_unstemmed Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants
title_short Tomato Brown Rugose Fruit Virus Contributes to Enhanced Pepino Mosaic Virus Titers in Tomato Plants
title_sort tomato brown rugose fruit virus contributes to enhanced pepino mosaic virus titers in tomato plants
topic synergism
in situ immunofluorescence
mixed infections
url https://www.mdpi.com/1999-4915/12/8/879
work_keys_str_mv AT chenklap tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT netaluria tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT elishevasmith tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT liorhadad tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT elenabakelman tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT noasela tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT eduardbelausov tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT odedlachman tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT dianaleibman tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants
AT avivdombrovsky tomatobrownrugosefruitviruscontributestoenhancedpepinomosaicvirustitersintomatoplants