Tobamoviruses and Interacting Viruses in Modern Agriculture

A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Protection and Biotic Interactions".

Deadline for manuscript submissions: closed (30 June 2022) | Viewed by 38937

Special Issue Editors


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Guest Editor
Department of Plant Pathology and Weed Research, Agricultural Research Organization ARO | aro, Bet Dagan, Israel
Interests: tomato; viruses; TMV; ToMV; ToBRFV; cucumber green mottle mosaic virus (CGMMV)

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Guest Editor
Department of Plant Pathology, University of Florida, Southwest Florida Research and Education Center, 2685 State Road 29 North, Immokalee, FL 34142, USA
Interests: plant virus and virus-like pathogen detection; identification and characterization; epidemiology and etiology of pathogens; virus-vector-host interaction; use of viruses in biotechnology, and integrated pest management

Special Issue Information

Dear Colleagues,

Viruses in the genus Tobamovirus (family Virgaviridae) traditionally caused severe losses in many economically important crops such as tomato, pepper, and cucurbits. Implementation of hygiene measures, virus-free seeds and virus-resistant crop varieties helped effectively manage these viruses and reduce economic losses worldwide. However, this situation has recently changed with the re-emergence (e.g., cucumber green mottle mosaic virus [CGMMV]) and the emergence (e.g., tomato brown rugose fruit virus [ToBRFV]) of several tobamoviruses. CGMMV has spread worldwide in cucurbits, and ToBRFV spread is occurring in Mediterranean, European, Asian, and American tomatoes amid the background of pepino mosaic virus (PepMV), a potexvirus already established worldwide. The extreme persistence and robust infectivity of these viruses, ever increasing global seed and fruit trade, and the widespread use of tolerant- rather than resistant-crop varieties, together with intricate interaction of these viruses with other plant viruses in mixed infections, undoubtedly played a substantial role in altering virus disease outbreak patterns, and are posing a great threat to today’s agriculture.

Biology, epidemiology and etiology of emerging and re-emerging tobamoviruses and their interacting non-tobamovirus partners in different host backgrounds are focus subjects for the forthcoming Special Issue of Plants. Therefore, we are excited to invite authors to contribute to their new, relevant, and important knowledge on the subject by submitting their applied and fundamental research reports. We welcome you to submit research or review articles, short notes, as well as communications related to tobamoviruses. Contents will also include efforts for developing new hygienic measures and effective disease management strategies in various production types, improving crops for resistance, and use of biotechnological and genomic approaches for tobamovirus control. We look forward to your contribution.

Dr. Aviv Dombrovsky
Dr. Ozgur Batuman
Guest Editors

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Keywords

  • epidemiology
  • etiology
  • plant-pathogen interaction
  • tobamovirus-tolerant/resistant varieties

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Published Papers (7 papers)

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Research

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14 pages, 4300 KiB  
Article
Pepper Plants Harboring L Resistance Alleles Showed Tolerance toward Manifestations of Tomato Brown Rugose Fruit Virus Disease
by Or Eldan, Arie Ofir, Neta Luria, Chen Klap, Oded Lachman, Elena Bakelman, Eduard Belausov, Elisheva Smith and Aviv Dombrovsky
Plants 2022, 11(18), 2378; https://doi.org/10.3390/plants11182378 - 12 Sep 2022
Cited by 12 | Viewed by 4478
Abstract
The tobamovirus tomato brown rugose fruit virus (ToBRFV) infects tomato plants harboring the Tm-22 resistance allele, which corresponds with tobamoviruses’ avirulence (Avr) gene encoding the movement protein to activate a resistance-associated hypersensitive response (HR). ToBRFV has caused severe damage to [...] Read more.
The tobamovirus tomato brown rugose fruit virus (ToBRFV) infects tomato plants harboring the Tm-22 resistance allele, which corresponds with tobamoviruses’ avirulence (Avr) gene encoding the movement protein to activate a resistance-associated hypersensitive response (HR). ToBRFV has caused severe damage to tomato crops worldwide. Unlike tomato plants, pepper plants harboring the L resistance alleles, which correspond with the tobamovirus Avr gene encoding the coat protein, have shown HR manifestations upon ToBRFV infection. We have found that ToBRFV inoculation of a wide range of undefined pepper plant varieties could cause a “hypersensitive-like cell death” response, which was associated with ToBRFV transient systemic infection dissociated from disease symptom manifestations on fruits. Susceptibility of pepper plants harboring L1, L3, or L4 resistance alleles to ToBRFV infection following HRs was similarly transient and dissociated from disease symptom manifestations on fruits. Interestingly, ToBRFV stable infection of a pepper cultivar not harboring the L gene was also not associated with disease symptoms on fruits, although ToBRFV was localized in the seed epidermis, parenchyma, and endothelium, which borders the endosperm, indicating that a stable infection of maternal origin of these tissues occurred. Pepper plants with systemic ToBRFV infection could constitute an inoculum source for adjacently grown tomato plants. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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11 pages, 718 KiB  
Article
New Weed Hosts for Tomato Brown Rugose Fruit Virus in Wild Mediterranean Vegetation
by Nida’ M. Salem, Motasem Abumuslem, Massimo Turina, Nezar Samarah, Abdullah Sulaiman, Barakat Abu-Irmaileh and Yousra Ata
Plants 2022, 11(17), 2287; https://doi.org/10.3390/plants11172287 - 1 Sep 2022
Cited by 18 | Viewed by 4085
Abstract
Tomato brown rugose fruit virus (ToBRFV; genus, Tobamovirus, family, Virgaviridae) was first reported in 2015 infecting tomatoes grown under protected cropping in the Jordan Valley. Since then, ToBRFV has been detected in tomatoes grown in both protected and open fields across Jordan. [...] Read more.
Tomato brown rugose fruit virus (ToBRFV; genus, Tobamovirus, family, Virgaviridae) was first reported in 2015 infecting tomatoes grown under protected cropping in the Jordan Valley. Since then, ToBRFV has been detected in tomatoes grown in both protected and open fields across Jordan. The increased incidence of ToBRFV prompted this investigation of the potential role of natural weed hosts in the dissemination of ToBRFV. A survey was conducted in the Jordan Valley and highlands to determine possible reservoir hosts of ToBRFV in fields and greenhouse complexes in which tomatoes were grown. Detection of ToBRFV infection was made by double-antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) and further confirmation by reverse-transcription polymerase chain reaction (RT-PCR), followed by DNA cloning and sequencing, and bioassays. Thirty weed species belonging to twenty-six genera from sixteen families were tested. Twelve species belonging to eight families were infected of which ten species are newly reported hosts for ToBRFV. Seed transmission of ToBRFV in Solanum nigrum was confirmed in a grow-out experiment. To our knowledge, this is the first report of the natural occurrence of ToBRFV on weed hosts. Identification of natural reservoirs of ToBRFV can help to develop management practices focused on weed plant species to prevent ToBRFV transmission. The extent to which ToBRFV survives in diverse alternate weed host species outside tomato growing seasons in different world regions requires further research in order to establish the risk associated with the possible contribution of weeds as a reservoir for primary infections in tomato crops. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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19 pages, 2030 KiB  
Article
Development and Validation of a One-Step Reverse Transcription Real-Time PCR Assay for Simultaneous Detection and Identification of Tomato Mottle Mosaic Virus and Tomato Brown Rugose Fruit Virus
by Antonio Tiberini, Ariana Manglli, Anna Taglienti, Ana Vučurović, Jakob Brodarič, Luca Ferretti, Marta Luigi, Andrea Gentili and Nataša Mehle
Plants 2022, 11(4), 489; https://doi.org/10.3390/plants11040489 - 11 Feb 2022
Cited by 10 | Viewed by 4490
Abstract
Tobamovirus species represent a threat to solanaceous crops worldwide, due to their extreme stability and because they are seed borne. In particular, recent outbreaks of tomato brown rugose fruit virus in tomato and pepper crops led to the establishment of prompt control measures, [...] Read more.
Tobamovirus species represent a threat to solanaceous crops worldwide, due to their extreme stability and because they are seed borne. In particular, recent outbreaks of tomato brown rugose fruit virus in tomato and pepper crops led to the establishment of prompt control measures, and the need for reliable diagnosis was urged. Another member of the genus, tomato mottle mosaic virus, has recently gained attention due to reports in different continents and its common features with tomato brown rugose fruit virus. In this study, a new real-time RT-PCR detection system was developed for tomato brown rugose fruit virus and tomato mottle mosaic virus on tomato leaves and seeds using TaqMan chemistry. This test was designed to detect tomato mottle mosaic virus by amplifying the movement protein gene in a duplex assay with the tomato brown rugose fruit virus target on the CP-3’NTR region, which was previously validated as a single assay. The performance of this test was evaluated, displaying analytical sensitivity 10−5–10−6-fold dilution for seeds and leaves, respectively, and good analytical specificity, repeatability, and reproducibility. Using the newly developed and validated test, tomato brown rugose fruit virus detection was 100% concordant with previously performed analyses on 106 official samples collected in 2021 from different continents. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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11 pages, 56592 KiB  
Article
Leaf Plasmodesmata Respond Differently to TMV, ToBRFV and TYLCV Infection
by Yaarit Kutsher, Dalia Evenor, Eduard Belausov, Moshe Lapidot and Moshe Reuveni
Plants 2021, 10(7), 1442; https://doi.org/10.3390/plants10071442 - 14 Jul 2021
Cited by 4 | Viewed by 3932
Abstract
Macromolecule and cytosolic signal distribution throughout the plant employs a unique cellular and intracellular mechanism called plasmodesmata (PD). Plant viruses spread throughout plants via PD using their movement proteins (MPs). Viral MPs induce changes in plasmodesmata’s structure and alter their ability to move [...] Read more.
Macromolecule and cytosolic signal distribution throughout the plant employs a unique cellular and intracellular mechanism called plasmodesmata (PD). Plant viruses spread throughout plants via PD using their movement proteins (MPs). Viral MPs induce changes in plasmodesmata’s structure and alter their ability to move macromolecule and cytosolic signals. The developmental distribution of a family member of proteins termed plasmodesmata located proteins number 5 (PDLP5) conjugated to GFP (PDLP5-GFP) is described here. The GFP enables the visual localization of PDLP5 in the cell via confocal microscopy. We observed that PDLP5-GFP protein is present in seed protein bodies and immediately after seed imbibition in the plasma membrane. The effect of three different plant viruses, the tobacco mosaic virus (TMV), tomato brown rugose fruit virus (ToBRFV, tobamoviruses), and tomato yellow leaf curl virus (TYLCV, begomoviruses), on PDLP5-GFP accumulation at the plasmodesmata was tested. In tobacco leaf, TMV and ToBRFV increased PDLP5-GFP amount at the plasmodesmata of cell types compared to control. However, there was no statistically significant difference in tomato leaf. On the other hand, TYLCV decreased PDLP5-GFP quantity in plasmodesmata in all tomato leaf cells compared to control, without any significant effect on plasmodesmata in tobacco leaf cells. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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11 pages, 1663 KiB  
Article
Differential Detection of the Tobamoviruses Tomato Mosaic Virus (ToMV) and Tomato Brown Rugose Fruit Virus (ToBRFV) Using CRISPR-Cas12a
by Dan Mark Alon, Hagit Hak, Menachem Bornstein, Gur Pines and Ziv Spiegelman
Plants 2021, 10(6), 1256; https://doi.org/10.3390/plants10061256 - 21 Jun 2021
Cited by 39 | Viewed by 8238
Abstract
CRISPR/Cas12a-based detection is a novel approach for the efficient, sequence-specific identification of viruses. Here we adopt the use of CRISPR/Cas12a to identify the tomato brown rugose fruit virus (ToBRFV), a new and emerging tobamovirus which is causing substantial damage to the global tomato [...] Read more.
CRISPR/Cas12a-based detection is a novel approach for the efficient, sequence-specific identification of viruses. Here we adopt the use of CRISPR/Cas12a to identify the tomato brown rugose fruit virus (ToBRFV), a new and emerging tobamovirus which is causing substantial damage to the global tomato industry. Specific CRISPR RNAs (crRNAs) were designed to detect either ToBRFV or the closely related tomato mosaic virus (ToMV). This technology enabled the differential detection of ToBRFV and ToMV. Sensitivity assays revealed that viruses can be detected from 15–30 ng of RT-PCR product, and that specific detection could be achieved from a mix of ToMV and ToBRFV. In addition, we show that this method can enable the identification of ToBRFV in samples collected from commercial greenhouses. These results demonstrate a new method for species-specific detection of tobamoviruses. A future combination of this approach with isothermal amplification could provide a platform for efficient and user-friendly ways to distinguish between closely related strains and resistance-breaking pathogens. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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16 pages, 2573 KiB  
Article
Identification and Mapping of Tomato Genome Loci Controlling Tolerance and Resistance to Tomato Brown Rugose Fruit Virus
by Avner Zinger, Moshe Lapidot, Arye Harel, Adi Doron-Faigenboim, Dana Gelbart and Ilan Levin
Plants 2021, 10(1), 179; https://doi.org/10.3390/plants10010179 - 19 Jan 2021
Cited by 35 | Viewed by 7244
Abstract
Tomato brown rugose fruit virus (ToBRFV) was identified in Israel during October 2014 in tomato plants (Solanum lycopersicum). These plants, carrying the durable resistance gene against tomato mosaic virus, Tm-22, displayed severe disease symptoms and losses to fruit yield [...] Read more.
Tomato brown rugose fruit virus (ToBRFV) was identified in Israel during October 2014 in tomato plants (Solanum lycopersicum). These plants, carrying the durable resistance gene against tomato mosaic virus, Tm-22, displayed severe disease symptoms and losses to fruit yield and quality. These plants were found infected with a tobamovirus similar to that discovered earlier in Jordan. This study was designed to screen and identify tomato genotypes resistant or tolerant to ToBRFV. The identified resistance and tolerance traits were further characterized virologically and genetically. Finally, DNA markers linked to genes controlling these traits were developed as tools to expedite resistance breeding. To achieve these objectives, 160 genotypes were screened, resulting in the identification of an unexpectedly high number of tolerant genotypes and a single genotype resistant to the virus. A selected tolerant genotype and the resistant genotype were further analyzed. Analysis of genetic inheritance revealed that a single recessive gene controls tolerance whereas at least two genes control resistance. Allelic test between the tolerant and the resistant genotype revealed that these two genotypes share a locus controlling tolerance, mapped to chromosome 11. This locus displayed a strong association with the tolerance trait, explaining nearly 91% of its variation in segregating populations. This same locus displayed a statistically significant association with symptom levels in segregating populations based on the resistant genotype. However, in these populations, the locus was able to explain only ~41% of the variation in symptom levels, confirming that additional loci are involved in the genetic control of the resistance trait in this genotype. A locus on chromosome 2, at the region of the Tm-1 gene, was finally found to interact with the locus discovered on chromosome 11 to control resistance. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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Review

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13 pages, 1909 KiB  
Review
To Be Seen or Not to Be Seen: Latent Infection by Tobamoviruses
by Rabia Ilyas, Mareike J. Rohde, Katja R. Richert-Pöggeler and Heiko Ziebell
Plants 2022, 11(16), 2166; https://doi.org/10.3390/plants11162166 - 21 Aug 2022
Cited by 18 | Viewed by 4204
Abstract
Tobamoviruses are among the most well-studied plant viruses and yet there is still a lot to uncover about them. On one side of the spectrum, there are damage-causing members of this genus: such as the tobacco mosaic virus (TMV), tomato brown rugose fruit [...] Read more.
Tobamoviruses are among the most well-studied plant viruses and yet there is still a lot to uncover about them. On one side of the spectrum, there are damage-causing members of this genus: such as the tobacco mosaic virus (TMV), tomato brown rugose fruit virus (ToBRFV) and cucumber green mottle mosaic virus (CGMMV), on the other side, there are members which cause latent infection in host plants. New technologies, such as high-throughput sequencing (HTS), have enabled us to discover viruses from asymptomatic plants, viruses in mixed infections where the disease etiology cannot be attributed to a single entity and more and more researchers a looking at non-crop plants to identify alternative virus reservoirs, leading to new virus discoveries. However, the diversity of these interactions in the virosphere and the involvement of multiple viruses in a single host is still relatively unclear. For such host–virus interactions in wild plants, symptoms are not always linked with the virus titer. In this review, we refer to latent infection as asymptomatic infection where plants do not suffer despite systemic infection. Molecular mechanisms related to latent behavior of tobamoviruses are unknown. We will review different studies which support different theories behind latency. Full article
(This article belongs to the Special Issue Tobamoviruses and Interacting Viruses in Modern Agriculture)
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