Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the <i>Tm‐2<sup>2</sup></i> resistance gene

Yan, Zhi‐Yong; Ma, Hua-Yu; Wang, Lu; Tettey, Carlos Kwesi; Zhao, Meisheng; Geng, Chao; Tian, Yanping; Li, Xiangdong

doi:10.1111/mpp.13115

Cited by 28 publications

(31 citation statements)

References 40 publications

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“…The ORF3‐encoded 30‐kDa is a movement protein (MP) that is essential for viral cell‐to‐cell movement. Two recent studies have shown that ToBRFV MP is the key factor for overcoming Tm‐2 2 ‐mediated resistance (Hak & Spiegelman, 2021 ; Yan et al, 2021a ). The coat protein (CP) encoded by ORF4 has a predicted mass of 17.5 kDa and is involved in viral particle assembly and long‐distance movement (Ishibashi & Ishikawa, 2016 ).…”

Section: Genome Organization and Sequence Diversitymentioning

confidence: 99%

“…Using a hybrid protein approach, they further determined that the amino acids 1 to 266 rather than the C‐terminal region of the ToBRFV MP is responsible for breakdown of Tm‐2 2 resistance (Hak & Spiegelman, 2021 ). Concomitantly and independently, Yan et al ( 2021a ) conducted both loss‐of‐function and gain‐of‐function assays using chimeric TMV and ToBRFV infectious clones where the MP coding gene was reciprocally swapped, and concluded that the ToBRFV MP is the virulence determinant for ToBRFV to infect Tm‐2 2 plants. They further mapped the region of ToBRFV MP necessary for breakdown of Tm‐2 2 resistance to the central domain (amino acids 60–186) (Yan et al, 2021a ).…”

Section: Mp Is Responsible For Overcoming Tm‐2 ...mentioning

confidence: 99%

“…Concomitantly and independently, Yan et al ( 2021a ) conducted both loss‐of‐function and gain‐of‐function assays using chimeric TMV and ToBRFV infectious clones where the MP coding gene was reciprocally swapped, and concluded that the ToBRFV MP is the virulence determinant for ToBRFV to infect Tm‐2 2 plants. They further mapped the region of ToBRFV MP necessary for breakdown of Tm‐2 2 resistance to the central domain (amino acids 60–186) (Yan et al, 2021a ). Through the introduction of point mutations into this domain, they identified six residues, H67, N125, K129, A134, I147, and I168, to be critical for overcoming Tm‐2 2 ‐mediated resistance (Yan et al, 2021a ).…”

Section: Mp Is Responsible For Overcoming Tm‐2 ...mentioning

confidence: 99%

“…N. benthamiana has been recognized as an ideal model plant to study plant–microbe interactions (Bally et al, 2018 ). Indeed, the model plant N. benthamiana has already been used to study ToBRFV in several recent publications (Hak & Spiegelman, 2021 ; Ma et al, 2021 ; Yan et al, 2021a ).…”

Section: Introductionmentioning

confidence: 99%

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Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Zhang

Griffiths

Marchand

et al. 2022

Molecular Plant Pathology

101

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Tomato brown rugose fruit virus (ToBRFV) is an emerging and rapidly spreading RNA virus that infects tomato and pepper, with tomato as the primary host. The virus causes severe crop losses and threatens tomato production worldwide. ToBRFV was discovered in greenhouse tomato plants grown in Jordan in spring 2015 and its first outbreak was traced back to 2014 in Israel. To date, the virus has been reported in at least 35 countries across four continents in the world. ToBRFV is transmitted mainly via contaminated seeds and mechanical contact (such as through standard horticultural practices). Given the global nature of the seed production and distribution chain, and ToBRFV's seed transmissibility, the extent of its spread is probably more severe than has been disclosed. ToBRFV can break down genetic resistance to tobamoviruses conferred by R genes Tm‐1 , Tm‐2 , and Tm‐2 2 in tomato and L 1 and L 2 alleles in pepper. Currently, no commercial ToBRFV‐resistant tomato cultivars are available. Integrated pest management‐based measures such as rotation, eradication of infected plants, disinfection of seeds, and chemical treatment of contaminated greenhouses have achieved very limited success. The generation and application of attenuated variants may be a fast and effective approach to protect greenhouse tomato against ToBRFV. Long‐term sustainable control will rely on the development of novel genetic resistance and resistant cultivars, which represents the most effective and environment‐friendly strategy for pathogen control. Taxonomy Tomato brown rugose fruit virus belongs to the genus Tobamovirus , in the family Virgaviridae . The genus also includes several economically important viruses such as Tobacco mosaic virus and Tomato mosaic virus . Genome and virion The ToBRFV genome is a single‐stranded, positive‐sense RNA of approximately 6.4 kb, encoding four open reading frames. The viral genomic RNA is encapsidated into virions that are rod‐shaped and about 300 nm long and 18 nm in diameter. Tobamovirus virions are considered extremely stable and can survive in plant debris or on seed surfaces for long periods of time. Disease symptoms Leaves, particularly young leaves, of tomato plants infected by ToBRFV exhibit mild to severe mosaic symptoms with dark green bulges, narrowness, and deformation. The peduncles and calyces often become necrotic and fail to produce fruit. Yellow blotches, brown or black spots, and rugose wrinkles appear on tomato fruits. In pepper plants, ToBRFV infection results in puckering and yellow mottling on leaves with stunted growth of young seedlings and small yellow to brown rugose do...

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Section: Genome Organization and Sequence Diversitymentioning

confidence: 99%

Section: Mp Is Responsible For Overcoming Tm‐2 ...mentioning

confidence: 99%

Section: Mp Is Responsible For Overcoming Tm‐2 ...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Zhang

Griffiths

Marchand

et al. 2022

Molecular Plant Pathology

101

View full text Add to dashboard Cite

show abstract

“…The key role of MP in triggering resistance was confirmed by transient expression of ToBRFV MP in resistant tomato and also in N. benthamiana in which the MP gene of ToBRFV and the Tm-2 2 resistance gene of tomato were transiently co-expressed [ 23 ]. Interestingly, Yan et al [ 24 ], using chimeric MP proteins of TMV and ToBRFV, demonstrated that six residues in the central 60–186 region of the ToBRFV MP are critical for overcoming Tm-2 2 resistance in tomato and transgenic N. benthamiana .…”

mentioning

confidence: 99%

Isolation and molecular characterization of a tomato brown rugose fruit virus mutant breaking the tobamovirus resistance found in wild Solanum species

et al. 2022

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A new tobamovirus named tomato brown rugose fruit virus (ToBRFV) overcomes the effect of the Tm-1, Tm-2, and Tm-22 resistance genes introgressed from wild Solanum species into cultivated tomato (Solanum lycopersicum). Here, we report the isolation and molecular characterization of a spontaneous mutant of ToBRFV that breaks resistance in an unknown genetic background, demonstrated recently in Solanum habrochaites and Solanum peruvianum. The wild isolate ToBRFV-Tom2-Jo and the mutant ToBRFV-Tom2M-Jo were fully sequenced and compared to each other and to other ToBRFV sequences available in the NCBI GenBank database. Sequence analysis revealed five nucleotide substitutions in the ToBRFV-Tom2M-Jo genome compared to ToBRFV-Tom2-Jo. Two substitutions were located in the movement protein (MP) gene and resulted in amino acid changes in the 30-kDa MP (Phe22 → Asn and Tyr82 → Lys). These substitutions were not present in any of the previously described ToBRFV isolates. No amino acid changes were found in the 126-kDa and 183-kDa replicase proteins or the 17.5-kDa coat protein. Our data strongly suggest that breaking the newly discovered resistance in wild tomatoes is associated with one or two mutations on the MP gene of ToBRFV.

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Tobamoviruses: old and new threats to tomato cultivation

Ishibashi,

Kubota,

Kano

et al. 2023

J Gen Plant Pathol

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Mosaic diseases caused by tobamoviruses have posed significant threats to tomato production. In this review, we overview studies of tomato mosaic diseases published over the past century, which have led to several important discoveries in plant virology, such as the application of attenuated strains. A resistance breeding program established in the 1970s successfully controlled tomato mosaic virus for over 40 years; however, newly emerging tobamoviruses are posing serious challenges in current tomato production. We introduce recent biotechnological attempts to engineer tobamovirus-resistant tomato plants, which offer promising technologies for eradicating the current outbreak.

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Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm‐2² resistance gene

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri butio n-NonCo mmerc ial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Cited by 28 publications

References 40 publications

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Isolation and molecular characterization of a tomato brown rugose fruit virus mutant breaking the tobamovirus resistance found in wild Solanum species

Tobamoviruses: old and new threats to tomato cultivation

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Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm‐22 resistance gene

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri butio n-NonCo mmerc ial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Cited by 28 publications

References 40 publications

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Tomato brown rugose fruit virus: An emerging and rapidly spreading plant RNA virus that threatens tomato production worldwide

Isolation and molecular characterization of a tomato brown rugose fruit virus mutant breaking the tobamovirus resistance found in wild Solanum species

Tobamoviruses: old and new threats to tomato cultivation

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Identification of genetic determinants of tomato brown rugose fruit virus that enable infection of plants harbouring the Tm‐2² resistance gene