In a new review paper published in the Agronomy journal, VIRTIGATION partner Wageningen University (WU) looks to nature for strategies to halt devastating disease outbreaks of ToBRFV.
ToBRFV: a succesful tobamovirus devastating tomato
According to the WU authors, which include VIRTIGATION principal investigators Yuling Bai and Romanos Zois, tomato is a model crop for genetic research because the genome sequence is available, it can easily be transformed, and interspecific crosses can be generated between tomato cultivars and many wild relative Solanum species. It is also a model plant for studying immunity because it is susceptible to a wide range of pathogens, including viruses. Tomato crops are infected by 312 different plant viruses, which is possibly the highest number of recorded viral species in a single crop.
The WU authors focus in their review paper on ToBRFV, one of the most successful tobamoviruses affecting tomato crops so far. ToBRFV, like many tobamoviruses, spreads easily and rapidly through mechanical transmission, i.e. by contact (e.g. injuries on plants). Viral particles enter the plant cells after wounding the epidermal cells. Therefore, the virus can spread rapidly with all plant handling, and a gentle touch is already sufficient as virus concentrations are very high, even in trichome.
ToBRFV disease symptoms in tomatoes can be severe. The most obvious ones are curling, malformation of the leaves (shoestring or fern leaf), and stunting of the whole plant. Additional symptoms on the leaves are mosaic discoloration, mottling, and necrosis. Deformation and necrosis can also occur on the stem. Additionally, ToBRFV infection reduces fruit number due to early flower abortion and reduced fruit size. Symptom development can vary due to environmental growth conditions, age during viral infection initiation, and the genetic background of the tomato plant. ToBRFV benefits especially from its presence in greenhouses: the WU authors cite studies that demonstrated that only two ToBRFV-infected tomatoes could contaminate the entire tomato crop under normal cultivation procedures within 9 months!
Learning from viral disease resistance strategies in plants to prevent further spread of ToBRFV
To halt the spreading of ToBRFV and the possibility of new ToBRFV variants evolving, the WU researchers deem the development of tomato cultivars with durable ToBRFV resistance as necessary prerequisite. Although ToBRFV is a fairly recently emerged virus species (i.e. first detection in 2014 in Israel), scientists have found high genomic similarity of ToBRFV to the three tobamoviruses TMV (Tobacco Mosaic Virus), ToMV (Tomato Mosaic Virus), and ToMMV (Tomato Mottle Mosaic Virus). This genomic similarity is helpful in deducing the biological function of the viral proteins and how they can establish disease.
The four well-known strategies that plants use to become resistant against plant viruses are: (1) RNA silencing mediated by the plant, (2) the presence of dominant plant resistance proteins (R-proteins), (3) plant hormone-mediated resistance, and (4) absence of a functional plant susceptibility factors (S-factors). Resistance strategies can differ in expected durability, and a strategy with high durability is preferred. In addition to this, a selected resistance strategy should have a low likelihood for pleiotropy, e.g. a negative impact on plant physiology.
The WU scientists then analyse in detail these strategies in terms of their suitability to halt devastating disease outbreaks of ToBRFV. ToBRFV resistance conferred by host-based viral RNA silencing, ToBRFV resistance conferred by host resistance (R) proteins, hormone-based ToBRFV resistance and ToBRFV resistance based on dysfunctional host susceptibility (S) proteins. For each of the four given strategies, the WU researchers then provide the expected durability and likelihood of pleiotropic plant phenotypes (see figure below).
Absence of Susceptibility Genes (S-factors) as best strategy for durable resistance against ToBRFV
The WU authors also review the various molecular factors of plant host and tobamoviruses like ToBRFV, that are instrumental for viral proliferation. Following this, the WU researchers conclude that among the highlighted four strategies to achieve durable ToBRFV-resistance in tomatoes, the best strategy for durable resistance is an absence of functional susceptibility genes. This is because viruses fully depend on host proteins for their proliferation, due to the small number of viral proteins. Most viral proteins interact with S proteins. Therefore, the WU scientists deem it necessary to investigate which amino acids from the S protein are relevant for viral protein binding and responsible for the S factor function.
Simultaneously, the WU authors consider it crucial to identify which amino acid variants of the S protein can prevent viral protein binding and proliferation, while maintaining the intrinsic protein function for the host plant. Deployment of S protein variants that lost their viral “helper” ability, but kept their intrinsic in planta function, is expected to result in durable virus resistance of tomato against ToBRFV. Ultimately, identifying mutant variants of S genes with no pleiotropic effects is essential for exploring impaired S genes in breeding tomatoes resistant to ToBRFV, according to the WU experts.
More info about VIRTIGATION partner WU's research
The full version of WU’s review paper in the Agronomy journal titled “Directions from Nature: How to Halt the Tomato Brown Rugose Fruit Virus” is available online here since 5 May 2023. It has been co-authored by WU’s leading scientists in VIRTIGATION, Yuling Bai and Romanos Zois. The supplementary information supporting their review paper can be found in the VIRTIGATION Zenodo community here. More about VIRTIGATION’s scientific publications on our website here.
© Title image: 2019 Camille Picard, EPPO
