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Tomato virus ToBRFV has changed the sector beyond recognition

ToBRFV has turned the tomato sector upside down worldwide. The virus is harmless to humans but can cause significant damage to cultivation. Moreover, it is highly contagious and can survive for a long time. While the sector is learning to deal with the virus, breeders are also looking at it from a broader perspective: this is not the last virus the sector will have to deal with. What lessons are they taking into the future? Jan Barten, strategic project leader for ToBRFV at Bayer Crop Science, where breeding company De Ruiter is part of, updates us.

Jan Barten, Bayer Crop Science

First reports
ToBRFV stands for Tomato Brown Rugose Fruit Virus and has been circulating in the tomato sector for ten years now. In 2014, the first reports came from the Middle East: Jordan and Israel. "After that, it remained dormant for a few years, without us being aware of the potential danger," Jan reconstructs. "From 2018, it began spreading rapidly to other markets: Mexico and Germany."

According to him, the virus spreading globally has multiple causes. "In the Middle East, growers initially chose varieties whose fruits showed few symptoms, and they started using vigorous rootstocks. They found a way to live with the virus. The infected fruits then circulated around Europe. We believe that this contributed to the rapid spread of the virus." Additionally, the virus's stability plays a role. "It can live for years in organic material, such as soil, but it also remains stable on inorganic material. It can sit on a surface for months and still be infectious. A doorknob, a computer, a mobile phone, or even a harvesting cart. Mechanical transmission is also very efficient, making it very easy for the virus to spread."

From panic to Q-status
All of this was not known in those years. However, more and more growers were dealing with the mysterious and particularly stubborn virus. It resulted in a panic in the tomato sector. In November 2019, ToBRFV was given the Q-status in Europe. This means that growers are required to report an outbreak and take strict measures to prevent its spread. But it was too late. "Ultimately, the entire greenhouse horticulture sector was affected: a large percentage of the area was infected with the virus." Tomato growers switched to other varieties or chose to grow cucumbers.

In addressing ToBRFV, breeders were quickly looked at. It was also a major threat to them. "The virus turned out to be much more dangerous than initially thought, and had a much greater impact. With De Ruiter, we also have a large share in the tomato market, and we saw that as a risk."

The company decided to focus broadly on knowledge sharing, to educate growers about the virus and the necessary phytosanitary measures. Regarding breeding, Bayer developed a two-track strategy. For the longer term, a large-scale search for more resistance genes has been initiated. "There are wild tomato species: with green, or small fruits, or even without. These are related to tomatoes and may possess resistant genes. Introducing them into our commercial range is a lengthy and complicated process. The results of this will appear in the coming years."

The availability of many resistant varieties already is due to Bayer's short-term strategy. Here, work was done with resistant genes already present in varieties with some cultural value but not suitable for greenhouse horticulture. By combining those genes in the right genetic background, a high level of resistance was developed. "This way, we believe we can solve the acute problem in the sector reasonably quickly."

Most complex situation
Now that sounds simple, but it wasn't. In fact, Jan, with over 30 years of experience in breeding, calls the outbreak the most complex situation he has encountered in tomato diseases. There are several reasons for this. For example, the severity of the symptoms during an outbreak of the virus is partly determined by the crop's conditions. "In a stressed crop, we see much more severe symptoms than in a vegetative crop." The phytosanitary measures taken in a greenhouse also play a major role in the severity of the infestation. But most importantly, the resistance to the virus is not determined by one or two genes, as is the case with many other viruses, but by a much larger number. "For most viruses, you look for a resistance gene in your genetics. You either have it or you don't. Sometimes you need two genes, or it's recessive, requiring two recessive parent lines. With ToBRFV, many more genes are involved."

Study of the virus taught breeders that there are both leaf and fruit symptoms. "How the symptoms manifest depends on the plant's genes, and different varieties therefore respond differently to the virus. Some are strong against leaf symptoms, and not against fruit symptoms, and vice versa." This was already evident during the initial outbreak in the Middle East, where growers chose varieties that seemed less susceptible to fruit symptoms. But building resistance to such a virus requires complex breeding. "The more genes you have to follow, the more complex it is. That's why it takes longer to develop something that can come to market." Moreover, each introduced gene can also affect other traits of the variety. All in all, this made it a new situation for the breeders. "Multiple factors influence the severity of the symptoms, and resistance is not black and white."

To gain control over this, Bayer has invested heavily in research. For example, a greenhouse has been built in Wageningen where varieties are artificially infected. The facility has a considerable capacity and is suitable for commercial, long-term tomato cultivation, similar to the conditions in glass greenhouses. It's a challenging task because ToBRFV is a quarantine disease, and the facility must therefore meet strict requirements. "Now we can see, for example, how varieties respond to infection under stress, and we can study the effects on a plant and fruit level."

This does not mean that all Bayer varieties are now resistant, or that all growers are using resistant varieties. It's still too complex for that. "Finding the right resistances and the quality of the variety is about finding a balance. You don't want to compromise on yield or taste." Moreover, the company sets high standards. "Because it's such a complex virus, there is no such thing as a single general resistance. We want to provide detailed information to the market about to what extent the varieties may still show symptoms of the virus in the crop and fruits in the event of heavy infestation. We do a lot of research on that." So it's not a simple story, and he sees that reflected in the sector as well. "You hear a lot about resistant varieties - but it's not that simple. There hasn't been a clear line drawn on what resistance exactly means, although work is being done on that."

For Jan, one thing is more than clear: this was not the last virus that will affect horticulture. In tomatoes, but also in other crops. "Viral diseases will continue to be a problem in the future. They also seem to mutate more aggressively, and are better and faster at breaking resistances."

At the same time, the outbreak has resulted in a vast amount of knowledge being gained. "Looking back, it's logical that ToBRFV spread so quickly," Jan refers to the virus's stability and its broad transmission capabilities. "We knew much less about that at the time. By studying the various transmission methods of a virus more intensively, we can assess much better whether future viruses could become dangerous. Allowing a virus to remain dormant for so long without studying it will not happen in the future. We are more alert in identifying potentially dangerous diseases."

The virus outbreak has also led to the tomato sector changing beyond recognition. "This was the first serious case where we see the importance of phytosanitary measures. That won't go away. No visits in the greenhouses, disinfecting hands, no phones," he lists as examples. "Especially early in the cultivation. Some of the stricter measures may be economically difficult to maintain, but the basic principles will certainly remain."

The view and approach to already known viruses have also been adapted due to the knowledge gained. Jan refers to the TMV virus, of which ToBRFV is a mutant. "The resistant gene against TMV is Tm2-2. As a result, the virus cannot multiply, and the cells containing the virus die. This works so well that it has actually been crossed into all tomatoes worldwide. But now we see the consequences of ToBRFV, which has bridged this resistance. Suddenly, the entire tomato genetics is susceptible. In hindsight, maybe we shouldn't have put all our eggs in one basket, but should have looked for alternative genes that also provide resistance, to build more certainty." Bayer is now also focusing on that. "The resistance we are introducing to the market now has multiple resistance: different genes act at different times. As a result, the possibility that the virus will overcome those genes simultaneously is much smaller. Looking to the future, we need to think about a joint approach: intensive monitoring of potential new diseases and phytosanitary awareness, combined with resistance preferably based on stacked resistance genes. That won't go away."

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