Plant viruses in vegetable cultivation: Sources of infection through water, soil, and compost

Invisible ways of virus transmission in vegetable cultivation

Research clearly shows that plant viruses are more stable and adaptable than previously thought. For vegetable cultivation, this means that only consistent hygiene management, which also takes compost, irrigation water, and drainage into account, can minimize the risk of infection and ensure yield security.

For successful vegetable cultivation, it is crucial to take these practical recommendations into account:

• Viruses can be transmitted without insect vectors—via water, soil, and plant debris.

• Compost and irrigation water can harbor infectious plant viruses and should be carefully monitored.

• Hydroponic cultivation systems offer advantages such as accelerated plant growth, savings in water and fertilizers, and a reduction in fertilizer entering the groundwater, but they carry a particularly high risk of spreading pathogens in the plant population via the nutrient solution.

• Prevention through hygiene remains the most effective measure—from the removal and disposal of plant debris to the disinfection of irrigation water.

Many vegetable growers primarily associate virus transmission with insects such as aphids or whiteflies. However, it should not be underestimated that many plant viruses spread even without insects—solely via water, soil, or organic material. Such vectorless spread of viruses can occur underground when viruses are released from the roots or from decaying remains of infected plants into the surrounding medium and are then absorbed by the roots of healthy plants through small wounds that occur naturally during the growth process. This type of vector-free transmission has become increasingly important in practice, particularly in intensive cultivation, with the introduction of modern hydroponic cultivation methods.

Stable, mechanically transmissible viruses could easily spread among plants via irrigation water or nutrient solutions (Fig. 1). In addition, many viruses can be transferred from infected plants to machines, tools, or human clothing through simple mechanical contact, and can then be transmitted to healthy plants through simple contact with these contaminated materials, leading to the spread of the disease. While the risk of introduction and spread through infected seeds, bulbs, tubers, or pollen can be effectively counteracted by using certified virus-free seeds/planting material, the aforementioned silent, virtually invisible transmission routes via contaminated materials pose a major challenge.

Fig. 1: Spread of stable plant viruses through transmission of these viruses with irrigation water or nutrient solution in a recirculating hydroponic cultivation system.

And by the way...vectorless transmission is nothing new. As early as 1898, Beijerinck, the father of modern plant virology, observed that tobacco plants became infected with tobacco mosaic virus (TMV) when grown in pots to which he had added small pieces of soil in which TMV-infected plants had previously grown. He concluded that the virus had been released from the infected plants and that healthy plants were able to absorb it from the soil.

Viral infections can lead to severe growth impairments and yield losses and/or a reduction in the quality and market value of plant products, which may, for example, exhibit defects in their shape, color, taste, or shelf life (Fig. 2). The response of plants to viral infections can range from symptom-free to severe or even fatal, depending on the plant species/variety, the age of the plants, the virus species/strain, and environmental conditions. The yield losses caused by viral infections in various crops are estimated at several billion dollars per year. However, accurate calculations are difficult, if not impossible, as most of the available data is based on small-scale trials that tend to be published in annual reports and are not sufficiently accessible internationally. There are often differences in recording and measurement, which makes comparison difficult. In addition, losses caused by a particular virus in a particular crop can vary from year to year, from region to region, and depending on the presence of other pathogens.

Fig. 2: Damage—color and shape changes—to virus-infected vegetables. A: Tomato brown rugose fruit virus-infected tomato, B: Tomato spotted wilt virus-infected tomato, C: Leek yellow stripe virus-infected leek, D: Healthy (top) and tomato spotted wilt virus-infected zucchini (bottom), E: Cucumber green mottle mosaic virus-infected cucumber.

Virus transmission via water

Let's take a brief look back. Plant viruses have been detected in ponds, ditches, streams, rivers, lakes, and other surface waters, as well as in seawater, and the corresponding studies have been published since the 1980s. Some of the plant viruses found in surface waters have long been known as pathogens from various crops, while for others, the natural hosts are not yet known.

The tomato mosaic virus (ToMV), which is highly contagious to plants and infects many different crops, has even been found in ancient glacial ice and in clouds and fog. The virus was detected in more than half of the fog samples tested on a mountain peak in New York State and along the coastal regions of the northeastern United States. The researchers concluded that soil particles contaminated with ToMV can serve as cloud condensation nuclei and that atmospheric spread of the virus without vectors can serve as a means of long-distance transport for stable viruses such as ToMV. The coronavirus pandemic, or rather the causative coronavirus (SARS-CoV-2), has taught us in recent years how quickly and efficiently infection can spread via aerosols or droplets, leading to high infection rates in the population.

Human activities can increase the amount of plant viruses present in the environment. It has long been known that crop residues such as those from tomatoes, cucumbers, peppers, strawberries, root vegetables, and asparagus are sources of infection for subsequent crops. Water from a pond into which drainage water from composted cucumbers infected with cucumber mosaic virus (CGMMV) had been discharged was identified as the source of infection for greenhouse cucumbers. In the Netherlands, CGMMV was also detected in drainage water from greenhouses with infected plants. Compost heaps and landfills containing unsold and infected vegetables in the immediate vicinity of irrigation ditches and other sources released the plant viruses over a period of several months. Noteworthy is the stabilization of viruses through apparently pH- and salt-dependent adsorption to plant debris and other organic matter or to organic and inorganic colloidal materials, clay particles, etc., which has been confirmed by several scientists.

Sewage treatment plants also proved to be a rich source of certain plant viruses. This is not surprising, as several plant viruses, such as tomato bushy stunt virus (TBSV) and cucumber green mottle mosaic virus (CGMMV), retain their infectivity even after passing through the digestive tract of humans or cattle. In a study on virus diversity in human feces, researchers found more than 30 different plant viruses. By far the most common virus was Pepper mild mottle virus (PMMoV). This virus retained its infectivity for several host plants, such as bell peppers. The occurrence of PMMoV in human fecal samples from the US and Singapore has been attributed to diet, as it has also been detected in bottled chili sauces and chili powder. Another study showed that PMMoV occurs frequently in wastewater in the US. Its occurrence appears to be limited to human feces. It was not found in feces from pigs, cows, horses, sheep, dogs, raccoons, or turkeys, but only in chicken and seagull feces. The virus can therefore be used as an indicator of human fecal contamination in coastal and lake areas. In Germany, PMMoV was also detected in abundance in wastewater and water samples from the Rhine and Ruhr rivers, confirming its suitability as an indicator of fecal contamination in surface waters. In France, PMMoV was detected in foods containing paprika and in stool samples from patients suffering from fever, abdominal pain, and itching who tested seropositive for anti-PMMoV IgM antibodies. These observations seem to indicate that PMMoV could cause clinical symptoms in humans.

Under natural conditions, the efficiency of vectorless transmission of plant viruses via water and soil can be relatively low due to the high dilution of virus particles in the environment. This is different in large horticultural monocultures, especially when closed recirculating irrigation techniques are used. These, as well as irrigation systems for outdoor crops that are fed with surface water, especially from drainage ditches, often introduce plant pathogens into the plant population or spread them within it. And in the case of viral infections, this happens faster than one might think. A single virus-infected plant can infect many other plants over the growing season and contaminate the entire irrigation system—tanks, pipes, hoses, and drippers. And virus infections spread faster than you might think. If no countermeasures are taken, it often takes only a few weeks or months to infect the majority of plants in a greenhouse.

A significant number of plant viruses spread rapidly when nutrient film techniques (NFT) and other closed systems, such as ebb and flow systems, are used with circulating nutrient solutions. In an NFT model setup, it was demonstrated that ToMV spread from a single infected tomato plant via the soil into the nutrient medium and infected the other tomato plants in the setup within two to seven weeks. We have also observed similar patterns of spread in soilless cultures of ToMV, cucumber mosaic virus (CMV), CGMMV, and pepino mosaic virus (PepMV). Viruses can be detected in roots within a short time and soon thereafter in above-ground plant parts and in the nutrient solution. Many viruses remain infectious in the nutrient solution for a very long time. 

Checklist: Farm hygiene to combat plant viruses in vegetable cultivation

Seedlings

• Only use certified, virus-free seeds and seedlings

• Regularly check deliveries on a random basis (health status, origin)

Tools & Equipment

• Disinfect knives, scissors, and bandaging sites daily (e.g., with peracetic acid, sodium hypochlorite, or commercial disinfectants)

• Clean machines and transport trolleys regularly

Water & Nutrient Solutions

• Evaluate and monitor drainage and irrigation water for contamination with plant viruses

• Disinfect drainage and irrigation water thermally (heat), physically/biologically (membrane/bio/sand filters, UV light, heat) or chemically (ozone, sodium hypochlorite)

• No discharge of drainage water into surface waters

Compost & plant debris

• Do not add virus-infected plant debris to the farm's own compost

• Only hot rotting (>70 °C over several days) can reliably inactivate viruses

• Better: external disposal via thermophilic biogas plant or waste management

Personal hygiene

• Wash your hands before working with plants and wash and disinfect them after working

• Change work clothes regularly

• Provide employees with targeted training in dealing with plant viruses

Vector control

• Consistently monitor and control whiteflies, aphids, and thrips

• Use biological antagonists or preparations that are harmless to beneficial organisms

Note: Once a plant has been infected with a plant virus, it cannot be cured. Only consistent hygiene and prevention measures can ensure yields and quality.

Closed irrigation systems

1. Nutrient film technique (NFT) A thin film of nutrient solution flows continuously over the roots of the plants. Often used for tomatoes, cucumbers, and lettuce.

2. Flood and drain systems Plant substrate is periodically flooded with nutrient solution and then drained again. Promotes oxygen supply to the roots between flood cycles.

3. Drip irrigation with return flow Drippers deliver nutrient solution directly to the roots; excess solution is collected, filtered, and reused.

4. Deep-water crops are placed in a net pot on a floating platform. The roots are always suspended in the nutrient solution, giving them optimal access to water and nutrients at all times. Used for lettuce or herbs, for example.

5. Aeroponic roots hang in the air and are regularly moistened with a fine nutrient solution spray. High oxygen supply, rapid root development, very efficient use of resources.

6. Combination systems Hybrids of NFT, ebb-and-flow, or drip irrigation, depending on the crop and operation.

Carmen Büttner¹ und Martina Bandte² und Ute Vogler³

^{1, 2}   Humboldt-Universität zu Berlin, ADTI, Fachgebiet Phytomedizin, Berlin, Deutschland

³      Julius Kühn-Institut, Bundesforschungszentrum für Kulturpflanzen, Institut für Pflanzenschutz im Gartenbau und Urbanen Grün, Braunschweig, Deutschland