water research 46 (2012) 4902e4917 Available online at www.sciencedirect.com journal homepage: www.elsevier.com/locate/watres Review Plant viruses in aqueous environment e Survival, water mediated transmission and detection Natasa Mehle a,b, Maja Ravnikar a,b,* a National Institute of Biology, Vecna pot 111, 1000 Ljubljana, Slovenia b Centre of Excellence for Biosensors, Instrumentation and Process Control, Velika pot 22, 5250 Solkan, Slovenia article info abstract Article history: The presence of plant viruses outside their plant host or insect vectors has not been Received 16 April 2012 studied intensively. This is due, in part, to the lack of effective detection methods that Received in revised form would enable their detection in difficult matrixes and in low titres, and support the search 12 July 2012 for unknown viruses. Recently, new and sensitive methods for detecting viruses have Accepted 15 July 2012 resulted in a deeper insight into plant virus movement through, and transmission Available online 23 July 2012 between, plants. In this review, we have focused on plant viruses found in environmental waters and their detection. Infectious plant pathogenic viruses from at least 7 different Keywords: genera have been found in aqueous environment. The majority of the plant pathogenic Plant virus viruses so far recovered from environmental waters are very stable, they can infect plants Water via the roots without the aid of a vector and often have a wide host range. The release of Survival such viruses from plants can lead to their dissemination in streams, lakes, and rivers, Transmission thereby ensuring the long-distance spread of viruses that otherwise, under natural Irrigation conditions, would remain restricted to limited areas. Hydroponic The possible sources and survival of plant viruses in waters are therefore discussed. Due to the widespread use of hydroponic systems and intensive irrigation in horticulture, the review is focused on the possibility and importance of spreading viral infection by water, together with measures for preventing the spread of viruses. The development of new methods for detecting multiple plant viruses at the same time, like microarrays or new generation sequencing, will facilitate the monitoring of environmental waters and waters used for irrigation and in hydroponic systems. It is reasonable to expect that the list of plant viruses found in waters will thereby be expanded considerably. This will emphasize the need for further studies to determine the biological significance of water-mediated transport. ª 2012 Elsevier Ltd. All rights reserved. Contents 1. Introduction . 4903 2. The origin and presence of plant viruses in environmental waters . 4903 3. The survival of plant viruses in waters . 4904 4. Infection of plants with contaminated water . 4907 * Corresponding author. National Institute of Biology, Vecna pot 111, 1000 Ljubljana, Slovenia. Tel.: þ386 59 232 801; fax: þ386 1 25 73 847. E-mail address: [email protected] (M. Ravnikar). 0043-1354/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.watres.2012.07.027 water research 46 (2012) 4902e4917 4903 5. Water as an effective route for spreading of viruses . 4907 5.1. The spreading of viruses in irrigation systems by water or nutrient solutions . 4908 6. Preventing plant viruses from spreading with water . 4909 6.1. The elimination of plant viruses from water . 4909 7. Methods for detecting plant viruses in water . 4910 7.1. Concentration . 4910 7.2. Biological assays . 4911 7.3. Detection of viral protein . 4911 7.4. Observation of viral particles . 4911 7.5. Detection of nucleic acids . 4911 7.6. Future development of methods for monitoring plant viruses in water . 4912 8. Conclusions . 4912 Acknowledgements . 4913 References ................................................................................................ 4913 1. Introduction water-transmissible plant pathogens throughout the whole crop, increasing the chance of epidemics if not managed In certain cases, such as floods, earthquakes, pollution intensively (Stanghellini and Rasmussen, 1994a; Schnitzler, (Szewzyk et al., 2000; Casteel et al., 2006; Abraham, 2011) and 2004; Stewart-Wade, 2011). Plants will be repeatedly inocu- terrorist attacks (Khan et al., 2001; Gu¨ nter, 2006; Gleick, 2006; lated with viruses, independently of whether the initial source Costigliola and Quagliata, 2010; Ping, 2010; Knutsson et al., of water harbours the viruses or whether they enter the water 2011), water can be an important source of human, animal along the path of distribution. Therefore, the risk of dissemi- and plant infection by pathogenic microbes. The pollution of nation and required management of plant viruses, often environmental waters (for different definitions of term ‘envi- resulting in crop losses, has to be evaluated before recircu- ronmental waters’ see Hamstead (2007)), such as rivers, lakes, lating used water (Bandte et al., 2009). sea, tap and irrigation water, with human and animal viruses In this review we will discuss the presence and survival has received considerable attention (see reviews, e.g., Rudolfs of plant viruses in aqueous environments, the possibility of et al., 1950; Gerba and Schaiberger, 1975; Labelle and Gerba, water mediated transmission, how to minimize the risk of 1980; Szewzyk et al., 2000; Griffin et al., 2003; Scott et al., viruses spreading through irrigation systems, and the 2004; Toze, 2006; Reynolds et al., 2008). It is only 30 years methods adapted for detecting plant viruses in the aqueous since plant viruses were first shown to be present in envi- environment. Our objectives are to highlight the knowledge ronmental waters in considerable amounts (Koenig, 1986). that is the basis of our current understanding of plant viruses Since then, many questions have been raised concerning the in water systems and to emphasis the need for additional survival and spread of plant viruses by water, especially in the research to attack this issue of global importance. light of increased irrigation and use of hydroponic systems in agriculture. Agricultural irrigation consumes enormous quantities of 2. The origin and presence of plant viruses water; in developing countries, irrigation often exceeds 80 in environmental waters percent of total water use (Riley et al., 2011). Irrigation water can be sourced from surface water supplies such as ponds, The first results of studies on plant viruses in environmental lakes, rivers, and reservoirs and, as such, can harbour disease- waters were reviewed by Koenig (1986). Their possible sources causing microorganisms, including several plant viruses. were proposed to be the roots of infected plants growing in an Additionally, crop production in soilless cultures, using open ecological niche near the water, injured or decaying plant or closed hydroponic systems, has been increasing world- material, and sewage. As discussed later, a number of plant wide. In a closed system, the nutrient solution is recovered, viruses present in vegetables or fruits can pass through the replenished, and recycled following its delivery to the root alimentary tract as infective virions, to be released into system. In an open system, the nutrient solution is not sewage water that could find its way into environmental replenished or recycled, although it may be recovered waters. Additionally, the surface wash-out of locally scattered (Stanghellini and Rasmussen, 1994a). Soilless culture has and infected decaying plant residues and of the related soil provided an alternative to plant growers who face soil-related surface layer, including animal faeces, could bring the plant problems such as nematodes, pathogens, and nutrient viruses into waters. Virus-containing seeds and virus- imbalance (Stanghellini and Rasmussen, 1994a; Schnitzler, transmitting nematodes, zoospores or, more so, resting 2004). Water is becoming more costly and harder to access sporangia of fungi, may also be washed away by running soil in many countries, therefore it is necessary to use its sources water or drainage water. more responsibly, e.g., use of recycled water for irrigation in The pioneer report on the release to drainage water of commercial plant nurseries and greenhouses. On the other Tobacco necrosis virus (TNV) and Tobacco mosaic virus (TMV) hand, the use of circulating nutrient solutions in hydroponic from infected roots of Cleome spinosa and tobacco plants, systems holds the potential for rapid and effective spread of respectively, is more than 50 years old (Yarwood, 1960). In 4904 water research 46 (2012) 4902e4917 1969, van Dorst reported viruses in irrigation waters (cited in Infectious TNV, a member of the genus Necrovirus, was Pares et al. (1992)). However, the first observations on the confirmed to be present in ditches, streams and canals in presence of plant viruses in rivers and lakes, date from the Germany (Koenig et al., 1989; Yi et al., 1992), in rivers Cam, 80’s, when only a few research groups in Europe were focused Thames, Avon and in its tributaries, and in Esthwaite Water in on the problem (Koenig, 1986). During the last ten years there England (Tomlinson et al., 1983). Infectious Cucumber mosaic has been an increase in reports on the presence of plant virus (CMV), a member of the genus Cucumovirus, was isolated viruses in waters. Infectious plant pathogenic viruses from at from waters of Italian river Bradano (Piazzolla et al., 1986). least 7 different genera (Carmoviruses, Cucumoviruses, Dia- Carnation