Detalle de: Ecology and diversity of plant viruses, and epidemiology of plant virus‐induced diseases

At a time when the world needs to produce more food, pathogens pose a major constraint on agricultural production reducing yields 10–16% (Oerke, 2006), compromising quality, affecting trade and jeopardising the sustainability of global agriculture and farming. With changing climate patterns, the spread of pathogens is predicted to increase (Chakraborty & Newton, 2011; Pautasso et al., 2012), placing agriculture under severe pressure in many sensitive areas of the world. Fungi, oomycetes, viruses and bacteria are the major agricultural pathogens worldwide, with viruses causing almost half of the reported emerging infectious diseases in plants (Anderson et al., 2004). Plant virus control still relies heavily on the use of pesticides against virus vectors, despite the fact that they are often inefficient for that purpose. Virus-resistant crop varieties may be very effective, but are not available for all viruses and all crops, and resistances can be overcome by newly emerging resistance-breaking viral strains (Gómez et al., 2009). In this context, there is a need to manage crops and agricultural systems in the most appropriate way to effectively mitigate the impact of virus-induced diseases. Management has to be knowledge-based, and therefore it is important to understand the role of ecological factors in the emergence and development of virus epidemics, as well as acquiring better knowledge on the genetic diversity and evolution of plant virus populations. Ecological factors influencing the behaviour of virus populations within their habitats refer to interactions among viruses, vectors and hosts, and include host range, symptom expression, tissue tropism, transmission modes and mechanisms, virus persistence in the environment, and a diverse range of cultural practices and human activities having an impact in these interactions. Annals of Applied Biology has a long-standing tradition of publication of reviews and research papers in these topics (Jones, 2014) and the journal continues to do so; recent important examples have been gathered for this virtual issue. For instance, in a recent paper, Macharia et al. (2016) performed an extensive survey of weeds in tomato production systems in Kenya. The authors also conducted mechanical and thrips-mediated tomato spotted wilt virus (TSWV) transmission assays and evaluated the development of Frankliniella occidentalis in a subset of the 43 identified weed species in order to determine their suitability as hosts for the virus and the vector. Although practically all of the identified weed species were hosts to the virus, only some of them could be highlighted as being likely relevant for the epidemiology of tomato spotted wilt disease. Amaranthus hybridus, Datura stramonium and Solanum nigrum were prevalent in the assessed areas and also favoured thrips reproduction. Among those three, A. hybridus seemed to be of particular relevance, since it spreads fast and yields several generations per year, which could lead to the increase of thrips populations in the fields, thereby supporting high vector transmission rates. Other important species included Oxalis latifolia, Commelina benghalensis, identified for the first time as TSWV hosts in this study, and Malva parviflora (Macharia et al., 2016). Another recently published and interesting study in Annals of Applied Biology dealt with the identification of tolerance in sunflower genotypes against tobacco streak virus (TSV) in Queensland, Australia. Sharman et al. (2016) applied robust Bayesian statistical methods to assess the response of 23 sunflower hybrids to TSV in several field trials conducted over 5 years, taking into consideration external factors that may interfere with the disease epidemiology but that are often overlooked. Regardless of the intensity of the disease, the authors confirmed differences in the response of sunflower genotypes to TSV infection, with hybrids NH2201, Hysun 304 and Galah standing out as tolerant even under high inoculum pressure. The authors argued that field trials might be more appropriate for the assessment of tolerance than more controlled experiments in greenhouses, as mechanical inoculation under experimental conditions may mask differences among genotypes that could only be detected under field conditions; also, other external factors have an influence in field trials, leading to more realistic results (Sharman et al., 2016). Viral transmission is a key factor for disease epidemiology, and Annals of Applied Biology has a history of publishing relevant manuscripts on this subject as well. We selected three recent manuscripts on viral transmission/virus–vector interactions and their potential impact on the diseases epidemiology. The study conducted by Bertin et al. (2016) dealt with a challenging system. The authors investigated the acquisition, retention and transmission of grapevine leafroll-associated viruses 1 and 3 (GLRaV-1, GLRaV-3) and grapevine virus A (GVA) by the mealybugs Planococcus citri and Planococcus ficus after feeding on multiple infected plants. Their data showed that nymphs of both vector species were able to efficiently acquire all three viruses and retained very low titres of them up to 72 h after acquisition, which is in accordance with the semi-persistent mode of transmission proposed for these viruses. Once acquired, however, transmission efficiency rates varied between vectors and viruses. While P. ficus efficiently transmitted GVA and GLRaV-3, P. citri was more efficient in transmitting GLRaV-1. Moreover, the authors demonstrated that GLRaV-1 was acquired mainly with the other two viruses, but inoculated as single infection to the test plants. Although the three viruses are often found together, it appears that neither GLRaVs are necessary for GVA transmission nor do they depend on GVA for their own transmission (Bertin et al., 2016). Such information improves our understanding on the transmission biology and epidemiology of grapevine viruses that often occur in co-infections around the world. In a different approach, Carmo-Sousa et al. (2016) described a solid study on how a virus can manipulate its vector in such a way that its own transmission is enhanced. The authors showed, using the electrical penetration graph (EPG) technique, that cucurbit aphid-borne yellows virus (CABYV) induces changes in its cucumber host that modifies the Aphis gossypii vector feeding behaviour in order to favour its acquisition by non-viruliferous aphids. Higher numbers of individual aphids fed from the phloem of infected cucumber plants, and this involved a shorter time to reach the phloem ingestion phase and a longer time in phloem-related activities than the insects feeding in non-infected plants. Interestingly enough, once viruliferous, alatae aphids preferred to feed from healthy, rather than CABYV-infected plants, when they were under free choice settling conditions. Conversely, such preference was not observed for aviruliferous aphids (Carmo-Sousa et al., 2016). Altogether, such manipulation of the vector must have a direct role in virus transmission and epidemiology of the disease through both increasing viral acquisition and its spread to new host plants. This could be a generalised phenomenon worth studying using other experimental systems. Still on the viral transmission subject, Garzón et al. (2016) brought yet a new player to the already intricate host–virus–vector interactions. Nymphs of Chrysoperla carnea and adults of Adalia bipunctata are aphidophagous predators and their effect on the dispersion of the A. gossypii vector and spread of CABYV from cucumber plants were assessed under semi-field conditions. Both predators induced the sedentary aphids to leave the plants 14 days after setting the experiment, resulting in an increase in aphid dispersal in the long term. Such dispersal was always higher from plants with C. carnea than those with A. bipunctata, probably due to the mobility of the predators. Chrysoperla carnea larvae are apteral and remain in CABYV-infected plants, promoting aphids to flee from the colony. On the other hand, some of the A. bipunctata alatae adults flew away without triggering the "danger alarm" to the aphid colony. Because of that, the decrease in the initial aphid population was higher for C. carnea than for A. bipunctata at short times after release, although values equalised at longer times. Differently from what was observed for aphid dispersion, in this study CABYV spread was not significantly affected by the presence of the predators (Garzón et al., 2016). Nevertheless, natural enemies used as biological control agents should be considered relevant in the epidemiology of viral diseases, and certainly more studies should be conducted in this regard. Tobamoviruses cause severe crop diseases and are responsible for significant economic losses worldwide. A key aspect of the epidemiology of the diseases they cause is that their particles are remarkably stable and remain infectious for prolonged periods even in adverse conditions. Cucumber green mottle mosaic virus (CGMMV) is a tobamovirus that affects cucurbit crops and has, since the 1930s, caused occasional outbreaks of local importance. The distribution and impact of CGMMV seems, however, to have increased in recent times, as is the case for cucurbit crops in Israel. Reingold et al. (2016) conducted a series of epidemiological studies by monitoring the patterns of CGMMV distribution in commercial greenhouses, studying the effects of cultural practices on disease spread, and identifying a combination of simple cultural techniques that may reduce the spread of the disease in commercial cucumber greenhouses. Thus, the rapid identification and removal of diseased plants, combined with the addition of intermediate substrates at the planting stage, resulted in a significant reduction of disease incidence. These techniques are useful, and indeed have been implemented under the framework of the CGMMV-Initiative National Project from Israel (Reingold et al., 2016). Understanding the genetic diversity of viruses provides a perfect complement to ecological studies and may contribute significantly to the better understanding of disease epidemiology; again Annals of Applied Biology has a history of publishing relevant manuscripts on this subject, and the next five papers constitute recent interesting examples. Begomoviruses belong to the family Geminiviridae, and include a large number of members that are able to cause epidemics of disastrous consequences in economically and/or socially important crops worldwide. The diversity of the genus is amazing, with geographical areas that are hotspots for that, including Brazil. Ferro et al. (2017) used rolling circle amplification, a powerful technique for detection and amplification of circular DNA molecules, to characterise begomoviruses infecting wild hosts from two plant genera, Sida and Leonorus, in Brazil. After sequencing 78 DNA clones, the authors identified isolates not only from four known begomoviral species, but also belonging to three new begomoviral species, as well as a new alphasatellite (Ferro et al., 2017). Cataloguing the viral diversity in wild species is highly significant and interesting, as wild species may constitute a diversity reservoir for viruses which may jump from wild to cultivated hosts resulting in emerging diseases in crops (Woolhouse et al., 2005), and these may have potentially devastating consequences. Sugarcane mosaic disease (SMD) is widespread worldwide and may cause losses of up to 17–50% in some cultivars. SMD has been associated to a number of potyviruses which vary depending on the geographical area. Luo et al. (2016) carried out a survey to identify potyviruses associated to SMD in sugarcane crops in China and found that sorghum mosaic virus (SrMV) was prevalent, but sugarcane mosaic virus and sugarcane streak mosaic virus were also present though infecting a minority of the samples. They also analysed the genetic diversity of SrMV, identifying three major lineages with several phylogroups within lineages specific for China provinces. Interestingly, double infections between SrMV and one of the other two potyviruses were reported in a small but still important proportion of the cases (Luo et al., 2016). Understanding which specific potyvirus (and its diversity) causes SMD is critical for the design of efficient control strategies, more specifically the development of resistant sugarcane varieties. From a research point of view, minor crops are often neglected, although they may bring important nutritional components to our diets. Raspberry leaf blotch disorder (RLBD) is an important and severe disease associated to raspberry leaf blotch virus (RLBV), a recently described but poorly studied single stranded negative sense RNA virus. Dong et al. (2016) carried out an extensive survey in cultivated and wild raspberries in Finland, identifying RLBV in 93% of the samples from symptomatic plants. Partial sequencing of 21 RLBV isolates showed considerable genetic diversity; interestingly, diversity could be as high among isolates infecting geographically close hosts as among isolates from distant hosts, and no correlation could be identified between geography and genetic diversity (Dong et al., 2016). These results suggested the presence of RLBV in Finland since long ago, and that no important geographical barriers have shaped the population genetics of this virus in the surveyed area. Cucurbits comprise crop species of significant economic importance, including watermelon, melon, squash, cucumber and pumpkin, and can be affected by a large number of viruses which may become limiting factors for their cultivation. Juarez et al. (2013) carried out an exhaustive survey of cucurbit crops in Spain, analysing 1767 samples from symptomatic plants to detect up to nine different viruses. Prevalent viruses were CABYV, watermelon mosaic virus (WMV) and papaya ring spot virus (PRSV), but their frequency distributions depended on the geographical area surveyed. Perhaps more importantly, mixed infections of up to five different viruses in the same sample were very frequent, with double infections accounting for more than 10% of the samples. In addition, in this study, the genetic diversity of WMV was studied by partial sequencing of 39 isolates; phylogenetic analyses including old WMV isolates suggested a recent replacement of genetic types, with "emerging" isolates having replaced the "classic" ones (Juarez et al., 2013) as described for the southern regions of France. There is significant scarcity of data on the detection, nature, incidence and diversity of viruses in important crops in certain regions of the world, including legume crops in Southeast Asia. Tsai et al. (2013) carried out surveys in soybean, mungbean and bean crops in Vietnam, Java and Indonesia, and investigated the presence of begomoviruses in samples. All the isolates from Indonesia corresponded to Mungbean yellow mosaic India virus (MYMIV) strain-A, and all from Vietnam to Mungbean yellow mosaic virus (MYMV) strain-B. Epidemiological data together with the authors' phylogenetic analyses suggested a recent introduction of MYMIV in Indonesia, perhaps from North India. On the contrary, authors' data suggested that MYMV was in Vietnam for many years but remained undiagnosed until this study. Taken together, the above papers provide interesting examples of work on the ecology and diversity of plant viruses, and the epidemiology of plant virus-induced diseases published by Annals of Applied Biology. Emerging topics include the frequent occurrence of mixed infections and the eco-evolutionary consequences that this may have, the modification of vector behaviour as consequence of host infection, the consideration of multitrophic interactions and their ecological, epidemiological and evolutionary consequences, and the possibility of comprehensive virome description thanks to the availability of powerful techniques such as next generation sequencing. But more classical views and approaches should still be useful in providing insight into the diversity of problems and situations posed by plant viruses. Eminent plant virologists, including B.D. Harrison, R.A.C. Jones, J.M. Thresh and J.A. Tomlimson (Jones, 2014), have showed us the path, and we are proud to follow their indications.