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Scientific description of Potato Viruses (2020)

Based on Kreuze J.F., Souza-Dias J.A.C., Jeevalatha A., Figueira A.R., Valkonen J.P.T., Jones R.A.C. (2020) Viral Diseases in Potato. In: Campos H., Ortiz O. (eds) The Potato Crop. Springer, Cham

The authors of this chapter are J. F. Kreuze, J. A. C. Souza-Dias A. Jeevalatha, A. R. Figueira, J. P. T. Valkonen, R. A. C. Jones
Viruses are among the most significant biotic constraints in potato production.

In the century since the discovery of the first potato viruses we have learned more and more about these pathogens, and this has accelerated over the last decade with the advent of high-throughput sequencing in the study of plant virology.

Most reviews of potato viruses have focused on temperate potato production systems of Europe and North America. However, potato production is rapidly expanding in tropical and subtropical agro-ecologies of the world in Asia and Africa, which present a unique set of problems for the crop and affect the way viruses can be managed.

Most Damaging Potato Viruses (Yield)

Whereas more than 50 different viruses and one viroid have been reported infecting potatoes worldwide (Table 11.1, Fig. 11.1), only a handful of them cause major losses globally.

However, some are locally and/or temporarily relevant, while others are currently only of minor importance anywhere in the world. PVY (see Table 11.1 for virus acronyms) and PLRV are now the most damaging viruses of potato worldwide, with PVY having overtaken PLRV as the most important.

Tuber yield losses are caused by either of them in single infections and can reach more than 80% in combination with other viruses. PVX occurs commonly worldwide and causes losses of 10–40% in single infections and is particularly damaging in combination with PVY or PVA. This is due to its synergism with both potyviruses leading to tuber yield losses of up to 80%.

PVS also occurs commonly worldwide but generally causes only minor tuber yield losses unless severe strains are present or it occurs in mixed infection with PVX. PVA can cause yield losses of up to 40% by itself but is far less prevalent than PVY, PVS, or PLRV. PVM is relatively uncommon in most countries and, like PVS, mostly causes only minor tuber yield losses, except in mixed infection with PVX or other viruses.

Quality loss

Besides yield reduction, several viruses cause economic losses by affecting potato quality, particularly by inducing internal and surface tuber necrosis.

PLRV sometimes causes necrosis of the tuber vascular system known as “net necrosis.” Tuber necrosis, consisting of necrotic rings or arcs in the flesh, sometimes develop with the thrips-transmitted virus TSWV, and with soil-borne viruses like nematode vectored TRV (Sahi et al. 2016) and protist-transmitted PMTV (Abbas and Madadi 2016). TSWV generally infects potato in warmer regions but TRV and PMTV both occur globally in cooler regions where their vectors are established. Certain phylogenetically defined recombinant strains of PVY cause similar necrotic symptoms known as “potato tuber ringspot disease.”

Over the last three decades, these have caused particularly heavy economic losses to potato industries in Europe and North America as well as in many developing countries in Asia and South America but have not yet reached all parts of the world, e.g. south-west Australia (Kehoe and Jones 2016) or Peru (Fuentes et al. 2019a).

Therefore, PVY “strains” have been heavily studied worldwide over the past two decades revealing an exceptional amount of variation and a plethora of genotypes, many of them recombinants. PVY “strains” separate into at least 13 different subgroups defined either biologically or by phylogenetics (Karasev and Gray 2013; Kehoe and Jones 2016; Glais et al. 2017; Gibbs et al. 2017).

Control of Potato Viruses

Potato is clonally propagated by planting tubers, which increases the risk of virus accumulation in the next crop and tuber generations. Apart from semi-persistently or persistently vector-transmitted viruses, such as PLRV, for which insecticide application as seed tuber dressings or foliar sprays are effective during seed potato production, such treatments are generally ineffective at controlling nonpersistently vector-borne viruses like PVY (Jones 2014).

Thus, most potato viruses are controlled by three principal methods:

  • Clean seed systems
  • Cultural practices
  • Host plant resistance

Clean Seed Systems

Nowadays, in developed countries potato viruses are by and large controlled through formal certified clean seed production systems and to some extent through virus resistance. On the other hand, despite many years of intensive investment, formal certified seed systems have had only very limited, if any, penetration in many developing countries, where farmers mostly obtain their seed from their previous crop or through informal trade involving low-quality planting material. High cost of seed production, lack of adequate infrastructure and economic resources of small scale family farms are some of the reasons contributing to this situation.

In the past, simple seed potato schemes that, for example, relied solely on visual inspection and roguing combined with flooding and livestock to remove any tubers left behind after harvest proved effective at removing PLRV and other viruses causing obvious foliar symptoms, but ineffective at removing viruses causing mild symptoms e.g. PVS and PVX.

Formal certified seed systems are expensive to implement in most developing countries as they require rigorous visual inspections and diagnostic testing. Relying solely on visual inspections is cheaper but leads to selection of viral strains that show few foliar symptoms, as occurred with some strains of PVY.

Diagnostic testing

Diagnostic testing often requires laboratories. While well-established method such as ELISA (Enzyme Linked Immunosorption Assay) are relatively cheap, they may lack sensitivity. Various PCR (Polymerase Chain Reaction), reverse transcription PCR and real-time PCR, protocols have been developed and multiplexed (e.g. Raigond et al. 2013; Meena et al. 2017; Jeevalatha et al. 2016a) which can provide ultrasensitive detection of viruses in samples.

Field diagnostics with viruses is also possible using lateral flow devices that are commercialized by several companies globally but suffer from similar sensitivity issues as regular ELISA and are not available for all viruses.

Loop Mediated Isothermal Amplification (LAMP) has recently emerged as a technology that can provide highly sensitive in field detection of potato viruses, with assays developed for PVY (Treder et al. 2018), PLRV (Ahmadi et al. 2013; Almasi et al. 2013), PVX (Jeong et al. 2015), PSTVd (Learcic et al. 2013) and ToLCNDV (Jeevalatha et al. 2018). LAMP assays can rapidly be designed to detect newly identified viruses and can be multiplexed, making it a flexible technology. LAMP is also compatible with crude nucleic acid extractions, can achieve high sensitivity, and be combined with the availability of relatively cheap battery powered real-time devices, such as Bioranger or real-time Genie series of devices, so may soon see more routine use in determining virus infections.

Cultural Practices

Cultural practices (such as roguing out plants with obvious virus symptoms, removing volunteer potato plants or weeds likely to harbor potato viruses, deploying reflective mulches to deter insect vector landings, manipulating the planting date to avoid peak flights of insect vectors, and early haulm destruction to avoid late virus infections) are rarely used by developing country farmers unless they are seed producers.

In fact, the common habit of small holder farmers of selling and or consuming large tubers and keeping the small ones as seed for a next crop probably maintains virus loads in the seed high, as virus-infected plants often are the ones producing the smallest tubers. Gildemacher et al. (2011)and Schulte-Geldermann et al. (2012) showed how positive selection of healthy looking mother plants to provide seed tubers could reduce virus incidences in subsequent crops by 35–40% and a corresponding yield increase of 30%.

The seed plot technique as practiced in India (whereas it starts out with certified virus free seed) is largely based on cultural practices to keep tuber seed healthy, growing during seasons and areas with low vector pressure coupled with IPM (Integrated Pest Management), rouging (negative selection), and dehaulming the seed crop before vectors reach a critical threshold limit.

The use of straw mulch (Kirchner et al. 2014), mineral oil sprays and intercropping has been shown to enable control of PVY infection, particularly when used in combination (Dupuis et al. 2017a, b), although the economics of it would only justify their application for seed potato production (Dupuis 2017).

Insecticide application to prevent PLRV spread in seed potato crops is also routinely used where seed potato stocks are multiplied in more aphid vector prone areas, especially in developed countries.

A unique practice is performed in the Andean region (and also the Himalayas) where farmers traditionally grow their potatoes at higher altitudes to reinvigorate them after several years of cultivation at lower altitudes (De Haan and Thiele 2003).

Host Plant Resistance

Potato is clonally propagated by planting tubers, which increases the risk of accumulation of viruses in the next crop and tuber generations. Apart from semi-persistent or persistently transmitted viruses such as PLRV, viruses cannot be controlled readily with pesticides, so chemical control of virus vectors provides only partial protection at best or is ineffective. On the other hand, production of healthy seed tubers is an expensive process. Therefore, resistance to viruses in potato cultivars is the most efficient and cost-effective means to control virus diseases in potato when effective seed production systems are absent, as in most developing countries. In developed countries with sophisticated and effective seed tuber production schemes, virus resistance becomes less important than other cultivar characteristics, such as high yield, tuber quality, and adaptation to the local environment.

Resistance against Potato Virus Y

PVY is now the most widespread viral pathogen in potatoes in most countries. Fortunately, breeders have introduced resistance genes that control PVY to many potato cultivars. Many of them, however, recognize only certain PVY strains. These strain-specific resistance genes can act quickly upon recognition of PVY and kill most of the PVY-infected cells at an early stage of infection leading to localized necrotic lesions, although they are sometimes slower acting resulting in systemic movement followed by single shoot or complete plant death. Therefore, they are called “hypersensitivity resistance” (HR) genes and contrast to “extreme resistance” (ER) genes which do not lead to any visible lesions during the resistance reaction. Furthermore, plasmodesmata connecting the plant cells and used by viruses for movement from cell to cell are sometimes blocked, preventing further spread of the virus.

However, mutations in the viral genome can overcome resistance.

Resistance against Potato Virus X

Presence of extreme PVX resistance gene Rx was identified in four Australian, two European cultivars, and one North American cultivar. PVX hypersensitivity gene Nx was identified two Australian, four European, and one North American cultivar. PVX hypersensitivity gene Nb was identified in one Australian, five European, and one North American cultivars. When breeding new PVX-resistant cultivars potato cultivars for developing countries, incorporation of gene Rx is the best option. However, Andean PVX resistance breaking strain XHB not only overcomes Rx, but also overcomes Nx and Nb, so Rx is likely to be less effective in potato cultivars growing in the center of origin of the crop.

Resistance against other Potato Viruses

Additional resistance genes to PVA, PVV, PVS and PVM have also been identified (Palukaitis 2012) and mapped in potatoes but have to date not been widely utilized due to the considered limited importance of these viruses.

Looking Forward

Viruses remain a problem for global potato production, even though, over the years, the importance of certain viruses has increased or decreased globally. These changes in relative importance result from a range of factors including not only increased global trade but also regional changes in cultivar usage, cropping patterns, implemented seed systems and diagnostic testing regimes, appearance and evolution of new viruses and virus strains, and vector populations. All of these factors interact with each other and are further affected by climate change, making it difficult to predict what the future will hold.