Plantago asiatica mosaic virus
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Seedborne Aspects
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Wood Packaging
- Impact Summary
- Economic Impact
- Risk and Impact Factors
- Uses List
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Principal Source
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Plantago asiatica mosaic virus
Other Scientific Names
- Nandina mosaic virus
Summary of InvasivenessTop of page
PlAMV was first described from the wild/weedy plant Plantago asiatica in the Russian Far East, and a Nandina mosaic isolate from cultivated Nandina domestica in the USA. PlAMV also naturally infects P. asiatica and Rehmannia glutinosa in the Republic of Korea, and N. domestica, Primula sieboldii, Lilium maximowiczii [Lilium leichtlinii var. maximowiczii] and Viola grypoceras in Japan. PlAMV has also been detected in commercially grown lilies in the Netherlands and elsewhere in Europe, Taiwan, the USA, Republic of Korea, Chile, China, New Zealand, India and Costa Rica. Japanese lily isolates are distinct from ‘European-like’ lily isolates, suggesting more than one introduction into lilies. Widespread occurrence in cultivated lilies is likely due to international distribution of infected bulbs. Losses of up to 80% have been reported in commercial greenhouse cut-flower production. PlAMV is able to spread readily through soil by uptake (and probably exudation) through the roots and is quite stable in contaminated planting media; no animal vector is known. PlAMV has a wide experimental host range.
Taxonomic TreeTop of page
- Domain: Virus
- Unknown: "Positive sense ssRNA viruses"
- Unknown: "RNA viruses"
- Order: Tymovirales
- Family: Alphaflexiviridae
- Genus: Potexvirus
- Species: Plantago asiatica mosaic virus
Notes on Taxonomy and NomenclatureTop of page
Plantago asiatica mosaic virus (PlAMV) was initially reported from naturally-infected plants of Plantago asiatica from the Russian Far East by Kostin and Volkov (1976). Also reported in the same year was a then-unidentified potexvirus infecting Nandina domestica (heavenly bamboo) in California, USA (Moreno et al., 1976), later named Nandina mosaic virus (Zettler et al., 1980). However, Nandina mosaic virus was only ever recognized as a tentative species in the genus Potexvirus, whereas PlAMV was accepted as a species in the genus Potexvirus by the International Committee on Taxonomy of Viruses (ICTV) in the ICTV 7th Report (Brunt et al., 1999), after the complete sequence was determined (Solovyev et al., 1994). When the full sequence of an isolate of Nandina mosaic virus was determined, it was identified as an isolate of PlAMV (Hughes et al., 2005).
DescriptionTop of page
PlAMV is a member of the genus Potexvirus, family Alphaflexiviridae. The sequence (NC_003849) of the type isolate is 6128 nucleotides in length, excluding the poly(A) tail, and is derived from that of the initial P. asiatica isolate (Solovyev et al., 1994).
The virus particles are flexuous virions, 490-530 nm long and about 11-13 nm wide, with a single molecule of linear positive-sense single-stranded RNA of c. 6.13 kb encapsidated within a helical arrangement of 1000-1500 subunits of the c. 22 kDa coat protein (Solovyev et al., 1994; Adams et al., 2009).
DistributionTop of page
PlAMV has been reported naturally infecting Plantago asiatica in the Russian Far East (Kostin and Volkov, 1976), the Republic of Korea (Lim et al., 2016) and Japan (K. Komatsu, Tokyo University of Agriculture and Technology, personal communication, 2018). It has also been reported infecting Nandina domestica in the USA (Moreno et al., 1976; Zettler et al., 1980) and Japan (Komatsu et al., 2017). The natural ranges of P. asiatica and N. domestica overlap in eastern Russia and Asia, raising the question of which is the original natural host (Hughes et al., 2005). Indeed, although P. asiatica is native to East Asia (including at least the Russian Far East, China, Japan and Republic of Korea), it is also used in traditional medicine and cultivated for this purpose in China, Japan and Republic of Korea (e.g. Ravn et al., 1990; Huang et al., 2009; Kim et al., 2009). N. domestica has a native range across Asia, from India to Japan, but is grown as an ornamental in many other countries, although PlAMV infection has been reported only in the USA and Japan (Moreno et al., 1976; Zettler et al., 1980; Tang et al., 2010; Komatsu et al., 2017).
PlAMV has also been reported naturally infecting Rehmannia glutinosa, another medicinal plant commercially grown in the Republic of Korea (Kwak et al., 2018; Kwon et al., 2017). R. glutinosa is native to China, where it is widely cultivated for its rhizomes (Flora of China Editorial Committee, 2017), and is also cultivated in Japan (Oshio and Inouye, 1982). It would therefore not be surprising if PlAMV infection is found to occur in P. asiatica, N. domestica and R. glutinosa across more of their native ranges in East Asia, and in N. domestica in other countries where it has been distributed as vegetative propagations of selected cultivars. Primula sieboldii, Viola grypoceras, Achyranthes bidentata and Stellaria sp. are also reported as naturally infected hosts in Japan (Komatsu et al., 2008; 2017; K Komatsu, Tokyo University of Agriculture and Technology, personal communication, 2017). S. media and Urtica urens have been reported infected in the Netherlands (de Kock et al., 2013a).
PlAMV has been detected in commercially grown lilies in the Netherlands and elsewhere in Europe, Taiwan, the USA, Republic of Korea, Chile, China, New Zealand, India and Costa Rica. Widespread occurrence in cultivated lilies is likely due to international distribution of infected bulbs. PlAMV is likely to be present in multiple countries, in addition to those in which it has been reported, as lilies are widely traded internationally.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present||Present, based on regional distribution|
|-Beijing||Present||2015||Xu et al., 2017||Detected in Asiatic hybrid lily|
|-Jilin||Present||Introduced||Li et al., 2017||Detected in lily imported from the Netherlands|
|India||Present||Present, based on regional distribution|
|-Tamil Nadu||Present||Rajamanickam et al., 2016||Currently reported only as GenBank sequences|
|Japan||Present||Native||Present, based on regional distribution|
|-Honshu||Present||Native||Komatsu et al., 2008; Komatsu et al., 2017|
|Korea, Republic of||Present||Native||2010||Kim et al., 2015; Lim et al., 2016; Kwon et al., 2017; Kwak et al., 2018|
|Taiwan||Present||Introduced||2011||Chen et al., 2013||Detected in lilies grown from imported bulbs|
|USA||Present||Native||Moreno et al., 1976; Hammond et al., 2015||Present, based on regional distribution|
|-California||Present||Native||1975||Moreno et al., 1976; Zettler et al., 1980||Described as Nandina mosaic virus. Widespread in certain cultivars of Nandina|
|-Maryland||Present||Introduced||2013||Hammond et al., 2015||Detected in multiple Lilium hybrids imported from the Netherlands|
|-Oklahoma||Present||2009||Tang et al., 2010||Detected in plants of Nandina domestica also infected with Alternanthera mosaic virus|
|-South Carolina||Present||Hughes et al., 2002||Widespread in certain cultivars of Nandina|
Central America and Caribbean
|Costa Rica||Present||Introduced||2013||Montero-Astúa et al., 2017||Detected in Asiatic lily plants grown from imported bulbs|
|Chile||Present||2013||Vidal et al., 2016||First detected in Asiatic lily hybrids in 2013|
|Hungary||Present only under cover/indoors||Introduced||2013||Pájtli et al., 2015||Identified in greenhouse-grown Oriental lily hybrids in plants grown from imported bulbs|
|Italy||Present only under cover/indoors||Introduced||2013||Parrella et al., 2015||Detected in several cultivars of both Asiatic and Oriental lily grown in greenhouses in Southern Italy from imported bulbs|
|Netherlands||Present||2010||Plant Protection Service of the Netherlands, 2010||Detected in Oriental lily in 2010 and subsequently reported in multiple lily types originating in the Netherlands|
|Russian Federation||Present||Native||Present, based on regional distribution|
|-Russian Far East||Present||Native||1976||Kostin and Volkov, 1976||Reported from naturally infected Plantago asiatica|
|UK||Present||Introduced||2012||Anderson et al., 2013||Detected in cut-flower lily stems|
|New Zealand||Present||Introduced||2013||Veerakone and Tang, 2015||Currently reported only as a GenBank sequence|
History of Introduction and SpreadTop of page
The natural occurrence of PlAMV in Plantago asiatica in the Russian Far East was reported in the 1970s (Kostin and Volkov, 1976), and during the same period in Nandina domestica in California, USA (Moreno et al., 1976; Zettler et al., 1980). The occurrence in lilies and primula (Ozeki et al., 2006; Komatsu et al., 2008), and in Stellaria sp. and Achyranthes bidentata var. fauriei in Japan (K Komatsu, Tokyo University of Agriculture and Technology, personal communication, 2017), should also be considered as natural infections of wild-growing plants. Infected S. media and Urtica urens were found in the Netherlands growing in soil in which infected lilies had previously been grown (de Kock et al., 2013a).
It is also not clear whether the identification of PlAMV infection of lilies in the Netherlands (Plant Protection Service of the Netherlands, 2010; EPPO, 2011) should be considered as an introduction with lily bulbs imported to the Netherlands, or as a further example of natural infection resulting from transmission within the Netherlands from an unknown host. According to Hammond and Reinsel (2018), the available sequences of lily isolates from the Netherlands, and all countries other than Japan, form a clade of 'European-type' isolates distinct from both the Japanese lily and primrose isolates, and from the P. asiatica and N. domestica isolates. In contrast, based on phylogenetic analysis carried out by Komatsu et al. (2017), 'European-type' isolates and Japanese lily and primrose isolates cluster together with high bootstrap support, sharing approximately 85% whole nucleotide identity. The low degree of diversity of the 'European-type' lily isolates (Hammond and Reinsel, 2018) suggests a single introduction from an unknown source (not necessarily in the Netherlands) that has subsequently been spread through the international trade in bulbs. The identification of 'European-type' isolates of PlAMV in lilies in the Republic of Korea (Kim et al., 2015; Hammond and Reinsel, 2018) suggests a probable origin from the Netherlands, as the only sequence available to date from natural infections of P. asiatica in Korea (Lim et al., 2016) is phylogenetically distinct (Lim et al., 2016; Hammond and Reinsel, 2018).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Netherlands||2010||Nursery trade (pathway cause)||Yes||No||Plant Protection Service of the Netherlands (2010)||Origin of infections in lily in the Netherlands is unknown; possibly imported in lily. No prior reports in other hosts in the Netherlands|
|Taiwan||2011||Nursery trade (pathway cause)||No||No||Chen et al. (2013)||Accidental|
|UK||Spain||2012||Nursery trade (pathway cause)||No||No||Anderson et al. (2013)||Accidental|
|USA||Netherlands||2013||Nursery trade (pathway cause)||No||No||Hammond et al. (2015)||Accidental; note that Nandina mosaic isolate is established in N. domestica, first detected in the USA|
|Hungary||2013||Nursery trade (pathway cause)||No||No||Pájtli et al. (2015)||Accidental|
|Italy||2013||Nursery trade (pathway cause)||No||No||Parrella et al. (2015)||Accidental|
|New Zealand||2013||Nursery trade (pathway cause)||No||No||Veerakone and Tang (2015)||Accidental|
|Costa Rica||Netherlands||2013||Nursery trade (pathway cause)||No||No||Montero-Astúa et al. (2017)||Accidental|
|Korea, Republic of||2013||Nursery trade (pathway cause)||No||No||Kim et al. (2015)||Accidental; sequence closely related to 'European-type' lily isolates and distinct from isolate found occurring naturally in P. asiatica|
|India||2015||Nursery trade (pathway cause)||No||No||Rajamanickam et al. (2016)||Accidental|
|China||Netherlands||2015||Nursery trade (pathway cause)||No||No||Li et al. (2017); Xu et al. (2017)||Accidental|
Risk of IntroductionTop of page
As multiple lily types are widely traded internationally, it is expected that PlAMV will be detected in many more countries where lilies are commonly grown, and potentially become established in areas where lilies are field-grown, or in greenhouse culture systems in which growing media is recycled between successive crops without thorough sanitation for long enough to inactivate the virus. In such systems, lily stocks initially free from PlAMV may rapidly reach high levels of infection, if planted in media contaminated from the prior growing cycle, or due to transmission during bulb-washing operations (de Kock, 2013; Conijn, 2014; Chastagner et al., 2017). Over-wintering weeds and infected volunteer plants may serve as on-going reservoirs of the virus in field situations (Chastagner et al., 2017). Plants of Stellaria media and Urtica urens growing in soil previously planted with infected lilies were apparently infected from virus remaining in the soil or crop residues (de Kock et al., 2013a).
PlAMV has an experimental host range including species from at least 16 taxonomically diverse plant families (Kostin and Volkov, 1976; Zettler at al., 1980; Ozeki et al., 2006; Hammond et al., 2015; J Hammond, unpublished). Many of these families include plants grown as ornamentals. If transmission through contaminated soil results in infection of such experimental hosts, PlAMV may become established in new areas where infected lilies or medicinal plants have previously been grown, and potentially be transplanted elsewhere.
HabitatTop of page
The original report of PlAMV from the Russian Far East was of distribution in wild populations of the weedy plant Plantago asiatica (Kostin and Volkov, 1976). PlAMV has also been found in weedy P. asiatica in an apple orchard in the Republic of Korea (Lim et al., 2016) and in the cultivated medicinal plant Rehmannia glutinosa, also in Korea (Kwak et al. 2018; Kwon et al., 2017). Infected weedy or uncultivated plants of Lilium maximowiczii [Lilium leichtlinii var. maximowiczii], Primula sieboldii, Nandina domestica, Viola grypoceras, Achyranthes bidentata and Stellaria sp. have also been reported from abandoned or neglected farmlands, gardens, or a cemetery (Ozeki et al., 2006; Komatsu et al., 2008; K Komatsu, Tokyo University of Agriculture and Technology, personal communication, 2017). The Nandina mosaic isolates of PlAMV reported in the USA were from commercially propagated cultivars of N. domestica, but the origin of the infection is unknown. Apart from the Japanese isolates from lily, all other reports in lily refer to cultivated varieties distributed in international trade. The cultivated hosts are frequently grown in protected agricultural environments (greenhouses, screenhouses, etc.).
Habitat ListTop of page
|Host||Principal habitat||Harmful (pest or invasive)|
|Soil||Present, no further details||Harmful (pest or invasive)|
|Cultivated / agricultural land||Present, no further details||Harmful (pest or invasive)|
|Managed forests, plantations and orchards||Present, no further details||Harmful (pest or invasive)|
|Protected agriculture (e.g. glasshouse production)||Secondary/tolerated habitat||Harmful (pest or invasive)|
|Natural grasslands||Principal habitat||Harmful (pest or invasive)|
Hosts/Species AffectedTop of page
Various types of lilies (Lilium spp. and hybrids) are the main crop hosts of economic importance. Lilium longiflorum (Easter lily) can be infected by PlAMV, but never exhibits the symptoms during the forcing process (iBulb, 2016). Symptom expression in other lily types is dependent on both the cultivar and environmental conditions, with symptoms typically more prominent under strong temperature fluctuations or poor cultivation conditions (iBulb, 2016). Mixed infections with Lily symptomless virus or Lily mottle virus can result in increased symptom severity and dwarfing of plants.
Some cultivars of Nandina domestica in the USA are frequently infected by PlAMV, sometimes in mixed infection with Cucumber mosaic virus (CMV) or Nandina stem pitting virus (NSPV), or occasionally with Alternanthera mosaic virus (Tang et al., 2010).
The medicinal plant Rehmannia glutinosa has been reported to be commonly affected in the Republic of Korea, but only in mixed infections with Ribgrass mosaic virus and Broad bean wilt virus 2 in greenhouse cultivation (Kwak et al., 2018), or with Rehmannia mosaic virus, Youcai mosaic virus and Broad bean wilt virus 2, which were ubiquitous in field-grown plantings (Kwon et al., 2017).
PlAMV also infects weed populations of Plantago asiatica in the Russian Far East (Kostin and Volkov, 1976), a host which is also cultivated as a medicinal plant. Natural infections have also been recorded from Primula sieboldii (Komatsu et al., 2008), Viola grypoceras (Komatsu et al., 2017), Achyranthes bidentata, Stellaria sp. (K Komatsu, Tokyo University of Agriculture and Technology, personal communication, 2017), S. media and Urtica urens (de Kock et al., 2013a).
PlAMV has an experimental host range including species from at least 16 taxonomically diverse plant families, including the Aizoaceae, Amaranthaceae, Asteraceae, Balsaminaceae, Berberidaceae, Brassicaceae, Chenopodiacea, Fabaceae, Lamiaceae, Plantaginaceae, Polemoniaceae, Primulaceae, Scrophulariaceae, Solanaceae, Tropaeolaceae and Violaceae (Kostin and Volkov, 1976; Zettler at al., 1980; Ozeki et al., 2006; Hammond et al., 2015; J Hammond, unpublished). Many of these families include plants grown as ornamentals.
Host Plants and Other Plants AffectedTop of page
|Achyranthes bidentata||Amaranthaceae||Wild host|
|Lilium leichtlinii var. maximowiczii||Liliaceae||Main|
|Lilium longiflorum (Easter lily)||Liliaceae||Other|
|Nandina domestica (Nandina)||Berberidaceae||Main|
|Plantago asiatica||Plantaginaceae||Wild host|
|Primula sieboldii (Primrose)||Primulaceae||Wild host|
|Stellaria media (common chickweed)||Caryophyllaceae||Wild host|
|Urtica urens (annual nettle)||Urticaceae||Wild host|
|Viola grypoceras||Violaceae||Wild host|
Growth StagesTop of page Flowering stage, Fruiting stage, Post-harvest, Pre-emergence, Vegetative growing stage
SymptomsTop of page
Symptoms vary with crop type and between lily cultivars. Lilies may be essentially symptomless (especially Lilium longiflorum), or may show generalized foliar chlorosis or chlorotic streaking, which may also become necrotic, especially along the veins, mostly on the underside of the leaf. Necrotic streaks may also occur on the stems. Chlorotic or necrotic streaking on upper foliage and flower buds may result in cut-flower stems being unsaleable, or of reduced quality. Symptom severity is enhanced by significant temperature variations. Lily roots developing pre-planting may show some signs of surface necrosis, but this may also result from secondary infections. Similarly, necrotic flecking on bulbs may also result from additional infections. Mixed viral infections, especially with Lily symptomless virus or Lily mottle virus, may cause intensified symptom expression, including stunting.
Infected plants of Nandina domestica often show intermittent symptoms (Zettler et al., 1980), with the proportion of symptomatic leaves (mosaic and some reddening) varying between plants, and probably influenced by environmental conditions. Chlorotic or reddish ringspots may be observed in plants infected with either PlAMV, or with Alternanthera mosaic virus, or both (Tang et al., 2010), but the primary symptom noted for an infected plant in Japan was leaf narrowing (Komatsu et al., 2017). Increased leaf reddening, leaf narrowing, mosaic and distortion may be observed in mixed infection with Cucumber mosaic virus.
All plants of Rehmannia glutinosa naturally infected with PlAMV were also infected with either two or three other viruses (Kwak et al., 2018; Kwon et al., 2017), and therefore none of the symptoms observed (leaf mottling, yellowing, discoloration and vein banding) could be attributed specifically to PlAMV.
Symptoms in Plantago asiatica were described as mosaic (Kostin and Volkov, 1976), or mottle or mottled yellowing (Lim et al., 2016). Infected plants of Viola grypoceras showed mosaic symptoms (Komatsu et al., 2017).
Symptoms in experimental hosts vary from latent infections to obvious visible symptoms. Latent infections are restricted to the inoculated leaves of several hosts, with no systemic infection. However, essentially symptomless systemic infections occur in a number of experimental hosts. Other hosts may show systemic mosaic, with or without veinal and/or spreading necrosis, and leaf collapse (J Hammond, unpublished). Symptom expression may be influenced by significant temperature fluctuations, as with lilies.
List of Symptoms/SignsTop of page
|Inflorescence / discoloration (non-graminaceous plants)|
|Inflorescence / distortion (non-graminaceous plants)|
|Inflorescence / lesions; flecking; streaks (not Poaceae)|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / abnormal patterns|
|Leaves / necrotic areas|
|Roots / necrotic streaks or lesions|
|Stems / discoloration|
|Stems / necrosis|
|Stems / stunting or rosetting|
|Whole plant / discoloration|
|Whole plant / dwarfing|
|Whole plant / early senescence|
Biology and EcologyTop of page
The genome of PlAMV is a single segment of single-stranded, positive sense RNA of c. 6.13 kb. Isolates for which sequence is available fall into three clades, composed of 1) 'European-type' lily isolates; 2) 'Japanese' lily and primula isolates; and 3) isolates from Plantago asiatica, Nandina domestica and Viola grypoceras (Hammond and Reinsel, 2018; Komatsu et al., 2017).
As for all plant viruses, reproduction can only take place in living cells of a susceptible infected host plant. In some hosts, infection is limited to inoculated leaves - a failure to move long distance within the plant due to incompatibility with host factors (non-host resistance), or specific response of the host in response to recognition of a viral effector protein. In susceptible plants, infected tissues remaining in the field may serve as a source of inoculum for mechanical infection or root uptake of a subsequent crop. A lectin gene in Arabidopsis thaliana has been shown to confer resistance against PlAMV (Yamaji et al., 2012) and a GYF domain-containing protein in the same host was shown to be essential for PlAMV infection (Hashimoto et al., 2016).
Physiology and Phenology
Most (almost all) of the natural hosts of PlAMV identified to date are perennial plants, thus allowing the virus to survive through multiple seasons in its native range. The virus is quite stable in contaminated planting media, in addition to being readily transmissible by sap (de Kock, 2013; Conijn, 2014). PlAMV is also relatively resistant to heat inactivation, while transmission between lily bulbs occurs readily via contact with contaminated water during bulb washing and dipping (de Kock et al., 2013b; Chastagner et al., 2017).
Lily and other ornamental plants, and also medicinal plants, are typically produced in protected agricultural situations - in greenhouses or relatively protected field situations, such that regional climate is not a good indication of growing conditions. Symptom severity may be enhanced by significant temperature fluctuations (iBulb, 2016).
ClimateTop of page
|BS - Steppe climate||Tolerated||> 430mm and < 860mm annual precipitation|
|Cs - Warm temperate climate with dry summer||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
|Cf - Warm temperate climate, wet all year||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Ds - Continental climate with dry summer||Tolerated||Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)|
|Dw - Continental climate with dry winter||Tolerated||Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)|
Means of Movement and DispersalTop of page
PlAMV is known to be transmitted from healthy plants through the soil in the absence of any biological vector, presumed to result from both exudation of virus from the roots of infected plants and uptake by the roots of healthy plants (de Kock, 2013). It is not clear whether this occurs through minor wounds or through active uptake by intact roots. It survives and can be transmitted through water used to wash or dip commercial lily bulbs, even if the bulbs are apparently undamaged (de Kock et al., 2013b; Chastagner et al., 2017).
No specific vector is known. PlAMV is quite stable in contaminated planting media, in addition to being readily transmissible by sap, so it is possible that passage of animals or equipment in natural or cultivated plant communities may spread the virus (de Kock, 2013; Conijn, 2014).
The most economically important hosts (Lilium species and hybrids, Nandina domestica and Rehmannia glutinosa) are typically propagated vegetatively, so an infected plant may give rise to almost 100% infected progeny plants. National and international trade of ornamental bulbs are the main means of introduction.
Although the international bulb trade is clearly a deliberate means of shipment of bulbs between countries, no obvious intentional introduction of PlAMV by this means is known to have occurred.
Seedborne AspectsTop of page
No seed transmission has been reported.
Pathway CausesTop of page
|Cut flower trade||International movement in infected cut flowers has been reported||Yes||Yes||Anderson et al., 2013|
|Horticulture||Extensive exports from the Netherlands occurred prior to introduction of certification programmes. Still likely to be some infected bulbs in export stocks||Yes||Yes||Plant Protection Service of the Netherlands, 2010|
|Medicinal use||Detected in first greenhouse-grown, and then field-grown, plants of R. glutinosa in Korea||Yes||Kwak et al., 2018; Kwon et al., 2017|
|Nursery trade||Distribution of infected plants of cultivars of N. domestica through the nursery trade||Yes||Yes|
Pathway VectorsTop of page
|Containers and packaging - wood||PlAMV has been detected in wood shavings used to package lily bulbs imported from the Netherlands; if this packaging is mixed into plant growth medium without sterilization, transmission to susceptible hosts could occur||Yes||Yes||,|
|Containers and packaging - non-wood||PlAMV has been detected in milled sphagnum used to package lily bulbs imported from the Netherlands; if this packaging is mixed into plant growth medium without sterilization, transmission to susceptible hosts could occur||Yes||Yes||,|
|Plants or parts of plants||Living plants or fresh or dried plant parts||Yes||Yes|
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bulbs/Tubers/Corms/Rhizomes||Yes||Pest or symptoms usually invisible|
|Flowers/Inflorescences/Cones/Calyx||Yes||Pest or symptoms usually invisible|
|Fruits (inc. pods)||Yes||Pest or symptoms usually invisible|
|Growing medium accompanying plants||Pest or symptoms usually invisible|
|Leaves||Yes||Pest or symptoms usually invisible|
|Roots||Yes||Yes||Pest or symptoms usually invisible|
|Seedlings/Micropropagated plants||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||Yes||Pest or symptoms usually invisible|
Wood PackagingTop of page
|Wood Packaging liable to carry the pest in trade/transport||Timber type||Used as packing|
|Loose wood packing material||Sawdust, shavings||Yes|
Impact SummaryTop of page
Economic ImpactTop of page
Considerable losses have been reported in commercial production of ornamental lilies, with losses of up to 80% reported in commercial greenhouse cut-flower production (Plant Protection Service of the Netherlands, 2010). No specific records of losses in lily bulb production are available (National Plant Protection Organization, 2012), but infected stocks are less valuable than stocks free from PlAMV and may not be acceptable for export.
Risk and Impact FactorsTop of page Invasiveness
- Proved invasive outside its native range
- Highly adaptable to different environments
- Tolerant of shade
- Has high genetic variability
- Host damage
- Negatively impacts agriculture
- Negatively impacts livelihoods
- Damages animal/plant products
- Negatively impacts trade/international relations
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
UsesTop of page
PlAMV has been examined as a research model to compare properties of different viruses in the genus Potexvirus (e.g. Yamaji et al., 2001; Senshu et al., 2009; Gaguancela et al., 2016) and basic biology of potexviruses, including their interactions with model plant hosts (e.g. Komatsu et al., 2011; Yamaji et al., 2012; Okano et al., 2014; Brosseau et al., 2016; Gaguancela et al., 2016; Hashimoto et al., 2016; Keima et al., 2017). Additional work has focused on sequence variability between isolates (e.g. Komatsu et al., 2008; 2017; Lim et al., 2016; Hammond and Reinsel, 2018). PlAMV has also been explored as a potential plant viral vector for efficient expression of foreign proteins (Minato et al., 2014). However, there is no obvious economic value to date, except potential means of introducing transgenic resistance to crop plants to negate yield and quality losses caused by infection.
Uses ListTop of page
- Laboratory use
- Research model
DiagnosisTop of page
Several groups have produced antisera against either Nandina (Zettler et al., 1980) or lily isolates (Chen et al., 2013; the Dutch Bloembollenkeuringsdienst, BKD – see Hammond et al., 2015, Parrella et al., 2015; J Hammond and K Rane, unpublished) of PlAMV. These have been used in a variety of applications, including immunodiffusion (Zettler et al., 1980), direct and indirect tissue blotting, antigen-coated plate ELISA (ACP-ELISA; Chen et al., 2013) and double antibody sandwich ELISA (DAS-ELISA; e.g. Hammond et al., 2015; Parrella et al., 2015). The BKD recommends testing lily leaves at the time of flowering, from leaves collected at ¾ of the stem height, while bulbs that have been stored for a long period generally give better results than those which have been recently lifted (AR van Schadewijk, Flower Bulb Inspection Service (BKD), the Netherlands, personal communication, 2017). Sampling of roots that have emerged during bulb storage are also useful for either ELISA or molecular testing; levels of PlAMV may be significantly higher in roots than in bulb scales (Chen et al., 2013). The Nandina mosaic and lily isolates are both detected by commercially available DAS-ELISA kits for Nandina mosaic virus, but there are reciprocal differences in detection efficiency (i.e. a nandina isolate reacted more efficiently with the ‘Nandina mosaic virus’ ELISA kit, and lily isolates yielded higher values than a nandina isolate using ELISA with a PlAMV-lily antibody; J Hammond, unpublished).
A number of PlAMV-specific primer sets for RT-PCR have also been published (Chen et al., 2013; Hammond et al., 2015; Parrella et al., 2015; Xu et al., 2017). RT-PCR tests may identify some infected samples not detected by DAS-ELISA (Hammond et al., 2015).
A macroarray/microtube hybridisation assay for detection of four viruses affecting lilies, including PlAMV, has been described (Sugiyama et al., 2008). This incorporates RT-PCR amplified cDNA probes spotted on a nylon membrane, and a target amplification primer incorporating a T7 promoter sequence linked to a conserved PlAMV sequence. Biotin-labelled target cRNA is then transcribed from double-stranded cDNA using T7 polymerase, and hybridized to the macroarray on nylon membrane, washed and blocked, and mixed sequentially with streptavidin and biotinylated alkaline phosphatase, followed by colorimetric detection (Sugiyama et al., 2008).
A reverse-transcription loop-mediated isothermal amplification (RT-LAMP) assay based on six primers within the PlAMV coat protein gene sequence has been developed. It has been shown to detect several lily isolates, the primrose isolate and a lily isolate with the coat protein gene of a nandina isolate substituted in place of the endogenous sequence (Komatsu et al., 2015).
PlAMV isolates have also been detected, and fully sequenced, by next generation sequencing from RNA extracts of Plantago asiatica (Lim et al., 2016), and from an Asiatic lily hybrid (Xu et al., 2017). In both cases, the sequences obtained by next generation sequencing were confirmed by PCR amplification and sequencing of essentially the full genome as five fragments. The complete sequences of isolates from Viola grypoceras and Nandina domestica have also been obtained by full genome amplification using a 5'-terminal primer linked to a T7 promoter sequence, and a 3'-tagged oligo(dT) primer (Komatsu et al., 2017).
Bioassay is also potentially a useful means of detecting PlAMV (e.g. Kostin and Volkov, 1976; Zettler et al., 1980; Ozeki et al., 2006; Hammond et al., 2015; Parrella et al., 2015). Among the useful local lesion hosts are Chenopodium quinoa, C. amaranticolor, Tetragonia expansa and Gomphrena globosa (Zettler et al., 1980; Ozeki et al., 2006; Hammond et al., 2015). The most useful systemic hosts include C. quinoa, Nicotiana benthamiana, N. megalosiphon, N. occidentalis and Celosia spicata, which all show obvious systemic symptoms (Moreno et al., 1976; Zettler et al., 1980; Ozeki et al., 2006; Hammond et al., 2015; J Hammond, unpublished).
Detection and InspectionTop of page
Infected plants may be essentially symptomless, or may show generalized chlorosis, mottle, or mosaic, including chlorotic or necrotic flecking or streaking of leaves and stems. The viral symptoms may have initially been mistaken for a nutritional disorder (Chastagner et al., 2017). Veins on the underside of lily leaves may appear rust-coloured, and then become necrotic, later becoming apparent on the upper leaf surface also, especially towards the end of vegetative growth and the onset of flowering (Chastagner et al., 2017). Lily leaves may also be somewhat twisted or distorted, and often brittle. The symptoms may be more prominent in the case of mixed infections with other viruses, and may also be difficult to differentiate from the symptoms induced by other individual viruses or mixed infections. Mixed infections of PlAMV with either Lily symptomless virus or Lily mottle virus, in particular, can result in much more severe symptoms, including significant stunting (Chastagner et al., 2017). There is wide variation in symptom expression between different lily species and cultivars, also dependent upon culture conditions (iBulb, 2016), and there is also variation between some isolates of the virus, at least in experimental hosts including Nicotiana benthamiana (Ozeki et al., 2006; Komatsu et al., 2008). Visible symptoms should not be relied upon for diagnosis, but obvious visible symptoms may aid selection of samples for specific testing. Infected lily bulbs do not necessarily show any external signs of infection. Some roots developed during bulb storage may show uneven surfaces and browning, but this may also reflect presence of, or interactions with, other pathogens. Serological or molecular tests are required for specific identification, and recommended to confirm any presumed visual symptoms associated with PlAMV infection.
Similarities to Other Species/ConditionsTop of page
PlAMV is serologically unrelated to the type member of the Potexvirus genus Potato virus X (Minskaya et al., 1977) and is also reported to be distinct from three other potexviruses infecting species of Plantago (Solovyev et al., 1994): Plantago severe mottle virus (Rowhani and Peterson, 1980); Plantain virus X (Hammond and Hull, 1981); and Argentine plantago virus [Papaya mosaic virus] (Gracia et al., 1983). However, PlAMV is relatively closely related to Tulip virus X in all viral proteins, except for the TGB3 protein (Yamaji et al., 2001).
Prevention and ControlTop of page
At present, the most likely avenues for international distribution appear to be the international lily bulb trade and, to a much lesser extent, vegetative material of Nandina domestica. Several countries require quarantine measures in the form of testing of bulb lots for the presence of PlAMV prior to import from specified sources, with specific limits on the tolerance for the presence of the virus. For example, Taiwan imposed specific restrictions on the import of lily bulbs from Chile in 2014 (BAPHIQ, 2015), even prior to the first published report of PlAMV in Chile (Vidal et al., 2016). The restrictions are based on visual inspection in the field, with less than 0.5% symptomatic plants per lot number allowed for export to Taiwan, with at least 10,000 plants per lot number visually inspected. In addition, bulbs from lot numbers approved for export based on <0.5% symptomatic plants must be separated properly from lot numbers not meeting this standard. Growers must take precautionary measures to prevent virus infection during harvest, with tools and machinery used for the harvest being sanitized prior to use. Bulbs for export must also be labelled with information on the name of the grower, lot number, scientific name of the product, name of the variety and quantity of each package. In the case of a high level of damage caused by PlAMV observed during flower production in Taiwan following import, the Taiwanese quarantine authority will inform the Chilean authority. Any further bulbs of the same lot numbers already in transit must be subjected to sampling for laboratory tests for PlAMV and only lots passing the test will be permitted to enter Taiwan. Bulbs of other lot numbers from the same producer must then also be tested by the Chilean authority and only bulb lots free from PlAMV will be allowed to be exported, with test results declared on the phytosanitary certificate. Occurrence of three or more incidents of high level damage in a single growing season in Taiwan would result in the requirement for all further Chilean bulb lots to be subjected to sampling and laboratory tests prior to release of lots passing the test for entry to Taiwan, with results declared on the phytosanitary certificate. Significantly, all expenses incurred by Taiwanese quarantine inspectors to monitor inspections and testing in Chile are required to be borne by the Chilean authority (BAPHIQ, 2015). Taiwan has established a similar <0.5% PlAMV occurrence by visual inspection in production fields for bulbs originating in the Netherlands (BAPHIQ, 2017).
New Zealand requires dormant lily bulbs from the Netherlands to be accompanied by a phytosanitary certificate issued by the national plant protection organization (NPPO), under which bulbs must have been produced in accordance with the Bloembollenkeuringsdienst (BKD) Class 1 bulb certification scheme. This means they have to have been inspected with appropriate official procedures and found free of visibly detectable regulated pests, sourced from a ‘pest free production site' free of regulated bacteria and viruses, and held in a manner to ensure that infestation/reinfestation does not occur following certification (Plants Food Environment Directorate, 2017). Interestingly, PlAMV is not listed as a regulated pest for Lilium in New Zealand. However, it is specifically mentioned for importation of Nandina, for which whole plants must be certified to originate in areas in which PlAMV is not known to occur, and for which tissue cultures must be declared to be ‘derived from parent stock tested and found free of Plantago asiatica mosaic virus’ (Plants Food Environment Directorate, 2017).
According to Anderson et al. (2013), lily bulb stocks for propagation under the Netherlands’ lily certification scheme should contain <1% of PlAMV infection. The current BKD standards for starting lots state that lots may be classified as Class I at up to 2% PlAMV infection, at grade ST for 2-5% infection and as not suitable for planting if there is >5% infection, as determined by ELISA testing. During growth, inspection of field-grown or glasshouse-grown crops may not detect any more than a maximum of 0.5% PlAMV for either Class I or Standard grades, while plants grown from bulb scales are permitted a maximum of 0.4% PlAMV (BKD, 2017).
International movement of micropropagated tissue culture plants does not guarantee freedom from virus as tissue culture can, in some instances, depress virus replication to below the sensitivity of even RT-PCR assays. The potential for spreading viruses in tissue culture can be minimized by acclimating the original tissue-cultured plantlets to soil and growing them in optimum greenhouse conditions for a minimum of three months. This will allow possible virus infections to reach readily detectable levels, and enable reintroducing back into tissue culture only material from plants testing negative for any virus infection. By this means, a high degree of confidence in the absence of virus infection can be obtained.
Early warning systems
There is no effective early warning system for PlAMV other than testing samples of bulbs (or other known hosts) prior to planting.
Unless PlAMV is detected in bulbs prior to planting, the first visible appearance of infection may not appear until the lily crop is close to flowering, at which time culling of unsaleable stems and destruction of infected plant material is of limited effect in minimising further infection.
Public awareness is not easy, as the symptoms of PlAMV in lilies are unlikely to be readily differentiated from those caused by other lily viruses by most members of the public or even many growers, without exposure to training by extension personnel or other experts.
Thorough and effective destruction of infected plants by burning, or by autoclaving for a sufficient time, will remove a major source of inoculum. However, as multiple weeds are known to be susceptible to PlAMV infection, and the virus is taken up through the roots of at least some susceptible hosts (de Kock, 2013; de Kock et al., 2013b; Chastagner et al., 2017), it is probably necessary to maintain infected fields fallow for at least one season, with removal of weeds that might allow continued replication of the virus. Cultivation may lead to earlier breakdown of contaminated plant residues in the soil (de Kock et al., 2013b).
Physical separation of lots of PlAMV-infected and presumed healthy plant stocks (particularly lily and nandina), and strict sanitation of any tools and equipment used with both types of plant, will serve to prevent or minimize cross-contamination. Avoidance of planting presumed healthy plants in locations where infected crops have previously been grown will also minimize the probability of introduction into presumed healthy plant material (de Kock et al., 2013b).
Cultural control and sanitary measures
Planting in contaminated growing media or soil should be avoided (de Kock et al., 2013b; Chastagner et al., 2017), as rates of infection of 0-8% have been observed when virus-free bulbs were planted in fields in which infected lilies had been grown previously (de Kock et al., 2013b). Although to date there does not appear to be adequate information on the longevity of viable virus in soils, it may require more than one season of growing a non-host before fields may be considered free of inoculum. However, this will likely vary with soil type and environmental factors, and the absence of infected weeds and volunteer plants. Provided that uncontaminated growing media or soil are available, purchase of bulb lots which have been tested and found virus-free will minimize the possibility of virus introduction; isolation of virus-free bulbs from other bulb stocks should be practiced wherever possible (iBulb, 2016).
Weed control contributes to reduction of carryover in field plots, as several weed species, such as Stellaria media and Urtica urens, and volunteer plants, contribute to retention of infectivity in plots where infected crops have previously been grown (de Kock et al., 2013b; Chastagner et al., 2017).
As infection may be transferred to previously healthy bulbs during bulb washing and processing (de Kock et al., 2013b), it is important that the highest quality bulb lots be treated before lots having a higher percentage of infection, that processing equipment should be sanitized between lots and that wash water be decontaminated, in order to minimize the risks of transmission between lots (de Kock, 2013; de Kock et al., 2013b; Conijn, 2014, Chastagner et al., 2017). A single disinfectant is recommended for cleaning surfaces in the Netherlands (de Kock et al., 2013b). Disinfection of wash or rinse water by heating to 65⁰C for 10 minutes has been recommended prior to reuse (Conijn, 2014).
Symptom expression (but not infection) in lilies may be minimized by avoiding major temperature fluctuation (providing supplemental heat during cold periods) or growing at temperatures lower than 12⁰C, by providing supplemental lighting during periods of low light and sufficient, but not excessive, fertilizer, and by managing relative humidity, as symptoms increase under higher relative humidity (iBulb, 2016).
Heating of contaminated soil or growing media to a high enough internal temperature for a sufficiently long time will destroy infectivity, which may be monitored by placing virus-containing capsules within the load for subsequent biological assay for infectivity (de Kock et al., 2013b). Physical or mechanical control consists mainly of minimizing damage to bulbs during processing and of performing frequent and thorough sanitation of tools and equipment during horticultural operations to avoid mechanical transmission or virus entry from contaminated solutions during bulb washing and processing.
There is no practical chemical control of plant virus infections; inclusion of antiviral compounds, such as nucleotide analogues, in meristem cultures, may result in recovery of some virus-free material from initially infected stocks. Any such attempts should include repeated re-testing of the plant material, as tissue culture procedures may result in levels of virus in plant tissues dropping below the level detectable even by RT-PCR. Retesting of tissue-culture derived plants for at least three months after acclimation to soil is recommended, to ensure that plants are truly virus-free.
Host resistance (incl. vaccination)
Lilium longiflorum is reported to be infected, but never to show symptoms during forcing. Many hybrids between L. longiflorum and other lily types may also show symptoms only rarely, most often under strong temperature fluctuations or poor cultivation conditions (iBulb, 2016). Resistance to PlAMV has been identified in Arabidopsis thaliana (Yamaji et al., 2012; Hashimoto et al., 2016) and transferred to transgenic plants of Nicotiana benthamiana (Yamaji et al., 2012). No resistance has yet been reported in lilies, other than the typical lack of symptoms in L. longiflorum.
A combination of virus exclusion, separation of healthy and infected stocks, rigorous sanitation, avoidance of contamination through infested growing medium (soil or water) and weed control, will reduce virus levels more than any one measure alone.
Monitoring and Surveillance (Incl. Remote Sensing)
Infection in lilies can be monitored either by symptom expression, especially during the period when flowers develop and open, or by screening randomly selected plants by ELISA, RT-PCR, or other diagnostic methods noted above. Specific diagnostic methods are more reliable, as some lily types or cultivars may not show any obvious visible symptoms under typical growing conditions. However, visual screening at the appropriate crop developmental stage can be an effective method for screening large numbers of plants (e.g. Pájtli et al., 2015) and is the primary means of screening production bulb lots prior to harvest for export (e.g. BAPHIQ, 2015; 2017; BKD, 2017). RT-PCR is typically more sensitive than DAS-ELISA, such that not all plants detected as infected by RT-PCR will yield positive ELISA results (e.g. Hammond et al., 2015). This may reflect the recency of infection and uneven distribution of the virus in plants within the season of infection. Samples must be taken from the appropriate tissue and at the correct stage of bulb development to obtain the most relevant results (de Kock, 2013).
Surveillance of fields in which PlAMV-infected crops have previously been planted could include RT-PCR or ELISA sampling of weeds, testing especially from the roots, as the virus may remain restricted to the root in some weed species, without moving into the aerial portions of the plant (yet still potentially allowing infection of the crop through root uptake).
Efforts to return to lily cultivation with zero or minimal occurrence of PlAMV will vary with the type of growth system utilized. In protected growing conditions (greenhouses), it would likely be necessary to thoroughly decontaminate all tools and equipment, including benches or growing containers, and to utilize fresh growing medium from an uncontaminated source. In addition, certified virus-tested bulb lots would need to be physically separated and handled separately from any plant material known or suspected to be infected, even at a low level. Recycled used growing medium would need to be thoroughly disinfested by heat treatment for long enough, at high enough temperature, to inactivate any virus particles present from a prior crop. This can be practically monitored by inclusion of data loggers to verify temperatures and duration at different positions within batches during the inactivation treatment, or by inclusion of vials of known infected tissue in the batch, followed by bioassay of the treated tissue after the procedure to ensure than no infectivity is retained (de Kock et al., 2013b). Bulb lots believed to be free from PlAMV, or to have very low levels of infection, should also be processed separately from, and prior to, handling any lots known to have any significant level of infection. The washing and processing equipment should be thoroughly disinfested prior to treatment of healthy bulb lots, and the wash solutions heated to 65⁰C for 10 minutes prior to reuse (Conijn, 2014).
In the case of field production, fields in which infected bulbs have been grown previously, should not be used for planting of healthy bulb lots, if possible, as multiple weed species are susceptible to PlAMV infection (de Kock et al., 2013a,b). If it is necessary to reuse such fields, it would be advisable to allow a fallow period with cultivation, in order to control growth of any volunteer plants or weeds that might allow the virus to persist between crops, and to encourage degradation of any plant tissues and virus from the prior crop remaining in the soil. Growth of a cover crop, or an alternative crop demonstrated to be insusceptible to PlAMV, would also help to reduce the potential for carry-over of viable virus. However, additional research on the experimental host range of PlAMV is required to identify suitable crops which are not susceptible to the virus.
Gaps in Knowledge/Research NeedsTop of page
An examination of the ability of PlAMV to infect other crops which might be used in rotation with lilies, or other crops known to be susceptible to PlAMV, would be of value, as would studies of the potential susceptibility of common weeds. An examination of the weeds commonly occurring in production fields used for known susceptible crop species would also be valuable.
ReferencesTop of page
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OrganizationsTop of page
Netherlands: Bloembollenkeuringsdienst, BKD, Postbus 300, 2160 AH Lisse, www.bkd.eu/bkd
Principal SourceTop of page
Draft datasheet under review
ContributorsTop of page
08/01/18 Original text by:
John Hammond, USDA-ARS, Floral and Nursery Plants Research Unit, 10300 Baltimore Avenue, B-010A, Beltsville MD 20705, USA
Distribution MapsTop of page
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