Pepper mild mottle virus (PMMV)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Seedborne Aspects
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Pepper mild mottle virus
Preferred Common Name
Other Scientific Names
- bell pepper mottle virus
- Capsicum mosaic virus
- pepper mild mosaic virus
- pepper mild mottle tobamovirus
- pepper mild tigre virus
- pepper mosaic virus
- Samsun latent strain of tobacco mosaic virus
- PEPMTV (Pepper mild tigré ?begomovirus)
- PMMOV0 (Pepper mild mottle tobamovirus)
- Samsun latent virus
- tobacco mosaic virus, P8 isolate
Taxonomic TreeTop of page
- Domain: Virus
- Family: Virgoviridae
- Genus: Tobamovirus
- Species: Pepper mild mottle virus
Notes on Taxonomy and NomenclatureTop of page PMMV was first recognised as a distinct virus in Europe in 1984 (Wetter et al., 1984), but it had first been described previously in the USA as the latent strain (McKinney, 1952) and 12 years later as the Samsun latent strain of tobacco mosaic virus (Greenleaf et al., 1964). Some strains of the virus have been differentiated (Rast, 1979; Rast and Maat, 1986; Betti et al., 1988; Tanzi et al., 1988). Isolates of PMMV with the ability to overcome resistance genes in several Capsicum species have been designated pathotypes P1,2 and P1,2,3 (Garcia-Luque et al., 1992; Luis-Arteaga and Gil-Ortega, 1992; Marte et al., 1992).
The virus is now considered to be a distinct species of the tobamovirus genus (Wetter et al., 1984) which currently contains 13 species and two tentative species (van Regenmortel and Meshi, 1995).
A tobamovirus from pepper originally described in Argentina as an unusual strain of tobacco mosaic virus (Feldman and Oremianer, 1972), sometimes considered to be PMMV, differs significantly from PMMV and other tobamoviruses (Tobias et al., 1982; Pares, 1988); it was shown to be a distinct virus and is now designated bell pepper mottle virus (Wetter et al., 1987). Similarly, a tobamovirus isolate from pepper tentatively designated P11 in the Netherlands (Tobias et al., 1982) has molecular properties that distinguish it from PMMV and other tobamoviruses; it is thus considered to be a distinct virus for which the proposed name is paprika mild mottle virus (Garcia-Luque et al., 1993).
DescriptionTop of page
The virus has rod-shaped particles measuring 18 x 297-312 nm (Wetter et al., 1984; Pares, 1985, 1988) which sediment as a single component. Particles have an isoelectric precipitation point of c. pH 3.7, and a specific extinction coefficient (A0.1%/1 cm, 260 nm) of 3.18. The coat protein has a molecular mass, estimated by polyacrylamide gel electrophoresis, of 17-21 kDa (Othman, 1991; Xiang et al., 1994). It contains 158 amino acids, and has a composition which differs significantly from that of other tobamoviruses (Wetter et al., 1984; Creaser et al., 1987; Xiang et al., 1994). PMMoV has been identified by PCR based on the coat protein gene (Jarret et al., 2005).
The virus particles contain single-stranded RNA with an estimated molecular mass of 210,000 (Xiang et al., 1994). The genomic RNA of several isolates from different countries have been fully sequenced (Avila-Rincon et al., 1989; Alonso et al., 1991; Garcia-Luque et al., 1993; Oliviera et al., 2010). shown to contain 6357 nucleotides, and had four open reading frames (ORFs) which encoded, respectively, a 126 K protein and a readthrough 183 K protein (nucleotides 70-4908), a 28 K protein (nucleotides 4909-6582) and a 17.5 K coat protein (nucleotides 5685-6158).
DistributionTop of page
PMMoV was first described in the USA as the latent strain of Tobacco mosaic virus (McKinney, 1952). As at least six tobamoviruses naturally infect peppers, there is some doubt about the identity and, therefore, the geographical distribution of tobamoviruses reported to infect peppers before 1984 (Wetter, 1984; Wetter et al., 1984); some, if not most, of these reports (e.g., Murakishi, 1960; Murakishi and Honma, 1960; Demski, 1981) could well refer to PMMoV. Nevertheless, the virus has been reported in some countries in North and Central America, Africa, Asia, Australasia and Europe. The virus is seedborne in Capsicum species and infected seed has probably been inadvertently distributed internationally; it is thus possibly more widespread than reported and now perhaps occurs worldwide (Lamb et al., 2001). For example, an unidentified tobamovirus from pepper in South America induced inclusions characteristic of PMMoV (Herold and Munz, 1967) but unlike those of other well characterized tobamoviruses it may well be PMMV (Wetter et al., 1984). During studies on the distribution of Pepper veinal mottle virus in Africa, unidentified tobamovirus particles were detected in samples from several countries although PMMoV was identified in two samples from Senegal (Huguenot et al., 1996).
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|
|-Beijing||Present||Wang et al., 2009|
|-Liaoning||Present||Li et al., 2016a; Li et al., 2016b; Wei and Fang, 1989; CABI/EPPO, 2009||Huludao|
|-Xinjiang||Present||Xiang et al., 1994; CABI/EPPO, 2009|
|Israel||Present||Cohen and Ben-Josef, 1989|
|Japan||Present||VIDE, 1996; CABI/EPPO, 2009|
|-Honshu||Present||Nagai & Fukami, 1986; Nagai et al., 1981; Nagai et al., 1987; CABI/EPPO, 2009|
|Korea, Republic of||Present||CABI/EPPO, 2009|
|Pakistan||Present||Ahmad et al., 2015|
|Taiwan||Present||Green and Wu, 1991; CABI/EPPO, 2009|
|Turkey||Present||Güldür and Çaglar, 2006; Sevik, 2011|
|Egypt||Present||Othman, 1991; CABI/EPPO, 2009|
|Ethiopia||Present||Sidaros et al., 2009|
|Senegal||Present||Huguenot et al., 1996; CABI/EPPO, 2009|
|South Africa||Restricted distribution||IPPC, 2007; CABI/EPPO, 2009|
|Tunisia||Present||Mnari-Hattab and Ezzaier, 2006; CABI/EPPO, 2009|
|Zambia||Present||Ndunguru and Kapooria, 1996; CABI/EPPO, 2009|
|Canada||Present||Beczner et al., 1997; CABI/EPPO, 2009|
|-British Columbia||Present, few occurrences||CABI/EPPO, 2009|
|Mexico||Present||CABI/EPPO, 2009; EPPO, 2014|
|USA||Restricted distribution||VIDE; CABI/EPPO, 2009; EPPO, 2014|
|-Louisiana||Present||Escalante et al., 2018||mixed infection with Tobacco mild green mosaic virus|
|-Oklahoma||Present||Ali and Ali, 2015|
|-Oregon||Present||Hamm et al., 1995; CABI/EPPO, 2009|
|-South Carolina||Present||McKinney, 1952; Greenleaf et al., 1964; McKinney, 1968; CABI/EPPO, 2009|
Central America and Caribbean
|Antigua and Barbuda||Present||Schotman, 1989; CABI/EPPO, 2009|
|Barbados||Present||Schotman, 1989; CABI/EPPO, 2009|
|Haiti||Present||Schotman, 1989; CABI/EPPO, 2009|
|Jamaica||Present||McGlashan et al., 1993; CABI/EPPO, 2009|
|Montserrat||Present||Schotman, 1989; CABI/EPPO, 2009|
|Saint Lucia||Present||Schotman, 1989|
|Trinidad and Tobago||Present||Schotman, 1989; CABI/EPPO, 2009|
|Argentina||Present||VIDE, 1996; CABI/EPPO, 2009|
|Brazil||Present||Cezar et al., 2003; Lima et al., 2011|
|-Sao Paulo||Present||Cezar et al., 2003|
|Suriname||Present||Schotman, 1989; CABI/EPPO, 2009|
|Venezuela||Present||Rodríguez et al., 2004|
|Belgium||Present||Verhoyen, 1994; CABI/EPPO, 2009|
|Czech Republic||Present||CABI/EPPO, 2009|
|Denmark||Present||VIDE, 1996; Paludan, 1982; CABI/EPPO, 2009|
|France||Present||GebreSelassie et al., 1981; VIDE, 1996; CABI/EPPO, 2009|
|Greece||Present||Avgelis, 1986; CABI/EPPO, 2009|
|Hungary||Present||VIDE 1996; Burgyan et al., 1978; CABI/EPPO, 2009|
|Iceland||Present||VIDE, 1996; Wetter and Conti, 1987; CABI/EPPO, 2009|
|Italy||Present||VIDE, 1996; Betti et al., 1982; Conti and Marte, 1983; Wetter et al., 1984; Betti et al., 1988; CABI/EPPO, 2009|
|Netherlands||Present||VIDE, 1996; Rast, 1979; Boukema, 1980; Rast, 1982; Tobias et al., 1982; CABI/EPPO, 2009|
|Spain||Present||VIDE, 1996; Wetter et al., 1984; Marte and Wetter, 1986; Alonso et al., 1989; Garcia-Luque et al., 1990; Garcia-Luque et al., 1993; CABI/EPPO, 2009|
|-Spain (mainland)||Present||CABI/EPPO, 2009|
|UK||Present||VIDE, 1996; Fletcher, 1984; Brunt, 1986; CABI/EPPO, 2009|
|Australia||Present||VIDE, 1996; CABI/EPPO, 2009|
|-New South Wales||Present||Pares, 1985; Creaser et al., 1987; Pares, 1988; CABI/EPPO, 2009|
|New Zealand||Present||CABI/EPPO, 2009|
Risk of IntroductionTop of page
RISK CRITERIA CATEGORY
ECONOMIC IMPORTANCE Moderate
SEEDBORNE INCIDENCE High
SEED TRANSMITTED Yes
SEED TREATMENT Yes
OVERALL RISK Moderate
Notes on phytosanitary risk
PMMoV is seedborne in Capsicum species and infected seed has probably been inadvertently distributed internationally; it is thus possibly more widespread than reported and may even occur worldwide (Lamb et al.,2001). If, as current records suggest, PMMV has a limited geographical distribution, there is a great risk that it could be further disseminated in contaminated seed. Precautions are necessary, therefore, to ensure that only seed stocks that do not contain any seedborne virus are distributed.
Hosts/Species AffectedTop of page Peppers (Capsicum spp.) are the only major natural hosts of the virus. However, PMMV is transmissible experimentally to at least 24 species of six genera of the Solanaceae and to five species of four genera in four other families, Chenopodiaceae, Cucurbitaceae, Labiatae and Plantaginaceae (Wetter et al., 1984; Avgelis, 1986).
Growth StagesTop of page Fruiting stage
SymptomsTop of page The virus induces small malformed mottled fruits (which sometimes have sunken necrotic spots), mild leaf mottling and stunting of plants. Symptoms are often more severe in plants infected early (Wetter et al., 1984). The severity of symptoms depends on the virulence of the infecting virus strain, the tolerance of the cultivar and, possibly, environmental factors. As the virus does not initially induce conspicuous symptoms, it can only be reliably identified by diagnostic procedures.
List of Symptoms/SignsTop of page
|Fruit / abnormal shape|
|Fruit / lesions: black or brown|
|Leaves / abnormal patterns|
|Stems / stunting or rosetting|
|Whole plant / dwarfing|
Biology and EcologyTop of page PMMV is seedborne in Capsicum annuum and C. frutescens. The virus commonly occurs on the outer seed coat but only very rarely in the endosperm of seeds of infected plants. The level of transmission decreases markedly during seed storage (Avgelis, 1986). After storage for 11 months, levels of transmission in cvs Cleopatra No.4 and Yolo Wonder decreased from 36 to 12% and from 32 to 4.5%, respectively. Therefore, reported levels of seedborne transmission vary greatly. Levels of seedborne infections ranging between 0.23 and 100% have been reported (McKinney, 1952; Greenleaf et al., 1964; Tosic et al., 1980; Paludan, 1982; Avgelis, 1986; Tanzi et al., 1990).
As the virus is seedborne, seedlings can be infected by mechanical contamination from their contaminated seed coats during transplanting or other cultural procedures. Such seedlings are often the primary foci of infection until they are detected and removed. The virus can also persist in soil in infected debris of previous crops and this can also be a very important primary source of infection (Pares and Gunn, 1989).
The virus is very stable in vitro, highly infectious and, like other tobamoviruses, can be spread from infected to healthy plants when plants are handled during normal crop maintenance. Infectious virus (up to 0.5 yg/ml) is present in guttation fluid, and the presence of such inoculum also greatly facilitates secondary spread (French et al., 1993).
Like tomato mosaic and other tobamoviruses (Pares et al., 1992), the virus is likely to spread rapidly in crops grown in hydroponic systems if the circulating nutrient solution becomes infected and is not sterilized.
Seedborne AspectsTop of page
PMMoV is seedborne in Capsicum annuum and C. frutescens. Avgelis (1986) reported that 100% of seeds harvested from fruits of pepper plants naturally infected by PPMV were infected by the virus. Levels of seedborne infections ranging between 0.23 and 100% have also been reported (McKinney, 1952; Tosic et al., 1980; Paludan, 1982; Avgelis, 1986; Tanzi et al., 1990). Even after prolonged storage, seeds can remain infected (Genda et al., 2005).
The virus remains infective for prolonged periods in soils containing infected plant components (Ikegashira et al., 2004) and can act as sources of infection for subsequent susceptible crops (Lamb et al., 2001).
Effect on Seed Quality
Seeds extracted from fruits of pepper plants naturally infected by PMMV had transmission rates as high as 36% when planted in steam-sterilized soil (Avgelis, 1986). McKinney (1952), Tosic et al. (1980) and Tanzi et al. (1990) also demonstrated seed transmission of PMMV in grow-out experiments. The level of transmission decreased markedly during seed storage. After storage for 11 months, levels of transmission in cvs Cleopatra No.4 and Yolo Wonder decreased from 36 to 12% and from 32 to 4.5%, respectively (Avgelis, 1986).
PMMV can also persist in soil in infected debris of previous crops which can be an important primary source of infection (Pares and Gunn, 1989).
Genda et al., 2005) showed that PMMoV occurred in epidermis and parenchyma of most infected seeds but not the endosperm or embryo, but that in some it occurred only in the outer surfaces of the epidermis and placenta.
Heating seeds at 80°C for 3 days inactivated PMMV but germination was significantly reduced (Avgelis, 1986). Treating seeds with trisodium phosphate (TSP) reduced, but did not eliminate, the virus (Avgelis, 1986). Jarret et al. (2008) found that treatment of seed with 10% TSP for 2.5 h at room temperature reduced infectivity but failed to eliminate it, and reduced germination and significantly increased the number of abnormal seedlings in 11 of 50 accessions tested. The recommended treatment of seed by many, therefore, is treatment with 10% TSP for 2.5 hours, although this may result in some loss of germination (Jarret et al., 2008.). Although virus would not be eliminated in all instances, short term treatment of seed before sowing would probably reduce its incidence in crops (Jarret et al., 2008). The variable efficacy of responses of seed lots to treatment is probably attributable to virus strain and genotype, differences, and the location and concentration of virus in seed (Jarret et al., 2008).
Seed Health Tests
Indicator plants (Avgelis, 1986)
Individual seeds were triturated and inoculated onto leaves of Nicotiana glutinosa. Each seed was considered infected when it induced at least two lesions/plant.
Grow-out (Avgelis, 1986)
Seeds are planted in steam-sterilized soil. Mosiac symptoms of PPMV infection appear within 30 days of emergence.
Direct immunostaining assay (Takeuchi at al., 1999)
A new method (direct immunostaining assay, DISA) for the detection of tobamoviruses in C. annuum seeds is reported. The method allows the use of the seeds after testing. Rabbit antisera were raised against purified Tobacco mild green mosaic virus (TMGV) and Pepper mild mottle virus (PMMV). Both antisera reacted with a number of tobamoviruses including Tobacco mosaic virus, PMMV, TMGV and Tomato mosaic virus when tested. Germination of the seeds was not adversely affected by the test and sterilization of the seeds did not affect the staining of the seeds by DISA. When DISA was compared with ELISA, using 33 C. annuum cultivars, there was good agreement between the tests. It is suggested that DISA is a practical technique for the primary screening of tobamoviruses in C. annuum seeds.
The virus can be detected in developing seeds by immunoflourescence (Genda et al., 2005); this method showed that PMMV was present in the epidermis and parenchyma but not the embryo of immature seeds.
ImpactTop of page
PMMV causes considerable yield losses (ca 20-30%) in field-grown and protected infected pepper crops as well as causing significant loss of quality of fruits (e.g., Conti and Marte, 1983; Marte and Wetter, 1986; Alonso et al., 1989). In addition, rogueing of infected and adjacent plants to minimize secondary spread of infection in protected crops also results in greatly reduced potential yields. Even the mild strain used for cross protection in Italy has some debilitating effect on protected plants (Cartia et al., 1985). None of several attenuated strains of PMMoV failed to confer significant levels of cross-protection in Japan (Tsuda et al., 2007).
Total infection can occur in field-grown crops resulting in greatly reduced yields of marketable fruit (Conti and Marte, 1983; Marte and Wetter, 1986)
DiagnosisTop of page
PMMV is mechanically transmissible to a range of plant species, but the following are useful diagnostic hosts (e.g., McKinney, 1952; Greenleaf et al., 1964; Betti et al., 1982; Tobias et al., 1982; Wetter et al., 1984; Avgelis, 1986):- Capsicum annuum, C. chacoense, C. frutescens, C. praetermissum, Chenopodium amaranticolor, C. quinoa, Datura stramonium, Lycopersicon esculentum, Nicotiana clevelandii, N. debneyi, N. glauca, N. glutinosa, N. sylvestris and N. tabacum cvs White Burley and Xanthi-nc and Samsun.
Although many other species in the Solanaceae are susceptible to infection by PMMV, it does not infect Lycopersicon esculentum (tomato) or Nicotiana glauca.
Aggregates of PMMV particles occur within infected cells as hexagonal stacked-plate crystals (Wetter et al., 1984; Xiang et al., 1994), inclusions which are characteristically induced by tobamoviruses (Edwardson and Christie, 1986).
The virus is readily detected and identified by serological procedures including gel double diffusion (Wetter, 1984; Green and Wu, 1991; Xiang et al., 1994), ELISA (Wetter et al., 1984; Marte et al., 1992; French et al., 1993; Garcia-Luque et al., 1993; Gera et al., 1994), immunosorbent electron microscopy (Wetter et al., 1984; A A Brunt, c/o CABI, Wallingford, UK, personal communication, 1997) and Polymerase Chain Reaction (e.g., Jarret et al, 2008). More recently, the immuno-capture polymerase chain reaction (IC-PCR) has been shown to be a more sensitive method of identification than either ELISA or unmodified PCR (Nolesco et al., 1993).
PAGE analysis of viral coat proteins can be used to differentiate PMMV from other tobamoviruses (Garcia-Luque et al., 1990)
Detection and InspectionTop of page PMMV induces symptoms that are not readily distinguishable from those of other tobamoviruses infecting peppers. It is necessary, therefore, to use specific diagnostic procedures to identify the virus.
Similarities to Other Species/ConditionsTop of page
At least five other tobamoviruses (Tobacco mosaic, Tobacco mild green mosaic, Tomato mosaic, Paprika mild mottle and Bell pepper mild mottle) that are very similar to PMMoV occur naturally in Capsicum species (Wetter, 1984; Wetter et al., 1984; Wetter et al., 1987; Garcia-Luque et al., 1993). These can be distinguished by their serological and molecular properties (Wetter, 1984; Wetter et al., 1984; Garcia-Luque et al., 1993).
PMMoV is serologically related to Bell pepper mottle, Odontoglossum ringspot and Tobacco mild green mosaic, more distantly to Tobacco mosaic and Tomato mosaic, and only remotely so to Cucumber green mottle and Sunn-hemp mosaic viruses (Wetter et al., 1984, 1987; Brunt, 1986; Garcia-Luque et al., 1990). Genomic analysis of 26 isolates from Spain and Sicily suggests that each is a very stable population from which, if closely related variants do arise, they will not replace the parental strain (Rodriguez-Cerezo et al., 1989).
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
PMMV can be substantially eliminated from seed coats by soaking seeds in 4.2% sodium hypochlorite for 15 min or in 10% trisodium phosphate for 30 min, or by dry-heating seed for 72 h at 70°C (Demski, 1981; Avgelis, 1986).
To minimize secondary spread of infection, plants infected with PMMoV should be detected and removed as soon as possible. Milk, the proteins of which act as inhibitors of infection, is usually sprayed on infected and adjacent plants to reduce the possibility of accidental mechanical spread of virus when removing infected plants (Hare and Lucas, 1959; Jaeger, 1966).
Efficient steam sterilization of soil can sometimes reduce the subsequent levels of infection of healthy pepper seedlings. However, it is extremely difficult to sterilize soil to a depth that eliminates virus that may be present in plant debris. Stijger (1993) has also shown that virus in fresh and dried infected pepper leaves and roots cannot be eliminated by exposure to formaldehyde, nitric acid, trisodium phosphate, hydrogen peroxide with activators and an unnamed organic acid; these results confirm the virus is extremely stable. However, composting infective material is very effective in inactivating PMMoV (Aguilar et al., 2010).
Virus contamination of glasshouse structures can be substantially reduced by carefully swabbing their surfaces with 3% trisodium phosphate solution; great care, however, is necessary when handling this very corrosive alkali.
The most effective way to control the adverse effects of PMMoV is obviously avoidance (e.g., Lamb et al., 2001); Wang (2006) and Lamb et al. (2001) have reiterated the need for certified virus-free seed.
To prevent secondary spread from seed borne infection, cultural practices should be used that minimize contact with plants by workers and equipment.
In Japan, beneficial microbes in soil have been shown to inactivate PMMoV and so suppress soil borne infections (Ikegashira et al., 2010).
Induced Resistance (Cross Protection)
Avirulent strains of PMMoV, which can mitigate artificially inoculated pepper plants from the severe effects of subsequent natural infection by virulent isolates, have been obtained and used effectively in Japan (Nagai, 1987) and Italy (Tanzi et al., 1986b; Betti et al., 1991, 1992). However, even protective mild strains can have a slightly debilitating effect on artificially-infected pepper seedlings (Cartia et al., 1985) or some produced in Japan confer no significant benefit.
Natural resistance to PMMV, although yet to be exploited commercially in Capsicum annuum, occurs in some C. chilense and C. chacoense accessions, and has been attributed to a gene located at the L locus (van den Berkmortel, 1977; Boukema, 1980; Marte et al., 1992). L3 gene mediated-resistance, the so-called hypersensitive response, is elicited by the coat protein of the virus (Berzal-Herranz et al., 1995). Such resistance is associated with the presence in resistant plants of an inhibitor of virus replication which occurs in other plant species (Gera et al., 1994). The pathogenesis related protein 4 induced in C. chinensis L3 plants has been shown to have dual RNAse and DNAse activities (Guevara-Murato et al., 2010). Stable inheritance of the L4 allele for resistance to PMMV pathotype L 1.2.3 ha been reported by (Allersma et al., 2007). A pepper rootstock cultivar (cv. Dai-Power) has been shown to be resistant to PMMV (Saito et al., 2011).
Non-conventional forms of resistance have also been found to confer resistance to PMMV in experimental systems. Thus, Nicotiana benthamiana transgenic plants containing the viral replicase gene sequence were highly resistant to PMMV or showed delayed resistance to the virus (Tenllado et al., 1995, 1996). Transgenic tobacco plants expressing the coat protein gene of tobacco mosaic virus showed resistance to PMMV (Nejidat and Beachy, 1990).
ReferencesTop of page
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