Papaya ringspot virus

Pictures

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Identity

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Preferred Scientific Name

• Papaya ringspot virus

Other Scientific Names

• papaw distortion ringspot virus
• papaw mosaic virus
• papaw ringspot virus
• papaya distortion mosaic virus
• papaya distortion ringspot virus
• papaya leaf distortion virus
• papaya ringspot potyvirus

International Common Names

• English: cucurbits PRSV - strain W: watermelon; papaya PRSV - strain P: papaya

Local Common Names

• Colombia: mancha anular de la papaya
• Germany: Papaya Ringfleckenvirus; Wassermelonenvirus 1
• Venezuela: deformación foliar y manchas en anillos; mosaico

English acronym

• PRSV
• PRSV-P
• PRSV-W

EPPO code

• PRSV00 (Papaya ringspot potyvirus)

Taxonomic Tree

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• Domain: Virus
•     Group: "Positive sense ssRNA viruses"
•         Group: "RNA viruses"
•             Family: Potyviridae
•                 Genus: Potyvirus
•                     Species: Papaya ringspot virus

Notes on Taxonomy and Nomenclature

Top of page Two strains of Papaya ringspot virus (PRSV) are recognized: PRSV-type P and PRSV-type W. PRSV-P and PRSV-W have been classified as strains of the same virus on the basis of morphological and serological similarities (Yeh et al., 1984). They also have a high percentage of nucleotide and amino acid sequence homologies on the NIb and coat protein genes (Quemada et al., 1990; Bateson and Dale, 1992; Wang and Yeh, 1992; Jain et al., 1998; Wang et al., 1998). They are distinguished only by host range. PRSV-P infects papaya and cucurbits, but causes a destructive disease only on papaya. PRSV-W infects cucurbits, but not papaya. Type W, which causes severe damage to cucurbits, was previously referred to as watermelon mosaic virus 1 (WMV-1) (Van Regenmortel, 1971). The International Committee on Taxonomy of Viruses still lists WMV-1 as a synonym for PRSV (Fauquet and Martelli, 1995). However, from recent results in Australia (J.L. Dale, personal communication, Queensland University of Technology, Australia, 1996), Brunt et al. (1996) treat PRSV and WMV-1 as separate viruses. The complete nucleotide sequence and genetic organization of the RNA genome of isolates of PRSV-P from Hawaii and Taiwan were determined by Yeh et al. (1992) and Wang and Yeh (1997), respectively. Based on the nucleotide sequence of the genomic RNAs, Wang and Yeh (1997) suggested that both PRSV-P strains were derived from different evolutionary pathways in different geographic areas.

Papaya ringspot disease was referred to as papaya mosaic in literature before the 1940s (Rezende, 1984). The latter name is presently associated with a disease caused by Papaya mosaic virus. The two viruses can be distinguished readily by particle morphology, the type of intracellular inclusion they induce in the host and by serological tests (Zettler et al., 1968; Purcifull et al., 1984). Also, Papaya mosaic virus does not have a known vector, being readily transmitted by mechanical inoculation.

Description

Top of page PRSV-P belongs to the the family Potyviridae, genus Potyvirus which typically have flexuous, filamentous particles, ca 760-800 nm long and 12 nm in diameter (Herold and Weibel, 1962; Purcifull et al., 1984; Murphy et al., 1995).

Distribution Table

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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.

Last updated: 01 May 2020

Risk of Introduction

Top of page RISK CRITERIA CATEGORY

ECONOMIC IMPORTANCE High
DISTRIBUTION Worldwide
SEEDBORNE INCIDENCE Yes
SEED TRANSMITTED Disputed
SEED TREATMENT None

OVERALL RISK Low

Hosts/Species Affected

Top of page The host range of PRSV-P is limited to plants in the families Caricaceae, Cucurbitaceae and Chenopodiaceae.

In addition to the cultivated species Carica papaya, PRSV-P was also experimentally transmitted to C. goudotiana, C. horovitziana, C. microcarpa, C. monoica, C. parviflora and C. quercifolia (Conover, 1964a; Torres and Giacometti, 1966; Horovitz and Jiménez, 1967; Costa and Carvalho, 1971; Magdalita et al., 1988).

Within the family Cucurbitaceae, the following species were already tested with positive systemic infection with PRSV-P: Citrullus fistulosus; C. vulgaris [C. lanatus]; Cucumis anguria var. anguria, C. anguria var. longipes, C. melo var. reticulatus; C. metuliferus, C. sativus; Cucurbita maxima; C. pepo; C. pepo var. medullosa; C. pepo var. melopepo; C. moschata; Cyclanthera pedata; Diplocyclos palmatus; L. siceraria; Luffa acutangula; Melothria guadalupensis; M. pendula; Momordica charantia; and Trichosanthes anguina [T. cucumerina] (Capoor and Varma, 1948, 1958; Adsuar, 1950; Ishii and Holtzman, 1963; Conover, 1964b; Bokx, 1965; Story et al., 1968; Zettler et al., 1968; Costa et al., 1969; Cook, 1972; Pinto, 1972; Wang et al., 1978; Chang, 1979; Lana, 1980; Provvidenti and Gonsalves, 1982; Magdalita et al., 1990; Provvidenti, 1996; Kader et al., 1997).

Chenopodium amaranticolor and C. quinoa are reported as local lesion hosts of PRSV-P. However, local symptom expression on these species is apparently related to the virus strain and the 'variety' of the test plant.

Local lesions on both species have been reported for inoculation with PRSV-P strains from Ecuador, Florida (Yeh et al., 1984), Hawaii (Cook and Milbrath, 1971; Gonsalves and Ishii, 1980), India (Sureka et al., 1977), Nigeria (Lana, 1980) and Taiwan (Wang et al., 1978; Lin, 1980). Strains from Australia (Thomas and Dodman, 1993), Brazil (Lima and Gomes, 1975; A.S. Costa, Instituto Agronomico, Campinas, SP, Brazil, personal communication, 1985), Colombia (Sánchez de Luque and López, 1976, 1977), Dominican Republic (Story et al., 1968; Story and Halliwell, 1969) and Venezuela (Pinto, 1972) have failed to cause local symptoms on both species of Chenopodiaceae.

Rezende and Costa (1985) tested C. quinoa grown from seeds received from Taiwan, from the National Seed Storage Laboratory at Colorado State University, USA, and from a Brazilian stock. They showed that only plants originated from seeds obtained in the USA developed local lesions when inoculated with some Brazilian isolates of the virus. However, recent tests with other Brazilian isolates of PRSV-P failed to cause local lesions on the USA 'variety' of C. quinoa (J. A. M. Rezende, Universidade de Sao Paulo, Piracicaba, SP, Brazil, personal communication, 1983).

Host Plants and Other Plants Affected

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Growth Stages

Top of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

Top of page Papaya plants are susceptible to PRSV-P at any age and generally show symptoms 2-3 weeks after inoculation.

Symptoms may vary in intensity according to the age at which the plant becomes infected and the strain of the virus. Leaf symptoms are characterized by intense yellow mosaic and leaf distortion. The leaf laminae are markedly reduced in size, and may develop a shoestring appearance. The reduction of the leaf laminae can be confused with that caused by broad mite (Polyphagotarsonemus latus). Dark-green blisters may be present and mosaic may also occur on leaves.

Oily streaks on the stem and petioles of the leaves are frequently observed on diseased plants. Dark-green rings are almost always present on fruits. The number of rings on the fruit can vary, and the rings become less distinct as the fruit mature and yellow.

The canopy of diseased plants become smaller due to the development of smaller leaves, reduced petioles and stunting.

Fruit yield of affected plants is markedly lower than that of healthy plants. Trees infected at a very young age never produce marketable fruit but rarely die, except when infected with certain strains from Taiwan that cause wilting and sometimes death of young papaya trees (Gonsalves, 1994).

List of Symptoms/Signs

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Biology and Ecology

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PRSV-P is transmitted in nature by several species of aphids in a non-persistant manner (Adsuar, 1947b; Jensen, 1949b; Namba and Kawanishi, 1966; Acosta, 1969; Bhargava and Khurana, 1970; Namba and Higa, 1975, 1977, 1981; Hwang and Hsieh, 1984; Purcifull et al., 1984; Hsieh and Hwang, 1986; Taya and Singh, 1997). More than 20 species of aphids have been experimentally tested for PRSV-P transmission with positive results, including Myzus persicae, Aphis coreopsidis, A. craccivora, A. fabae, A. gossypii and Toxoptera citricidus.

Although several species of Cucurbitaceae are susceptible to PRSV-P, they are apparently not important as alternative hosts for the virus. The spread of PRSV-P into and within an orchard is primarily from papaya to papaya. The introduction of the virus into a new orchard always comes from outside, primarily from diseased papaya trees. The amount of primary infection is directly related to the distance from the infected papaya (Wolfenbarger, 1966). Once the virus is introduced into the orchard, secondary infection will occur and all plants can become infected in 3-7 months (Ishii, 1972; Conover, 1976; Barbosa and Paguio, 1982; Rezende and Costa, 1984). A slower spread of PRSV-P can occur in areas with a reduced population of aphids, as was reported for a partially isolated region of Sao Paulo, Brazil (Rezende et al., 1986, 1987; Yuki et al., 1987).

Means of Movement and Dispersal

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Natural Dispersal (Non-Biotic)

Unknown.

Vector Transmission

This is the most important and efficient way of transmission of PRSV, through short and long distance. Several species of aphids can transmit this virus. The virus-vector relationship is non-persistant (Adsuar, 1947b; Jensen, 1949b; Namba and Kawanishi, 1966; Acosta, 1969; Bhargava and Khurana, 1970; Namba and Higa, 1975, 1977, 1981; Hwang and Hsieh, 1984; Purcifull et al., 1984; Hsieh and Hwang, 1986; Taya and Singh, 1997). More than 20 species of aphids have been experimentally tested for PRSV-P transmission with positive results, including Myzus persicae, Aphis coreopsidis, A. craccivora, A. fabae, A. gossypii and Toxoptera citricida. Weed hosts in papaya orchards may serve as reservoirs of aphid vectors of PRSV-P (Martins et al., 2016). 

Seedborne Spread

Until recently there was no experimental evidence to suggest that PRSV-P was seed-transmissible. However, tests carried out by Bayot et al. (1990) in the Philippines showed that two out of 1335 seedlings (0.15%) of 'Cavite' papaya grown from seeds taken from PRSV-P infected fruits showed symptoms similar to those of papaya ringspot. In another study, no seed transmission of the virus was detected in papaya (Prasad and Sarkar, 1989).

Agricultural Practices

Not known to be involved on the transmission of PRSV in the field.

Seedborne Aspects

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Tripathi et al. (2008) reported that PRSV is typically not seed transmitted; however, Laney et al. (2012) recorded a high incidence of seed transmission of the virus in Robinia pseudoacacia.

Pathogen Transmission

Tests carried out by Bayot et al. (1990) in the Philippines showed that two out of 1335 seedlings (0.15%) of 'Cavite' papaya grown from seeds taken from PRSV-P infected fruits showed symptoms similar to those of papaya ringspot. In another study, no seed transmission of the virus was detected in papaya (Prasad and Sarkar, 1989). Further studies are required for confirmation of seed transmissibility of PRSV-P.

Laney et al. (2012) reported a high incidence of seed transmission of PRSV in black locust (R. acacia) suggesting that this may be an important route for virus dissemination.

Plant Trade

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Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Growing medium accompanying plants
True seeds (inc. grain)
Wood

Vectors and Intermediate Hosts

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Impact

Top of page PRSV-P causes one of the most destructive diseases of papaya in nearly every region of the world where papaya is grown. The decline of the papaya industry due to papaya ringspot disease has been observed in some regions. In Taiwan, PRSV-P was first recorded in 1975 and within 4 years the virus had destroyed most of the papaya production along the west coast of the island. The total yield of papaya dropped from 41,595 tons in 1974 to 18,950 tons in 1977 (Yeh et al., 1988).

In Southern Tagalog, Philippines, where the virus was first detected in 1982, papaya production was reduced drastically from 36,000 metric tons in 1981 to 10,000 metric tons in 1987 (Bayot et al., 1990).

In Brazil, the disease caused by PRSV-P was responsible for the almost total disappearance of the papaya crop from the state of Sao Paulo. The area planted with papaya trees was reduced from aproximately 7188 ha in 1977 to 4374 ha in 1980, 906 ha in 1986 and 234 ha in 1989.

Diagnosis

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Symptoms induced by PRSV-P in Carica papaya can be used for detection and diagnosis, although they show certain variation depending on the stage of infection, plant vigour, temperature, virus strain and plant size. Key symptoms are the intense mosaic on leaves and the presence of oily streaks on the stems and petioles. Another key symptom, for plants bearing fruits, is dark-green rings on fruits.

The virus is a good immunogen and antisera with high titres have been produced. Liquid immunoprecipitin test (Webb and Scott, 1965), SDS-immunodiffusion test (Purcifull and Hiebert, 1979; Gonsalves and Ishii, 1980), ELISA (Gonsalves and Yshii, 1980; Ben-Ze'ev et al., 1988; Husain, 1997) and immunosorbent electron microcopy (ISEM) can be used for the detection of virus in infected tissues.

Particle morphology and cytoplasmic inclusions in the host tissue, viewed by electron microscopy, may also be used in diagnosis. Cytoplasmic inclusions are of two types: cylindrical and amorphous. The cylindrical inclusions are striated, with a periodicity of 5 nm, and are associated with scrolls. They aggregate to form fibrous structures that are clearly visible by light microscopy of epidermal strips stained with luxol brilliant green-calcomine orange (Purcifull et al., 1984).

RT PCR is identified as a rapid and important diagnosis method for PRSV by Vucurovic et al. (2009).

Detection and Inspection

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Symptoms of the disease are very characteristic and easily visible on plants infected in the field. During the early stage of infection PRSV can be identified by the presence of oily stains in the base of the petioles and in the stem (Cortez-Madrigal and Mora-Aguilera, 2007). When confirmation of the disease agent is required, leaf samples should be collected for identification using the methods described under Diagnostic methods.

Prevention and Control

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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.

Introduction

Due to the economic importance of the papaya crop and the damage caused by papaya ringspot disease, scientists from different parts of the world have made efforts to develop methods to control or minimize the effects of the disease on papaya production. Different approaches have been investigated, such as planting in partially isolated areas and roguing; planting under screenhouses; breeding for resistance or tolerance to the virus; using virus-resistant transgenic plants; and cross protection.

Cultural Control

Planting in partially isolated areas and roguing
PRSV may be controlled by preventive practices that reduce or delay the spread of the virus within the orchard. These practices include the use of virus-free seedlings to start new crops, planting in partially isolated areas or as far as possible from old infected papayas, roguing of diseased plants once every 2 weeks, avoidance of cucurbit plants in or near the orchard, and systematic weed control to reduce the aphid population (Costa et al., 1969; Ishii, 1972; Martinez, 1980; Gonsalves, 1994). Practical application of these measures, especially roguing of diseased plants, has been reported in Hawaii (Namba and Higa, 1977; Gonsalves, 1994). In Brazil, roguing of diseased papayas allowed satisfactory control of the disease in orchards in Espírito Santo for more than 10 years, with an eradication rate of between 5 and 10% of diseased trees per year (JA Ventura, EMCAPA, Vitoria, ES, Brazil, personal communication, 1986). Due to the effectiveness of this practice, the state of Espírito Santo passed a law which requires all growers to adopt roguing of diseased papayas for control of the disease; failure to follow the rules can result in complete elimination of the orchard by official authorities.

In Sao Paulo, Brazil, Rezende et al. (1986, 1987) demonstrated that papayas could be grown satisfactorily in certain areas in the Ribeira Valley, which is situated in the south-east of the state between the coastal mountain range and the ocean. The spread of the virus in this region is slower than in other parts of the state due to the reduced aphid population and the partial isolation of areas with native forest (Yuki et al., 1987).

Planting under screenhouse
Several studies have been carried out in order to find chemical or physical methods of protecting papaya trees from aphid vectors. These methods include the use of insecticides, mineral oils, and protective barriers of other species of plants (Acosta, 1969; Harkness, 1967; Nakasone, 1980; Becerra Leon, 1989). None of these methods have been sufficiently effective in controlling papaya ringspot because of the large number of aphid species that may act as vectors and their non-persistant relationship with the virus.

Another alternative is to prevent viruliferous aphids landing on papaya trees by planting the crop under screenhouses. This technique was first tried in Taiwan and has produced satisfactory results (Rezende and Costa, 1995). Sheen et al. (1998) reported that Taiwan has more than 1000 ha of papayas growing under screenhouses (net-house) annually. The incidence of PRSV-P in the screenhouse was 0.3%, 6 months after transplanting, compared to 96% plants infected in the field.

Planting date and mineral nutrition
Studies in India have shown that transplanting papaya in October, with heavy but balanced fertilization, helped reduce the incidence and severity of papaya ringspot disease in plantations. The best fertilization dose consisted of 10 kg FYM, 2 kg castor cake, 1 kg cake-0-meal, 200 g N, 200 g K2O and 200 g P2O5 (Kudada and Prasad, 1999; Ray et al., 1999).

Effective microorganisms (EM), a mixture of beneficial microoganisms including lactic acid bacteria, yeasts, actinomycetes and photosynthetic bacteria, have been reported to reduce papaya ringspot incidence in Taiwan (Tsai, 1998).

Host-Plant Resistance

Resistance to PRSV-P does not occur within Carica papaya. Although high levels of resistance or immunity have been found in some wild species of Carica, interspecific reproductive barriers make it difficult to incorporate resistance genes into C. papaya (Horovitz and Jiménez, 1967; Nagai, 1980; Nakasone, 1980; Magdalita et al., 1988, 1997; Manshardt and Wenslaff, 1989a, b; Chen et al., 1991; Fitch et al., 1992; Drew et al., 1998).

The development of tolerant cultivars of C. papaya has minimized the damage caused by papaya ringspot. Conover et al. (1986) developed the cultivar Cariflora, which is tolerant to papaya ringspot in southern Florida, USA, and the Caribbean. In Taiwan, Lin et al. (1989) reported the development of the hybrid Tainung No. 5 with good level of tolerance to the disease and horticultural characteristics that satisfy both farmers and consumers.

Cross Protection

Cross protection has been used for the control of papaya ringspot in different countries with varying degrees of success. This technique involves the inoculation of papaya seedlings with a mild strain which protects plants against damage caused by infection with a severe strain of the virus in the field.

A nitrous acid-induced mutant of PRSV-P from Hawaii, designated HA 5-1, was introduced into Taiwan and used to protect papaya trees in the field (Yeh and Gonsalves, 1984, 1994; Yeh et al., 1988). Although cross protection has helped papaya growers to produce a fruitful crop during 8 years, there are several drawbacks including adverse effects of mild strains on papaya under cool and rainy conditions; the additional cost of inoculating and indexing the seedlings; difficulties in propagation and preservation of the inoculum; the possible occurrence of severe revertants; breakdown under severe disease pressure; and strain-specific protection (Yeh and Gonsalves, 1994; Sheen et al., 1998). Currently, the mild strain is sparsely used in Taiwan, mainly because it does not provide consistent economic returns to farmers (Gonsalves, 1998).

Extensive field trials on the Island of Oahu, Hawaii showed that cross protection with the mild strain HA 5-1 was more effective in Hawaii than in Taiwan, as protection is strain-specific. The mild strain HA 5-1 was selected from a common strain from Hawaii and therefore offers better protection against the parental strain. The mild strain HA 5-1 gave good protection in field experiments, although it produced noticeable symptoms on leaves and fruits, with the degree of symptom severity markedly dependent on the cultivar (Gonsalves, 1998). Cross protection has not been widely adopted on Oahu for several reasons including adverse effects of the mild strain on papaya cultivars, the extra cultural management and care required, and the reluctance of farmers to infect their trees with a virus (Gonsalves, 1998). The introduction of the mild strain to Thailand and Mexico did not show promising results, apparently due to strain-specific protection (Yeh and Gonsalves, 1994; Gonsalves, 1998).

In Brazil, attempts to control papaya ringspot by cross protection have failed due to the apparent instability of the selected mild strains (Rezende, 1985; Rezende and Costa, 1987; Rezende and Costa 1995; Rezende and Müller, 1995).

Transgenic papaya

The development of transgenic papaya, containing the coat protein gene of PRSV-P, has offered a new approach for controlling papaya ringspot. The first successful effort to develop transgenic papaya resistant to PRSV-P was initiated in late 1980s through a co-operative project involving Cornell University, the UpJohn Company, the University of Hawaii and the Papaya Administrative Committee from Hawaii (Gonsalves, 1998). Fitch et al. (1990, 1992) obtained a Sunset Solo-derived transgenic line, named 55-1, that expressed the coat protein gene from the mild strain PRSV-P HA 5-1, which was highly resistant to Hawaiian strains of the virus, but susceptible to strains outside Hawaii (Tennant et al., 1994). The transgenic papaya showed excellent resistance throughout the 2-year field trial in Hawaii (Lius et al., 1997). In 1998, two trangenic papaya varieties resistant to PRSV-P, Rainbow and Sun Up, were commercially released in the USA. Sun Up is line 55-1, which is homozygous for the coat protein transgene, and Rainbow is an F1 hybrid between Sun Up and the yellow-fresh variety, Kapoho Solo. These trangenic, resistant varieties promise to revive the Hawaiian papaya industry (Gonsalves, 1998).

Further studies with transgenic papaya have shown a breadth of resistance reactions to PRSV-P strains. Tennant et al. (1997) showed that SunUp has a broader spectrum of resistance than Rainbow or the R1 hemizygous 55-1, suggesting that gene dosage affects the resistance. Sunset Solo-derived transgenic line 63-1 has shown resistance to PRSV-P isolates from Brazil and Thailand (Souza et al., 1998; Souza, 1999). Yeh et al. (1997) obtained transgenic papaya expressing the coat protein gene from a Taiwanese PRSV-P isolate and resistant to isolates from Taiwan, Hawaii and Thailand. The production of PRSV-P resistant transgenic papaya plants expressing untranslatable versions of the coat protein gene (Souza and Gonsalves, 1998; Cai et al., 1999), together with results from northern blots and nuclear run on assays from line 55-1 (Tennant et al., 1997; Souza, 1999) suggested that post transcriptional gene silencing is the underlaying mechanism for the PRSV:transgenic papaya resistance system.

In 1992, a collaborative effort was initiated between Cornell University and the National Center for Research in Cassava and Tropical Fruits (CNPMF, EMBRAPA, Cruz das Almas, BA, Brazil) with the objective of developing transgenic papaya expressing the coat protein gene of a Brazilian isolate of PRSV-P. An initial evaluation revealed that some phenotypes were apparently immune to Brazilian isolates of the virus. The first field trial with transgenic papaya in Brazil was initiated in January 2000 (Souza and Gonsalves, 1998, 1999; Souza, 2000).

New transgenic lines expressing the coat protein genes of PRSV-P isolates from Jamaica, Thailand and Australia have been produced (Gonsalves, 1998).

According to Gonsalves (1998), proof of success in controlling papaya ringspot throughout transgenic resistant plants will be determined in the next few years, as the transgenic papaya is currently widely planted in Hawaii and as more transgenic papaya is produced and tested worldwide.

References

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Verma R, Gaikwad P, Mungekar D, Tripathi S, Datar V, Singh J, 2014. First report of mixed infection of Papaya ringspot virus and phytoplasma in papaya in India. Journal of Plant Pathology. 96 (2), 438. http://www.sipav.org/main/jpp/

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Wang H L, Wang C C, Chiu R J, Sun M H, 1978. A preliminary study of papaya ringspot virus in Taiwan. Plant Protection Bulletin. 20 (2), 133-140.

Xiao HuoGen, Tetsuo MaoKa, Luo XueHai, 1997. Investigation and identification of papaya ringspot virus and papaya leaf - distortion mosaic virus in South China. Journal of South China Agricultural University. 18 (4), 52-53 (Ch), 58 (En).

Yeh S D, Gonsalves D, 1994. Practices and perspective of control of papaya ringspot virus by cross protection. In: Advances in Disease Vector Research. 10 237-257.

Distribution Maps

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