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Papaya pests and diseases were described in a review in which Fitch (2010) cited a compendium by Nishijima (1994). The major pests are bacteria, fungi, oomycetes, viruses and arthropods. While most pests can be adequately controlled by chemical treatments, bacterial and viral diseases require breeding and/or other solutions.

BACTERIAL DISEASES. In Malaysia where ‘Eksotika’, ‘Eksotika II’, ‘Solo’, ‘Hong Kong’ and ‘Sekaki’ are important, papaya dieback is a major disease (Chan, 2007; Maktar et al., 2008). Identified earlier as being caused by Erwinia papayae (Maktar et al., 2008), it was renamed Erwinia mallotivora (Amin et al., 2011). There is no known resistance to this serious rotting disease (Bunawan and Baharum, 2015). Erwinia papayae has been reported as the causal agent of bacterial canker in the Caribbean region (Gardan et al., 2004) and in Tonga (Fullerton et al., 2011); bacterial crown rot (BCR) is caused by an E. papayae-like bacterium. BCR in the Philippines is a destructive disease and is caused by E. mallotivora (Dela Cueva et al., 2017; P.M. Magdalita, Philippines, 2018, personal communication). Another Erwinia sp. that has caused papaya stem canker in a University of Ibadan garden (Nigeria) has been reported (Olabiyi, 2010), but its impact on the Nigerian papaya industry was not described. The Nigerian disease symptoms were like those of stem canker disease caused by E. papayae in the Caribbean region.

Another rotting disease, bacterial decline caused by Erwinia sp., decimated the ‘Solo’ fields in the Virgin Islands and Venezuela (Ollitrault et al., 2007). It is not known if papaya decline and stem canker are caused by the same or a related bacterium. Two Erwinia spp. were observed in the Northern Marianas (Trujillo and Schroth, 1982). One caused decline and the other caused mushy cankers. It is likely that these two species were E. mallotivora and E. papayae, respectively.

Enterobacter cloacae is the causal agent of internal yellowing (IY) disease. The coliform bacterium has been an occasional problem in ripe papayas (Nishijima et al., 1987; Nishijima, 1994). It has the potential to jeopardize food safety of minimally processed fresh fruit and impact consumers with low tolerance of contaminated foods. The popularity of packaged convenience fruit mixtures, frozen cubes and cut fruit on buffet platters could result in increased incidences of IY. The susceptible cultivar ‘Kapoho Solo’ (Nishijima et al., 1987) is a parent of transgenic ‘Rainbow’.

Papaya bunchy top (PBT) disease was originally believed to be caused by a virus, but was later attributed to a phytoplasma and is now associated with a Rickettsia-related proteobacterium that is not culturable (Davis et al., 1996; Luis-Pantoja et al., 2015). PBT is a serious problem in Cuba and the Caribbean region, and its only host is papaya.

New hybrids with tolerance of both BCR and PRSV, ‘Hirang’, ‘Liyag’ and ‘Timyas’, are undergoing field trials (P.M. Magdalita, Philippines, 2018, personal communication). Nine parental lines, six inbred lines and five accessions with resistance to BCR are being evaluated for horticultural qualities (Dela Cueva et al., 2017).

Breeding involving Erwinia disease-resistant or -tolerant wild papayas from Guadeloupe could result in improved papayas for Malaysia and elsewhere in the Caribbean region. Tolerance from ‘Saipan Red’, ‘Dwarf 7355’ and ‘Waimanalo Solo’ (Trujillo and Schroth, 1982) could be incorporated into breeding programmes. For PBT, avoidance and planting of tolerant cultivars are currently the only solutions.

Papayas with tolerance of or resistance to bacterial dieback in Malaysia are unknown (Bunawan and Baharum, 2015). The bacterium was identified after its 16S rRNA gene was sequenced and biochemical tests confirmed that it differed from E. papayae based on 16S rRNA sequence similarity with the Caribbean pathogen (Maktar et al., 2008). A draft of the bacterium genome sequence was further confirmation of its identity (Amin et al., 2011; Redzuan et al., 2014). In Johor State, the bacterium associated with dieback was identified as E. papayae because of its 16S rRNA sequence similarity to E. papayae from the Caribbean region (Maktar et al., 2008). E. papayae is the causal agent of bacterial canker (Gardan et al., 2004). Malaysia apparently has two Erwinia species, E. mallotivora and E. papayae, that cause different diseases.

Selection for papaya lines that are tolerant of bacterial decline (Erwinia sp.) was reported in Guadeloupe where the disease was first reported (Ollitrault et al., 2007). Researchers crossed tolerant but poor-quality accessions with susceptible but high-yielding ‘Solo’. Backcrossing and endogamy strategies were reported; however, there have been no further reports. Bacterial dieback and decline diseases could be caused by the same pathogen. Hawaii papaya cultivars and clones were inoculated with suspensions of E. cloacae to determine if tolerant or resistant lines could be identified. A concentration of 9–10 log10 colony-forming units per millilitre (cfu/ml) reliably differentiated between resistant and susceptible lines. Red-fleshed cultivars and lines were the most resistant, corroborating earlier results (Nishijima et al., 1987). A yellow-fleshed inbred F5/F6 line derived from yellow-fleshed ‘Rainbow’, an F1 hybrid of IY susceptible ‘Kapoho Solo’ and IY resistant ‘Sunset’, was resistant and offered potential for improving resistance in yellow-fleshed cultivars (Nishijima et al., 2010).

VIRAL DISEASES. The most destructive disease of papaya is caused by PRSV (Jensen, 1949; Gonsalves, 1998; Constantinides and McHugh, 2008). A seed-borne virus, it occurs in all papaya growing regions. Symptoms are mottled green and yellow canopies, streaked stems and petioles, ring spots on fruit, collapse of fruit production and eventual death of the trees. New reports of PRSV appear from time to time, e.g. confirmation in Laos and an initial report in Cambodia (Chittarath et al., 2017).

The less well-known but destructive Papaya leaf distortion mosaic virus (PLDMV) is important in Taiwan and Okinawa (Maoka et al., 1996; Bau et al., 2008) and is second in importance to PRSV. Papaya lethal yellowing virus (PLYV; Daltro et al., 2012), Papaya mosaic virus (PMV) (Noa-Carrazana et al., 2006) and Papaya meleira virus (PMeV) (Abreu et al., 2012) are also important viruses. PMeV is seed transmitted making it an especially serious threat to growers worldwide (Tapia-Tussell et al., 2015). A less destructive virus, Papaya leaf curl virus (PaLCuV) (Srivastava et al., 2010) was reported in India. Papaya apical necrosis, a disease associated with a rhabdovirus, was reported in Venezuela (Lastra and Quintero, 1981) and Cuba, (Hernandez et al., 1990). Papaya droopy necrosis virus (DNV), also associated with a rhabdovirus, has been reported in Florida (Wan and Conover, 1983). The two rhabdovirus-associated diseases are probably caused by the same pathogen. Vectors and alternative hosts of DNV were not known at the time of the report. Roguing and avoidance of overlapping successive papaya crops reduced incidence of the disease.

Virus diseases occur wherever papayas are grown extensively. Growers can relocate plantings to virus-free areas until the virus appears or grow plants in protective enclosures (net houses in Taiwan; typhoon-proof greenhouses in Japan). In Hawaii, where land is limited, an alternative was to control arthropod pests, e.g. the vector, Myzus persicae; however, this has not prevented the spread of PRSV (Namba and Kawanishi, 1966). A mild strain of PRSV was developed by nitrous oxide treatment of a virulent strain (Yeh and Gonsalves, 1984). Cross protection, the deliberate inoculation of plants with the mild strain (Yeh and Gonsalves, 1984; Wang et al., 1987), provided limited protection for certain cultivars (Mau et al., 1989).

Transgenic PRSV-resistant papayas have been developed by 15 different research groups (Table 6.1.1; Fitch, 2016); Guangdong province in China commercialized resistant ‘Huanong#1’ (Fitch, 2016). The United States Department of Agriculture (USDA), the Environmental Protection Agency (EPA) and the Food and Drug Administration (FDA) have approved deregulation for a new red-fleshed transgenic papaya, X17-2, a ‘Sunrise’ × Chinese papaya (T65) hybrid developed by the University of Florida, and commercialization agreements are being sought (Davis and Ying, 2002; M. Davis, Florida, 2018, personal communication).

Table 6.1.1. Summary of papaya transformation projects for virus resistance.^a

Governmental policy issues with the engineered fruit have terminated most deregulation processes. Only a few locations still pursue transgenic virus resistance, e.g. China (Hainan Island) (Jia et al., 2017).

A programme to address PRSV in Florida where the virus had caused serious crop losses for many years was initiated by Conover (1976). Tolerant accessions were screened, and intergeneric hybrids involving PRSV-resistant Vasconcellea spp. to papaya were made (Conover, 1976, Conover and Litz, 1978; Litz and Conover, 1981). In Australia and Hawaii, intergeneric hybridizations with Vasconcellea species were also reported (Manshardt and Wenslaff, 1989a,b; Drew et al., 1998; Magdalita et al., 1998): Vasconcellea candicans, Vasconcellea cauliflora, V. pubescens, Vasconcellea quercifolia, V. stipulata and V. × heilbornii nm. pentagona (Manshardt and Wenslaff, 1989a).

C. papaya crosses with V. pubescens, V. quercifolia and V. stipulata resulted in PRSV-resistant F1 hybrids (Manshardt and Wenslaff, 1989b); however, these plants were either sterile or very difficult to backcross to papaya. In another study, V. quercifolia × papaya backcross hybrids were created that exhibited tolerance; however, loss of resistance occurred after 18 months in the field (Siar et al., 2011). While the V. quercifolia hybrids could be shown to be resistant to PRSV for a while, the resistance gene(s) was not identified until transcriptional profiling was assessed after PRSV inoculation (Kanchana-udomkan et al., 2016a). A putative resistance gene, VQ_STK2, was significantly and differentially up-regulated in Vasconcellea, but the papaya STK2 homologue was significantly down-regulated, indicating the STK2 may be the source of PRSV resistance.

The V. pubescens introgression project was refocused to overcome breeding incompatibilities with papaya. Bridge-cross hybrids were created involving V. pubescens (PRSV resistant) × Vasconcellea parviflora (PRSV susceptible). Since V. parviflora F1 hybrids with papaya are somewhat fertile, backcrosses were made (O’Brien and Drew, 2009). Individuals carrying the putative resistance gene, a serine/threonine kinase (STK) (Dillon et al., 2006b; Razean Haireen, 2013), were backcrossed with V. parviflora to produce fertile backcross 4 (BC4) hybrids. The line with the highest fertility, #113, was crossed with local papayas in Australia, Hawaii, India and Malaysia (Kanchana-udomkan et al., 2018; M. Fitch and S. Tripathi, unpublished results) to transfer the STK resistance gene. The groups recovered F1 hybrids that were screened for the resistance gene by polymerase chain reaction (PCR) and digestion (Dillon et al., 2006b; Kanchana-udomkan et al., 2018; X. He, M. Fitch, S. Tripathi, unpublished results); however, subsequent BC1 crosses with papaya were unsuccessful. In Hawaii, about half of the 66 seedling lines derived from embryo rescue contained the resistance gene. Three resistance gene-positive lines that were inoculated three times with local strains of PRSV did not show virus symptoms. The F1 plants in India were PRSV resistant but were difficult to maintain. Flowering was infrequent with the two Hawaii hybrids that bloomed: one was female and the other was a hermaphrodite. Pollinations with ‘Waimanalo’ papaya aborted. The single female fruit that developed was identical to one in Australia (Kanchana-udomkan et al., 2018).

Conover et al. (1986) developed a PRSV-tolerant dioecious cultivar ‘Cariflora’ that has been exploited in several countries. Tolerant dioecious individuals were selected, backcrossed and screened until ‘Cariflora’, a warm lowland line, was identified. In Hawaii, ‘Cariflora’ was crossed with local hermaphroditic cultivars and lines, but with many segregating traits besides PRSV tolerance, it was difficult to develop new cultivars suitable for the industry (Zee, 1985). Breeding involving ‘Cariflora’ in Taiwan and elsewhere has resulted in new PRSV-tolerant selections.

In north-eastern Thailand, PRSV-tolerant cultivars were developed from ‘Cariflora’ that were adopted by growers. ‘Cariflora’ (‘Florida Tolerant’) seeds introduced by Hawaii researchers (Prasartsri et al., 1997) were crossed with local important cultivars, ‘Khaek Dam’ and ‘Khaek Nuan’, and several hybrids and inbreds were approved for commercial production in 1997 and 2010 and from which improved cultivars, ‘Khaek Dam Tha Phra’ and ‘Khon Kaen 80’, were adopted by growers (Somsri, 2014). Selections from later crosses, ‘Khaek Dam’ (R3 300KD), ‘Khaek Nuan’ (R3 319-1KN-180, and R3 319-1KN-181), were also selected for PRSV tolerance (Somsri, 2014); however, these selections are no longer grown (S. Somsri, Thailand, 2018, personal communication).

After PRSV was discovered in the Philippines, researchers have screened foreign and local papayas for tolerance (Villegas et al., 1996). Tolerant selections were selfed or sib-mated, and after six or seven generations of inbreeding, six tolerant inbred selections were made. The popular ‘Sinta’ (Sweetheart) is an F1 hybrid of Py 5 × Py 3 (Villegas et al., 1996) and was released in 1995. ‘Sinta’ was further improved to produce ‘Hirang’, ‘Liyag’ and ‘Timyas’ and moderately PRSV- and BCR-tolerant lines that are being grown in multi-location field tests (Magdalita and Signabon, 2017; P.M. Magdalita, Philippines, 2018, personal communication).

Two PRSV-tolerant cultivars, ‘Tainung#5’ and ‘Cariflora’, were crossed with local lines for improved quality and PRSV tolerance at the Malaysian Agricultural Research and Development Institute (MARDI; Chan, 2004). The popular but highly PRSV susceptible ‘Eksotika’ was crossed with ‘Cariflora’ and ‘Tainung#5’. The F1 plants had intermediate PRSV tolerance compared with the parental lines, but sweetness and total soluble solids (TSS) ratings were highest in the ‘Cariflora’ F1 plants. This hybrid was recommended for F5 inbred line development by single seed descent. Hybrids with ‘Tainung#5’ were further characterized, although no further information is available.

In India, attempts to develop introgressed PRSV resistance using materials from Australia were difficult (Mitra et al., 2017; S. Tripathi, India, 2018, personal communication). Therefore, plants identified by growers were used to identify lines with PRSV tolerance and marketable qualities. The India Agricultural Research Institute (IARI) developed Pune Selection Lines 1, 3 and 5 that were sib-mated and that performed well in farmers’ fields but are not available for commercial release. The lines are being further improved (S. Tripathi, India, 2018, personal communication). At the Horticultural College and Research Institute, tolerance has been observed in CP-50, a hybrid between a field tolerant ‘wild’ papaya and CO 6, a cultivated papaya (Balamohan et al., 2010).

A dioecious Florida selection, FL-77-5, was crossed with ‘Costa Rica Red’ in Taiwan and ‘Tainung#5’ a dwarf cultivar with high tolerance of PRSV and high yields was selected (Lin et al., 1989). PRSV-tolerant ‘Known-You#1’ and ‘Red Lady’ are advertised on a Taiwanese website that markets seed worldwide. Mexican breeders have collected wild germplasm to screen for virus and other pest-tolerant genotypes (Pesqueira et al., 2017) to breed with with popular cultivars to develop new lines that could help farmers grow fruit in PRSV-infested fields as practiced in the Philippines.

FUNGAL AND OOMYCETE DISEASES. Papayas have many destructive fungal and oomycete rot and spot problems during rainy seasons. Different growing regions have different pathogens, but the most important fungal diseases are caused by Colletotrichum gloeosporioides (anthracnose), Asperisporium caricae (black leaf spot) and Phytophthora palmivora (phytophthora fruit and stem rot) (Nishijima, 1994, 2002; Constantinides and McHugh, 2008). Phytophthora is the most serious disease (M. Kamiya, Hawaii, 2018, personal communication). Less serious papaya fungal pathogens are Cercospora papayae (cercospora black spot), powdery mildew (Oidium caricae), Rhizopus ssp. and Mycosphaerella caricae (black rot) (Nishijima, 1994; Constantinides and McHugh, 2008).

ARTHROPOD PESTS AND NEMATODES. The most important insect pests in Hawaii include white peach scale (Pseudaulacaspis pentagona) and papaya mealy bug (Paracoccus marginatus) and, seasonally, Stevens leafhopper (Empoasca stevensi) (Follett, 2000; Constantinides and McHugh, 2008). A soft green scale pest, Philephedra tuberculosa, and grey scale, Pseudoparlatoria ostreata, have been reported on papaya (Matsunaga, 2018), but the extent of the infestations are unknown. Thrips parvispinus (Karney) was identified in Hawaii growing areas (Villalobos et al., 2007). Spider mites (Tetranychus cinnabarinus, Eutetranychus banksi and Panonychus citri), broad mite (Polyphagotarsonemus latus), flat mite (Brevipalpus phoenicis) and leaf edgeroller mite (Calacarus flagelliseta) require chemical pest control (Follett, 2000; Constantinides and McHugh, 2008).

Scale pests in Brazil include Aonidiella comperei, Coccus hesperidum, Dysmicoccus grassii, Phenacoccus solenopsis, Pseudococcus sp. and Selenaspidus articulatus (Martins et al., 2015). A. comperei is the most important and widespread scale insect pest in Brazilian papaya growing regions. About 26 of the 48 species of scale insect pests of papaya worldwide are found in Brazil.

India, Indonesia and other Asian countries have the serious pest, papaya mealy bug, which was introduced from Mexico. Integrated pest management (IPM) was implemented to combat the infestations and considered to be a success (IPM Innovation Lab, 2008; Rich, 2008). Other insect pests of India are the ash weevil (Myllocerus sp.), green peach aphid (M. persicae) and white fly (Bemisia tabaci) (TNAU Agritech, 2015).

The papaya mealy bug is a worldwide pest. It was described in 1992 in Mexico and Central America and soon became a pest in the Caribbean region, South America, Pacific Islands and South Asia (Muniappan et al., 2008). In West Africa, after being found in Reunion in 2010, it was reported in Ghana and coasts of neighbouring countries. From Tanzania, the spread was rapid around the coastal areas (Chuki, 2015), alarming growers in Africa (SciDev.Net, 2015). The pest spread from the coastal area inland mainly along major roads. Great concern existed because 85% of the major farms were destroyed initially, impacting export earnings. The economic and ecological impact of an outbreak in Nigeria where 94% of the West African papayas are grown was expected to be devastating. Since the mealy bugs were controlled by the introduction of natural enemies in the Caribbean region, South America, Guam, Palau and Hawaii, a similar joint effort was initiated in 2010 between the Plant Protection and Regulatory Services Directorate (PPRSD), Ghana, the Food and Agriculture Organization of the United Nations (FAO) and the International Institute of Tropical Agriculture (IITA) in collaboration with USDA and Animal and Plant Health Inspection Service (APHIS) to provide mealy bug-specific parasitoids from the mass-rearing facilities in Puerto Rico (Goergen et al., 2011). Australia has not yet reported this serious pest, but growers are forewarned of the threat (Farmbiosecurity, 2018).

The papaya fruit fly, Toxotrypana curvicauda Gerstaecker, is a major pest in the Americas. No effective control has been found for this pest, although pheromone lures, traps and sanitation are used. Its host range is small, i.e. papaya, mango and milkweed (Selman et al., 2015). The female pest resembles a wasp with its long 9–14 mm ovipositor. The female oviposits into the central cavity of unripe papaya fruits where larvae feed on seeds. Infected fruit drop prematurely from the tree. Damage levels in Florida during spring and summer range from 2% to 30%.

The oriental fruit fly Bactrocera dorsalis (Hendel), Mediterranean fruit fly, Ceratitis capitata (Wiedemann) and melon fly, Bactrocera cucurbitae (Coquillett), oviposit in ripening papaya fruits. These pests pose serious threats to agriculture in many countries, e.g. the state of California’s US$ 20.8 billion fruit and nut industry (CDFA, 2017). Therefore, all Hawaii papayas entering California are vapour heat-treated or irradiated at levels that are lethal to these pests (Armstrong et al., 1995; Follett, 2000). In Australia, papaya pests include the Queensland Bactrocera tryoni and the Mediterranean fruit fly (Farmbiosecurity, 2018). India lists only the oriental fruit fly (TNAU Agritech, 2015).

Reniform (Rotylenchulus reniformis) and root knot (Meloidogyne incognita) nematodes are usually economically important in irrigated fields (Constantinides and McHugh, 2008).

Breeding for tolerance of arthropod and other pests has not received much attention since management is afforded by agrichemical spray routines. Pests are adequately controlled by a variety of chemical applications aimed at avoiding development of resistance in pests (Follett, 2000; Constantinides and McHugh, 2008). A cross between ‘Sekaki’ and Hawaii cultivars resulted in increased thrips tolerance (R. Manshardt, Hawaii, 2018, personal communication).