Correlation of Leaf Parameters with Incidence of Papaya Ring Spot Virus in Cultivated Papaya and its Wild Relatives

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Papaya is ranked as the third most traded tropical fruit (excluding bananas). The area and production of papaya is on the increase in recent years due to its wide ecological adaptability, easiness in cultivation, high palatability, early fruiting, year round bearing, higher productivity and economic returns. Papaya is a nutrition basket filled with vitamins (2020 IU of vitamin A, 40 mg of vitamin B1 and46 mg ofvitamin C per 100g of fruit), minerals, carbohydrates, proteins, iron, calcium and phosphorous (Dinesh, 2010). However, the production of papaya is hampered by a serious outbreak of viral disease caused by Papaya ring spot virus (PRSV-P). This virus affects production and productivity by decreasing photosynthetic capacity of plant, and subsequently leading to stunted growth, deformed and inedible fruitsand early mortality. PRSV is transmitted by several species of aphids in a non-persistent manner. Generally, aphids do not colonize papaya and transmission of PRSV is through transient aphid vectors. Aphis gossypii is the predominant vector followed by A. craccivora and Myzus persicae. Recent study suggested that M. persicae is more efficient than the other two species with 52.5 % transmission after the first inoculation access period (IAP) (Kalleswaraswamy and Krishnakumar, 2008).

Field tolerance towards PRSV varies between the Carica papaya varieties as well as the Vasconcellea species. Vasconcellea species viz., V. cundinamarcensis,V. candicans, V. stipulata, V. cauliflora andV. quercifolia are reported to be resistant to PRSV. Even though the genetic variability within the Carica genus for PRSV resistance is very low, a few varieties have shown tolerance to PRSV. This might be due to the non-preference of aphids to these varieties or species in addition to the innate resistance mechanism in Vasconcellea genepool. Morphological traits such as higher density of simple and glandular trichomes, epicuticular waxes and leaf thickness are reported to hinder the aphid attack in plants (Bin, 1979; Guerrieri and Digilo, 2008; Wojcicka, 2015). A preliminary study was carried out to explore the possibility of aphid tolerance in papaya varieties as well as Vasconcellea species.

Leaf thicknessat three months of transplanting ranged from 0.22 mm to 0.40 mm. The thickest leaf was observed in Pusa Nanha (0.40 mm) which was on par with V. cundinamarcensis (0.38 mm) and V. cauliflora (0.37 mm), followed by V. parviflora (0.35 mm). Among the accessions, thinnest leaves were noticed in TNAU papaya CO8, Arka Parbhath and IGH2 (0.22 mm) which was on par with IGH1 and Arka Surya (0.23 mm).

The accessions such as Arka Surya, Arka Prabhath, Red Lady, Pusa Dwarf, Pusa Nanha, TNAU Papaya CO8, IGH1, IGH2 and V. goudotiana lack leaf pubescence on both dorsal and ventral surfaces (Fig.1). However, the wild species viz., V. cauliflora, V. cundinamarcensis and V. goudotiana had leaf pubescence with higher trichome density on ventral surface than dorsal surface. Trichome density was highest in V. cundinamarcensis (192.75/cm2 ) followed by V. cauliflora (25.25/cm2) and V. goudotiana (14.88/cm2).

The type of trichome on the leaves were also observed under scanning electron microscope. V. cundinamarcensis consisted of single celled non- glandular trichomes, whereas V. cauliflora and V. goudotiana comprised of multicellular glandular trichomes (Fig.2). Trichomes were present as extension of veins in V. cauliflora and V. goudotiana, while these were distributed throughout the leaf surface in V. cundinamarcensis.

Studies suggested that trichome density has more impact on entry of aphids rather than the type of trichomes, as higher trichome density blocked aphids (Musetti and Neal, 1997). It is the first feature affecting the selection behaviour of an aphid. Most of the resistant varieties or wild relatives are characterized by presence of trichomes (Bin, 1979). However, the glandular trichomes might have produced toxic exudates or acyl sugars that repel aphids (Goffreda et al., 1989).

Table.1
Leaf thickness, leaf epicuticular wax content, trichome density, PRSV percentage infection, disease intensity score and PDI at field condition

Values inparentheses are arc sine transformed values

A correlation was drawn between the leaf parameters and disease scoring (Table.2). Epicuticular wax content in leaves was negatively and significantly correlated with percentage of infection. Epicuticular waxes are complex mixture of long chain aliphatic and cyclic components such as fatty acids, hydrocarbons, alcohols, aldehydes, ketones, esters, terpenoids, sterols, flavanoids and phenolic substances. Higher epicuticular wax content might be a reason for reduction in aphid landing or movement, which in turn could have contributed, to inhibition of the sap transmission of PRSV. Similar negative effects of leaf epicuticular waxes were reported on neonate larval movement of Spodoptera frugiperda on Zea mays (Ostrand et al., 2008), resistance in cabbage to aphids Bravicoryne brassicae, sorghum to green bug (Schizaphis graminum) and winter wheat to English grain aphid (Sitobion avenae) (Shepherd et al., 1999). The presence of thick wax content might have affected the probing and feeding by aphids, thereby rejecting the particular variety or species.

Leaf thickness was negatively correlated with PDI and infection percentage. Leaf thickness was positively contributed by the epicuticular wax content, which indirectly influences the disease tolerance or resistance. Thick cell wall has been attributed to resist the feeding activity of aphids (Guerrieri and Digilo, 2008).

The association analysis reveals that there is a significant negative correlation between trichome density and infection percentage. Surface resistance is the first barrier against aphid attack (Wang et al., 2004). Either or both of epicuticular wax content or presence of trichomes is known to hinder the aphid movement and stylet insertion (Bin, 1979).

Table.2
Correlation between disease incidence and leaf parameters

First value represents ‘r’ value and second value represents p value.

* <0.05 p value shows significant correlation

Higher field tolerance to PRSV was observed in ‘Pusa Nanha’, which had thicker leaves. The PRSV incidence was significantly low in both V. cauliflora and V. cundinamarcensis, which registered thicker leaves, higher epicuticular wax content and denser trichomes. The preliminary study broadly indicates that leaf thickness, presence of trichomes in higher density and epicuticular wax content in papaya is likely to play a definitive role towards reduction in PRSV incidence probably by restricting the aphid vector incidence.

Higher leaf thickness, epicuticular wax content and trichome density in papaya is found to have negative impact on the incidence of Papaya ring spot virus in papaya and these factors may have a role to play in restricting the virus transmission by aphid vector. Future research needs to be focussed on the biochemical constituents of glandular trichomes and its effect on aphids.

Fig. 1
Stereo microscope view of leaf ventral surface pubescence

Fig. 2
Scanning electron microscope view of leaf ventral surface pubescence at 500 µm

a) V. cauliflora (b) V. cundinamarcensis (c) V. goudotiana

Guidance and technical support rendered by Dr. M. Krishna Reddy, Dr.C.Vasugi, Ms. Jayanthi Mala, and Dr. Kalaivannan, ICAR-IIHR are gratefully acknowledged.