Postharvest Diseases of Indian Gooseberry and Their Management: A Review

ABSTRACT

This review describes different postharvest fungal diseases like blue mold, Anthracnose and fruit rot of Indian gooseberry along with its management strategies that covers physical, chemical and biological methods. The physical methods of management include osmo-drying, hot water treatment, UV-C treatment, application of high electric field current, efficient packaging in low and high density polythene pouches.Chemical methods involve treatment with different synthetic fungicides like Bavistin, Mancozeb, Gibberellic acid, Carbendazim, Calcium nitrate and Calcium sulphate. Lastly, the biological control methods have been mentioned, which includes application of microbial antagonists and naturally occurring antifungal compounds.

KEYWORDS:

• Anthracnose
• control strategies
• Emblica officinalis
• fruit rot
• fungal diseases

Introduction

Emblica officinalis Gaertn belongs to the family Euphorbiaceae, and it is known to be an important minor crop of India (Kumar and Sagar, 2009). It is also referred to as an underutilized crop (Scartezzini et al., 2006). However, underutilized crops often have the potential to contribute to the food security of the nation (Mayes et al., 2012). Emblica officinalis grows abundantly in the tropical and subtropical areas of India, China, Indonesia, Myanmar, Sri Lanka and the Malay Peninsula (Benthal, 1946; Liu et al., 2008; Macmillan, 1943; Perianayagam et al., 2005; Thakur et al., 1989). Indian gooseberry has also been reported to grow naturally in other parts of the world like Cuba, Puerto Rico, Iran, Iraq (Hooper and Field, 1937), Hawaii, Florida (Barrett, 1956; Sturrock, 1959), Java, West Indies and Trinidad (Webster, 1956). It is found to grow profusely in many northeastern states of India like Mizoram, Tripura, Assam particularly in the forests of Khasi and Garo hills of Meghalaya (Pandey et al., 1993). However, intensive cultivation is done in Uttar Pradesh, mainly in the districts of Pratapgarh, Azamgarh, Varanasi, and Jaunpur (Bajpai and Shukla, 2002). Cultivation of Indian gooseberry is also done in other states of India like Maharashtra, Gujarat, Rajasthan, Madhya Pradesh, Jharkhand Chhattisgarh, Bihar, West Bengal, Orissa, Andhra Pradesh, Karnataka, Haryana, and Himachal Pradesh (Chandra and Singh, 2015; Rawat and Uniyal, 2003).

Indian gooseberry can be grown in variable soil conditions-from sandy loam to clay. It grows well in arid and semi-arid regions. Farmers can particularly benefit by its cultivation because Indian gooseberry can thrive well in marginal lands as well. Indian gooseberry is known to possess a number of health benefits. It has been used frequently in the Ayurveda and Unani system of medicine (Pathak, 2003). It has very high Ascorbic acid, i.e., Vitamin C content, about 20 times higher than that of orange (Tarwadi and Agte, 2007). Juice of Indian gooseberry being highly acidic protects the vitamin C from degradation during heating or drying (Hassan et al., 2014). Ascorbic acid can act as an antioxidant by means of its free radical scavenging properties (Cort, 1982). However, in addition to ascorbic acid Indian gooseberry also contains polyphenols like ellagic acid, gallic acid, and hydrolysable tannins (Emblicanin A, Emblicanin B, punigluconin, pedunculagin) which have been reported to contribute to the antioxidant properties of the fruit (Bhattacharya et al., 1999; Ghosal et al., 1996). Ihantola-Vormisto et al. (1997) have demonstrated that Indian gooseberry has anti-inflammatory and antipyretic properties. Different types of extracts of fruits have been reported to show Hepatoprotective activity, like 50% hydroalcoholic extract (Tasduq et al., 2005), or even 5% aqueous extracts (Reddy et al., 2010). The anti-tumor properties of the extracts of Indian gooseberry can be attributed to the polyphenolic compounds principally tannins and flavonoids. Pyrogallol obtained from Indian gooseberry extracts, have an anti-proliferative effect on human lung cancer cell-lines (Yang et al., 2009); while gallic acid extracted from leaves of Indian gooseberry result in apoptosis of human hepatocellular carcinoma cells (Huang and Zhong, 2011). Extracts of E. officinalis fruits inhibit transcription factor AP1 as well as interfere with the expression of viral oncogenes that could lead to cervical cancer development and progression. Therefore, the fruit extracts could be a potential source for drug development against Human Papilloma Virus (HPV) induced cervical cancer (Mahata et al., 2013). Apart from these, fruits of Indian gooseberry have a wide range of other properties like hypolipidemic (Thakur and Mandal, 1984; Yokozawa et al., 2007), hypoglycaemic (Jamwal et al., 1959; Liu et al., 2012), and analgesic (Perinayagam et al., 2004) .

The different cultivars of Indian gooseberry, commercially cultivated in India are ‘Banarasi’, ‘Francis’, ‘Chakaiya’, ‘Kanchan (NA-4)’, ‘NA6ʹ and ‘NA7ʹ (Pathak, 2003; Scartezzini et al., 2006). In Pakistan, ‘Desi’, ‘Shisha’, and ‘Banarasi’ cultivars are available; while in China ‘Langen’, ‘Fen’gan’, ‘Liuyuebai’, ‘Bian’gan’, ‘Quibai’ and ‘Shan’gan’ cultivars are cultivated. Indian gooseberry can be processed into pickles, candy, Murabba (whole fruit preserve), juices, mouth fresheners, fruit leathers, etc. (Bhattacherjee et al., 2011; Daniel and Dudhade, 2010; Nath and Sharma, 1998), which have real economic importance. Fruits of Indian gooseberry form the base ingredient for Chyavanprash, an Ayurvedic preparation. Presently in India Chyavanprash is processed by some large companies and some small-scale producers as well; the total Chyavanprash industry in the country is worth Rs 200 crore. In fact, because of their sour and astringent taste, the fruits are consumed more in processed form than raw.

However, ripe fruits of Indian gooseberry have a low shelf-life of 5–6 days and are highly perishable (Pathak et al., 2009). The fruit is susceptible to number of postharvest fungal pathogens among them most prevalent are blue and black mold. Thom (1930) reported annual yield loss up to 50% due to fruit rot of Indian gooseberry caused by blue mold. The fungal diseases deteriorate the fruit quality and lower its marketability which affects the fruit production severely. Taking into consideration its enormous health benefits as well as economic importance, it is necessary that the post-harvest losses of Indian gooseberry be curtailed. This review focuses on the different postharvest diseases of Indian gooseberry and the management strategies adopted to tackle those diseases.

Postharvest Diseases of Indian Gooseberry

Numerous postharvest diseases caused by fungal pathogens have been reported in Indian gooseberry. Some of these diseases along with their respective causal organisms and symptoms have been presented in Figure 1 and Table 1.

Figure 1. Postharvest fungal diseases of Indian gooseberry: (I) Anthracnose by Colletotrichum gloeosporioides. (II) Fruit rot by Penicillium digitatum, (III) Soft rot by Phomopsis Phyllanthus. (IV) Fruit rot by Aspergillus niger.

Table 1. Fungal diseases of Indian gooseberry.

Name of the disease	Causal organism	Symptom	Reference
Blue mold	Penicillium islandicum	i. Water soaked areas are formed initially ii. Whitish mycelia emerges from the infection locus iii. Ultimately, the fruit becomes covered with bluish green pustules that give it a beaded appearance	Setty, 1959
Anthracnose	Colletotrichum gloeosporioides	Small, sunken, circular, dark brown lesions are produced on fruit surface.	Mishra and Shivpuri (1983)
Fruit rot	Penicillium oxalicum	Round, golden coloured colonies develop on the fruit surface.	Kulkarni and Sharma, 1971
	Penicillium digitatum	Entire fruit becomes covered with green moldy growth.	Akhund et al., 2010
	Phoma putaminum	Small eye-shaped pinkish brown lesions appear which ultimately coalesce to give the fruit a crinkled appearance.	Pandey et al., 1980; Jamaluddin et al., 1975
	Aspergillus niger	i. Initially, discoloration in the rind region followed by water soaked lesions ii. Finally, the fruit becomes covered with black, sooty mass of spores.	Srivastava et al., 1964
	Nigrospora sphaerica	i. Small dots appear initially which develop into larger black spot rings. ii. Several adjacent rings coalesce that result in complete rotting of the fruit	Kamthan et al., 1981
	Alternaria alternata	Brown necrotic lesions appear; fruits eventually become crinkled and rotted.	Pandey et al., 1984.
	Pestalotia cruenta	i. Brownish discoloration on the fruit. ii. Ultimately, the entire fruit becomes dark brown and mummified.	Tandon and Shrivastava (1964)
	Cladosporium tenuissimum C. cladosporioides	During the months of November to February when colorless circular patches develop on the fruit surface covered by light brown mycelia growth. From February onwards, dark brown necrotic lesions on the fruit surface	Jamaluddin, 1978
	Rhizopus stolonifer	i Water soaked areas appeared initially which were replaced by greyish mycelia ii. Ultimately entire fruit becomescovered with dark brown mycelium	Rathod (2010)
Soft rot	Phomopsis phyllanthi	i. Watery spots develop initially. ii. In the later stages, olive brown discoloration appears, with water soaked areas. iii. Finally the whole fruit becomes soft and pulpy.	Lal et al., 1982

Strategies for Postharvest Management

A report by the Indian Council of Agricultural Research (ICAR) – Central Institute of Post-Harvest Engineering and Technology (CIPHET) in Ludhiana (2015) showed that postharvest loss was maximum (4.58–15.88%) in fruits and vegetables among other crops. Therefore, effective strategies need to be introduced in order to reduce the losses incurred through the postharvest damage to agricultural produce. In the following section, the different methods for postharvest disease management of Indian gooseberry have been discussed.

Physical Methods

The fruits of E. officinalis are highly susceptible to microbial decay at the postharvest stage which can be effectively controlled by various physical methods. Dehydration is the oldest and a very low-cost technique to prolong the shelf life of fruits and vegetables (Doymaz, 2007). Microbes need enough moisture to grow and cause spoilage. Dehydration or drying is the method of removing moisture from fruits and vegetables which in turn prevents the microbial growth and enzyme activities, minimizing many moisture mediated deterioration reactions (Boyer and Huff, 2008; Krokida and Marinos-Kouris, 2003). Different drying techniques like osmo-air drying, direct sun drying, indirect solar drying, and oven drying are used in present times to preserve the fruit and prolong its shelf-life. Direct sun drying was more prevalent in earlier times, mainly because of the low operational costs. Nevertheless, this method had a number of disadvantages-quality of fruits dropped due to direct exposure to UV rays, contamination by dust and insects (Ertekin and Valdiz, 2004). Osmo-air drying has lately garnered more of attention because it allows minimum thermal degradation of nutrients in the products (Shi et al., 1997). It is essentially a two-step dehydration process. In the first stage, water is removed from the fruit by dipping in 40% sucrose solution for 12 h (Sagar and Kumar, 2010). In the second stage, the drained products are dried in a hot vacuum drier to the desired moisture level. Recently an LPG-based CRIDA drier has been developed in Hyderabad which successfully dehydrated blanched Indian gooseberry segments (Gudapaty et al., 2010). Dahiya and Dhawan (2003) have shown that osmo-air drying helps in better retention of nutrients like ascorbic acid and sugars of Indian gooseberry fruit than other conventional methods of drying (Banerjee and Ghosh, 2015). Apart from dehydration techniques, hot water treatments have also been employed in a number of cases to curb postharvest losses (Gramaje et al., 2009; Kim et al., 2009; Olesen et al., 2004). Dipping of Indian gooseberry fruits in hot water (60°C for 2min) protected the fruits from Aspergillus niger infection, causing 100% inhibition of the spore germination (Sharma and Srivastava, 2014). Application of high electric field (HEF) to Indian gooseberry fruits has shown promising results in terms of shelf-life extension; fruits treated with alternating current (AC) HEF showed a better degree of freshness, as compared to untreated fruits (Bajgai et al., 2006). Indian gooseberry fruits, when treated with UV-C light, showed resistance towards A. niger infection; UV-C could induce resistance in fruits against the pathogen, thereby extending its shelf-life (Sharma and Srivastava, 2014).

Fruits can be stored for an extended period of time in refrigerated condition (Kore et al., 2013). Appropriate packaging methods and storage can reduce the postharvest losses by up to 30% (Goyal et al., 2008). Packaging of Indian gooseberry fruits in low-density polyethylene pouches reported minimum fruit decay (Singh and Kumar, 1987) compared to other treatments like storage at room temperature or at evaporative cooling conditions (Singh and Kumar, 1987). Storage in corrugated fiber boxes with newspaper liners prolonged the shelf life of Indian gooseberry fruits to 11 days (Singh et al., 2009). HDPE gauge polythene proved to be another effective packing material for Indian gooseberry fruits, showing an increase in shelf-life to 15 days along with retention of total sugar and ascorbic acid content (Vishwakarma et al., 2012).

Chemical Methods

Application of pesticides and fungicides is the usual methods of protection of the crops against infectious diseases. Pre-harvest application of several fungicides has resulted in reduction of post-harvest decay as well as increase in shelf-life of several crops. Dipping of Indian gooseberry fruits with Carbendazim at 500 and 1000 ppm, respectively, showed maximum resistance against Penicillium funiculosum when compared to treatments with other synthetic fungicides like benomyl, metallic copper, Captan, Mancozeb, etc. (Yadav et al., 2012a). Fungicides are often combined as co-formulations because they are capable of improved disease control, and resistance management. Mixture of Calcium Chloride, Bavistin, and Bayleton, when applied to leaves, was found to enhance the shelf–life of Indian gooseberry (Gupta and Singh, 2016). Many organic and inorganic compounds also enhance nutrient content of fruits, increase their shelf life as well as antagonists against different phytopathogens. Treatment of Indian gooseberry fruits with 1% Calcium nitrate helped in reducing physiological weight loss, retention of total sugar and ascorbic acid content along with increasing the shelf–life (Gangwar et al., 2012; Nath et al., 1992). GA3 can work efficiently with Calcium nitrate, thereby resulting in minimum spoilage of Indian gooseberry fruits (Singh et al., 2014). Foliar spray of Zinc sulfate, Magnesium sulfate and Copper sulfate (0.5% each) resulted in a better quality of fruits with a simultaneous rise in fruit yield (Chandra and Singh, 2015).

Biological Methods

Biological methods involve primarily the introduction of microbial antagonists like different fungal and bacterial species in controlling several plant diseases. These antagonists have various modes of action that include antibiosis and/or competition for nutrients and space (Wisniewski and Wilson, 1992). Few reports of the application of microbial antagonists to prevent postharvest diseases in Indian gooseberry have come up lately. Pre-harvest treatment with Lactobacillus acidophilus showed a reduction in pathogenesis caused by P. funiculosum in Indian gooseberry fruits (Sharma and Sumbali, 2009). Again, Trichoderma harzianum and Pseudomonas fluorescens have been reported to reduce the disease severity caused by P. funiculosum in Indian gooseberry (Yadav et al., 2012b). An in vitro evaluation of microbial antagonists against the fruit rot complex of Indian gooseberry has also been reported, where P. fluorescens recorded the maximum growth inhibition against A. niger and P. funiculosum (Wakade et al., 2015). Numerous other postharvest pathogens of Indian gooseberry like P. digitatum, Rhizopus stolonifer, A. niger, Colletotrichum gloeosporioides have been reported to be controlled by microbial antagonists in many other crops. Penicillium digitatum was shown to be controlled by Bacillus pumilus, and Saccharomycopsis schoenii (Huang et al., 1992; Pimenta et al., 2008). Rhizopus rot on apple, peach, and tomato is effectively controlled by the application of T. harzianum (Batta, 2007; El-Katatny and Emam, 2012). Aspergillus niger infection in lemons is controlled by B. subtilis (Manjula et al., 2004). A combination of Brevundimonas diminuta, Stenotrophomonas maltophilia, a member of Enterobacteriaceae and Candida membranifaciens has been successful in reducing the anthracnose disease of mango caused by C. gloeosporioides. However, publications regarding the biological control of the aforesaid pathogens in Indian gooseberry are lacking. Nevertheless, the reports that were obtained from these above mentioned crops can provide scope for further research on the various microbial antagonists that will curb the postharvest diseases of Indian gooseberry.

Use of Botanicals for Disease Management

Application of 6% onion extract (aqueous) has been reported to be useful in enhancing the shelf-life of Indian gooseberry (Kumar et al., 2009). Edible oils like mustard oil and linseed oil were successful in reducing the Penicillium rot of Indian gooseberry fruit; while among medicinal oil, neem oil was most effective (Baghel et al., 2009). Reduction of P. funiculosum rot in Indian gooseberry was achieved by the application of aqueous extracts of garlic bulbs (Goswami and Sumbali, 2010). Application of Azadirachta indica extract was also reported to inhibit P. funiculosum growth in Indian gooseberry (Yadav et al., 2013). Aspergillus and blue mold fruit rots are effectively controlled by the application of Curcuma longa rhizome extract (5%), A. indica leaf extract (5%), and Carbendazim (0.1%) as pre- and post-inoculation treatments. In pre inoculation treatment fruits were first dipped in the treatment solution for about 7–8 min then inoculated while in post-inoculation treatment fruits were inoculated first and then treated with the treatment solution. In both the cases, the interval between inoculation and treatment or vice versa was 12 h (Jat et al., 2013).

Conclusion

There is a pressing need to introduce effective strategies to control post-harvest diseases which will pose minimum risk to human health and the environment as a whole. Biological control of pests is being introduced lately in agricultural practices in place of fungicides, because they are economically viable and environment friendly. The main aim of this review was to discuss the various post-harvest disease management strategies of Indian gooseberry that included physical, chemical and ultimately biological methods. Reports regarding the biological control of pathogen involving a microbial antagonist in Indian gooseberry are rather limited. Therefore, in the future, there is scope for research in this sector of biological control practices as well as for other novel strategies that might come up to combat post-harvest diseases.