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Advances in False Smut of Rice and its Integrated Diseases Management: A Review
First Online 08-09-2021|
History and distribution
False smut of rice caused by fungus U. virens with its perfect state as Villosiclava virens Tanaka also known as (Green smut and considered as Lakshmi disease) of rice was first reported from Tirunelveli district of state Tamil Nadu of India in 1878 by Cooke. Later U. virens was reported to cause false smut of rice in many countries including almost all rice growing regions of the world viz. Philippines, Myanmar, Colombia, Peru, Bangladesh, Mauritious, Nigeria, Myanmar, Srilanka, Fiji, Africa (Biswas, 2001). After the first report of occurrence of false smut in India from Tamil Nadu (Cooke, 1878), False smut outbreak has been reported from other states of India like Haryana, Punjab, Uttar Pradesh, Uttarakhand, Karnataka, Andhra Pradesh, Bihar, Jharkhand, Gujarat, Maharashtra, Jammu and Kashmir and Pondicherry (Dodan and Singh, 1996 and Mandhare et al., 2008).
The causal organism affects the rice plant at flowering stage resulting in the development of false smut balls (Fig 1). The symptoms of the disease have been described by number of workers from different regions of the world. Under suitable climatic conditions pathogen infects the rice plant at the time of panicle development and colonizes the internal part of rice flowers with mycelia (Tang et al., 2013). Young ovary of the single spikelet transformed into large velvety yellow to green color balls (Gupta et al., 2019). Dhua et al., (2015) reported that the smut balls formed not only block rice grain milking but also increases the sterility of spikelet and formation of balls resulting in poor yield. Quintana et al., (2016) reported that these smut balls represent more than twice the diameter of normal grain and at initial stage are yellow and then change to dark green or almost black colour. Initially occurs on few grains which later infects the whole panicle but the number may increase up to 100% in case of severe disease incidence (Ladhalakshmi et al., 2012). It was also reported that the causal organism produced large amount of mycotoxin such as Ustiloxins and Ustilaginoidins (Zhou et al., 2012). Several workers (Koyama et al., 1988 and Wang et al., 2017) reported that these toxins have phytotoxic effect and suppress shoot and root growth of germinating rice seeds. Lu et al., (2015) observed that Ustilaginoidins have antibacterial activity to plant and human pathogens.
The economic as well as nutritive loss due to this pathogen can be more serious than any other pathogen under congenial environmental conditions. False smut causes both qualitative and quantitative losses to the rice crop and also affects the germination vigor of the rice seedlings (Sanghera et al., 2012). The toxins produced by the pathogen are lethal to both human body and animals (Koiso et al., 1994). Pannu et al., (2010) recorded that false smut of rice causes a losses of up to 44% in Punjab. Upadhyay and Singh (2013) also recorded that yield losses due to pathogen in many areas ranges from 1 to 75%. Several workers reported that in India the percentage of infected tiller ranges from 5 to 85 per cent, which result in yield loss of 0.2 - 49 per cent depending of rice cultivar and disease severity (Dodan and Singh, 1996; Kumari and Kumar, 2015; Ladhalakshmi et al., 2012). Tokpah et al., (2017) in their study reported that RFS (Rice False Smut) disease induced infertility in infected spikelets, reduce rice grain weight and responsible for up to 75 per cent yield loss.
Cooke (1878) gave the first binomial name to the causative agent responsible for false smut of rice as Ustilago virens, but the taxonomic position of the pathogen has remained uncertain. Patouillard (1887) after studying the sample from Japan named it as Ustilaginoidea oryzae based on the imperfect stage and by characterization of conidial stage. Takahashi (1896) merged the pathogen name Ustilaginoidea oryzae and Ustilago virens based on their identical nature and named as Ustilaginoidea virens. Sakurai (1934) reported that false smut rice balls have sclerotia which are horse-shoe shaped, oblong or flat. Hashioka (1971) named Claviceps oryzae-sativa as the telemorphic stage of rice false smut pathogen. Bischoff et al., (2004) in a phylogenetic study of Ustilaginoidea reported that Ustilaginoidea is not showing affinity towards Claviceps. Tanaka et al., (2008) renamed the teleomorphic stage as Villosiclava virens. Presently U. virens has been placed in kingdom: Fungi, phylum: Ascomycota, class: Sordariomycetes, order: Hypocreales, family: Incertae sedis genus: Ustilaginoidea, Species: virens (Tanaka et al., 2008). The genus U. virens Cooke has been reported to be sporadic with in the rice crop causing smut balls on rice panicle by various workers (Nessa et al., 2015; Ashizawa et al., 2012). However, Baite and Sharma (2015) isolated the fungus from the infected spikelet of the rice plant on different cultural media such as potato dextrose agar (PDA), rice yeast dextrose agar (RYDA) and potato sucrose agar (PSA) but growth of fungus was obtained on PSA medium. Growth was creamy-white and colony attained a diameter of 40 mm after 30 days of incubation at 27°C and pH 6. Fungus growth texture was flat or raised with minor undulations and mycelium appeared fluffy, compact and leathery. The pathogen was found to be sensitive to light and the growth of colony reduced in the presence of light as compared to darkness. Ladhalakshmi et al., (2012) also reported that the growth of U. virens on PDA was slower and the fungus formed a tiny white colony after 7 days of inoculation. After 15 days the mycelium of the fungus changes from white to yellow chlamydospores, which were yellow initially, changes to olive green. The chlamydospores of the fungus are round to elliptical and size of 3-5 µm in diameter (Kim and Park, 2007). Ladhalakshmi et al., (2012) recorded that chlamydospores germinated by short germ tubes and produced conidiophores, which has large number of conidia at the apex. These conidia are small and ovoid in shape and responsible for fresh infection. Fan et al., (2016) reported that at low temperature false smut pathogen induced sclerotium formation. These sclerotia are black, horse shoe-shaped and irregular oblong as flat of 2 to 20 mm length. Yong et al., (2018) reported that sclerotia germinates under favourable environmental conditions and produces yellow mycelium that formed fruiting bodies. These fruiting bodies develop stromata full of perithecia in which large amount of ascospores are produced and these ascospores may act as primary source of infection. Fan et al., (2014) observed that both ascospores and chlamydospores of the fungus produced conidia. These conidia can also infect the roots and coleoptiles of rice seedling stage. It has been also reported that sclerotium and chlamydospore can survive for 10 months in the soil or crop debris (Wang, 1995). Therefore both act as primary source of inoculum for infecting new crop.
False smut of rice pathogen has wide host range. The pathogen survive as alternate host on barnyard grass (Echinochloa crusgalli), Cogan grass (Imperata cylindrical) and common rice weed (Digitaria marginata) (Shan et al., 2013). Shetty and Shetty (1987) also reported two common weeds of rice Panicum trypheron and Digitaria marginata which act as the alternative hosts of false smut of rice in India. In addition to rice crop U. virens has been found to be pathogenic on corn and other weeds displaying similar symptoms (Atai, 2004).
The fungus U. virens completes both sexual (Sclerotia) and asexual (Chlamydospore) stages of life cycle (Gupta et al., 2019). It has been reported that pathogen first infect coleoptiles and seedlings of the rice plant but these infection do not spread to the spikelets and does not show similar symptoms of the RFS (Zheng et al., 2009). During sexual life cycle, sclerotia are the main source of primary inoculum. These sclerotia after completing dormancy period of 2-5 months germinate (Wang, 1995), which after germination produces millions of ascospores. These ascospores produce conidia and hyphae of conidia which may infect panicle of rice plant at booting stage and spread over the surface of spikelets (Ashizawa et al., 2012). During asexual stage chlamydospore is responsible for secondary infection and germinates in soil and produces secondary conidia which results in secondary infection through wind and rain (Huang et al., 2019).
The pathogenesis and epidemiology of rice false smut is influenced by some important and critical aspects such as host plant, pathogen and its structure and environmental conditions. Weather plays an important role in determining the course and intensity of disease epidemic. Wang et al., (2005b) reported that the disease level will be high if temperature is in between 22°C-28°C, rainy and humid climate coinciding with rice booting stage. Atia (2004) also observed that high RH (>90%) with temperature between 25-30°C and rainy days at the time of flowering are congenial for RFS infection. Wang (1988) observed that high moisture with warm temperature of 26°C can break the dormancy of chlamydospores which inturn helps in germination. Saha (2019) reported in a predication model that when spore inoculum load over rice canopy increases by one unit can results in 0.981 unit increase in disease severity. Bhargava et al., (2018) found that maximum disease incidence and severity were recorded at temperature between 24-32°C, relative humidity 74-88%, rainfall 6.66-6.67 mm and sunshine hrs 6.20-6.29 in many varieties. Chaudhari et al., (2019) reported that maximum and average temperature, morning and average relative humidity, morning and average cloudy and sunshine hours were found to be responsible for disease severity.
Integrated disease management
The crop yield loss by false smut of rice can be minimized through adapting certain cultural practices, biological control, host resistance, nutrition, bio-pesticides and use of chemical fungicides.
Early sown crop has less disease incidence or severity than late sown crop. Sanne (1980) also reported that false smut can be avoided by early sowing. While some workers reported that disease incidence level will be high if crop is transplanted earlier (Dodan and Singh, 1996; Chhottaray, 1991). Several workers also found that if crop is transplanted closely and enormously irrigated, it can increase the incidence of RFS and also water-logging at late stage of rice crop will lead to high humidity and results in high occurrence of disease (Wang et al., 2010; Yang, 2007). Zhou et al., 2010 reported that the occurrence of RFS is more in the old disease areas due to the inoculum of previous year infected crop. Kumar et al., (2018) found that furrow irrigated rice cultivation system recorded low disease severity compared to flooded rice field. It is due to the reduction of the survival period of chlamydospores in soil.
Biological control is an eco-friendly tool to manage plant diseases and successfully used by many workers in their research studies. Kannahi et al., (2016) studied the disease control potential of 9 isolates of Trichoderma viride, Trichoderma virens, Trichoderma harzianum and Trichoderma reesei that were isolated from the rhizosphere of rice crop and found that all the isolates have antagonistic properties against the fungal pathogen. Liang et al., (2014) reported that if wenquning a combi-product of Bacillus subtilis (BS-916) and validamycin 2.5% is used against the causal organism, it may provide >90% reduction in disease with one spray at the late booting stage of rice crop. Andargie et al., (2017) in their in vitro and in vivo study found first time that plant extract potential in reducing the negative effect of Rice false smut. Raji et al., (2016) studied different plant extract such as bulb extract of garlic (Allium sativum), bael (Aeglemarmelos ), leaf extract of lantana (Lantana camara), extract of turmeric (Curcuma longa), Lemon grass (Cymbopogan flexuous), cinnamon (Cinnamomum zeylanicum) and palmarosa (Cymbopogan martini) under in vitro conditions against U. virens and found that these extract have completely inhibited the growth of pathogen.
Type of fertilizers, dosage and time of application have significant effect on incidence and severity of the rice false smut. Several workers observed that if nitrogen fertilizers applied late in the season, the incidence of RFS was high (Bhardwaj, 1990). Rani et al., (2015) reported that incidence of RFS infected panicles and number of balls/plant were increased with increase in the level of nitrogen and disease severity was maximum at 100 kg of nitrogen dosage in tested cultivar.
Host plant resisitance
Host plant resistance is the most effective, low-cost and environmental friendly mechanism for disease management. Singh and Singh (2005) evaluated 27 rice genotypes from 98 rice germplasn which are resistant to false smut pathogen. Kaur et al., (2015) identified nine varieties VNR-211, GK-5025, HRI-140, IRH-74, PRSH-9018, KPH-467, RH-10488, 27P64 and KR4-4 that are completely resistant to rice false smut disease. Chaudhari et al., (2019) evaluated eighteen varieties against the pathogen and found that seven viz. GNR-2, GNR-3, GNR-5, GNRH-1, Mahirajan, NAVR-1 and Dandi were found completely resistant to the pathogen.
Use of chemical can be effective method of disease control but it may not be economical and environmental friendly. Dodan and Singh (1997) found that copper oxychloride and copper hydroxide are highly effective in managing the disease. Application of propiconazole 25EC (0.1%) and copper oxychloride 50WP (0.3%) were found most effective (Bagga and Kaur, 2006). Combination of azoxystrobin and difenconazole spray was effective and reduced disease upto the 94% (Maniraju et al., 2017). Raji et al., (2016) found that propiconazole 25 EC (0.1%) treatment resulted in lowest disease severity than other fungicides followed by trifloxistrobin and tebuconazole 75 WG combination when applied at 50% panicle emergence. Barnwal et al., (2010) found that application of propiconazole and hexaconazole were effective in managing the disease.
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