Int.J.Curr.Microbiol.App.Sci (2019) 8(11): 388-396

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 8 Number 11 (2019) Journal homepage: http://www.ijcmas.com

Review Article https://doi.org/10.20546/ijcmas.2019.811.049

Eco-friendly Management of False Smut ( virens) of

Aman Kumar Gupta1*, Jiwan Paudel2, Dipak Yadav1, Devansh Kumar2, Ramu Yadav2 and Shrvan Kumar3

1IAS, Banaras Hindu University, Varanasi-221005, (U.P.), India 2Rajiv Gandhi South Campus, Banaras Hindu University, Barkachha, Mirzapur 231001, UP, India 3Department of Mycology and Plant Pathology, IAS, Banaras Hindu University, Varanasi-221 005, (U.P.), India

*Corresponding author

ABSTRACT

False smut of rice caused by , perfect sexual stage Villosiclava virens. Ustilaginoidea virens belongs Division – , Class – , Order – , Family – Incertaesedis. The yield losses due to RFS 1 -75% is K e yw or ds measured. The symptoms are visible only after flowering when the transforms into globose structures or yellowed carbonaceous masses of individual grains of panicle. These False smut of Rice, masses are dusty representing more than twice in diameter of normal grain. At early stage, Ustilaginoidea , development of fungus areshow yellow and then changed in dark green or almost black Integrated , Bio color, and explode releasing the of the fungal causal agent. The pathogen survives control agents, Chemical control both in seed and also in collateral host. The fungus by the means of sclerotia and chlamydospores overwinters in soil. Ascospores produce by sclerotiaare primary source of Article Info infection to rice plants, whereas air-borne chlamydospores may cause secondary infection. The seed should be treated through biological control agents like Trichoderma viride, Accepted: Trichoderma virens, Trichoderma harzianum and Trichoderma reesei against 04 October 2019 Ustilaginoidea virens find more effective to control diseases. Growing of resistant hybrids Available Online: 10 November 2019 variety like VNR-211, GK-5025, HRI-140, IRH-74, PRSH-9018, KPH-467, RH-10428, 27P64 and KRH-4. By spraying of Carbenadazim 50% WP (0.1 %) at the booting stage.

Treatment with Copper Oxy Chloride (Blitox) 50 WP (0.3%) and Propiconazole (tilt) 25

EC (0.1%) were found as the most effective to control false smut.

Introduction Nadu in India and later in many countries of world (Singh and Pophaly, 2010). False smut False smut or green smut is a common disease of rice caused by a fungal pathogen, of rice caused by Ustilaginoidea virens in rice Ustilaginoidea virens (Cooke) Takahashi, is a growing regions of India. Epidemics of false common grain disease of rice around the smut disease of rice were reported in Tamil world. The disease was first reported from

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Tinnevelli in Tamil Nadu, India by Cooke in quality and imposes health hazards 1878 (Ou, 1972). significantly in all rice producing areas. (Tanaka et al., 2008), Infection by the In recent years, it has emerged as the most pathogen transforms individual grains of devastating grain disease in the majority of infected panicles into initially orange, rice growing areas of the world. In India, the becoming yellowish green or greenish black at disease has been observed in severe form maturity (Ou, 1972; Lee and Gunnell, 1992). since 2001 in major rice growing states, viz., Haryana, Punjab, Uttar Pradesh, Uttaranchal, Economic importance Tamil Nadu, Karnataka, Andhra Pradesh, Bihar, Jharkhand, Gujarat, Maharashtra, Upadhyay and Singh (2013) reported that Jammu & Kashmir and Puducherry (Dodan yield loss due to RFS disease from many rice and Singh, 1996 and Mandhare et al., 2008). growing areas ranges from 1 to 75%. (Pannuet Antimitotic cyclic peptides, ustiloxin from its al., 2010) also reported losses up to 44 per chlamydospores are produced by pathogen on cent in Punjab. In Uttar Pradesh, yield losses infected grains, poisonous to both humans and up to 44 percent were observed by (Singh and animals (Nakamura et al., 1994; Koiso et al., Dube, 1978). In some rice growing districts of 1994). Ascospores produce by sclerotiaare Bihar, 15-50 percent losses occurs due to false primary source of infection to rice plants, smut of rice when comes as medium to severe whereas air-borne chlamydospores may cause form (Lahaet al., 2013). In Bangladesh 10- secondary infection (Ashizawa et al., 2010). 15% of annual production loss was due to The pathogen survives as dormant structures false smut disease (Latifet al., 2007). The such as sporeballs, chlamydospores, sclerotia disease causes both quantitative and etc. in soil, stubbles of the crop and also in qualitative losses. The losses in grain yield collateral hosts (Singh and Dube, 1976; occur due to chaffiness, reduction in test Yashoda and Anahosur (2000). The collateral weight and sterility of the spikelets hosts aid in the off-season active survival of neighbouring smut balls. The yield losses have the pathogen. The reported collateral hosts of been estimated to vary between 0.2 - 49% in U. virens include Oryza officinalis, Digitaria different states of the country. (URL-1). marginata, Panicum trypheron, Echinochloa crusgalli, Imperata cylindrical etc. (Rao and Host Range Reddy, 1955; Shetty and Shetty, 1985; Shetty and Shetty, 1987; Atia, 2004). There have The alternate host through which pathogen been many reports of severe outbreaks of RFS survivesare, barnyard grass (Echinochloa since 2001 in many rice-growing provinces of crusgalli), Imperata cylindrical, and common China, such as Liaoning, Hubei, Sichuan, and rice weed Digitaria marginata. (URL-1) Anhui; the yield loss ranged from 20 to 50% During infection, U. virens produces indifferent areas and varied with rice varieties. mycotoxins such as Ustilotoxins A and B In 2005, the occurrence area of RFS disease which contaminate rice seeds and straw, man was approximately 330,000 ha and a third of and livestock are also harmed by these the panicles in Sichuan were affected (Lu et mycotoxins(Shan et al., 2013). The fungus al., 2009). attacks some of the weed species that commonly occur in rice fields and may also RFS having causing significant yield losses serve as sources of inoculums (Atia, 2004). globally has become an important disease of The pathogen survives as dormant structures rice. The disease reduces yield, affects grain such as sporeballs, chlamydospores, sclerotia

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Int.J.Curr.Microbiol.App.Sci (2019) 8(11): 388-396 etc. in soil, stubbles of the crop and also in Symptom collateral hosts (Singh and Dube, 1976; Yashoda and Anahosur, 2000). Rice false smut disease is also known as green smut and considered as Lakshmi disease, Taxonomic Position because it was always found associated with bumper harvest. The false smut pathogen, U. virens, the causal agent of false smut, Ustilaginoidea virens, infects rice at the time belongs to the division Ascomycota, of panicle development and affects the young subdivision Pezizomycotina, and class ovary of the individual spikelet transforming it Sordariomycetes (Nguyen et al., 2012). into large, yellow to velvety green balls (smut Ustilaginoidea virens (Cooke) Takah., (1896) balls) and the symptoms produced are visible Synonyms Tilletiaoryzae Pat., (1887) from milky stage onwards. Initially, the smut Sphacelotheca virens Omori{?}, (1896) balls are small in size and remain confined Ustilagovirens Cooke, (1878) Ustilaginoidea between glumes. They gradually enlarge and oryzae (Pat.) Bref., (1895) (URL-4). enclose the floral parts. The individual grain get converted into yellowish smut ball then Morphology of Pathogen changes to yellowish orange to green, olive green and greenish black on maturity. In order to study the detailed cultural Powdery dark green spores are released when characteristics of the pathogen, 5 mm mycelial smut balls burst open (Biswas, 2001; Atia, discs were collected from ten days old culture 2004). of U. virens and inoculated at the center of PSA plates under aseptic cultural condition in If the infection occurs before fertilization most three replicates (27 ± 2°C temp). (Manu et al., of the glumes remain sterile without any 2017).The fungus produces ustilotoxin, a visible sign of infection. Typical large, phytotoxin and a mycotoxin thus velvety, green smut balls develop when contaminating rice products (Koiso et al., infection occurs after fertilization. The 1992 and Li et al., 1995). Smut balls are fructifications replacing the grains represent initially yellow in colour and are covered by a the conidial, pseudosclerotial and sclerotial membrane, later the membrane bursts and the stages of the pathogen. The pseudosclerotia colour changes to yellowish green and finally (green smut balls) consist of mycelial tissue greenish black (Gulzar et al., 2012). and masses, remnants of anthers and Chlamydospores formed in the masses of portions of palea and lemna. In general only spores are spherical to elliptical, warty, of few grains are affected in a panicle but the olive color, and 3 to 5 × 4 to 6 μm. Colonies number may rise up to 100 in case of severe on PDA developed in approximately 14–15 disease incidence (Ladhalakshmi et al., days.(Quintana et al., 2012). 10- 15 days after 2012).The symptoms are visible only after rice anthesis the balls begin to appear. Balls flowering when the fungus transforms the consist of white hyphae, at the beginning, individual grains of the panicle into globose which later forms thick yellow, loose outer structures or yellowed carbonaceous masses. layer of chlamydospores in summer and early These masses are dusty representing more autumn, and an olive to black, hard outer layer than twice the diameter of normal grain and at in late autumn. With higher and lower early development are yellow and then acquire temperature differences between day and dark green or almost black color, and explode night- especially in later autumn- sclerotia releasing the spores of the fungal causal agent often form on the colony surfaces (Zhang et (Quintana et al., 2012). The disease has been al., 2013). reported on the male inflorescence of Zea 390

Int.J.Curr.Microbiol.App.Sci (2019) 8(11): 388-396 mays and on wild species of Oryza (Mulder filament. Thus, this is regarded as the plant and Holliday, 1971). stamen-filament disease (Tang et al., 2013).

Diseases cycle Epidemiology

Fungus Ustilaginoidea virens insight the False smut (Ustilaginoidea virens) was disease. U. virens produces both sexual observed during Oct II and III week and that (sclerotia) and asexual (chlamydospores) coincided with average temperature 27.42o C, stages in its life cycle. Sclerotia are the major relative humidity of 83 per cent and rainfall of source of primary inoculum. In nature, over 12.1 mm (Vakiti et al., 2017). High relative wintered sclerotia germinate and produce humidity (>90%), temperature between 25 and ascospores and coincides with the anthesis of 30°C and rainy days at the time of flowering early sown rice crop. Ascospores feed on the are the favourable environmental factors for floral parts and initiate infection. Air-borne the disease infection, as mentioned by chlamydospores play an important role in the (Atia2004). Fungi can reproduce by selfing or secondary infection, which is a major part of outcrossing. In heterothallic ascomycetes such disease cycle (URL-1). Various disease as Tuber melanosporum Vittad (Rubini et al., incidents and severity significantly varies 2011). The maximum disease severity and between seasons and locations. Seed incidence were occurred at temperature range germination in smut-infected samples was of 32-24ºC, relative humidity (88-74%), 72.4% which is 21.45 per cent lower than the rainfall (6.67-6.66 mm) and sunshine hrs non - smutted samples (92.20%) (Gulzar and (6.20-6.29 hrs) both in case of variety Sanghera et al., 2012). Sabourardhajal and 25th June sown crop whereas, minimum disease incidence and During the surveys common graminaceous disease severity occurred when temperature grasses and sedges in the rice fields like and relative humidity was same but their Echinochloa colona, Echinochloa crussgalli, sunshine hrs and rainfall was lower than both Digitaria longifolia, Leersiahex andra, Sabourardhajal and 25th June sown crop in Fimbristylis milliaceae, Cyperus rotundus, case of Sahbhagi variety and 15th July sowing weedy rice etc. were observed for the presence (Priya et al., 2017). of false smut disease. Observations were made on any other modes of active survival as well. Integrated diseases management (Rashmi et al., 2016). Prediction or forecasting Proper management The fungus overwinters as sclerotia in the soil. strategies with non- chemical means are They germinate and produce spores that infect needed to be framed to control the disease. the grain. The disease first appears as a large More emphasis should be given for achieving gray to brownish green fruiting structure the resistance varieties and management of covered by a thin membrane that replaces one false smut needs. This review summarizes the or more grains of the mature panicle (URL-3). present status of the disease and progress in Ascospores produce by sclerotia are primary the field of its integrated management by source of infection to rice plants, whereas air- resistant varieties, exploration of resistance borne chlamydospores may cause secondary genes, chemical and non-chemical means of infection (Ashizawa et al., 2010). The RFS control including the use of bio-control agents pathogen grows and contaminates the infected (Sanjeet et al., 2018). Management of the plant tissues, including the stamen and disease has been achieved through cultural,

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Int.J.Curr.Microbiol.App.Sci (2019) 8(11): 388-396 biological and chemical control. (Pannuet al., seeds for sowing and cleaning of bunds may 2010; Mohiddin et al., 2012) reported the help the farmers to reduce the initial effectiveness of various fungicide against false occurrence of the disease. smut. According to farmers, inadequate management of these diseases resulted in poor In respect of cultivation practices, furrow production in crops (Nelson et al., 2001). The irrigated rice cultivation system recorded less strategic management of the disease may be disease severity compared to flooded fields directed to the specific areas of the fields (Sanjeet et al., 2018). The mechanism behind where there is a history of the disease through is the reduction on the survival period of manipulating genotypes and transplanting time chlamydospores in soil and occurrence of (Sarker et al., 2017). physiological changes in the host plant in response to shift of rice cultivation from Resistant cultivars anaerobic to aerobic growing conditions (Brooks et al., 2010). The management of the Research on rice false smut resistance rice seedling and adult plants were the same as screening and molecular mechanism of false the conventional method except for an extra smut resistance is not sufficient (Zhang et al., application of 75 kg/hm2 urea at the beginning 2014). Phenotyping of rice cultivars for false of rice booting stage (Zhang et al., 2014). smut is based on scoring system as per the Cultural practices like bunds and fields standard evaluation system (SES) scale of cleaning reduce the incidence as the disease IRRI (2002).(Singh and Singh 2005) evaluated has been reported on some of the weeds. and screened 27 rice genotypes resistant to false smut from 98-rice germplasm (Yan et Biological control al., 2014). Screened 186 rice hybrids to false smut resistance was done who identified few Biological control should done by hybrids with low disease incidence. Screening Trichoderma viride, Trichoderma virens, of 125 rice genotypes by artificial inoculation Trichoderma harzianum and Trichoderma of false smut (Kaur et al., 2015) identified reesei against Ustilaginoidea viren (Kannahi nine hybrids namely Hybrids VNR-211, GK- et al., 2016). Raji et al., (2016) studied plant 5025, HRI-140, IRH-74, PRSH-9018, KPH- extracts under in vitro against rice false smut 467, RH-10428, 27P64 and KRH-4 which pathogen which was considerably inhibited by shown complete resistance to rice false smut. bulb extract of garlic (Allium sativum), rhizome extract of turmeric (Curcuma longa), Cultural control leaf extracts of lantana (Lantana camara) and bael (Aeglemarmelos), whereas plant oils of Weeding and insecticides application were lemon grass (Cymbopogon flexuous) done at appropriate time for best management cinnamon (Cinnamomum zeylanicum), and practices (Priya et al., 2017). Early palmarosa (Cymbopogon martinii) have transplanted rice had higher disease incidence completely inhibited the growth of U. virens. when compared to late planting (Chhottaray, Bacillus subtilis (Liu et al., 2007) was found 1991; Dodan and Ram Singh, 1995). effective against the fungus.

Conservation tillage, continuous rice cropping Andargie et al., (2017) reported first time and moderate nitrogen fertility rates reduced Antennariella placitae effective against rice false smut disease in susceptible cultivars false smut (Ustilaginoidea virens) both in (Brooks et al., 2009). Use of sclerotic free vitro and in vivo condition.

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Chemical control 33(6): 120-125. Ashizawa T, Takahashi M, Moriwaki J, Hirayae (Liang et al., 2014) found the control K. Quantification of the rice false smut efficiency of 91.92 % by spraying 2.5 % pathogen U.virens from soil in Japan Wenquning, a solution of validamycin using real-time PCR. European J Plant suspension of Bacillus subtilis@ 4.5 Litre/ha Pathol. 2010; 128: 221-2. at 6 days before heading. Bagga and Kaur Atia MMM, Rice false smut (Ustilaginoidea (2006) evaluated and reported significant virens) in Egypt. Journal of Plant reduction in false smut incidence by spraying Disease and Protection. 2004; 111: 71- with Carbenadazim 50% WP (0.1 %) and 82. fujione 40 EC (0.1, 0.2 and 0.3%) at the Atia MMM. Rice false smut (Ustilaginoidea virens) in Egypt. Journal of plant disease booting stage. Treatment with Propiconazole protection. 2004; 14:71- 82. (tilt) 25 EC (0.1%) and Copper Oxy Chloride Atia, M MM. 2004.Rice false smut (Blitox) 50 WP (0.3%) were found as the most (Ustilaginoidea virens) in Egypt. J. Plant effective. Application of prochloraz + Dis. Protection. 111: 71-82. carbendazim followed by chlorothalonil was Atia, M. M. M. 2004. Rice false smut in Egypt. effective in controlling the false smut of rice J. Pl. Dis. Prot., 111:71-82. (Mohiddinet al., 2012) Spraying of Bagga PS, Kaur S. Evaluation of fungicides for chlorothalonil 75 WP (Kavach) @ 2 ml/l or controlling false smut (Ustilaginoidea Propiconazole 25 EC (Tilt or Result) during virens) of rice. J Indian Phytopath.2006; flowering reduce the disease incidence (URL- 59:115-117. 1). The fungicides evaluated exhibited 100% Biswas A. False smut disease of rice: a review. inhibition on the growth of U. virens eight Environment and Ecology. 2001; 19:67- days after inoculation in vitro in Nordox 83. (copper fungicide), Mancozan super Brooks SA, Anders MM, Yeater KM. Effect of (Mancozeb 640 g /kg + Metalaxyl 80 g/kg), cultural management practices on the Suncozeb (80% WP Mancozeb) and Sidalco severity of false smut and kernel smut of defender (435 g/l copper oxycholoride), rice. Plant Dis. 2009; 93:1202-1208. however, after 23 days only Nordox inhibited Brooks SA, Anders MM, Yeater KM. Effect of mycelium growth (Daniel et al., 2017). furrow irrigation on the severity of false (Researchers) reported that two sprays of 50% smut in susceptible rice varieties. Plant propiconazole EC at 300 g a.i. ha-1 and of 10% Dis. 2010; 94: 570-574. difenoconazole GR at 225 g a.i. ha-1, exhibited Chhottaray PK. Doctor of Philosophy Thesis, the best control of rice false smut. Treated Orissa University of Agriculture and Technology, Bhubaneswar, Orissa, seed with trifloxystrobin (Trilex 2000), and 1991, 175. propiconazole plus trifloxystrobin (Stratego) Cooke, M. C. 1878.Some extra-European fungi. were also effective in reducing false smut with Grevillea. 7: 13-15. foliar application at the heading stage (X Zhou Daniel Dokie Tokpah, Charles Kwoseh, Eric et al., 2012). Saye Tokpah and David Kolleh (2017). Rice false smut and its management in References major rice growing areas in Ashanti region of Ghana. Andargie M, Congyi Z, Yun Y, Li J.). Dodan DS, Ram Singh. Effect of planting tim on Identification and evaluation of potential the incidence of blast and false smut of bio control fungal endophytes against rice in Haryana. Indian Phytopathol. Ustilaginoidea virens on rice plants. 1995; 48:185-186. World J Micrbiol Biotechnol. 2017; Dodan, D. S. and Singh, S. R. 1996. False smuit 393

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How to cite this article:

Aman Kumar Gupta, Jiwan Paudel, Dipak Yadav, Devansh Kumar, Ramu Yadav and Shrvan Kumar. 2019. Eco-friendly Management of False Smut (Ustilaginoidea virens) of Rice. Int.J.Curr.Microbiol.App.Sci. 8(11): 388-396. doi: https://doi.org/10.20546/ijcmas.2019.811.049

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