Review Article

Brown Leaf Spot: An Exacerbated Embryonic Disease of Rice: A Review

Muhammad Imran1,2*, Shahbaz Talib Sahi1, Muhammad Atiq1 and Amer Rasul3

1Department of Plant Pathology, University of Agriculture, Faisalabad, Pakistan; 2Pest Warning and Quality Control of Pesticides, Punjab, Lahore, Pakistan; 3Department of Entomology, University of Agriculture, Faisalabad, Pakistan.

Received | September 26, 2020; Accepted | November 5, 2020; Published | November 21, 2020

*Correspondence | Muhammad Imran, Department of Plant Pathology, University of Agriculture, Faisalabad, Pakistan; Email: agripp.uaf.pk@gmail.com

Citation | Imran, M., Sahi, S.T., Atiq, M. and Rasul, A., 2020. Brown leaf spot: An exacerbated embryonic disease of rice: A review. Journal of Innovative Sciences, 6(2): 108-125.

DOI | http://dx.doi.org/10.17582/journal.jis/2020/6.2.108.125

Keywords | Bipolaris oryzae, Epidemic, Ecofriendly, Phytoextracts, Managemen

1. Introduction

Rice (Oryzae sativa L.) crop (family Poaceae) is known as staple food in world (FAO, 2004) and its production have a direct impact on the poor’s life (Seck et al., 2012). Its production is exaggerated with many factors (abiotic and biotic). Mostly biotic causing agents (pathogens) like fungus, nematodes, bacteria and virus are dominant in reducing the production in a qualitative and quantitative way by causing different diseases of rice crops in the world. (John and Fielding, 2014).

Diseases are reported to cause the losses of about $5 billion annually by destroying the rice crop (Asgher et al., 2007). Nearly seventy-four diseases have been reported in the world (Wubneh and Bayu, 2016) in which fifteen are present in Pakistan (Mustafa et al., 2013). Brown leaf spot (BLS) appeared as destructive diseases with diversified nature, has severed distribution and existence in different physiological races (Arshad et al., 2008). BLS disease has a great concern in the rice cultivated areas (Quintana et al., 2017). In 1900, Breda de Haan first reported the BLS pathogen as Helminthosporium oryzae Breda de Haan. Subramanian and Jain in 1966 reassigned the name as Drechslera oryzae (Breda de Haan. Subram, and Jain) belong to the genus Drechslera genus. While in 1959, Shoemaker proposed the named B. oryzae (Breda de Haan) Shoemaker, which is recently used now a days. Its perfect stage is Ophiobolus miyabeanus that was reported in 1927 by Ito and Kuribayashi. In 1934, it was reported that this pathogen belongs to Cochliobolus genus. Then Dasture transfer the pathogen into Cochliobolus in 1942 and now it is known as Cochliobolus miyabeanus (Ito and Kuribayashi) Drechsler ex Dastur. (Breda de Haan) Shoemaker (Palla, 2012). This disease caused 50-90% yield losses. In 1942, it became the source of Bengal Famine with death of two million people. This pathogen attacked on plants at seedling and mature stages, mostly reported in poor soil has fewer nutrients (Agarwal et al., 1989; Mia and Safeeulla, 1998; Zadoks, 2002). B. oryzea attacked on all parts of the rice plant and symptoms mainly appeared on coleoptile, leaf sheet, leaves, glumes and spikelet’s leading to 6-90% decrease rice yield (Webster and Gunnell, 1992; Padmanabhan, 1973; Estrada, 1984; Mew and Gonzales, 2002). Choudhury et al. (2019) reported its high incidence in district Sargodha and less in Okara (Pakistan). Maximum disease incidence has been reported on Basmati super variety (51.43%) and less on Basmati-38 (6.57%) Choudhury et al. (2019).

The pathogen mycelium enters through epidermal cells or stomata of the leaf. (Ou, 1985) after 18 hours, the entry regions are observed on leaves (Dallagnol et al., 2009). When fungal mycelium enters next to the invaded cell, brownish appearance occurred. (Tullis, 1935). These spots merged and bigger chlorotic lesions developed having a halo around them and rice leaf blades totally destroyed (Dallagnol et al., 2009). Pathogen after infection produced toxins that produced dead browning parenchyma cells (Tullis, 1935). Xiao et al. (1991) reported two main toxins named ophiobolin A and ophioboloin B from the conidia of pathogen and leaves, which causing chlorosis. These toxins cause the enhancement of electrolyte leakage in root cells (Tipton et al., 1977), electrical potential in transmembrane and permeability variation in plasma membrane due to Potassium and electrolyte leakage efflux (Cocucci et al., 1983). The infection of pathogen and production of lesions reduced the photosynthetic area of leaves leading to less tillering nodes (Lee, 1992), grains weight and numbers in panicles (Aluko, 1975). Pathogen infection also decrease green pigment in leaves which are involved in photosynthesis (Abdel-Fattha et al., 2007; Shabana et al., 2008). 

The infection occurred at seedling, leaf, culm and on the kernel, which causes huge loss of yield. The symptoms appeared as minute spots of brown to reddish brown, circular to oval, older spots are light reddish brown or grey center along dark to reddish-brown margins (Quintana et al., 2017). Similarly, Ou (1985) and Mew and Gonzales (2002) described symptoms of this disease in the form of small dark brown spots or purple-brown oval to a circular shape having a gray center. Mycelium grey to dark grey, having septation, solitary or in a group, straight or flexuous with conidia on the sides and ends. Conidia are curved, club or cylindrical shape, light to a golden brown and have 6-13 cell walls transversely. Dallagnol et al. (2009) reported the lesions in the form of light reddish color along dark or reddish brown margin on glumes and leaves.

Dasgupta and Chattopadhyay (1977) reported that two environmental factors like temperature and relative humidity have a significant role in disease development. High humidity more than 90% with a high temperature of 24-30 °C favors the development of this disease. Other factors like wind speed and rainfall also support the spread of inoculum from infected to healthy areas. If the condition becomes favorable, then severe losses occur and disease can prevail whole growth period. Pathogenic symptoms are present on the leaves in early-stage and observed on the panicles in a later stage (Liu et al., 2008). Long time exposure to saturated condition during pre and after inoculation decreases the disease development and don’t observe usual rainfall years (Singh et al., 2005). Whereas limited rains along with heavy dew favour the epidemic (Sherf et al., 1947). Similarly, Pannu et al. (2005) describe the disease severity of BLS observed lower in the years with heavy rains as compared to fewer rains. Generally during extended periods of leaf wetness support enhance the density of lesions in the canopy area of rice (Percich et al., 1997). More than 89% relative humidity and 25°C temperature along free water on surfaces of leaves are required by conidia to establish successfully. Dry, intermediate and less wet soil favors the increase in disease frequency (Ou, 1985). Similarly, higher disease severity and yield losses were observed by the researchers in water shortage and rained conditions (Kulkarni et al., 1979, 1981; Kauraw and Samantaray, 1982; Hegde et al., 1999).

Singh et al., 2005 observed that BLS disease did not occurred in those years that had continuous rainfall whereas Sherf et al. (1947) reported severe epidemic of disease in those seasons which have less rainfall and more dew conditions. Similarly, the seasonal condition was observed by Pannu in five years 2000-2004 and found high disease severity in the 2002 year where less rainfall occurred as compared to other years where the disease occurred in less severity of 8.8-9.2%. (Pannu et al., 2005). Similarly, the quantitative relationship of environmental variables and BLS disease is described by Choudhry et al., 2019 the maximum disease incidence is observed in the month of October ranging as 1.12-14.37% during 2014-2017. The relative humidity also has a strong relationship with disease incidence observed that year having more value.

The primary infection occurred through seed while secondary from the wind. Other inoculums sources are weeds, soil and infested debris. Conidial germination occurred at 25-30°C and hyphal growth at 27-30°C optimum temperature along high relative humidity over 90%. The disease wide spread occurred by continuous rain and cloudy weather with 25-30°C temperature along with leaf wetness of 8-24 (hours) (Percich et al., 1997). It becomes an epidemic where the soil has a poor nutritional profile and low pH (Carvalho et al., 2010).

Therefore, seeing the importance of this emerging disease, the present study is undertaken to explain the brief history of the disease in relation to its management with different suitable approaches which are in practice under the view of disease progress which not only assist to form a good management strategy but, also support the farmers for prediction of time frame for disease control. Management with different suitable approaches (Figure 1) which are in practice under the view of disease progress which not only assist to form a good management strategy but, also support the farmers for prediction of time frame for disease control.

 

1.2 Management strategies

1.2.1 Resistant source

The selection of resistant sources is the simple, reliable, operative and cost-effective method to control the diseases of rice. It helps to maximize the yield in a limited time (Katasntonis et al., 2007). Several studies are conducted on BLS disease to find out the resistance level. They are reported to be highly infected with BLS at seedling, booting and flowering stages (Chakrabarti, 2001). A native rice variety of Korean (Kutto-urupe) in 1930 are first reported to be more prone to disease as compared to others in the field under natural conditions (Nagai and Hara, 1930) that discussed the resistance level of different varieties against BLS. Then the resistant cultivar Mubo-Aikoku was found resistant to BLS in United States (Adair, 1941). Similarly, Yoshii and Matsumoto used another inoculation method of spray the plants on various life stages i.e. seedling, tillering, booting and flowering to demonstrated the disease levels on rice cultivars as found six moderately resistant (MR) and two cultivars (Tetep and Ginnen) resistant (R) (Yoshii and Matsumoto, 1951). Balal found two cultivars (Pi1 and YNA282) resistant in Egypt (Balal et al., 1979). This disease also related to soil fertility (Barnwal et al., 2013: Ou, 1985). The effect of the nutrient also subjected to soil structure as severe disease reported on the soil having the deficiency of K (Ono, 1953), in sandy loam and peat soil (Ohata, 1989). Another study resistant variety were observed over 11 years in soil having different conditions i.e. peat soil, sandy loam, K deficient field and found two cultivars and twenty breeding lines resistant against BLS (Yasumasa et al., 1962). Similarly, this disease was severely found in the soil having a deficient level of Silicone (Datnoff et al., 1997), and recently BLS resistance was determined through Silicone transporter mutant (Dallagnol et al., 2014).

Deren evaluated different cultivars and lines in the soil which have low Si and found two resistant cultivars (Deren et al., 1994). Eighty rice cultivars in 1974 were screened and found eight cultivars resistant to BLS (Ohata, 1989). The cultivars (Choukakou, Tadukan, Ginnen, Tetep,) were found resistant (Ohata, 1989). Similarly, Tetep cultivar was found in United States (Eruotor, 1986). Mostly BLS was reported until the 20th century in Japan but later it severely appeared in South Asia (Chakrabarti, 2001). The rice line-139 found resistant in Bangladesh (Hossain et al., 2004) and twenty cultivars among one eighty-three were found partial resistance to BLS in India in a separate study (Misra, 1985; Shukla et al., 1995; Satija et al., 2005). Pannu et al. (2006) found three susceptible cultivars under field conditions while 4 accessions found resistant of wild rice to BLS (Goel et al., 2006). Aryal et al. (2016) screened out the different varieties and found Radha-4 Rice variety as a resistant source which is used in a breeding program and found maximum disease severity on Poonam variety as 51.47% against brown leaf spot of rice. He explained that it is a quick and alternative way to manage the disease and enhance production. Fourteen rice varieties evaluated by Magar, 2013 against BLS and did not found any resistant variety. Hj-g1 was found high yielding and tolerant variety as compared to others. Alam et al. (2016) also explained the importance of screening of resistant varieties which provides information to the farmer to increase their yield and economy. He evaluated twenty-five varieties against BLS. He selected four highly resistant varieties out of these varieties against this disease. Seven were found resistant and six were moderately resistant. Three were moderately susceptible, two susceptible and three were to be highly susceptible against BLS. While Magar, 2015 found no rice variety resistant against disease among the screened out 14 varieties with disease severity range 21.73-58.07%. Two varieties (HJ-G1 and HJ-G2) observed moderately resistant. The HJ-G1 was observed highly yielding 5.10 ton per hectare along with minimum disease severity 21.73%. Bisen et al. (2015) evaluated twelve rice varieties against this disease on the base of total phenolic content and protein. He reported different levels of disease incidence on these varieties ranging from 5 to 38% at different growth stages. 

Those varieties having a high level of phenolic and protein content are highly resistant cultivars and had low disease incidence. Irron M2 205 was reported to be highly resistant cultivars having maximum protein and phenolic contents. Yaqoob et al. (2011) screened 31 rice cultivars against BLS under the field of low water application in NARC, Islamabad. Four lines i.e. IR84677-34-1-B, HHZB, HHZ11-Y6-Y1-Y1 and IR80416-B-32-3 were reported high resistant. The lines which were late and early sowing had disease response and medium type lines were highly resistant against BLS. Channakeshava and Pankaja (2018) determined the disease severity after 30, 60, 90 days on 51 rice varieties. The severity was more on the mature crop as compared to early crops. No disease severity observed after thirty days while after sixty days’ disease severity was found up to 13.55% and up to 21.20% after 90 days. The moderately resistant actions observed on thirty-one genotypes and eleven were found resistant. Mwendol et al. (2017) evaluated a hundred lines of rice at NaCRRI (National Crops Resources Research Institute) Namulonge, Uganda against this disease and found three lines susceptible, eighteen were highly resistant, fifty-two resistant, twenty-seven moderately resistant (Table 1).

1.2.2 Management through fungicides

Due to changing the environmental conditions and appearance of the disease epidemic, the use of fungicides judiciously is a significant method for quick and efficient control of diseases and improving the yield of rice. These fungicides manage the diseases as well as increase the production of rice. Different researchers used different fungicides and reported their efficacy against this disease. Such as application of Switch DF 80WG fungicide reduced the disease incidence up to 10% (Qudsia et al., 2017). Likewise, Kumar et al., 2017 evaluated four different fungicides i.e. Carbendazim 50WP, Carboxin 50 WP, Propiconazole 25 EC and Hexaconazole 25EC. Propiconazole was reported effective fungicides at 500ppm concentration that inhibited the fungus growth of 96.58% in the lab. Seed treatment by carbendazim @ 2g/kg along with the foliar application of Propiconazole @1ml/L under field condition reduces the disease severity significantly 37.26% and increases the yield 55.49%. Sandeep (2015) reported that the use of fungicides is effective for the control of BLS. All the used fungicides controlled the fungus growth significantly in vitro experiment as compared to the control condition. Bavistin was the best fungicides among other @1500ppm to inhibit the growth of fungus after the incubation period of 144 hrs. Sunder et al. (2005) used seven different fungicides in a laboratory experiment for efficacy against fungus growth and found two fungicides such as Hexaconazole and propiconazole most prominent in result following by iprobenphos and edifenphos. Similarly, infield, these two also have a good result as reduction of disease leaf spot 86.2 and 78.7% and stalk rot 71.5 and 63.5% and enhance the production of

 

Table 1: List of resistant germplasm source.

Sr. No.	Rice varieties evaluated	Finding	Reference
1	Korean (Kutto-urupe)	More prone to disease	Nagai and Hara, 1930
2	Mubo-aikoku	Resistant cultivar	Adair, 1941
3	Tetep and ginnen	High resistant cultivar	Yoshii and Matsumoto, 1951
4	cultivars Pi1 and YNA282	Resistant cultivar	Balal et al., 1979
5	Eighty rice cultivars	Eight cultivars resistant	Ohata and Kubo, 1974
6	Tadukan, tetep, choukakou and ginnen	Resistant cultivar	Yoshii and Matsumoto, 1951
7	Tetep	Resistant cultivar	Eruotor, 1986
8	Line-139	Resistant cultivar	Hossain et al., 2004
9	One eighty-three	Twenty cultivars partial resistance Misra 1985
10	One eighty-three	Twenty cultivars partial resistance Misra 1986	Shukla et al., 1995
11	One eighty-three	Twenty cultivars partial resistance Misra 1987	Satija et al., 2005
12	150 accessions	4 accessions resistant	Goel et al., 2006
13	Radha-4	Resistant cultivar	Aryal et al., 2016
14	Poonam variety	More susceptible	Aryal et al., 2016
15	Fourteen rice varieties	No resistant variety,	Magar, 2013
16	Twenty-five varieties	Four highly resistant	Alam et al., 2016
17	14 varieties	No resistant variety, HJ-G1, HJ-G2 were found moderately resistant	Magar, 2015
18	Twelve rice varieties	Irron M2 205 highly resistant	Bisen et al., 2015
19	Thirty-one rice cultivars	Lines i.e. HHZB, IR80416-B-32-3, IR84677-34-1-B and HHZ11-Y6-Y1-Y1high resistant	Yaqoob et al., 2011
20	51 rice varieties	Eleven were found resistant	Channakeshava and Pankaja, 2018
21	Hundred lines of rice	Eighteen were highly resistant	Mwendol et al., 2017

 

14.6 and 14.2% in grain yield, respectively, followed by mancozeb and edifenphos and in 2010, Sunder et al., 2010 used six fungicides against this disease. Among these, two (Propiconazole (1 ml per l): Hexaconazole (2 ml per l) appeared efficient to reduce severity from 22.34% to 5.19 and 7.98%, respectively and increased the grain yield significantly. While Gupta et al. (2013) described the efficacy of seven different fungicides at five different concentrations to control the BLS disease. Propiconazole @250 ppm approved to be the best among others in controlling the fungus growth by about 97% in the lab. Infield conditions, Basmati-370, Jaya and PC-19 were tested against these fungicides at 0.1% concentration. Among seven, Propiconazole was effective to decrease the disease severity 69, 73 and 70 and enhanced the production i.e. 19, 12, 21% as compared to control respectively.

Iqbal et al. (2015) evaluated the different fungicides (Mencozeb @1250 g/hec, Propineb @ 1250 g/hec, Chlorothelonil +Metalyxal @ 750 g/hec, Difenaconazol @ 313 ml/hec and Copper hydro-oxide @ 1250 g/hec) against BLS. Copper hydroxides significantly decrease disease intensity and improved rice production as compared to others. Mustafa et al. (2013) also determined the efficacy of different new fungicides against BLS disease by sowing the susceptible variety Super basmati is filed. After the severe disease prevalence, I applied the fungicides. He reported that the score (250EC) @308.2mlha-1 proved to be the most effective treatment in controlling the BLS. Asghar et al. (2007) performed the experiments to control the BLS by using the fungicides along with macronutrients NPK in Adaptive Research Farm, Gujranwala, Pakistan. Super Basmati variety was sown under three replications in field conditions. The fungicide difenoconazole along with NPK at rate 315 ml/ha + 500g/ha controls the disease incidence significantly 9.31% and increases yield (3.57 tha-1). Chemical efficacy of Carbendazim 12% + Mancozeb 63% (SAAF), Propiconazole 25 EC (Tilt) and Carbendazim 50% W.P (Bavistin) at different concentration i.e. 1.5, 2 and 2.5 g is determined by Shrestha et al., 2017 on Sabha Mansuli rice cultivars. Propiconazole at 2 ml/lit water have considerably less AUDPC value 373.7 then at Carbendazim + Mancozeb2 gm/lit have 374.9 value and Carbendazimhigh as 2gm/lit (590.1). By application of chemicals SAAF® at 2gm/lit (5.220 t/h), Tilt® at 2ml/lit water (5.210t/ha) and Bavistin® at 1.5gm/lit (3.320t/ha) yield obtained respectively. Jatoi et al. (2016) evaluated four fungicides in vitro and found Mencozeb and Thiomal reducing the fungus growth completely at 150 and 200 ppm (00. mm) as related to control treatment (36.62 mm) respectively. The fungicide bavistin was observed moderately effective (10.50 mm) and Melody due was found less effective (12.87 mm) as compared to control (36.62 mm). Thind et al. (2004) found the excellent inhibitory effect of azoxystrobin, trifloxystrobin and kresoxim-methyl, Pereira et al. (2002) used iprodione to control the mycelial growth of B. oryzae.

1.2.3 Management through phytoextract

The use of plant extracts against plant pathogen causing diseases is considered to be safe, ecofriendly, cost-effective economically and biodegradable. These are secure plant products in their uses to manage plant diseases (Mariappan, 1995). Botanicals are reported by the different pathologists for the control of plant pathogens. 10% Azadirachta indica has significantly controlled the disease (Kumar, 2018). Similarly, neem extract and Nerium oleander are reported to be effective against B. oryzae reducing disease incidence 66 % and 52% (Harish., 2008). These extracts have been reported to be efficient in reducing the spore germination and development of mycelium of fungus (Fiori et al., 2000). Similarly, Al-Mughrabi (2003) has been describing the efficient efficacy of the extract of Euphorbia macroclada to control many fungus species. Likewise, Kumar and Simon (2016) found Azadirachta indica best out of the different treatment of plants extracts against this disease. Jatoi et al. (2015) used five plant extracts i.e Azadirachta indica (Neem), Calotropi sprocera (Akk), Allium sativum (Garlic), Datura stramonium (Datura) and Zingiber officinale (ginger) with three concentrations of (5, 10 and 15ml) against B. oryzae under CRD design. Three replication of each treatment was used through poisoned food techniques. Ginger and garlic were proved to be most effective by using the dose of 2.75mm for inhibiting the fungus colony growth as compared to other like Dhatura, neem and Akk at a dose of 4.62, 20.00, 13.37 mm respectively as comparing control (38.12mm). The use of phytoextracts against BLS attempted by (Nguefack et al., 2005, 2007, 2008; Harish et al., 2008; Khoa et al., 2011). Nguefack et al., 2008 treated the seed by using oil extract of plants (Thymus vulgaris, Cymbopogon citratus, Ocimum gratissimum) against fungus in rice. Similarly, Harish et al. (2008) sprayed extract of neem and Neriumoleander twice in vivo and found 70% and 53% reduced the severity of BLS respectively and enhance the production 23 %, 18 % respectively. Similarly, Khoa et al. (2011) used Chromolaena odorata aqueous extract and reduced growth of B. oryzae up to 57 % under semi-controlled conditions.

Nguefack et al. (2007) applied the extract of ethanol and essential oil of Callistemon citrinus and Ocimum gratissimum for seed treatment and compared with fungicides carbendazim plus chlorothalonil (100 mg/ml + 550 mg/ml) in field and lab conditions. He found 42-100% decreased disease incidence. In the field, seed treatment with essential oil of Callistemon citrinus increased three rice varieties emergence and Farm production than using carbendazim plus chlorothalonil.

Nguefack et al. (2013) observed the effects of Callistemon citrinus L. and Cymbopogon citratus (DC) on B. oryzae radial growth. The use of extract C. citrinus 4520μg per ml and C. citratus 452μg per ml reduced the fungus growth completely and treatment of seed in a lab conditions by using of C. Citrinus decreased the incidence of fungi 85-100%. Also, the germination of the rice plants enhanced 10.06%. The use of extract of C. citrinus for seed treatment in combined spray with ethanol (2%) and extracts of C. citrinus (2% w/v) improved emergence, tillering and yield by 25-55%. 

Jyotsna et al. (2017) evaluated the leaves extract (aqueous) of different medicinal plants at the concentration of 0.20% and 0.50% in vitro against Pyricularia oryzae and Helminthosporium oryzae causes diseases in rice to inhibit the mycelium growth of both fungus and found maximum inhibition at 0.50%. Devi and Chhetry (2013) used different plant extracts at 5, 10, 15, 20% in vitro and vivo condition against BLS disease. The 80% mycelium growth inhibition at 20% conc. of an extract of Acorus calamus found as compared to others. Infield trial, 45.29% disease incidence was observed with aqueous extract of Acorus calamus. Sunder et al. (2010) evaluated ten plant extracts against BLS and found Neemazal (3ml/l) and Wanis (5ml/l) best as compare to other at leaf spot phase as (which decreased disease about 26% and others like Neemgold, Achook, Tricure, Thuja leaves and garlic cloves decreased stalk rot intensity about 16-19%. B. oryzae growth inhibitory effects were observed by using Artabotrys hexapetalus leaf extracts (Grainge and Alvarez, 1987) and garlic extract, peppermint and piper nigrum (Alice and Rao, 1987). About 64% decreased mycelial growth of this fungus was obtained by Juglans regia (Bisht and Khulbe, 1995), 80% by aqueous extracts of Acorus calamus and 45.3% decreased incidence of BLS (Jitendiya-Devi and Chhetry, 2013). Ganesan and Krishnaraju (1995) reported Spermacoce articularis, Leucas aspera and Polygonum chinense extracts out of twenty-three plant species showed inhibition of spore germination. Likewise, the germination of conidia was inhibited by the extracts of Ichnocarpus frutescens, Leea species, Anacardium occidentale, Macaranga peltata, Bixa orellana,

 

Table 2: List of of phytoextract for the control of BLS disease.

Sr. No.	Plants used	Finding	Reference
1	Azadirachta indica	Reduced the fungus growth	Kumar, 2018
2	Neem extract and Nerium oleander	Reducing disease incidence 66 % and 52%	Harish., 2008
3	Euphorbia macroclada	Reduced the fungus growth	Al-Mughrabi, 2003
4	Azadirachta indica	Best	Kumar and Simon, 2016
5	Five plant extracts i.e Azadirachta indica (Neem), Calotropi sprocera (Akk), Allium sativum (Garlic), Datura stramonium (Datura) and Zingiber officinale (ginger	Ginger and garlic were proved best	Jatoi et al., 2015
6	Thymus vulgaris, Cymbopogon citratus, Ocimum gratissimum)	Seed treatment	Nguefack et al., 2008
7	neem (cake) extract and leaf extract of Nerium oleander	70% and 53% reduced the severity	Harish et al., 2008
8	Chromolaena odorata aqueous extract	Reduced (Bipolaris oryzae) up to 57 %	Khoa et al., 2011
9	Extract of ethanol and essential oil of Callistemon citrinus and Ocimum gratissimum	Seed treatment	Nguefack et al., 2007
10	Extracts of Callistemon citrinus L. and Cymbopogon citratus (DC)	Reduced the fungus growth completely	Nguefack et al., 2013
11	10 plnats extracts	Found maximum inhibition at 0.50%	Jyotsna et al., 2017
12	different plant extracts at 5,10,15,20%	80% mycelium growth inhibition at 20% conc. of extract of Acorus calamus found	Devi and Chhetry, 2013
13	Ten plant extracts	(Neemazal “3 ml/l) and (Wanis “5 ml/l) best	Sunder et al., 2010
14	Artabotrys hexapetalus leaf extracts	Best	Grainge and Alvarez, 1987
15	Garlic extract, peppermint and Piper nigrum	Best	Alice and Rao, 1987
16	Juglans regia	64% decreased mycelial growth	Bisht and Khulbe, 1995
17	Extracts of Acorus calamus	80%	Jitendiya-Devi and Chhetry, 2013
18	Twenty three plant	Spermacoce articularis, Leucas aspera and Polygonum chinense extracts best	Ganesan and Krishnaraju,1995
19	Exracts of Ichnocarpus frutescens, Leea species, Anacardium occidentale, Macaranga peltata, Bixa orellana, and Uvaria navum	Germination of conidia was inhibited	Ganesan and Krishnaraju,1995
20	Six plant extracts	Inhibited the germ tube elongation	Ganesan, 1994
21	Agave Americana	Inhibited the germ tube elongation	Kumar, 2006
22	Extract of A. sativum and Pithecellobium dulce	50 to 90% inhibition of spore germination	Raju et al., 2004
23	Seven plant extracts	Thuja orientalis more effected for decreasing the BLS	Krishnamurthy et al., 2001
24	Prosopis juliflora	Best	Raghavendra et al., 2002
25	A. indica extracts	Reduced the fungus growth	Amadioha, 2002

 

and Uvaria navum extracts completely. Ganesan (1994) reported that germ tube elongation was inhibited with extracts of Gliricidia sepium, Cleome aspera, Delonix regia, Zornia gibbosa, Quisqualis indica and Hibscus surattensis. Agave americana at 0.1% inhibited the germ tube elongation (Kumar, 2006). The use of 10% extract of A. sativum and Pithecellobium dulce gave 50 to 90% reduction of spore germination and mycelial growth of B. oryzae respectively (Raju et al., 2004). The plant extract of Thuja orientalis is reported to be more effective for decreasing the BLS disease incidence as compared to other plant extracts i.e. Tridax procumbens, Ruta graviolens A. indica, Clerodendron inermae, Catharanthus roseus, Colens aromaticus and L. aspera (Krishnamurthy et al., 2001). Prosopis juliflora extract also inhibited the mycelium fungus growth completely at 800 ppm (Raghavendra et al., 2002). A. indica extracts also reported to control of BLS in the field along with radial growth of C. miyabeanus in culture (Amadioha, 2002) (Table 2).

1.2.4 Management through plant activators

Plant activators have a significant role in reducing the disease like Benzoic acid applied at 20mM decrease the disease incidence and severity (Shabana et al., 2008). Hydroquinone, salicylic acid, and benzoic acid are used to enhance the resistance in plants against fungal disease (B. oryzae). Benzoic acid was best among others in both in vivo and in vitro conditions (Abbas at el., 2006). Similarly, sodium benzoate effectively controlled the growth of Geotrichum candidum and Candida albicans (Wen et al., 2016). Salicylic acid reduced the infection process of Rhizoctonia fungi and delayed symptoms on potato tubers (Hadi and Balali, 2010). Hydroquinone is also proved to be a relatively safe antioxidant to manage seed-borne fungi (Eakil and Metwally, 2000). Similarly, plant activators like salicylic acid, Shikimic acid, and jasmonic acid have a key role in the defense mechanism of plants resulting in increased plant development (Agrios, 1997). These chemical mobiles in the plant systems and activate the defense genes (Nino-Liu et al., 2006). Salicylic acid induced the PAL production having resistance response and jasmonic acid increase the host plant growth (Wen et al., 2005).

1.2.5 Management through biocontrol agents

The use of biocontrol microbes against plant pathogens are eco-friendly, cost-effective, safe to health (Law et al., 2017) and used preferably against diseases. Biocontrol by using bacteria and fungi against plant diseases have been taken preference. The main groups commonly used as an antagonist are Pseudomonas, Bacillus, and Trichoderma against many plant diseases (Nakkeeran et al., 2005; Saravanakumar et al., 2007). Tamreihao et al., 2016 has been reported about the significance of Streptomuces corchorusii strain UCR3-16 in controlling the diseases of rice and the development of plant growth and yield. Trichoderma harzianum is reported to be effective in controlling the plant diseases (Abdul-Fattah et al., 2007). Trichoderma viride has a significance role in reducing the spore germination 77.03% and mycelium growth 62.92%. Moura et al. (2014) evaluated the potential of biocontrol agents as a seed treatment to control the pathogen transmission in seedling through using the bacteria (Pseudomonas synxantha DFs185), (P. fluorescens DFs223), (unidentified DFs306) and (Bacillus sp. DFs418.) and noted that the isolate DFs223 approved to be better to decrease the incidence of B. oryzae. Manimegalai et al. (2011) determined the antagonist effects of Aspergillus terreus A. sulphureus, A. niger, A. flavus A. fumigates, Penicillium janthinellum, P. chrysogenum, Trichoderma harzianum and T. viride against B. oryzae and found the inhibitory effects to control the pathogen (Manimegalai et al., 2011). Nejad et al. (2014) evaluated 20 tested actinomycetes isolates and found that Streptomyces isolate G showed the highest inhibitory activity against B. oryzae. Tamreihaoa et al., 2016 isolated the UCR3-16 strain of Streptomyces corchorusii from the rhizosphere of rice plants and reported its antifungal effect against six fungal pathogens of rice crop including B. oryzae. The strain found best to produce cell wall degrading enzymes like protease, chitinase, β-1,3-glucanase, lipase and β-1, 4-glucanase. Similarly, Streptomyces philanthi produced VOCs that repressed the mycelial development of B. oryzae and other rice crop pathogens (Boukaew et al., 2013). The chitinase enzyme produced by the Streptomyces vinaceusdrappus inhibited mycelial growth of B. oryzae and other rice fungal pathogens (Ningthoujam et al., 2009).

Isolates of biocontrol agent fluorescent Pseudomonas obtained from the rhizosphere inhibited the B. oryzae growth and reduced the incidence of brown leaf spot disease (Ray et al., 1990). P. fluorescens in the form of talcum also proved effective in decreasing the BLS disease by spray application (Joshi et al., 2007). In the field experiments, Bacillus megaterium reduced the BLS disease severity (Islam and Nandi, 1985). T. viride and B. subtilis also had antagonistic effects against this fungus. (Sarala et al., 2004: Kumar and Mishra, 1994). Similarly, T. pseudokoningii showed antagonist effects to reduce the BLS disease incidence (Krishnamurthy et al., 2001). 

The Cladosporium species out of six phylloplane microorganisms, reported effective to reduce the spore germination and fungal growth of B. oryzae (Harish et al., 2007) and T. viride reduced the growth of mycelium and spore germination 63% to 77% (Harish et al., 2008). Bio formulation of T. harzianum reduced the infection of B. oryzae and mycelial growth (55-58%) (Biswas et al., 2008). More yield about 70% and reduced BLS disease obtained by seed treatment with different biocontrol agents like T. viride, T. harzianum and Pseudomonas species (Joshi et al., 2007; Ludwig et al., 2009; Biswas et al., 2010). Similarly, T. harzianum foliar application reduced the disease intensity. The concentration of protein and carbohydrates also enhanced photosynthesis in rice leaves (Abdel-Fattah et al., 2007). T. harzianum and T. viride spore pre-application safe the infection of B. oryzae in rice plants, which was attributed to the increased level of total soluble protein and total phenol content (Kumawat et al., 2008). Khalili et al. (2012) in Iran found the control of disease by two strains of T. harzianum and

 

Table 3: List of biocontrol agents used against Bipolaris oryzae.

Sr. No.	Biocontrol agents	Finding	Reference
1	Trichoderma harzianum	Reduced mycelium growth efficiently 65.33% in lab and 64% in field	Gupta et al., 2018
2	Streptomyces corchorusii strain UCR3-16	Antifungal effect against six fungal pathogen of rice	Tamreihaoa et al., 2016
3	Bacteria (Pseudomonas synxantha -DFs185), (P. fluorescens -DFs223), (unidentified -DFs306) and (Bacillus sp -DFs418.)	Isolate DFs223 approved to be better as seed treatment	Moura et al., 2014
4	20 tested actinomycetes isolates	Streptomyces isolate G showed best	Nejad et al., 2014
5	Streptomyces philanthi	Inhibited the mycelial growth	Boukaew et al., 2013
6	T. harzianum	Reduced infection and improved seedling growth	Khalili et al., 2012
7	Aspergillus niger, A. terreus, A. fumigates, A. sulphureus, A. flavus, , , Penicillium janthinellum, P. chrysogenum, Trichoderma harzianum and T. viride	Inhibitory effects against pathogen	Manimegalai, 2011
8	T. viride and T. harzianum	More yield about 70% and reduced BLS disease	Biswas et al., 2010
9	Streptomyces vinaceusdrappus	Inhibited mycelial growth	Ningthoujam et al., 2009
10	Pseudomonas species	Reduced the infection of pathogen	Ludwig et al., 2009
11	T. viride	Reduced the growth of mycelium and spore germination 63% to 77% of pathogen	Harish et al., 2008
12	T. harzianum	Reduced the infection of pathogen	Biswas et al., 2008
13	T. harzianum and T. viride	Reduced the BLS disease severity	Kumawat et al., 2008
14	Pseudomonas species	Reduced the infection of pathogen	Joshi et al., 2007
15	Trichoderma harzianum	Reducing the spore germination 77.03% and mycelium growth 62.92%	Abdul-Fattah et al., 2007
16	P. fluorescens	Reduced disease incidence	Joshi et al., 2007
17	six phylloplane microorganisms	Reduce the spore germination of pathogen	Harish et al., 2007
18	Trichoderma viride	Reducing the spore germination 77.03% and mycelium growth 62.92%	Harish et al., 2008
19	B. subtilis	Inhibited mycelial growth	Sarala et al., 2004
20	T. pseudokoningii	Reduce the BLS disease incidence	Krishnamurthy et al., 2001
21	Fusarium graminearum	Reduced the growth of C. miyabeanus	Kim et al., 1995
22	T. viride	Inhibited mycelial growth	Kumar and Mishra, 1994
23	Pseudomonas fluorescent	Reduced disease incidence	Ray et al., 1990
24	Bacillus megaterium	Reduced the BLS disease severity	Islam and Nandi, 1985

 

 

improved seedling growth by one strain of T. atrovirid. Fusarium graminearum produced antifungal substances that inhibited C. miyabeanus and gave 80% control of BLS disease (Kim et al., 1995). A virulent pathogen strain inoculation induced resistance in a susceptible host and decreased the disease index 83-85% (Sinha and Trivedi, 1969). Similar behavior found by pre-treating the plants with germinating spores (Sinha and Das, 1972) (Table 3).

1.2.6 Management through mineral nutrients

The plants which are scarce nutrients are more prone to disease as compared to nutrient deficient. The pathogen damage is compensating by a specific nutrient that reduces the disease through tolerance. The disease BLS incidence and severity influenced by different mineral nutrients i.e. Nitrogen, phosphorus, manganese, iron, and calcium (Ou, 1972: Ramakrishnan, 1971). The scarcity and surplus nitrogen enhance the level of BLS disease while in the form of ammoniacal, it decreases the disease severity if use it in the form of nitrate (Chattopadhyay and Dickson, 1960). Leaf dry matter Phosphorus (P) concentration threshold lies between 0.135 and 0.149% which limits brown spot disease development (Phelps and Shand, 1995). Leaf P content will have bearing on the concentration of other micronutrients which will ultimately reflect on brown spot severity (Kaur et al., 1982; 1984). If the quantity of P content high in soil correlated to decreased BLS incidence, study showed that the use of P as “48 kg ha-1 optimal and any increase of it have negative effects (Singh et al., 2005). 

Potassium (K) nutrition besides direct effect also enhances silication which restricts brown spot development in leaves (Nogushi and Sugawara, 1966) besides conferring resistance in several ways. Carvalho et al. (2010) reported that higher K and N levels lowered brown spot severity by increasing the incubation period and decreased the number of lesions per cm2 of leaf area. Jha et al. (2003) reported that higher K and higher N reduced brown spot severity while N alone showed a lower reduction of disease severity. Potassium in combination with zinc and iron were reported to bring about an increase in phenolic content which increased the incubation period and thus decreased sheath blight in rice (Prasad et al., 2010). Disease severity reducing effects of K was also well documented in other pathosystems as in soybean Phakopsora rust (Balardin et al., 2006). Blast severity of rice cultivar Guarani was less with high K and zinc (Filippi and Prabhu, 1998). Excess K increased resistance of barley to H. sativum (Sarhan et al., 1990). 

Similarly, Silicon (Si) also has a correlation with disease reduction in rice (Datnoff et al., 1997; Dallagnol et al. (2009). Zinc (Zn) deficiency produced more susceptibility to BLS infection. Lesser brown spot severity in zinc sulfate sprayed plots than other micronutrients and control treatments in Boron rice was recorded by Minnatullah and Jha (2002). Goel et al. (2003) observed that Zn (3 kg/ha) in combination with N (120 kg/ha), P (30 kg/ha) and K (30 kg/ha) reduced both brown spot and sheath blight severity. Zinc was known to increase host resistance to mildews and leaf spot diseases and thus a reduction in disease severity. Calcium (Ca) 30 ppm reduced the brown spot disease while 50 ppm increased it. (Kaur et al., 1986). Kaur et al. (1979) reported a decrease in brown spot severity with soil application of Manganese (Mn) (5 to 10 ppm) in susceptible Benibhog rice variety. They concluded that the incidence of disease could be brought down to a lower order of magnitude in the susceptible variety with proper manipulation of Mn. Calcium and manganese nutrition was shown to have a negative correlation with brown spot infection (Kaur et al., 1986, 1987). Junior et al. (2009) evaluated the method and source of Si applied on Metica-1 cultivars to find resistance against BLS. Wollastonite (calcium silicate) treatment used through the soil and potassium silicate and silicic acid by application on leaves. The severity of disease decreased when using as soil application as compared to foliar application. 

 

Conclusions and Recommendations

Different management practices are being used for the control of BLS disease. When disease appeared in epidemic form; one and only quick method is the application of the fungicide that control the disease earlier but it has a residual concern so, it should be used judiciously. Other management practices i.e. resistant varieties selection, appraisal of biocontrol agents, phytoextracts, nutrients and plant activators application were the safer having long last effects against brown leaf spot disease. The best control of this disease in current climate scenario is the use of the integrated different management approaches to cope the emerging threat of this disease for food security in future.

 

Acknowledgement

I am highly appreciated the scientist and researcher of Plant Pathology lab for providing me technical assistance in writing this manuscript.

 

Novelty Statement

A comprehensive information regarding infection and biochemical alterations in rice plant leaves due to Brown leaf spot along with its management through host resistance, plant activators, chemicals, nutrients, plant extracts and bio-control agents.

 

Author’s Contribution

First author write up the manuscript and three others authors were supervisor committee members of first authors that equally provides technical assistance in write up.

Future direction

It is the need of hour to develop such strategies which should be ecofriendly and can bear abrupt climatic variations.

Conflict of interest

The authors have declared no conflict of interest.

 

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