Abhay K. Pandey
Rishi R. Burlakoti
Lawrence Kenyon
Ramakrishnan M. Nair- 1World Vegetable Center South Asia, ICRISAT Campus, Hyderabad, India
- 2World Vegetable Center, Tainan, Taiwan
Mungbean (Vigna radiata var. radiata) is a key legume crop grown predominantly in South and Southeast Asia. Biotic and abiotic stresses cause significant yield reduction in mungbean, and among these, fungal diseases are particularly important. Although disease management practices, including physical, chemical, and biological methods have been researched and described in the literature, few of these are available or have been used by growers. Here we review the economic impact, and sustainable management options for the soil-borne and foliar fungal diseases of mungbean as well as major challenges to manage these diseases. Potential use of all possible components of integrated management practices including host resistance, fungicides, biocontrol agents, natural plant products, and cultural practices etc. are discussed. Major diseases include powdery mildew, anthracnose, Cercospora leaf spot, Fusarium wilt, Rhizoctonia root rot and web blight, Macrophomina charcoal rot/dry root rot and blight. Review of the literature indicated an absence of resistance to Rhizoctonia root rot, little sources of resistance for dry root rot and anthracnose. Major resistant genes (R genes) and quantitative trait loci (QTL) were identified for powdery mildew and Cercospora leaf spot, which may be potentially used in Marker assisted selection (MAS). Although the mechanisms of induced systemic resistance (ISR) by biocontrol agents have been studied with Macrophomina blight, there is little information on the mechanisms and use of systemic acquired resistance (SAR) in managing fungal diseases of mungbean. Several studies targeted exploiting biological control for soil-borne root rot diseases. Botanical products, such as plant extracts, are also found effective to manage root and foliar diseases. However, many of these studies were limited to laboratory and/or green house experiments. Thus, long-term field studies are required for further exploitation of biological methods and commercial applications.
Introduction
Mungbean (Vigna radiata (L.) R. Wilczek var. radiata) is one of the important pulse crops in South and Southeast Asia. About 90% of global production is in South Asia, where India is the largest producer (Nair et al., 2012). India produces about 1.5–2.0 million tons of mungbean annually from about 3–4 million hectares (2014–2015), with an average productivity of 0.5 t ha−1 (Jadhav et al., 2016). Mungbean is also grown in China (Zhang et al., 2011), Australia (Clarry, 2016), and United States of America (Fery, 2002). In Australia, acreage of mungbean has increased substantially with 125,000 ha planted in 2015–2016 compared to only 1,000 ha in 1970s (Clarry, 2016). Average yield of mungbean is 0.4 t ha−1 in Asia but yields up to 2.5 t ha−1 may be attained with selected varieties and good management (AVRDC, 2012). Mungbean seeds is a good source of dietary protein for humans including marginal people, and people who live in areas with less access to meat or where people are mostly vegetarian (AVRDC, 2012). Mungbean sprouts and green pods contain high level of vitamins and minerals (Keatinge et al., 2011; Nair et al., 2015).
Abiotic and biotic stresses caused significant decline in legume yield in South Asia and South East Asia. Among biotic stresses, fungal diseases are responsible for reducing yield up to 40–60% in mungbean (Kaur et al., 2011). Fungal pathogens can infect mungbean plants at different stages, such as during emergence, seedling, vegetative and reproductive stages and cause substantial damage leading to yield loss or complete failure of production. Species of the genera Fusarium (wilt), Rhizoctonia (wet root rot), and Macrophomina (dry root rot) infect mungbean plants during seed/seedlings stages (seed-borne or soil borne), while species of the genera Colletotrichum (anthracnose), Alternaria and Cercospora (leaf spot), Erysiphe/Podospheara (Sphaerotheca) (powdery mildew) affect plants during vegetative and reproductive stages (Figure 1; Ryley et al., 2010). Singh et al. (2013a) reviewed the status of web blight in mungbean and recently, Naimuddin and Singh (2016) published a review on yellow mosaic in mungbean and urdbean from India. However, reviews on fungal diseases of mungbean, their economic impact and major management practices have not been compiled. This manuscript reviews the economic impact of major fungal diseases in the mungbean growing areas of South and Southeast Asia and other areas in world as well as options available for sustainable management of these diseases. The review will also cover efforts in resistant breeding or pre-breeding activities including disease evaluation techniques.
Figure 1. Symptoms of fungal diseases of mungbean at World Vegetable Center, South Asia Hyderabad field, (a). Wilted plant with dry root rot symptom (Macrophomina phaseolina), (b,c). Root & stem infected with M. phaseolina, (d). Roots showing wet root rot (Rhizoctonia solani), (e). Leaf showing web blight (R. solani), (f). Leaf showing anthracnose (Colletotrichum spp.), (g). Leaf showing Cercospora leaf spot (Cercospora spp.), (h). Leaves showing powdery mildew.
Economic Impact of Mungbean Fungal Diseases
Mungbean mainly is grown in rain-fed climates and variability in climate such as elevated temperature and CO2 within the rain-fed ecologies leads to varying intensities of biotic stress (Chakraborty et al., 2000; Sharma et al., 2007) which cause significant loss in production. Foliar and root rot fungal diseases are major production constraints in South Asia and South East Asia. Charcoal rot/dry root rot (Figures 1a–c) (Macrophomina phaseolina) and Rhizoctonia root rot (Figure 1d) (Rhizoctonia solani) are economically important soil-borne vascular diseases, causing wilt and root rot complex (Alam et al., 1985; Iqbal and Mukhtar, 2014). Among major soil-borne vascular diseases, dry root rot and wilt is a major concern since the pathogen affects the plant during all growth stages and subsequently causes significant yield loss. Yield loss due to dry root rot was reported to be 11% in Northern India (Kaushik et al., 1987) and up to 44% in Pakistan (Bashir and Malik, 1988). Dry root rot was also reported first time in Shanxi province of China in 2010 (Zhang et al., 2011). Mungbean plants with wilt and root rot symptoms, with incidence of 80–90% in susceptible genotypes, was also reported in 1979 in southwest Ontario (Anderson, 1985).
Anthracnose (Colletotrichum lindemuthianum or C. truncatum or C. gloeosporioides) (Figure 1f; Shen et al., 2010), Cercospora leaf spot (Figure 1g) (Cercospora cruenta or C. canescens or C. kikuchii or C. caracallae) (Joshi et al., 2006), and powdery mildew (Figure 1h) (Erysiphe polygoni or Podosphaera fusca) (Ryley et al., 2010), Macrophomina blight (M. phaseolina) and web blight (Figure 1e) (R. solani) (Alam et al., 1985; Iqbal and Mukhtar, 2014) are the major foliar diseases of mungbean as causing yield loss ranging 20–60% in different continents. A wide range of yield losses (23–96%) due to Cercospora leaf spot was reported from field trials conducted at different states of India (Kaur, 2007; Chand et al., 2012; Bhat et al., 2014) and up to 61% from Pakistan (Iqbal et al., 1995). The impact of powdery mildew on mungbean also was reported from different countries. Yield loss due to powdery mildew was reported up to 21% in the Philippines (Quebral and Cowell, 1978), up to 40% in Australia (Kelly et al., 2017), and from 20 to 100% in different regions of India. Yield losses from powdery mildew was reported 35% from Gujarat, western India (Khunti et al., 2002), 20–40% from Chhattisgarh, central-eastern India (Khare et al., 1998) and 20–40% in Maharashtra, western-central India (Mandhare and Suryawanshi, 2008), and from 9 to 50% in Uttarakhand and Uttar Pradesh of Northern India (Pandey et al., 2009). Reddy et al. (1994b) also reported 100% loss from Maharashtra State, India due to powdery mildew diseases at seedling stage. A wide range of yield losses (24–67%) due to anthracnose disease was estimated from several mungbean growing areas in India (Deeksha and Tripathi, 2002; Kulkarni, 2009; Shukla et al., 2014). Alternaria leaf spot (Alternaria alternata) is also reported in South Asia, but economic impact is minor i.e., only 10% loss reported from Jammu and Kashmir, India (Maheshwari and Krishna, 2013). Web blight has been a problem for several decades in Pakistan (Alam et al., 1985) and in India, where it was reported from diverse geographical areas including Kanpur and Uttar Pradesh, northern India (Dwivedi and Saksena, 1974), Punjab, northwest India (Bains et al., 1988), Madhya Pradesh, central India (Tiwari and Khare, 1998), Rajasthan (south India), Bihar, Haryana, and Himanchal Pradesh (northern India) (Anonymous, 2014). About 30–40% of yield loss due to web blight was reported from Rajasthan (Anonymous, 2000) and 20–40% seedling mortality due to Rhizoctonia infection was reported from Jabalpur, central India (Tiwari, 1993).
There is a little information available regarding the dynamics in the prevalence and incidence of diseases in mungbean at temporal and spatial scale. Fusarium wilt caused by Fusarium oxysporum and/or F. solani was a minor disease of mungbean in Australia. However, the incidence and severity of the disease has increased substantially in recent years and yield losses of up to 80% were reported in the susceptible mungbean cultivars (Kelly, 2017). Outbreaks and spread of diseases were reported in other legume crops, such as soybean (Sconyers et al., 2006) and chickpea (Sharma and Ghosh, 2017). For example, Asian soybean rust (Phakospora pachyrhizi) was a problem in Asia and South America, but then spread rapidly across eight states of southeastern United States within a few years of first detection in Louisiana in 2004 (Sconyers et al., 2006). It was speculated that an extreme weather event (hurricane) was responsible for the introduction and spread of the Asian soybean rust. Sharma et al. (2015) also reviewed dry root rot (Macrophomina phaseolina) as an emerging disease of chickpea in semiarid tropic region and disease intensity has been increased in a past decade. They further speculated that changes in weather pattern, such as high temperature and drought stress during reproductive stages of the chickpea increased the dry root rot intensity. Climate change could have positive or negative or neutral impact on the dynamics of crop diseases depending on the types of crops, diseases or geographical regions (Luck et al., 2011). Climate change would increase average global temperature, CO2 level, and cause more extreme rain/drought events (Meehl et al., 2005). Severity of some diseases, such as brown spot of soybean (Septoria glycines) and sheath blight of rice (Rhizoctonia solani) increased with elevated levels of CO2 (Kobayashi et al., 2006; Eastburn et al., 2010), whereas variable results were reported for powdery mildew of wheat and barley (Thompson et al., 1993; Hibberd et al., 1996). In South Asia, spot blotch in wheat (Cochliobolus sativus) has increased substantially in recent years and it is speculated that elevated night temperatures due to climate change has contributed to this (Sharma et al., 2007). In Australia, root and crown rot of wheat (Fusarium pseudograminearum) is expected to increase due to climate change as the disease was high with elevated CO2, temperature, and drought (Melloy et al., 2010). There is no information available on the impact of climate change on the dynamics of mungbean diseases. However, based on knowledge of similar pathogens/diseases in other crops, we can speculate that the pressure of soil-borne diseases caused by Fusarium, Macrophomina, and Rhizoctonia in mungbean may increase due to climate change. It is difficult to predict the effect of climate change on foliar diseases since they are influenced by the combination of temperature, rainfall and relative humidity, which can't be precisely predicted in most situations of climate change.
Perspectives for Sustainable Disease Management
The options for sustainable management of fungal diseases of mungbean include cultural and physical methods, exploitation of host resistance, use of synthetic fungicides, use of natural products such as botanical extracts, bio-fungicides, and use of bio-stimulants or defense activators, and these are discussed below.
Cultural and Physical Practices
Use of different cultural practices and physical methods to eliminate seed-borne pathogens were found effective to reduce the foliar and root rot diseases of mungbean in fields. Field sanitation, crop rotation, removal of crop debris and weed hosts in the vicinity of the crop reduced the Cercospora foliar blight in mungbean (as reviewed in Sharma et al., 2011). Removing root rot infected mungbean plants reduced sclerotia loads in the field and delayed sowing and maintaining wider spacing between the plants reduced powdery mildew incidence (as reviewed in Satyagopal et al., 2014). Plastic mulching increased sclerotial mortality of M. phaseolina and reduced pathogen infection (Yaqub and Shahzad, 2009). Mungbean seed treatment with gamma rays (60Cobalt) for 0–4 min and 90 days of storage had a suppressive effect on root rot fungi (Ikram et al., 2010). Hot water emersion treatments (55–65°C) were effective to eliminate seed-borne infection with Colletotrichum acutatum and C. gloeosporioides of mungbean (Lee et al., 2007). In South Asia, mungbean is commonly rotated with rice and wheat. It is reported anecdotally that root rot diseases in mungbean have been increased in South Asia and other Asian countries due to continuous rotation with rice. Several soil-borne pathogens, such as Rhizoctonia, Fusarium etc. are common problem in rice and wheat (Kobayashi et al., 2006; Melloy et al., 2010). These fungal genera also infect mungbean, but more studies are required to determine if the same species and strains also infect mungbean. If it is practical, adding diversity in the crop rotations would help for the sustainable management of these soil-borne diseases in mungbean. Crop diversification and use of diverse cultural practices, such as crop rotation, plant residue management, adjusting the planting dates etc., are recommended as effective strategies for managing crop diseases in conditions of climate change (Juroszek and von Tiedemann, 2011).
Exploitation of Host Resistance
Use of host–resistance is an effective, economical, and eco-friendly method for managing mungbean fungal diseases. In this section, we synthesize the available information regarding the identification of sources of resistance, available methods for efficient and reliable disease reaction phenotyping, identification of molecular markers associated with disease resistance genes and their potential use to improve disease resistance traits in mungbean.
Resistant Sources for Major Fungal Diseases of Mungbean
Reliable and efficient methods are available to screen for reaction to foliar diseases of mungbean including Cercospora leaf spot, powdery mildew, and anthracnose. Screening of these foliar diseases can be successful in natural field conditions where disease pressure is high, or if artificial inoculation with pathogen spores is available (Iqbal et al., 2004; Yadav et al., 2014a,b). For other foliar diseases caused by hemibiotrophic (Cercospora spp.) or necrotrophic pathogens, disease can also be evaluated in the greenhouse with artificial inoculation. Several disease rating scales/systems were developed to assess foliar diseases of mungbean (Wongpiyasatid et al., 1999; Khunti et al., 2005; Suryawanshi et al., 2009). Mungbean germplasm accessions can be screened by inoculating with the pathogen in the controlled environments. Reliable and efficient methods were developed for screening mungbean seedlings against powdery mildew in the greenhouse (Wongpiyasatid et al., 1999; Kasettranan et al., 2010); and in the laboratory using a detached leaf assay (Reddy et al., 1987). For the assessment of foliar diseases, both qualitative and quantitative rating scales were used (Reddy et al., 1994b; Wongpiyasatid et al., 1999; Khunti et al., 2005; Marappa, 2008; Suryawanshi et al., 2009). Root rot and wilt diseases are sporadic and highly variables due to genotypes × environment (G × E) interaction, therefore it is very difficult to get consistent results while screening in natural fields. Therefore, host genotypes are usually screened by inoculation at seedling stages in controlled environment for soil-borne diseases (M. phaseolina, R. solani, and F. solani). Different methods such as paper towel (Khan and Shuaib, 2007) and sick pot/field inoculation methods by inoculating the fungus grown in sorghum or maize grains (Dubey et al., 2009; Choudhary et al., 2011) were used for the evaluation of root rot disease.
Sources of resistance against powdery mildew, Cercospora leaf spot, anthracnose, Macrophomina blight and dry root rot have been identified (Table 1). The majority of studies targeted resistance to Cercospora leaf spot and powdery mildews and were conducted in the field. There have been fewer studies to identify root rot and anthracnose resistance sources, and these were conducted in both lab/glasshouse and field experiments. Most of the identified resistant materials were derived from cultivars/recombinant lines /breeding lines/land races; however, some were from wild relatives (Marappa, 2008) and mutant lines (Wongpiyasatid et al., 1999). Since screening trials for resistance against Alternaria leaf spot, anthracnose, and root rot diseases are limited, more attention is required on these. These resistant lines from difference sources can be utilized as donors for developing resistant varieties.
Table 1. Resistant genotypes of mungbean against fungal diseases†.
Identification of Major Genes and Quantitative Trait Loci (QTL) Linked to Major Diseases
The success of developing varieties resistant to biotic stresses depends on the availability of good sources of resistance materials as well as identification of markers associated with disease resistance major genes or QTL, which can also be used in marker assisted selection (MAS) breeding program to accelerate the resistant screening for large population. In mungbean, exploitation of host resistance and identification of molecular markers associated with major genes or QTL were mainly targeted for powdery mildew and Cercospora leaf spot (Kasettranan et al., 2010), however, no QTL or associated molecular markers were reported for other major fungal diseases including dry root rot and anthracnose. The commercial breeding for powdery mildew and Cercospora leaf spot disease resistance in mungbean mostly utilized major Resistant (R) genes based on the classical gene-for-gene system (Kasettranan et al., 2009). To our knowledge, use of MAS has not been used for mungbean breeding programs targeted for fungal disease resistance in developing countries. However, identification of molecular markers associated with disease resistant major genes and QTL shows the potential application of MAS in mungbean disease resistance. Genetic studies using different sources of resistance revealed both monogenic (qualitative) and quantitative modes of inheritance in mungbean for powdery mildew resistance (Reddy et al., 1994a; Kasettranan et al., 2009). Gawande and Patil (2003) reported that both additive and dominant gene actions were important in inheritance of powdery mildew resistance including non-allelic interactions. Several earlier studies reported monogenic inheritance of powdery mildew resistance controlled by single dominant genes and studies were conducted using mungbean varieties ML3 and ML5 (AVRDC, 1979), and breeding lines VC 1560A (AVRDC, 1981), ATF 3640 (Humphry et al., 2003) and RUM (Reddy et al., 1994a). Using restriction fragment length polymorphism (RFLP) markers, Chaitieng et al. (2002) and Humphry et al. (2003) revealed single major locus conferring the resistance against powdery mildew with 65 and 80% R2, respectively. Khajudparn et al. (2007) found non-allelic dominant gene for powdery mildew in F2 populations developed from resistant lines V4718, V4758, and V4785 (obtained from World Vegetable Center) and susceptible line CN72. Reddy (2009) studied the inheritance of Pm3 gene (different from earlier identified resistant genes, Pm1 and Pm2), a new gene responsible for powdery mildew by using local mungbean cultivar Mulmarada from Maharashtra (India). He found that F1, F2, and F3 families exhibited complete resistance to powdery mildew is controlled by single dominant gene.
Several researchers reported quantitative mode of inheritance for powdery mildew resistance (Young et al., 1993; Sorajjapinun et al., 2005). Sorajjapinun et al. (2005) reported that additive gene action was found to play a major role in controlling powdery mildew (E. polygoni) resistance in the population of crosses developed between moderately resistant KPS 2 and resistant VC 6468-11-1A (sourced from the World Vegetable Center). Using mapping population developed from advanced mungbean breeding line VC3890 (from World Vegetable Center) as a resistance parent, Young et al. (1993) identified three QTL associated with powdery mildew (E. polygoni) resistance. These QTL explained 17 to 28 and 58% of phenotypic variation (R2) individually and together, respectively. Using SSR markers, Kasettranan et al. (2010) identified two major QTL (qPMR-1 and qPMR-2) associated with powdery mildew resistance, which explained R2 of 20 and 58%, respectively. They used 190 F7 recombinant inbred line (RIL) population developed from the crosses between a susceptible cultivar, Kamphaeng Saen 1 and a resistant line, VC6468-11-1A (sourced from World Vegetable Center). SSR markers flanking and closely associated with qPMR-1 (CEDG282 and CEDG191) and qPMR-2 (MB-SSR238 and CEDG166) can be useful for MAS powdery mildew resistant breeding program of mungbean. Chankaew et al. (2013) also identified a major QTL associated powdery mildew resistance on linkage group (LG) 9 and two minor QTL on LG4 in V4718 (sourced from World Vegetable Center). They also detected two major QTL on LG6 and LG9 and one minor QTL on LG4 in the mapping populations developed using mungbean genotype RUM5 (Chankaew et al., 2013).
In Cercospora leaf spot, genetic inheritance studies using different resistant sources revealed that the resistance is controlled by either a single dominant gene (Lee, 1980), a single recessive gene (Mishra et al., 1988) or quantitative genes (AVRDC, 1980; Chankaew et al., 2011). Although the above information is useful for breeders in developing the resistant varieties, progress in selecting CLS-resistant genotypes in large breeding programs is still limited. First QTL mapping for resistance to Cercospora leaf spot in mungbean was carried out in Thailand (Chankaew et al., 2011). Using F2 (CLS susceptible cultivar Kamphaeng Saen1, KPS1 × CLS-resistance mungbean line, V4718) and BC1F1 [(KPS1 × V4718) × KPS1] populations, they identified one major QTL (qCLS) on LG3 located between the markers CEDG 117 and VR 393, which explained 66–81% phenotypic variation. Their study further confirmed that SSR markers flanking qCLS will facilitate transfer of CLS resistance allele from V4718 into elite mungbean cultivars.
Protection With Synthetic Fungicides
Applications of fungicides are the most common approach of managing fungal diseases of crops. The traditional ways of disease management in mungbean include use of broad spectrum fungicides as a seed treatment chemicals and foliar spray. Efficacies of different mode of fungicides evaluated to reduce the major fungal diseases of mungbean are summarized in Table 2. Fungicides were evaluated mostly in the field trials as seed treatment and/or foliar sprays. Majority of trials were targeted for Cercospora leaf spot, anthracnose and powdery mildew and few trials were on Macrophomina blight, web blight and dry root rot (Table 2). Most of these studies assessed fungicide efficacies in reducing disease incidence and/or severity and yield benefit; however missed the economic analyses of the fungicide applications, which is critical component to recommend for farmers. The major group of effective fungicides to control foliar diseases including powdery mildew, Cercospora leaf spot, web blight, and Macrophomina blight were DMI, and MBC. Application of mancozeb (dithocarbmate) was not effective for powdery mildew; however, was effective for Cercospora leaf spot and Macrophomina blight. Dinocap (QiL) and tridemorph (amines groups) were effective for powdery mildew. Carbendazim and benomyl (MBC) were effective for anthracnose. Most of the foliar spray was applied immediately after the appearance of disease symptoms followed by 2nd and 3rd spray after 15–20 days of first spray for anthracnose, powdery mildew and Cercospora leaf spot as given in the Table 2. Seed treatment is applied mainly against wet and dry root rot, anthracnose and Alternaria leaf spot diseases before sowing. For dry and wet root rot disease, carbendazim was found to be most effective fungicides (Rathore, 2006). The other effective fungicides for wet root rot were flutolanil and tolclofos-methyl (SDHI), carbendazim (MBC) and pencycllron (Phenylureas) (Kumari et al., 2012).
Table 2. Efficacy of fungicides for the control of fungal diseases in mungbean.
To our knowledge, disease outbreak due to break down of fungicides has not yet been reported in mungbean. However, disease management failures in legume crops associated with fungicide resistance have been reported from several countries (Chang et al., 2007; Lonergan et al., 2015; Price et al., 2015). For example, Price et al. (2015) reported that isolates of C. kikuchii (Cercospora leaf spot) from soybean fields in Louisiana State, USA were insensitive to thiophanate methyl. Isolates of Ascochyta rabiei (ascochyta blight of chickpea) from Canada and USA showed insensitivity with fungicides pyraclostrobin, chlorothalonil, fluxapyroxad, and prothioconazole (Chang et al., 2007; Lonergan et al., 2015). More than 90% mungbean are produced in developing countries where strict regulations for fungicides are lacking and poor extension services to educate farmers to apply fungicides properly. This may lead in future the disease outbreak due to fungicide resistance problems. Therefore, fungicide resistance management strategies, such as rotation of fungicides with different mode of actions, tank mix of broad spectrum and selective fungicides, and integrate the fungicide spray programs with other components of disease management practices, should be implemented at regional and national level as recommended by Fungicide Resistance Action Committee (FRAC). Use of next generation fungicides derived from active constituents of natural products, which are ecologically safe and effective at lower doses, would also be beneficial (Sierotzki and Scalliet, 2013).
Biological Methods
Biological Control Agents
Very limited information is available on the biological methods to manage mungbean foliar diseases including powdery mildews, Cercospora leaf spot, and anthracnose. However, more information is available for the management of root rot pathogens. Most of these studies were conducted in the laboratories to evaluate the effects of bio-control agents (Trichoderma species, Pseudomonas, Bacillus etc.) to inhibit growth of root rot pathogens, Rhizoctonia and Macrophomina. Few studies were also conducted in the greenhouse to study the impact of seed or soil applications of the biocontrol agents to reduce the root rot; however, only very few studies were conducted in fields.
Sharma et al. (2017) recommended that application of biocontrol agents is more effective to suppress the soil-borne diseases as effective chemical protectants are either not available or not economical. Integrated applications of biocontrol agent with organic amendments were recommended to reduce root of mungbean in fields (Raghuchander et al., 1993; Ehteshamul-Haque et al., 1995). Dubey and Patel (2002) reported that soil application of T. viride (8 g/kg) multiplied in pulse bran and saw dust in the greenhouse experiment showed 75% reduction in root rot disease caused by R. solani and also promoted plant growth. A 76% reduction in Rhizoctonia root rot was reported when Gliocladium virens (Trichoderma virens) applied as seed treatment @ 106 spores/ml/10 g seeds (Dubey, 2003). Bioproducts Pusa 5SD (T. viride) showed 72% root rot reduction and 978 kg ha−1, Pusa 5SD (T. harzianum) showed 71% disease reduction and 940 kg ha−1 yield in sick field (Dubey et al., 2011). Similarly, T. harzianum, and T. viride reduced about 54–73% Rhizoctonia root rot incidences (Singh et al., 2008; Maheshwari and Krishna, 2013) in green house and field experiments, respectively.
Seed dressing and soil drenching with bacterial strains of Pseudomonas aeruginosa and Bacillus subtilis significantly reduced 42% Macrophomina root rot, 39% Fusarium root rot and 70% Rhizocotnia root rot incidences in mungbean (Siddiqui et al., 2001). Bacterial strain TNAU-1 (Burkholderia spp.) inhibited mycelial growth of M. phaseolina in in vitro dual culture and also reduced root rot incidence up to three-fold when applied as a seed treatment and soil application with talc based formulations (Satya et al., 2011). Trichoderma viride and T. harzianum were found to be reduced M. phaseolina growth (respective 42–33 and 42–25 mm) in dual culture (Ebenezar and Yesuraja, 2000). In the field study, Kumari et al. (2012) found that mixed application of vermicompost (10%) + bavistin (0.1%) + T. harzianum (4%) exhibited 100% reduction of Macrophomina root rot. Bacillus subtilis and T. longibrachyatum against M. phaseolina exhibited 64 and 63% antagonistic activity, respectively (Tandel et al., 2014). In greenhouse study, application of 4 g kg−1 seeds of T. harzianum with 25 g kg−1 of phosphate solubilizing bacteria as seed dresser reduced 26% incidence of Macrophomina root rot (Deshmukh et al., 2016).
The compatibility of different bioagents against root rot pathogens has also been studied. Application of plant growth promoting rhizobacteria, Pseudomonas aeruginosa, with a medicinal plant Launaea nudicaulis @ 0.5% as soil amendment reduced 51% of Macrophomina root rot, while combined application of L. nudicaulis (0.1% W/W) + P. aeruginosa and L. nudicaulis (1.0% w/w) + P. lilacinus gave 0% infection reduced of Rhizoctonia and Fusarium root rot, respectively (Mansoor et al., 2007). In the green house and field trials (Thilagavathi et al., 2007), soil application of Pseudomonas fluorescens strain Pf1+ Trichoderma viride strain Tv1 controlled 86% Macrophomina root rot in pot culture and 59% in field conditions with 833 kg ha−1 yield. The authors also found that T. viride strain is not compatible with B. subtilis (Bs16), but P. fluorescens strain is compatible with B. subtilis and T. viride in the management of dry root rot. Yadav et al. (2017) reported that T. viride, T. harzianum, and Pseudomonas fluorescens were effective to reduce powdery mildew of mungbean (~80–84% reduction).
Botanical Fungicides and Bio-Stimulants
The plant products, particularly plant extract and essential oils, showed prominent toxicity to the diverse genera of plant pathogenic fungi, bacteria, insects and nematodes (Pandey and Tripathi, 2011). Plants synthesize aromatic secondary metabolites in the form of terpenes, like phenols (carvacrol, eugenol, and thymol), phenolic acids, quinones, flavones, flavonoids, flavonols, tannins and coumarins (Cowan, 1999), these groups of compounds show fungicidal effect and serves as plant defense mechanisms against fungal pathogens (Slusarenko et al., 2008; Das et al., 2010). For mungbean diseases, most of studies were preliminary and different kinds of plant extracts or their products have been evaluated against mungbean fungal pathogens (Javaid and Amin, 2009; Murugapriya et al., 2011). Foliar spray of neem extract (1:4 w/v) was reduced 65% of Cercospora leaf spot and increased 25% yield in mungbean (Uddin et al., 2013). Leaves extracts behada (Terminali belerica), tapioca (Manihot utilissimum), and sadafuli (Vinca rosea) reduced 60–66% of conidial germination of powdery mildew fungus E. polygoni (Rakhonde et al., 2011). Similarly, in vitro evaluation of leaf extracts of Adenocalymma alliaceum and Allium spp. reduced about 75–77% mycelia growth of M. phaseolina, Macrophomina blight incidences in greenhouse experiments (Murugapriya et al., 2011; Rana et al., 2014). In the greenhouse experiments, combined applications of 10% extract of Allium spp., mancozeb (0.2%), and 10% extract of Allium spp. with zinc sulfate (0.5%) reduced about 88–94% incidence of Macrophomina root rot (Sundaramoorthy et al., 2013). Javaid and Saddique (2011) found that amendment of dry leaf manure of Datura metel (1.5% w/w) in the soil reduced 80% plant mortality caused by M. phaseolina. Similarly, soil application of L. nudicaulis (1% w/w) extract also reduced dry root rot (62%), wet root rot (75%) and Fusarium wilt (100%) incidences (Mansoor et al., 2007) in glasshouse. Mungbean seeds dressing with 2% concentration of palmarosa (Cymbopogon martinii) oil gave complete inhibition of M. phaseolina mycelial growth (100%) in poison food testing and also caused 72.33% reduction in dry root rot in the greenhouse trials (Kumari et al., 2012).
Induced systemic resistance (ISR) and systemic acquired resistance (SAR) are both important phenomenon in the interactions of plant-pathosystems. Both ISR and SAR increased productions of proteins (defense enzymes) like peroxidase (PO), pathogenesis related (PR), phenylalanine ammonia lyase (PAL), polyphenol oxidase (PPO), phenols etc. (Jones and Dangl, 2006; Walters et al., 2009), which showed positive associations with resistance for several fungal diseases of vegetable and legume crops (Vallad and Goodman, 2004; Abdel-Kader et al., 2013). In mungbean, limited studies have been conducted to understand the mechanism of ISR and SAR. Similar to other crops, increase production of plant defense enzymes were reported when mungbean plants were treated with bioagents and plant products and also challenged with plant pathogens. Application of 10% aqueous leaf extracts of Allium alliaceum and other Allium sp. exhibited increase in PO, PPO, PAL and total phenol contents in mungbean plants inoculated with Macrophomina phaseolina (Sundaramoorthy et al., 2013). Treatment of M. phaseolina pre-inoculated mungbean plants with Pf1 (Pseudomonas fluorescens) formulation amended with chitin increased the accumulation of PAL, PO, PPO, chitinase, β-1,3-glucanse and phenolics indicating that the PGPR strains amended with chitin bioformulation induced defense-related enzymes and pathogenesis related (PR) proteins (Saravanakumar et al., 2007). Higher levels of PO and PPO activity was observed in M. phaseolina infection treated with the bioformulation combination of plant growth promoting bacteria (P. fluorescens) and biocontrol agents (Trichoderma or Bacillus) than the plants treated with single biocontrol agent (Thilagavathi et al., 2007). Mechanism of SAR were studied for bacterial (Dutta et al., 2005; Farahani and Taghavi, 2016) and viral diseases (Rashid et al., 2004) of mungbean, but study regarding fungal diseases are still meager. Thus, more investigations are required to understand the SAR and ISR mechanisms in the interactions between mungbean and fungal diseases.
Challenges for the Sustainble Disease Management
More than 90% of mungbean are cultivated in the developing countries, where small farmers do not have proper knowledge on integrated pest management and several challenges exist in the implementation of integrated management options. For example, use of gamma rays for seed treatment is a good option to eliminate seed-borne pathogen from seed, but it is not viable for the small holder farmers since they produce seeds in their farm in a small scale. Several developing countries in south Asia do not have strong national breeding programs in mungbean to exploit host resistance for multiple diseases. Disease resistant genotypes identified in several studies were evaluated in few locations or seasons. Variability in pathogen populations exists among diverse geography; therefore, screening trials should be conducted multi-locations and years while developing breeding lines for disease resistance. Instability and breakdown of disease resistance in mungbean cultivars is a major challenge in breeding programs due to monogenic host resistance and high pathogenic variability (Nair et al., 2017). Integration of disease resistance traits without compromising valuable agronomic traits is a key challenge for mungbean breeders as linkage drags inhibit the proper use of genetic diversity from wild germplasm into the commercial cultivars (Acosta-Gallegos et al., 2008; Keneni et al., 2011). Further, undesired and desired traits co-inheritance may affect on seed quality.
In developing countries including India, fungicides are registered by CIBRC (Central Insecticide Board and Registration Committee) with their effective dose and label claim which provides guideline to the growers. However, where fungicides are not registered, agriculture officers or fungicide retailers provide fungicides spray guidelines to the growers. Several growers do not apply fungicides with appropriate doses and timing, although majority of fungicides used are preventative (broad-spectrum), which require applying prior to pathogen infection or prior to first symptoms appearance. In addition, farmers do not commonly rotate fungicides with different mode of actions due to poor knowledge and extension on IPM. As fungicides resistance is a big concern for legume industry in several countries (Chang et al., 2007; Lonergan et al., 2015; Price et al., 2015), the problem may arise in mungbean industry. Fungicide resistance could be significant challenge for the mungbean farmers in future to manage diseases effectively. Fungicide resistance management strategies recommended by FRAC, which we have described in the section “Protection With Synthetic Fungicide,” have not been deployed at regional or national levels in several developing countries.
Additionally, attempts have been made to produce and apply biopesticide commercially in the developing countries. Challenges also exist for the commercial use of biopesticides in mungbean. Most of biopesticides only suppress the diseases and are not effective as chemical fungicides, therefore growers are reluctant to use the products (Flexner and Belnavis, 2000; Felde et al., 2006). Due to poor extension, growers do not apply the biopesticides as a component of integrated approach. In addition, several abiotic and biotic factors make the biopesticides less effective in field (Meyer and Roberts, 2002; Sharma et al., 2017). Sharma et al. (2017) speculated that there could be risk of developing biocontrol agents as crop pests and therefore, careful attentions are required while developing/evaluating biocontrol agents. However, we did not find any reports in the literature showing the evidences of biocontrol agents shifted to crop pathogens. Few researchers suggested that application of biocontrol agent is effective when mixed with other biocontrol agents; however, other investigators reported that such combinations may not be always advantageous as antagonism can occur among biocontrol agents (Viaene and Abawi, 2000). Most of studies to exploit botanicals and other bio-based products were evaluated in laboratory or controlled environments and their efficacy has not been evaluated in fields. This shows future potentiality of these products for the sustainable management of diseases, however, growers do not have current access of these products.
Mungbean farmers in the developing countries are not well educated about the impact of global climate change in the disease management. Global climate change would influence the emergence of new diseases, biology of the plant pathogens, disease development and their management practices in different geographical regions (Chakraborty et al., 2000; Juroszek and von Tiedemann, 2011; Luck et al., 2011). Global rise in temperature and CO2 due to climate change may modify aggressiveness and fecundity of the plant pathogens, increase host susceptibility, and change host architecture and host-pathogen interaction (Chakraborty et al., 2000; Luck et al., 2011). The mungbean breeding programs in the developing countries does not have enough resources and strategies for developing resistant varieties for biotic and abiotic stresses associated with climate change elevation in temperature, CO2, and moisture stress due to climate change may also affect the efficacies and the durability of plant protection chemicals and biocontrol agents (reviewed in Juroszek and von Tiedemann, 2011), which could be also key challenge to manage mungbean diseases in future.
Conclusions and Future Prospects
The present review identified that root rot complex and wilt caused by soil-borne pathogens and foliar diseases are major fungal diseases impacting mungbean production in South Asia and South East Asia. Fusarium wilt and root rot and powdery mildew are problematic in Australia. For the management of these diseases potential options such as chemical and non-chemical (cultural, physical, host-plant resistance, biological) have been investigated by the researchers. Although several field trials were conducted to evaluate fungicides and other non-chemical management options by researchers from universities and governments, very little information has been transferred to the mungbean growers in South and Southeast Asia due to the poor linkage between research and extension activities. Deployment of Integrated Disease Management (IDM) to manage mungbean diseases in a coordinated approach requires good collaborations among academia, national and international research institutes, national extension agencies and growers.
Use of resistant varieties (if available) in combination with other components of management is a most effective option to combat with these fungal diseases. Described literature revealed that sources of resistant genotypes have been identified for Cercospora leaf spot, powdery mildew, and anthracnose diseases and few for dry root rot by screening mungbean germplasms in natural field/artificial conditions in few specific locations. The identified sources for resistance in these diseases could be region specific as they were tested in a few specific locations. For example, V4718 mungbean accession from the WorldVeg gene bank has been used as a source of resistance to powdery mildew in Thailand and India. Breeding lines developed from the above source through cross breeding, and selections have been shared to the partners in the ACIAR funded International Mungbean Improvement Network project. Therefore, evaluation of resistant genotypes for these diseases at multi-locations in a coordinated approach would help in deploying host resistance at a larger scale. Compared to foliar diseases, few resistant genotypes of mungbean are available for root rot diseases. This may be due to the less priority given to the screening of these diseases in the past. However, the incidence of dry root rot in mungbean grown as part of rice based farming system in eastern part of India (Odisha state) and in Myanmar has triggered the need for identification of sources of resistance. Sharma and Ghosh (2017) reported that chickpea genotype which showed a good level of resistance to Fusarium wilt at 24°C were susceptible at 27°C. Therefore, breeding programs should consider potential impact of climate change in the new and existing biotic stresses. Attention should be given to develop climate resilient cultivars (such as cultivars can show a good level of resistance at higher temperature) with greater diversity and incorporating traits for multiple disease resistance. Literature evidenced that molecular markers are available for powdery mildew and Cercospora leaf spot, however, there is need to validate them in breeding programs. More attention is required to develop the molecular markers for root rot and anthracnose diseases. Currently, as a part of the network, we are screening 296 mini-core accessions of mungbean (Schafleitner et al., 2015) for resistance to anthracnose, dry root rot, powdery mildew and Cercospora leaf spot diseases. The resistant accessions identified will be shared among the project partners for cultivar development.
Application of synthetic fungicides is a common practice to control fungal diseases of mungbean, and growers also integrate other cultural methods with chemical sprays. Efficacies of several fungicides (Table 2) were evaluated in fields and controlled environments at universities and research institutions, however, there is a knowledge gap regarding how much of these evaluated fungicides are currently used by mungbean growers. In addition, additional research are required for fungicide efficacy trials including rotating and tank mixing with different modes of actions, different rates as well as volume of water for spray coverage. Attentions should also be given to develop and evaluate new generation fungicides. Fungicide resistance problem has not yet been reported in mungbean growing areas, which could also be due to research gap to investigate fungicide sensitivity against mungbean pathogens. In literature, baseline sensitivity data are not available for any fungicides and pathogens. Therefore, future research is recommended for in vitro fungicide sensitivity test using large numbers of pathogen isolates from diverse areas. Fungicide resistance management strategies (such as integrating chemical fungicides with other management practices, judicial use of fungicides, rotation and tank mix of different groups of fungicides) should be deployed at regional and national level to reduce the risk of developing fungicide resistance fungal population. Future impact of climate change on diseases of other crops such as wheat, soybean, and potatoes etc. were studied (reviewed in Luck et al., 2011). Climate change could make crop disease management more challenging in the developing countries. To our knowledge, no studies have been conducted to understand the effect(s) of climate change on mungbean diseases, and thus future research should address this. Induced resistance due to bio-stimulants has been explored for a few diseases including Macrophomina blight and therefore, additional research is required to exploit induced resistance to manage anthracnose, powdery mildew, Cercospora leaf spot and root rot diseases. Regarding biological control, investigation has been focused for root rot pathogens using strains of Trichoderma, Pseudomonas, and Bacillus as seed dresser and soil application. Biocontrol agents were more effective in reducing diseases in controlled environments than in fields. Plant-based products as described understory have been extensively researched for the control of seed/soil borne and foliar pathogens, but few have yet reached the market due to lack of their large scale trials at field level. Use of genomics tools has opened avenue to understand the mode of actions of biocontrol agents and genes associated with it (Sharma et al., 2017), however, more research is required in this area. Coordinated approaches from researchers from the universities, private sectors, national and international research centers are required to evaluate promising biocontrol agents, biostimulants, and botanical products in fields at multilocations and commercialize these products. Compatibility between different products including fungicides and these bioagents should be also evaluated. Persistent efforts are required for refinement, validation, transfer and adoption of the integrated disease management modules by the mungbean growers.
Author Contributions
AP lead author in reviewing the literature, compiling the information preparing the reveiw draft and revising the manuscript. RB substantial contribution in writing the manuscript from the begining of the manuscript draft. Guided lead author to outline the sections and compile the manuscript. Critically reviewed and revised the manuscript, resturctured the entire manuscript with signifcant contribution to shape the manuscript for the final version. LK crtically reviewed the manuscript and contributed to rewrite and restructure the manuscript. Substanital contribution to revise the all sections of manuscript including abstract, prospects and conclusion. RN guided lead author to compile the manuscript, Significant contribution to revise the manuscript and contributed to write the Host Resistance section of the manuscript.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer RR and handling editor declared their shared affiliation
Acknowledgments
Funding for this review was provided by core donors to the World Vegetable Center: Republic of China (Taiwan), UK aid, United States Agency for International Development (USAID), Australian Centre for International Agricultural Research (ACIAR) through ACIAR Project on International Mungbean Improvement Network (CIM-2014-079), Germany, Thailand, Philippines, Korea, and Japan.
References
Abdel-Kader, M. M., El-Mougy, N. S., and Lashin, S. M. (2013). Biological and chemical resistance inducers approaches for controlling foliar diseases of some vegetables under protected cultivation system. J. Plant Pathol. Microb. 4:200. doi: 10.4172/2157-7471.1000200
Acosta-Gallegos, J. A., Kelly, J. D., and Gepts, P. (2008). Prebreeding in common bean and use of genetic diversity from wild germplasm. Crop Sci. 48, 3–16. doi: 10.2135/cropsci2007.04.0008IPBS
Akhtar, J., Lal, H. C., Kumar, Y., Singh, P. K., Ghosh, J., Khan, Z., et al. (2014). Multiple disease resistant in greengram and blackgram germplasm and management through chemicals under rain-fed conditions. Legume Res. 37, 101–109. doi: 10.5958/j.0976-0571.37.1.016
Alam, S. S., Qureshi, S. H., and Bashir, M. (1985). A report on web blight of mungbean in Pakistan. Pakistan J. Bot. 17:165.
Anonymous (2014). Project Coordinator's Report (mungbean and urdbean), All India Coordinated Research Project on MULLaRP. Indian Institute of Pulses Research. Kanpur, 2013–2014.
Anonymous (2000). Annual Report-AICRP on Pulses. Jaipur: Rajasthan Agricultural Research Institute (Sri Karan Narendra Agriculture University, Jobner), 1–23.
AVRDC (1979). Asian Vegetable Research and Development Centre. Mungbean report for 1975, (Tianan). 18.
AVRDC (1980). Asian Vegetable Research and Development Center. AVRDC Progress Report 1980, (Shanhua).
AVRDC (1981). Asian Vegetable Research and Development Center. AVRDC Progress Report 1981 (Shanhua).
AVRDC (2012). Asian Vegetable Research and Development Center, Mungbean, AVRDC Progress Report 2012, (Shanhua).
Bains, S. S., Dhaliwal, H. S., and Basandrai, A. K. (1988). A new blight of mung and mash in Punjab. Ann. Biol. Ludhiana 4, 113–114.
Bashir, M., Alam, S. S., Qureshi, S. H., and Malik, B. A. (1985). Control of mungbean anthracnose by foliar fungicides. Pakistan J. Agric. Res. 6, 173–175.
Bashir, M., and Malik, B. A. (1988). Diseases of major pulse crops in Pakistan—a review. Trop. Pest Manage. 34, 309–314. doi: 10.1080/09670878809371262
Bhaskar, A. V. (2017). Genotypes against major diseases in green gram and black gram under natural field conditions, A. Vijaya Bhaskar. Int. J. Curr. Microbiol. App. Sci. 6, 832–843. doi: 10.20546/ijcmas.2017.606.098
Bhat, F. A., Bhat, G. N., Anwar, A., and Mohiddin, F. A. (2015). Cost effective strategies for the management of fungal leaf spot of greengram caused by Cercospora canescens Ell. & Mart. under temperate condition of Jammu and Kashmir. Legume Res. 38, 109–114. doi: 10.5958/0976-0571.2015.00018.1
Bhat, F. A., Mohiddin, F. A., and Bhat, H. A. (2014). Reaction of green gram (Vigna radiata) to Cercospora canascens (ELL.) and Mart. Indian J. Agric. Res. 48, 140–144. doi: 10.5958/j.0976-058X.48.2.023
Chaitieng, B., Kaga, A., Han, O. K., Wang, X., Wongkaew, S., Laosuwan, P., et al. (2002). Mapping a new source of resistance to powdery mildew in mungbean. Plant Breed. 121, 521–525. doi: 10.1046/j.1439-0523.2002.00751.x
Chakraborty, S., Tiedemann, A. V., and Teng, P. S. (2000). Climate change: potential impact on plant diseases. Environ. Pollut. 108, 317–326. doi: 10.1016/S0269-7491(99)00210-9
Chand, R., Singh, V., Pal, C., Kumar, P., and Kumar, M. (2012). First report of a new pathogenic variant of Cercospora canescens on mungbean (Vigna radiata) from India. New Dis. Rep. 26:6. doi: 10.5197/j.2044-0588.2012.026.006
Chang, K. F., Ahmed, H. U., Hwang, S. F., Gossen, B. D., Strelkov, S. E., Blade, S. F., et al. (2007). Sensitivity of field populations of Ascochyta rabiei to chlorothalonil, mancozeb, and pyraclostrobin fungicides, and effects of strobilurin fungicides on the progress of ascochyta blight of chickpea. Can. J. Plant Sci. 87, 937–944. doi: 10.4141/CJPS07019
Chankaew, S., Somta, P., Isemura, T., Tomooka, N., Kaga, A., Vaughan, D. A., et al. (2013). Quantitative trait locus mapping reveals conservation of major and minor loci for powdery mildew resistance in four sources of resistance in mungbean [Vigna radiata(L.) Wilczek]. Mol. Breed. 32, 121–130. doi: 10.1007/s11032-013-9856-6
Chankaew, S., Somta, P., Sorajjapinun, W., and Srinives, P. (2011). Quantitative trait loci mapping of Cercospora leaf spot resistance in mungbean, Vigna radiata (L.) Wilczek. Mol. Breed. 28, 255–264 doi: 10.1007/s11032-010-9478-1
Choudhary, S., Choudhary, A. K., and Sharma, O. P. (2011). Screening of mungbean (Vigna radiata) genotypes to identify source of resistant to dry root rot. J. Food Leg. 24, 117–119.
Clarry, S. (2016). The Rise and Rise of Mungbeans. In GroundCover™ Supplement Issue 125 November-December. Grains Research and Development Corporation, 15. Available online at: https://grdc.com.au/resources-and-publications/groundcover/ground-cover-supplements/ground-cover-issue-125-pulse-breeding-advances/the-rise-and-rise-of-mungbeans. (Accessed Apr 4, 2018).
Das, K., Tiwari, R. K. S., and Shrivastava, D. K. (2010). Techniques for evaluation of medicinal plant products as antimicrobial agent: current methods and future trends. J. Med. Plants Res. 4, 104–111. doi: 10.5897/JMPR09.030
Das, S. R., and Narain, A. (1990). Management of powdery mildew of mungbean with fungicides. Indian Phytopath. 43, 100–101.
Deeksha, J., and Tripathi, H. S. (2002). Cultural, biological and chemical control of anthracnose of urdbean. J. Mycol. Plant Pathol. 32, 52–55.
Deshmukh, M. A., Gade, R. M., Belkar, Y. K., and Koche, M. D. (2016). Efficacy of bioagents, biofertilizers and soil amendments to manage root rot in greengram. Legume Res. 39, 140–144. doi: 10.18805/lr.v0iOF.6772
Dubey, S. C. (2003). Integrated management of web blight of urd/mung bean by bio-seed treatment Indian Phytopath. 56, 34–38.
Dubey, S. C., Bhavani, R., and Singh, B. (2009). Development of Pusa 5SD for seed dressing and Pusa Biopellet 10G for soil application formulations of Trichoderma harzianum and their evaluation for integrated management of dry root rot of mungbean (Vigna radiata). Bio. Contr. 50, 231–242. doi: 10.1016/j.biocontrol.2009.04.008
Dubey, S. C., Bhavani, R., and Singh, B. (2011). Integration of soil application and seed treatment formulations of Trichoderma species for management of wet root rot of mungbean caused by Rhizoctonia solani. Pest Manag. Sci. 67, 1163–1168. doi: 10.1002/ps.2168
Dubey, S. C., and Patel, B. (2002). Mass multiplication of antagonists and standardization of effective dose for management of web blight of urd and mung bean. Indian Phytopath. 55, 338–341.
Dutta, S., Singh, R. P., and Jindal, J. K. (2005). Effect of antagonistic bacteria and plant defence activators on management of bacterial leaf spot of mungbean. Indian Phytopath. 58, 269–275.
Dwivedi, R. P., and Saksena, H. K. (1974). Occurrence of web blight caused by Thanatephorus cucumeris on mungbean. Int. J. Farm Sci. 2:100.
Eastburn, D., Degennaro, M., Delucia, E., Dermody, O., and McElrone, A. (2010). Elevated atmospheric carbon dioxide and ozone alter soybean diseases at SoyFACE. Global Change Biol. 16, 320–330. doi: 10.1111/j.1365-2486.2009.01978.x
Ebenezar, E. G., and Yesuraja, I. (2000). Effect of fungal and bacterial antagonist on Macrophomina phaseolina (Tassi) Goid causing root rot in green gram. J. Trop. Agric. 38, 73–76.
Ehteshamul-Haque, S., Abid, M., and Ghaffar, A. (1995). Efficacy of Bradyrhizobium sp., and Paecilomyces lilacinus with oil cakes in the control of root rot of mungbean. Trop. Sci. 35, 294–299.
Farahani, A. S., and Taghavi, M. (2016). Changes of antioxidant enzymes of mung bean [Vigna radiata (L.) R. Wilczek] in response to host and non-host bacterial pathogens. J. Plant Prot. Res. 56, 95–99. doi: 10.1515/jppr-2016-0016
Felde, Z. A., Pocasangre, L. E., Carnizares Monteros, C. A., Sikora, R. A., Rosales, F. E., and Riveros, A. S. (2006). Effect of combined inoculations of endophytic fungi on the biocontrol of Radopholus similis. Info-Musa 15, 12–18.
Fery, F. L. (2002). “New opportunities in Vigna,” in Trends in New Crops and New Uses, eds J. Janick and A. Whipkey (Alexandria: ASHS Press), 424–428.
Flexner, J. L., and Belnavis, D. L. (2000). “Microbial Insectcides,” in Biological and Biotechnological Control of Insect Pests, eds J. E. Rechcigl and N. A. Rechcigl (Boca Raton, FL: CRC Press; Lewis Publishers), 35–56.
Gawande, V. L., and Patil, J. V. (2003). Genetics of powdery mildew (Erysiphe polygoni D.C.) resistance in Mungbean (Vigna radiata (L.) Wilczek). Crop Prot. 22, 567–571. doi: 10.1016/S0261-2194(02)00202-8
Hartman, G. L., Wang, T. C., and Kim, D. (1993). Field evaluation of mungbeans for resistance to Cercospora leaf spot and powdery mildew. Int. J. Pest Manag. 39, 418–421. doi: 10.1080/09670879309371833
Hibberd, J., Whitbread, R., and Farrar, J. (1996). Effect of 700 μmol mol−1 CO2 and infection by powdery mildew on the growth and carbon partitioning of barley. New Phytol. 134, 309–315. doi: 10.1111/j.1469-8137.1996.tb04635.x
Humphry, S. M. E., Magner, T., McIntyre, C. L., Aitken, E. A., and Liu, C. L. (2003). Identification of major locus conferring resistance to powdery mildew (Erysiphe polygoni D.C.) in mungbean (Vigna radiata L. Wiczek) by QTL analysis. Genome 46, 738–744. doi: 10.1139/g03-057
Ikram, N., Dawar, S., Abbas, Z., and Zaki, M. J. (2010). Effect of (60Co) gamma rays on growth and root rot diseases in mungbean (Vigna radiata L.). Pakistan J. Bot. 42, 2165–2170.
Iqbal, S. M., Ghafoor, A., Bashir, M., and Malik, B. A. (1995). Estimation of losses in yield components of mugbean due to Cercospora leaf spot. Pakistan J. Phytopath. 7, 80–81.
Iqbal, S. M., Zubair, M., and Haqqani, A. M. (2004). Resistant in Mungbean to Cercospora leaf spot disease. Int. J. Agric. Biol. 6, 792–793.
Iqbal, U., and Mukhtar, T. (2014). Morphological and pathogenic variability among Macrophomina phaseolina isolates associated with mungbean (Vigna radiata L.) Wilczek from Pakistan. Sci. World J. 2014:950175. doi: 10.1155/2014/950175
Jadhav, M. L., Taur, N., Sapkal, S., Tathe, S., and Quadri, F. (2016). Study on effect of caffeine on growth of Vigna radiata L. Int. J. Adv. Res. 4, 596–602.
Javaid, A., and Amin, M. (2009). Antifungal activity of methanol and n-hexane extracts of three Chenopodium species against Macrophomina phaseolina. Nat. Prod. Res. 23, 1120–1127. doi: 10.1080/14786410802617433
Javaid, A., and Saddique, A. (2011). Management of Macrophomina root rot of mungbean using dry leaves manure of Datura metel as soil amendment. Spanish J. Agric. Res. 9, 901–905. doi: 10.5424/sjar/20110903-394-10
Jhamaria, S. L., and Sharma, O. P. (2002). Management of web blight of mungbean through chemicals and plant product. Indian Phytopath. 55, 526.
Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286
Joshi, A., Souframanien, J., Chand, R., and Pawar, S. E. (2006). Genetic diversity study of Cercospora canescens (Ellis & Martin) isolates, the pathogen of Cercospora leaf spot in legumes. Curr. Sci. 90, 564–568.
Juroszek, P., and von Tiedemann, A. (2011). Potential strategies and future requirements for plant disease management under a changing climate. Plant Pathol. 60, 100–112. doi: 10.1111/j.1365-3059.2010.02410.x
Kapadiya, H. J., and Dhruj, L. U. (1999). Management of mungbean Cercospora leaf spot through fungicides. Indian Phytopath. 52, 96–97.
Kasettranan, W., Somta, P., and Srinives, P. (2009). Genetics of the resistance to powdery mildew disease in mungbean (Vigna radiata (L.) Wilczek). J. Crop Sci. Biotechnol. 12, 37–42. doi: 10.1007/s12892-008-0074-4
Kasettranan, W., Somta, P., and Srinives, P. (2010). Mapping of quantitative trait loci controlling powdery mildew resistance in mungbean (Vigna radiata (L.) Wilczek). J. Crop Sci. Biotechnol. 13, 155–161 doi: 10.1007/s12892-010-0052-z
Kaur, L. (2007). Multiple disease resistant sources of mungbean. Act Hort. 752, 423–426. doi: 10.17660/ActaHortic.2007.752.76
Kaur, L., Singh, P., and Sirari, A. (2011). Biplot analysis for locating multiple disease resistant diversity in mungbean germplasm. Disease Res. 26, 55–60.
Kaushik, C. D., Chand, J. N., and Saryavir (1987). Seedborne nature of Rhizoctonia bataticola causing leaf blight of mungbean. J. Mycol. Plant Pathol. 17, 154–157.
Keatinge, J. D. H., Easdown, W. J., Yang, R. Y., Chadha, M. L., and Shanmugasundaram, S. (2011). Overcoming chronic malnutrition in a future warming world: the key importance of mungbean and vegetable soybean. Euphytica 180, 129–141. doi: 10.1007/s10681-011-0401-6
Kelly, L. (2017). Fusarium Species Associated With Grain Sorghum and Mungbean in Queensland. MS thesis, The University of Queensland.
Kelly, L., White, J., Sharman, M., Brier, H., Williams, L., Grams, R., et al. (2017). Mungbean and Sorghum Disease Update. Grains Research and Development Corporation (GRDC) update paper. Available online at: https://grdc.com.au/resources-and-publications/grdc-update-papers/tab-content/grdc-update-papers/2017/07/mungbean-and-sorghum-disease-update. (Assessed Apr 4, 2018).
Keneni, G., Bekele, E., Getu, E., Imtiaz, M., Damte, T., and Mulatu, B. (2011). Breeding food legumes for resistance to storage insect pests: potential and limitations. Sustainability 3, 1399–1415. doi: 10.3390/su3091399
Khajudparn, P., Wongkaew, S., and Thipyapong, P. (2007). Mungbean powdery resistant identification of genes for resistant to powdery mildew in mungbean. Afr. Crop Sci. Conf. Proc. 8, 743–745.
Khan, A. A., Khan, R. U., and Singh, R. (2005). Management of Cercospora leaf spot and anthracnose diseases of mungbean by fungicides. Ann. Plant Prot. Sci. 13, 465–529.
Khan, K. S. H., and Shuaib, M. (2007). Identification of sources of resistant in mungbean (Vigna radiata L.) against charcoal rot Macrophomina phaseolina (Tassi) Goid. Afr. Crop Sci. Conf. Proc. 8, 2101–2102
Khare, N., Lankpale, N., and Agarwal, K. C. (1998). Epidemiology of powdery mildew of mungbean in Chhattisgarh region of Madhya Pradesh. J. Mycol. Plant Pathol. 28, 5–10.
Khunti, J. P., Bhoraniya, M. E., and Vora, V. D. (2005). Management of powdery mildew and Cercospora leaf spot of mungbean by some systemic fungicides. Legume Res. 28, 65–67.
Khunti, J. P., Bhoraniya, M. F., and Vora, V. D. (2002). Management of Powdery mildew and Cercospora leaf spot of mungbean by some Systemic Fungicides. J. Mycol. Pl. Pathol. 32:103.
Kobayashi, T., Ishiguro, K., Nakajima, T., Kim, H. Y., Okada, M., and Kobayashi, K. (2006). Effects of elevated atmospheric CO2 concentration on the infection of rice blast and sheath blight. Phytopathology 96, 425–431. doi: 10.1094/PHYTO-96-0425
Kulkarni, S. A. (2009). Epidemiology and Integrated Management of Anthracnose of Green Gram. M.Sc. thesis, University of Agricultural Sciences, Dharwad.
Kumar, A., Adarsha, H. S., Shanthala, J., and Savithramma, D. L. (2017). Differential response of F4 and F5 green gram [Vigna radiata (L.) Wilczek] recombinant inbred lines (RILs) to powdery mildew infection. J. Pharmacognosy Phytochem. 6, 1147–1153.
Kumari, R., Shekhawati, K. S., Gupta, R., and Khokhar, M. K. (2012). Integrated management against root rot of mungbean (Vigna radiata L. Wilczek) incited by Macrophomina phaseolina. J. Plant Pathol. Microbiol. 3, 1–5. doi: 10.4172/2157-7471.1000136
Lee, J. H., Han, K. S., Kim, T. H., Bae, D. W., Kim, D. K., Kang, J. H., et al. (2007). Effective heat treatment techniques for control of mungbean sprout rot, incorporable into commercial mass production. Plant Pathol. J. 23, 174–179. doi: 10.5423/PPJ.2007.23.3.174
Lee, Y. B. (1980). Inheritance Study on Resistance to Cercospora Leaf Spot in Mungbean. Shanhua: Asian Vegetable Research and Development Center.
Lonergan, E., Pasche, J., Skoglund, L., and Burrows, M. (2015). Sensitivity of Ascochyta Species Infecting Pea, Lentil, and Chickpea to Boscalid, Fluxapyroxad, and Prothioconazole. Plant Dis. 99, 1254–1260. doi: 10.1094/PDIS-06-14-0620-RE
Luck, J., Spackman, M., Freeman, A., Tre bicki, P., Griffiths, W., Finlay, K., et al. (2011). Climate change and diseases of food crops. Plant Pathol. 60, 113–121. doi: 10.1111/j.1365-3059.2010.02414.x
Maheshwari, S. K., and Krishna, H. (2013). Field efficacy of fungicides and bio-agents against Alternaria leaf spot of mungbean. Ann. Plant Prot. Sci. 21, 364–367.
Mandhare, V. K., and Suryawanshi, A. V. (2008). Dual resistant against powdery mildew and yellow mosaic virus in greengram. Agric. Sci. Digest 28, 39–41.
Mansoor, F., Sultana, V., and Ehteshamul-Haque, S. (2007). Enhancement of biocontrol potential of Pseudomonas aeruginosa and Paecilomyces lilacinus against root rot of mungbean by a medicinal plant Launaea nudicaulis L. Pakistan J. Bot. 39, 2113–2119.
Marappa, N. (2008). Screening of mungbean genotypes and its wild relatives for resistant sources to Cercospora leaf spot disease. Asian J. BioScience 3, 324–326.
Meehl, G. A., Washington, W. M., Collins, W. D., Arblaster, J. M., Hu, A., Buja, L. E., et al. (2005). How much more global warming and sea level rise? Science 307, 1769–1772. doi: 10.1126/science.1106663
Melloy, P., Hollaway, G., Luck, J., Norton, R., and Aitken, E. S. C. (2010). Production and fitness of Fusarium pseudograminearum inoculum at elevated carbon dioxide in FACE. Global Change Biol. 16, 3363–3373. doi: 10.1111/j.1365-2486.2010.02178.x
Meyer, S. L. F., and Roberts, D. P. (2002). Combinations of biocontrol agents for management of plant-parasitic nematodes and soil borne plant-pathogenic fungi. J. Nematol. 34, 1–8.
Mishra, S. P., Asthana, A. N., and Yadav, L. (1988). Inheritance of Cercospora leaf spot resistance in mungbean, Vigna radiata (L.) Wilczek. Plant Breed. 100, 228–229. doi: 10.1111/j.1439-0523.1988.tb00245.x
Murugapriya, E., Alice, D., and Jayamani, P. (2011). Antifungal activity of botanicals and micro-nutrients against Macrophomina leaf blight in mungbean. J. Food Leg. 24, 113–116.
Naimuddin, A. M., and Singh, N. P. (2016). Yellow mosaic of mungbean and urdbean: current status and future strategies. J. Food Leg. 29, 77–93.
Nair, R. M., Götz, M., Winter, S., Giri, R. R., Boddepalli, V. N., Sirari, A., et al. (2017). Identification of mungbean lines with tolerance or resistance to yellow mosaic in fields in India where different begomovirus species and different Bemisia tabaci cryptic species predominate. Eur. J. Plant Pathol. 149, 349–365. doi: 10.1007/s10658-017-1187-8
Nair, R. M., Schalfleitner, R., Kenyon, L., Srinivasan, R., Easdown, W., Ebert, A., et al. (2012). Genetic improvement of mungbean. SABRAO J. Breed. Gen. 44, 177–190.
Nair, R. M., Thavarajah, D., Thavarajah, P., Giri, R. R., Ledesma, D., Yang, R. Y., et al. (2015). Mineral and phenolic concentrations of mungbean [Vigna radiata (L.) R. Wilczek var. radiata] grown in semi-arid tropical India. J. Food Compost. Anal. 39, 23–32. doi: 10.1016/j.jfca.2014.10.009
Pandey, A. K., and Tripathi, N. N. (2011). Aromatic plants of gorakhpur division: their anti-mycotic properties and medicinal value. Int. J. Pharm. Sci. Rev. Res. 7, 142–147.
Pandey, S., Sharma, M., Kumari, S., Gaur, P. M., Chen, W., Kaur, L., et al. (2009). “Integrated foliar diseases management of legumes,” in International Conference on Grain Legumes: Quality Improvement, Value Addition and Trade (Kanpur: Indian Society of Pulses Research and Development, Indian Institute of Pulses Research), 143–161.
Price, P. P., Purvis, M. A., Cai, G., Padgett, G. B., Robertson, C. L., Schneider, R. W., et al. (2015). Fungicide resistance in Cercospora kikuchii, a soybean pathogen. Plant Dis. 99, 1596–1603. doi: 10.1094/PDIS-07-14-0782-RE
Quebral, F. C., and Cowell, R. (1978). “Powdery mildew and Cercospora leaf spot of green gram in philippines,” in First International Greengram Symposium, ed R. A. Cowell (Taiwan: The office of the Information Services), 147–148.
Raghuchander, T., Samiyappan, R., and Arjunan, G. (1993). Biocontrol of Macrophomina root rot of mungbean. Indian Phytopath. 46, 379–382.
Rakhonde, P. N., Koche, M. D., and Harne, A. D. (2011). Management of powdery mildew of green gram. J. Food Leg. 24, 120–122.
Ramakrishnan, C. K. D., and Savithramma, D. L. (2014). Screening of mungbean germplasm for powdery mildew disease Resistant. Int. J. Agronomy Agric. Res. 4, 16–21
Rana, M., Ashiq, R., and Virender, A. (2014). Systemic opposition of green gram against leaf blight caused by Macrophomina phaseolina. Int. J. Mycol. Plant Pathol. 1, 72–77.
Rashid, A., Harris, D., Hollington, P., and Ali, S. (2004). On-farm seed priming reduces yield losses of mungbean (Vigna radiata) associated with mungbean yellow mosaic virus in the North West Frontier Province of Pakistan. Crop Prot. 23, 1119–1124. doi: 10.1016/j.cropro.2004.04.002
Rathore, B. S. (2006). Management of diseases of greengram with fungicides. Indian J. Mycol. Plant Pathol. 36, 138–141.
Reddy, K. S. (2009). Identification and inheritance of a new gene for powdery mildew resistance in mungbean (Vigna radiata L. Wilczek). Plant Breed. 128, 521–523. doi: 10.1111/j.1439-0523.2008.01609.x
Reddy, K. S., Kao, K. C., and Reddy, M. S. (1992). Evaluation of some new fungicides against Rhizoctonia solani Kühn, the incident of damping-off in mungbean. Indian J. Plant Protect. 20, 37–42.
Reddy, K. S., Pawar, S. E., and Bhatia, C. R. (1987). Screening for powdery mildew (Erysiphe polygoni DC) resistance in mungbean (Vigna radiata L. Wilzek) using excised leaves. Proc. Indian Acad. Sci. U.S.A. 97, 365–369.
Reddy, K. S., Pawar, S. E., and Bhatia, C. R. (1994a). Inheritance of powdery mildew (Erysiphe polygoni D.C.) resistance in mungbean (Vigna radiata L. Wilczek). Theor. Appl. Gent. 88, 945–948.
Reddy, K. S., Pawar, S. E., Wanjari, K. B., and Bhatia, C. R. (1994b). “Development of powdery mildews resistant and high yielding varieties of mungbean,” in: International Symposium on Pulses Research (New Delhi), 146–147.
Ryley, M., and Toowoomba Tatnell, J. (2010). Management of the Major Foliar Diseases of Mungbeans and Peanuts in Australia. Kingaroy: Agri-Science Qld © The State of Queensland, Department of Employment, Economic Development and Innovation.
Saravanakumar, D., Harish, S., Loganathan, M., Vivekananthan, R., Rajendran, L., Raguchander, T., et al. (2007). Rhizobacterial bioformulation for the effective management of Macrophomina root rot in mungbean. Arch. Phytopathol. Plant Prot. 40, 323–337. doi: 10.1080/03235400600587326
Satya, V. K., Vijayasamundeeswari, A., Paranidharan, V., and Velazhahan, R. (2011). Burkholderia sp. Strain tnau-1 for biological control of root rot in mungbean (Vigna radiata l.) caused by Macrophomina phaseolina. J. Plant Prot. Res. 51, 273–278. doi: 10.2478/v10045-011-0045-5
Satyagopal, K., Sushil, S. N., Jeyakumar, P., Shankar, G., Sharma, O. P., et al. (2014). AESA based IPM package for Blackgram and Greengram. Hyderabad. 43.
Schafleitner, R., Nair, R. M., Rathore, A., Wang, Y., Lin, C., Chu, S., et al. (2015). The AVRDC – The World Vegetable Center mungbean (Vigna radiata) core and minicore collections. BMC Genomics 16:344. doi: 10.1186/s12864-015-1556-7
Sconyers, L. E., Kemerait, R. C., Brock, J., Phillips, D. V., Jost, P. H., Sikora, E. J., et al. (2006). Asian Soybean Rust Development in 2005: A Perspective from the Southeastern United States. APSnet Features.
Shahbaz, M. U., Iqbal, M. A., Rafiq, M., Batool, A., and Kamran, M. (2014). Efficacy of different protective fungicides against Cercospora leaf spot of mungbean (Vigna radiata l. Wilczek). Pakistan J. Phytopathol. 26, 187–191.
Sharma, M., and Ghosh, R. (2017). “Heat and soil moisture stress differentially impact chickpea plant infection with fungal pathogens,” in Plant Tolerance to Individual and Concurrent Stresses, ed M. Senthil-Kumar (New Delhi: Springer), 47–57.
Sharma, M., Ghosh, R., and Pande, S. (2015). Dry root rot (Rhizoctonia bataticola (Taub.) Butler): an emerging disease of chickpea – where do we stand? Arch. Phytopathol. Plant Prot. 48, 797–812. doi: 10.1080/03235408.2016.1140564
Sharma, M., Tarafdar, A., Ghosh, R., and Gopalakrishanan, S. (2017). “Biological control as a tool for eco-friendly management of plant pathogens,” in Advances in Soil Microbiology: Recent Trends and Future Prospects, Microorganisms for Sustainability, eds T. K. Adhya, B. B. Mishra, K. Annapurna, D. K. Verma, and U. Kumar (Springer), 153–186.
Sharma, O. P., Bambawale, O. M., Gopali, J. B., Bhagat, S., Yelshetty, S., Singh, S. K., et al. (2011). Field Guide Mungbean and Urdbean. New Delhi: National Centre for Integrated Pest Management. M/s Royal Offset Printers A-89/1, Naraina Industrial Area, Phase-I. 40.
Sharma, R., Duveiller, E., and Ortiz-Ferrara, G. (2007). Progress and challenge towards reducing wheat spot blotch threat in the Eastern Gangetic Plains of South Asia: is climate change already taking its toll? Field Crops Res. 103, 109–118. doi: 10.1016/j.fcr.2007.05.004
Shen, Y. M., Liu, H. L., Chang, S. T., and Chao, C. H. (2010). First report of anthracnose caused by Colletotrichum acutatum on mungbean sprouts in Taiwan. Plant Dis. 94:131. doi: 10.1094/PDIS-94-1-0131C
Shukla, V., Baghel, S., Maravi, K., and Singh, S. K. (2014). Yield loss assessment in mungbean [Vigna radiata (L.) Wilczek] caused by anthracnose [Colletotrichum truncatum (schw.) Andrus and moore]. Bioscan 9, 1233–1235.
Siddiqui, A., Ehetshamul-Haque, E., and Shaukat, S. S. (2001). Use of Rhizobacteria in the control of root rot–root knot disease complex of mungbean. J. Phytopathol. 149, 337–346. doi: 10.1046/j.1439-0434.2001.00630.x
Sierotzki, H., and Scalliet, G. (2013). A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology 103, 880–887. doi: 10.1094/PHYTO-01-13-0009-RVW
Singh, G., Sharma, Y. R., Shanmugasundaram, S., Shih, S. L., and Green, S. K. (2004). “Improving income and nutrition by incorporating mungbean in cereal fallows in the Indo-Gangetic Plains of South Asia DFID Mungbean Project for 2002-2004,” in Proceedings of the Final Workshop and Planning Meeting, Status of Mung Bean Yellow Mosaic Virus Resistance Breeding. Ludhiana: Punjab Agricultural University, 27-31 May 2004, 204–213.
Singh, J., Mishra, K. K., and Singh, A. K. (2013a). Current status of web blight of mungbean. Asian J. Soil Sci. 8, 495–504.
Singh, S., Chand, H., and Varma, P. K. (2008). Screening of bioagents against root rot of mungbean caused by Rhizoctonia solani. Legume Res. 31, 75–76.
Singh, S. P., and Singh, S. K. (2014). Sources of resistant in mungbean for Cercospora leaf spot diseases. Ann. Agric. Biosci. Res. 2, 280–281.
Singh, S. P., Singh, S. K., and Shukla, V. (2013b). Fungicidal management of Cercospora leaf spot of mungbean (Vigna radiata). Trends Biosciences 6, 861–863.
Slusarenko, A. J., Patel, A., and Portz, D. (2008). Control of plant diseases by natural products: allicin from garlic as a case study. Eur. J. Plant Pathol. 121, 313–322. doi: 10.1007/s10658-007-9232-7
Sorajjapinun, W., Rewthongchum, S., Koizumi, M., and Srinives, P. (2005). Quantitative inheritance of resistance to powdery mildew disease in mungbean (Vigna radiata (L.) Wilczek). SABRAO J. Breed. Gent. 37, 91–96.
Sujatha, K., Kajjidoni, S. T., Patil, P. V., and Somashekhar, G. (2011). Heterosis for productivity related traits involving diverse parents for powdery mildew reaction in mungbean. J. Food Legumes. 24, 101–105.
Sundaramoorthy, S., Murugapriya, E., Maharaja, L. G. J., and Alice, D. (2013). Induction of systemic resistant in green gram against leaf blight caused by Macrophomina phaseolina (Tassi.) Goid. Afr. J. Microbiol. Res. 7, 3976–3982. doi: 10.5897/AJMR2013.5719
Suryawanshi, A. P., Wadje, A. G., Gawade, D. B., Kadam, T. S., and Pawar, A. K. (2009). Field evaluation of fungicides and botanicals against powdery mildew of mungbean. Agric. Sci. Digest 29, 209–211.
Tandel, D. H., Sabalpara, A. N., Patel, R. C., Prajapati, V. R., and Patel, V. R. (2014). Antagonistic effect on growth and sclerotial formation of Macrophomina phaseolina (Tassi) goid. causing green gram leaf blight. J Life Sci. 11, 89–91
Thilagavathi, R., Saravanakumar, D., Ragupathi, N., and Samiyappan, R. (2007). A combination of biocontrol agents improves the management of dry root rot (Macrophomina phaseolina) in greengram. Phytopathol. Mediterranea 46, 157–167. doi: 10.14601/Phytopathol_Mediterr-2147
Thompson, G. B., Brown, J. K. M., and Woodward, F. I. (1993). The effects of host carbon dioxide, nitrogen and water supply on the infection of wheat by powdery mildew and aphids. Plant Cell Environ. 16, 687–694. doi: 10.1111/j.1365-3040.1993.tb00487.x
Tiwari, A. (1993). Studies on the Diseases Caused by Rhizoctonia Solani Kuhn in Green Gram (Phaseolus aureus Roxb). Ph.D. thesis, Rani Durgavati Vishwavidyalaya (Jabalpur), 338.
Tiwari, A., and Khare, M. N. (1998). Variability among isolates of Rhizoctonia solani infecting mungbean. Indian Phytopath. 51, 334–337.
Uddin, M. N., Bakr, M. A., Islam, M. R., Hossain, M. I., and Hossain, A. (2013). Bioefficacy of plant extracts to control Cercospora leaf spot of mungbean (Vigna radiata). Int. J. Agric. Res. Innov. Technol. 3, 60–65. doi: 10.3329/ijarit.v3i1.16094
Vallad, G. E., and Goodman, R. M. (2004). Systemic acquired resistance and induced systemic resistance in conventional agriculture: review and interpretation. Crop Sci. 44, 1920–1934. doi: 10.2135/cropsci2004.1920
Veena, Y. R. H., Math, G., and Kumar, A. G. V. (2013). Bioefficacy of fungicides against Cercospora canescens causing leaf spot of greengram. Crop Res. 46, 74–78.
Viaene, N. M., and Abawi, G. S. (2000). Hirsutella rhossiliensis and Verticillium chlamydospdoiorium as biocontrol agents of the root-knot nematode Meloidogyne hapla on lettuce. J. Nematol. 32, 85–100.
Walters, D. R., Paterson, L., Walsh, D. J., and Havis, N. D. (2009). Priming for plant defense in barley provides benefits only under high disease pressure. Physiol. Mol. Plant Pathol. 73, 95–100. doi: 10.1016/j.pmpp.2009.03.002
Wongpiyasatid, A., Chotechuen, S., Hormchan, P., and Srihuttagum, M. (1999). Evaluation of yield and resistance to powdery mildew, Cercospora leaf spot and cowpea weevil in mungbean mutant lines. Kasetsart J. 33, 204–215.
Yadav, D. L., Jaisani, P., and Pandey, R. N. (2014a). Identification of sources of resistant in mungbean genotypes and influence of fungicidal application to powdery mildew epidemics. Int. J. Current Microbiol. Appl. Sci. 3, 513–519.
Yadav, D. L., Pandey, R. N., Jaisani, P., and Gohel, N. M. (2014b). Sources of resistant in mungbean genotypes to Cercospora leaf spot disease and its management. African, J. Agric. Res. 9, 3111–3114.
Yadav, R. J., Kakraliya, S. S., Bajiya, M. R., and Abrol, S. (2017). Eco-Friendly management of powdery mildew of green gram (Vigna radiata L.). Int. J. Curr. Microbiol. App. Sci. 6, 435–439 doi: 10.20546/ijcmas.2017.607.052
Yaqub, F., and Shahzad, S. (2009). Effect of solar heating by polyethylene mulching on sclerotial viability and pathogenicity of Sclerotium rolfsii on mungbean and sunflower. Pakistan J. Bot. 41, 3199–3205.
Young, N. D., Danesh, D., Menancio-Hautea, D., and Kumar, L. (1993). Mapping oligogenic resistance to powdery mildew in mungbean with RFLPs. Theor. Appl. Gent. 87, 243–249. doi: 10.1007/BF00223772
Zhang, J. Q., Zhu, Z. D., Duan, C. X., Wang, X. M., and Li, H. J. (2011). First report of charcoal rot caused by Macrophomina phaseolina on mungbean in China. Plant Dis. 95:872. doi: 10.1094/PDIS-01-11-0010
Keywords: mungbean, fungal diseases, quantitative trait loci, host resistance, disease management
Citation: Pandey AK, Burlakoti RR, Kenyon L and Nair RM (2018) Perspectives and Challenges for Sustainable Management of Fungal Diseases of Mungbean [Vigna radiata (L.) R. Wilczek var. radiata]: A Review. Front. Environ. Sci. 6:53. doi: 10.3389/fenvs.2018.00053
Received: 20 December 2017; Accepted: 25 May 2018;
Published: 19 June 2018.
Edited by:
Andries B. Potgieter, The University of Queensland, AustraliaReviewed by:
Rao Chenchu Rachaputi, The University of Queensland, AustraliaPrakit Somta, Kasetsart University, Thailand
Raju Ghosh, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), India
Copyright © 2018 Pandey, Burlakoti, Kenyon and Nair. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Rishi R. Burlakoti, rrburlakoti@gmail.com
†Present Address: Rishi R. Burlakoti, Agriculture and Agri-food Canada, Agassiz, BC, Canada