Blast Disease of Millets: Present Status and Future Perspectives

*T. Tharana Poonacha, C.H. Sai Bhavana, Farooqkhan, G.V. Ramesh, Netravati Gavayi, Prasanna S. Koti, K.B. Palanna, H. Rajashekara, G. Rajesh and I.K. Das*

### **Abstract**

Millet crops are affected by various biotic and abiotic stresses. Among biotic stresses, blast disease caused by *Pyricularia grisea* (finger, pearl and proso millets) and *Pyricularia setariae* (foxtail millet) is the most devastating and widespread disease that causes substantial grain and forage yield losses and is a key constraint to pearl millet, finger millet and foxtail millet production in most of finger millet growing areas, and recently, it is also reported in barnyard millet in few locations. This book chapter emphasizes mainly on occurrence, distribution, symptoms, yield loss, etiology, genetic diversity, mode of spread of the pathogen and survival and integrated disease management approaches for mitigating of disease. This information will be highly helpful for better understanding of the disease. Further, it will be useful to enhance production and productivity of millets and to reinforce the food and nutritional security in the developing countries of Asia and Africa continents where the millets are mainly grown as staple food crops.

**Keywords:** millet, blast, *Pyricularia*, management and novel strategies, blast disease resistances

#### **1. Introduction**

Millets are small-seeded cereal crops widely known for its nutraceutical importance as well as food and fodder. The most frequently cultivated millets are sorghum (*Sorghum bicolor* L. Moench), finger millet (*Eleusine coracana* (L.) Gaertn.), foxtail millet (*Setaria italica* (L.) P. Beauvois), pearl millet (*Cenchrus americanus* (L.) Morrone.), kodo millet (*Paspalum scrobiculatum* L.), little millet (*Panicum sumatrense* Roth ex Roem. and Schult.), proso millet (*Panicum miliaceum* L.), browntop millet (*Brachiaria ramosa* (L.) Stapf) and barnyard millet (*Echinochloa crusgalli* (L.) P. Beauvois). In India, millets are cultivated for both grain and fodder. Though millets are regarded as hardy crops, present day climate change has rendered most of them susceptible to many pathogens.

Many diseases of millets regularly appear in a severe form under different climatic conditions and cause considerable economic loss, while others appear sporadically in specific climatic situations and have less damaging effect to the crop. Fungal diseases

are more than bacterial and viral diseases. Important fungal diseases of millets are grain mold, ergot, smut, anthracnose, downy mildew, blast, rust, charcoal rot, foot rot, banded sheath blight and sheath rot. The diseases infect different plant parts including root, stem, leaves, peduncle or grain and adversely affect yield and quality of the produce. These diseases assume different significances for seed production, certifications and marketing of millets.

Among all these diseases, blast is a serious disease of millets especially in finger millet, pearl millet and foxtail millet. It is caused by the fungi, *Pyricularia grisea* (finger, pearl and proso millets) and *Pyricularia setariae* (foxtail millet). In finger millet crop is affected at all stages of its growth, and the disease is diagnosed by the production of elliptical- or diamond-shaped lesions on the leaf, peduncle and fingers, depending on the stage of the crop. The most damaging stage is neck blast, followed by finger and leaf blast. In foxtail millet, barnyard millet, proso millet and pearl millet symptoms are confined to only leaf. Moderate temperature, high humidity, cloudy days with intermittent rainfall conditions are ideal for the quick disease spread. The disease occurs almost every year in most of the finger millet and foxtail millet growing areas during rainy season, and in other millets, the disease is confined to specific location. The yield loss varies depending on the time of onset of the disease, severity, plant variety and prevailing weather.

#### **1.1 Blast**

Blast caused by *Pyricularia* spp. is one of the serious threats and most destructive disease that occurs widely in major millet growing regions of world. It is the major production constraints under natural conditions especially in finger, pearl and foxtail millet cultivation causing considerable economic losses with varying degrees of damage. In India, the finger millet blast was first reported from Tanjore delta of Tamil Nadu [1]. While foxtail millet blast was recorded in 1917 by Nishikado from Japan [2], but in India, it was reported in 1919 from Tamil Nadu [1], which further has also been recorded from Maharashtra, Andhra Pradesh [3] and Uttarakhand [4]. Since 1970, blast disease in pearl millet has been prevalent in major growing states of India; increased incidence has been reported recently in most pearl millet growing states like Gujarat, Uttar Pradesh, Madhya Pradesh, Rajasthan, Delhi, Maharashtra and Karnataka [5]. The disease is prevalent in all the major millet growing areas and spreading to new location as well with emerging pathotypes showing varying intensities depending on the cultivar, favorable conditions and production techniques.

#### **1.2 Etiology**

*Pyricularia grisea* (Cooke.) Sacc. [Perfect stage: *Magnaporthe grisea* (Herbert) Barr] causing blast in finger and proso millet whereas *Pyricularia setariae* Y. Nisik. infects foxtail millet. Kulkarni and Patel [6] grouped *P. setariae* into four physiological races on the basis of physiological, cultural, morphological characters and pathogenic ability of the fungus. However, Gaikwad and D′ Souza [7] determined that the isolates of *P. setariae* that infect foxtail millet differ from those that infect rice, finger millet and pearl millet. In case of pearl millet, *Pyricularia grisea* is known to cause blast disease in pearl millet. However, recently Singh et al. [8] reported that the foliar blast of pearl millet in western arid Rajasthan, India, is caused by *Pyricularia pennisetigena.*

#### **1.3 Diagnostic symptoms**

Blast pathogen can infect all the stages of plant in both finger and foxtail millet, the young seedlings are more prone for the attack and showed burnt appearance in nursery under severe infection [9]. In finger millet, *P. grisea* attacks at different growth stages of the crop and leads to formation of typical symptoms like leaf blast, neck blast and finger blast while in case of foxtail millet, *P. setariae* attacks the leaf lamina producing leaf blast symptoms [10–13].

On leaf lamina, the pathogen produces typical symptoms of water-soaked, spindle- or diamond-shaped lesions which are initially surrounded by chlorotic halo. Typical leaf blast symptoms are the formation of elliptical- or diamond-shaped lesions containing grayish center with dark brown margins. Under severe infection, adjacent lesions enlarge and may coalesce to form large necrotic areas which gives the crop burnt appearance from far. The pathogen infects and develops lesions on the leaf, peduncle and finger depending on the stage of the crop. The most devastating stage of finger millet blast is neck blast, in which the pathogen targets the neck region, reducing the number and weight of grain per earhead and leading in earhead sterility [14]. In this, neck portion of 2–4 inches below the ear immediately turns initially brown and later to black, where olive gray fungal growth can be observed in the blackened portion under high humid climate. In finger blast where the pathogen attacks fingers, *i.e.,* attacks usually the apical portions running towards the base (**Figure 1**). Infection of finger blast results in shriveled and blackened seeds which makes unfit for seed purpose and human consumption because of loss of minerals and vitamins. Ramakrishnan [15] observed spindle-shaped dark brown leaf spots 1–3 mm in length with grayish center and brownish periphery on finger millet, rice and *Digitaria* spp. leaves*.*

Symptoms of foxtail millet leaves mainly developed as from a small water-soaked yellowish dot, which later turned circular to an oval spot with a grayish center surrounded by a brown margin. Spots measured an average 2–5 mm in diameter within 2–3 days. The spots then coalesce and resulted in drying of leaves. The disease starts with the lower leaves and extend to upper leaves. No symptoms were observed on neck of foxtail millet [16]. Sharma *et al.* [17] observed blast disease symptoms on

#### **Figure 1.**

*Typical blast disease symptoms of millets a&b) leaf blast of finger millet, c&d) neck blast of finger millet, e & f) finger blast of finger millet, g&h) blast of foxtail millet, i) blast of barnyard millet and blast of pearl millet.*

foxtail millet leaves as tiny circular spots with gray-colored centers measuring 3–5 mm in diameter surrounded by a brown margin and also observed high disease severity in dense plant stand with moist condition.

In barnyard millet, the symptoms appear on the young seedlings under the field conditions. The spots are spindle to circular shaped with varying sizes. Initially the spots showed yellowish margin with grayish center. Later, the centers turned ash colored. Fungus develops an olive-gray overgrowth at the center of the spots under humid conditions [10].

#### **1.4 Mode of spread and survival**

The blast fungus, *Pyricularia,* can invade the host either by piercing the epidermal cells directly or through stomatal opening. Pyriform air borne conidia serves as both primary and secondary source of inoculum. The pathogen survives on infected host species or on weed hosts.

#### **1.5 Host range**

Finger millet, proso millet, foxtail millet, pearl millet, rice and wheat, etc., are infected with the pathogen. Nagaraja *et al.* [18] described that *P. grisea* isolated from finger millet possess the potential to infect rice crop but not *vice-versa*. Likewise, *P. setariae* isolated from foxtail millet shows the ability to infect finger millet, pearl millet, wheat and *Dactyloctaenium aegyptium* [19].

Mackill and Bonman [20] proposed that diverse weed hosts growing adjacent to the cultivated plants could serve as possible sources of inoculum for the disease, providing the fungus with an alternate method of survival. Despite the fact that blast infects a wide variety of sympatric flora Hamer *et al.* [21] and Valent *et al*. [22] determined that *M. grisea* populations are strongly confined by host range. Under experimental conditions, inoculations of rice with isolates of from weeds resulted in successful [20] and unsuccessful [23] cross-inoculations. Viji *et al.* [24] reported that in the laboratory, ten isolates of *M. grisea* from rice did not infect finger millet and vice versa, confirming that the *M. grisea* populations infecting rice and fibger millet in India were distinct. Similar results were reported by Kato et al. [25] and Todman *et al*. [26], who found that *Magnaporthe* isolates from *Eleusine coracana* failed to incite disease on rice and vice versa. Contradictory results were reported by Kumar and Singh [27] which could be attributed to prevailing environmental conditions during the experiments and the soil's nutritional level [28, 29].

*Pennisetum* is a diverse genus with over 100 species [30]. Susceptibility of all the species of *Pennisetum* to *Magnaporthe grisea* infection is not yet clear. The available information indicates that the pathogen infects principally *Pennisetum glaucum*, *P. macroforum, P. squamulatum*, *P. pedicellatum* [31], *P. ciliare* [32], *P. purpureum* [33]. Other graminaceous hosts such as *Agrostis palustris*, *Brachiaria mutica*, *Eleusine indica, Cyperus rotundus*, *Eragrostis* sp., *Panicum miliaceum* serve as collateral hosts for the pathogen [34].

#### **1.6 Epidemiology**

The crop is susceptible to the blast disease during all stages of its growth, *i.e.,* seedling (vegetative) to grain formation (reproductive) stage. Especially, young seedlings more prone to the blast both in the nursery and field conditions with favorable weather [35]. Moderate temperature (25–30°C) with high relative humidity (>90%)

and cloudy days coupled with intermittent rainfall creating continuous leaf wetness for more than 10 hr. are congenial for rapid development and spread of the disease. Continuous rains during heading lead to the occurrence of finger blast, resulting in massive production losses in both finger and foxtail millet. Also, high nitrogen fertilizer application is reported to increase blast disease [36].

#### **1.7 Economic importance**

Finger millet blast is economically one of the most important diseases, while blast of proso and foxtail millet are relatively of minor occurrence. The disease occurs almost every year in finger millet during rainy season, and losses vary with the time of onset of the disease, severity, cultivar and climatic conditions. During late 1970s to 80s, 1% incidence of finger and neck blast by *M. grisea* resulted in a corresponding enhancement of yield losses by 0.32 and 0.084% for neck and finger blast, respectively. Grain yield losses in finger millet, on the other hand, ranged from 6.75 to 87.5% [37]. In its severe form, foxtail millet blast can lead up to 30–40% loss of economic yield [10] while mean yield loss of finger millet blast ranged from 28 to 36% and may go up to 90% in endemic areas with frequent disease [38]. In pearl millet also the blast disease causes considerable yield loss under favorable environmental conditions (**Table 1**).

### **1.8 Disease cycle**

The pathogen harbors in glumes, straw as well as on some graminaceous weeds. The blast pathogen is seed-borne with presence of inoculum in the pericarp and endosperm [19]. Blast fungal life cycle is complex due to its nature of disease which shows sensitivity to the weather conditions, survival and spread inoculum in different ways. During off-season, i.e., in the absence main host, it survives on the graminaceous weeds as collateral hosts who provides the primary inoculum for onset of infection. Further, the fungus spreads mainly by airborne conidia and occasionally through seeds.

#### **1.9 Characterization of the pathogen**

For proper diagnosis of the disease, the understanding of the pathogenic characteristics is needed as much of knowing symptomatology and disease cycle. Blast


#### **Table 1.**

*Yield loss caused by blast disease in different crops.*

caused by the *Pyricularia* spp. is identified based on its above-described symptoms in the field while *in vitro,* pathogen characterized based on cultural-morphological and molecular attributes. Morphological characterization includes studying mycelial features on agar plates, viz. appearance, color and amount of melanin pigment produced as well as the microscopic conidial characters. Molecular characterization of pathogen includes amplification of targeted genomic regions with fungal universal primers (*ITS)* as well as secondary barcoding regions such as *beta tubulin*, *TEF* and *LSU* and also by studying the DNA polymorphism using various molecular markers [46].

#### **1.10 Morphology**

*M. grisea* is a haploid, filamentous *Ascomycete* with morphological traits such as three-septate fusiform ascospores and black nonstromatic perithecia (ascocarp) with long hairy necks. The asexual stage *Pyricularia grisea* produces Conidia which are pyriform to obclavate, narrowed towards tip, rounded at the base, solitary, 2-septate, hyaline to pale brown, with a distinct basal hilum, sometimes with marginal frill. Studies on growth of *P. penniseti* on different media by Lukose *et al.* [47] indicated medium containing pearl millet leaf extract enriched with dextrose supported maximum growth of the pathogen. Light brown submerged growth was observed in potato dextrose agar medium, while pearl millet leaf extract medium showed grayish white superficial growth. Konda [48] tested effect of ten different solid media on growth of *P. setariae* and reported that maximum radial growth was observed in oat meal agar, PDA and malt extract agar followed by host leaf decoction +2 per cent sucrose agar medium. *M. oryzae* isolates were producing dull white to grayish-black colonies with regular margins. Conidia were pyriform, hyaline to pale olive and measured 16–23 x 4–7 μm in size [49].

Based on cultural and conidial variation, Viji *et al.* [24] differentiated *Pyricularia* isolates from different hosts. Sonah *et al.* [50] investigated that the cultural morphological variability of *M. grisea* isolates isolated from rice and other hosts and discovered that isolates with fast vegetative growth have gray-green or gray-white producing more spores than those with slower vegetative growth (submerged or subdued growth patterns). Isolates from non-rice hosts also have aberrant spore morphology, with longer, cylindrical and obpyriform spores. They also noticed a fair to good diversity in cultural and conidial characteristics among 17 field isolates of pearl millet [51].

#### **1.11 Genetic diversity**

Lot of information is available on variation among isolates of *Pyricularia* infecting various hosts like cereals and grasses. The pathogen is well studied in rice and is unfathomed in millets. The *Magnaporthe grisea* repeat sequence MGR586 was commonly used for studying population genetics of rice. Similarly fungal repetitive DNA or transposable elements are widely used for the purpose. The molecular level studies indicate the presence of variations among the isolates within or across the hosts. Several researchers have used molecular markers like RFLP [52] and SSR [53] and grouped the Indian isolates of *M. grisea* into two distinct populations—one finger millet group and other foxtail and rice group. Shivakantkumar et al. [51]. reported significant genetic variation among 17 *M. grisea* isolates infecting pearl millet with ITS, inter simple sequence repeats (ISSR) and simple sequence repeats (SSR) markers.

#### **1.12 Mating type**

Sexual reproduction is known to be a significant source of genetic variation in many fungi. Sexual compatibility in *M. grisea* is determined by the presence of two alleles (idiomorphs) at a single mating-type locus designated MAT1.1 and MAT1.2. MAT1.1 and MAT1.2 of *M. grisea* have been cloned and sequenced using a genomic subtraction strategy. The perfect stage of *P. grisea* was first described by Hebert [54] in crosses between isolates from cereals and wild grasses. Since then, efforts have been made to produce perithecia successfully on artificial media under controlled conditions using hermaphroditic tester isolates from finger millet and rice. Although both mating types have been found in the same field at the same time. However, it has not yet been possible to observe the perfect state in nature. The mating type assay *Magnaporthe* population infecting millets revealed that the matingtypes, male fertile, female fertile and hermaphrodite nature of fertility existed finger, foxtail and branyard millet in the country. Which indicates the possibility of sexual recombination in field level and which may lead to high variability in pathogenicity and diversity in *Magnaporthe* population adapted to millets in India. All the tested isolates of pearl millet showed unknown fertility in PCR assay with MAT primers. It indicates fertility of pearl millet isolates has to be confirmed using range of tester isolates [55].

## **2. Management strategy**

The integrated management strategies as well as novel approaches need to be adopted for the management of blast disease in millets. The integrated disease management strategies (**Figure 2**) for mitigating of millet blast are as follows.

#### **2.1 Cultural practices**

Several agricultural practices such as timely sowing, maintaining optimum plant populations and spacing, timely weeding, balanced use of fertilizers, crop rotation, deep plowing during summer season, removal of crop residues from the field, cleaning of field bunds after crop season, uprooting the diseased plant from the field and burning, regulating irrigation water from entering into other field, *etc*., will help in reducing chances of disease occurrence.

#### *2.1.1 Adjustment of date of sowing*

The choice of sowing date in relation to crop disease has one principal aim to reduce to a minimum the period over which infective agent meets the susceptible stage of the host. Early sowing reduces blast severity.

#### *2.1.2 Optimization of plant population*

Due to high plant density, humidity in the field is always high, temperature is low, there is lack of aeration, and pathogen grows rapidly. Maintaining optimal plant population in the field to reduce the relative humidity build up in the field help in reducing disease severity.

**Figure 2.**

#### *Integrated disease management strategies of millet blast.*

### *2.1.3 Use of disease-free seeds*

Use of pathogen free seeds is a pre-requisite of eco-friendly control of plant disease because numerous plant pathogens are transmitted to the field *via* infected or contaminated seeds and seedlings.
