Karnal Bunt (Neovossia indica) of Wheat, a review: Part 1

[Editorial Note: This paper presentation has been posted directly from an author-supplied computer file with only minimal editing from APS. Please contact the authors if you have questions.]

S. Nagarajan, S.S. Aujla, G.S. Nand, I. Sharma, L.B. Goel, J. Kumar 1 and D.V. Singh 3 1. Directorate of Wheat Research, P. Box 158, Karnal, India
2. Punjab Agriculture University, Ludhiana and
3. Indian Agriculture Research Institute, New Delhi

Contents:
I. Introduction
II. Economic importance
III. Taxonomic position
IV. Symptoms and histopathology
V. Soil bank
VI. Teliospore nature
VII. Teliospore germination

In Part Two
VIII. Microsporidia
IX. Dispersal from soil level to ear head
X. Proliferation inside ear head and ovary
XI. Levels of host-pathogen interaction
XII. Evaluating host resistance
XIII. Physiological specialization
XIV. IPM approaches

In Part Three
XV. Host resistance to KB
XVI. Predicting KB severity
XVII. Varietal resistance
XVIII. Seed certification
XIX. Quarantine
XX. Chemical control

In Part Four
XXI. Summary (and Notes)

Wheat (Triticum aestivum) is grown in India during the mild winter months of November to April. During 1995, from 24.0 m ha nearly 63 m tons of wheat were harvested. The widespread occurrence of Karnal bunt (KB) of wheat caused by Neovossia indica (Mitra) Mundkur, affects the quality of wheat grain. The KB was first detected in 1931 at Karnal (Haryana) and hence the name Karnal bunt (Mitra, 1931). The disease is known by varied names as kernal smut, Karnal bunt, partial bunt etc., and is native to South Asia. The disease is all over northwest India in an endemic form and occurs in traces of severity over a larger part of South Asia (Warham 1986). Besides India and Pakistan, KB is reported from Syria (Williams, 1983), Afghanistan, Mexico (Joshi et al. 1983), and Nepal (Singh et al. 1989).

Since 1931, KB appeared several times infecting the native wheats grown over northwestern India. The disease remained less damaging till 1970, and subsequently, severe epidemics started occurring, coinciding with the change over to high yielding irrigated, semidwarf and high fertilizer input farming. In India, KB occurs in the states of Punjab, Haryana, Jammu and Kashmir, Himachal Pradesh, Uttar Pradesh, Delhi, Rajasthan, and Bihar. The disease is endemic in Gurdaspur, Hoshiarpur, Jalandhar and Ropar districts (the sub-mountainous tracts) of Punjab, India and along the rivers and canal network of Satluj and Beas. (Gill et al, 1993).

ECONOMIC IMPORTANCE:

Brennan et al (1990) estimated the economic losses from Karnal bunt of wheat in Mexico. The direct quality and seed export losses were estimated about 0.12 per cent per year in northwestern Mexico. Indirect losses were those associated with the measures aimed to prevent the spread of Karnal bunt and to reduce the severity. This includes quarantine restrictions on planting in Karnal bunt infected areas, grain fumigation and restrictions on planting in Karnal bunt in infected grain fumigation seed. Thus the total losses (direct and indirect) due to Karnal bunt in Mexico was estimated to be US $ 7.02 million per year. No such information is available for India or Pakistan. More than the tonnage reduction and loss of grain quality the quarantine related procedural wrangles create trade barriers.

TAXONOMIC POSITION:

Tilletia indica, the causal agent of KB as described by Mitra (1931) was transferred to the genus Neovossia by Mundkur (1940) since the pathogen produces numerous independent sporidia. Based on detailed taxonomic study (Munjal, 1990) and Krishna and Singh (1982) justified the placement of N. indica under Neovossia. However, western science literature prefers to designate the KB causal agent as Tilletia indica (Duran and Fisher, 1961; Duran, 1972). The N. indica is pathogenic to T. aestivum, T. durum, T. boeticum, T. ovatum, T. variabilis and T. shareo nensis. Triticale and under artificial inoculations even Aegilops spp. are susceptible (Dhalival, 1986; Royer et al, 1986 and Warham et al, 1986).

SYMPTOMS AND HISTOPATHOLOGY:

Karnal bunt is a disease of the seed and symptoms become evident only when the grain fully develops. The pathogen converts the infected ovary into a sorus where a mass of dark brown colored teliospores are produced. If the host is vulnerable and the environment favorable, the entire grain turns into a sorus. During threshing the teliospores get released, and the severely infected grain gets blown off. In partially infected grain the embryonic tissue is not invaded and such KB infected seed do germinate and produce a weak plant that has poor survival chances. The infected grain emits a fishy odor due to trimethylamine and the wheat products from severely KB infected grain are unpalatable (Sekhon et al, 1980; Singh and Bedi, 1985).

In a stool, all the ear-heads do not get infected nor do all the grains in a spike. In fact, it gives a general impression as though fields, ear-head and grain are affected randomly. But in fact, partially infected grain occur a cluster of spikelets and in a cluster within the ear-head. In a standing wheat crop, the infected spike can be detected by the shining silvery black spikelets, with glumes spread apart, and swollen ovaries. The infected ears emit a foul smell, trimethylamine, a volatile compound, produced due to pathogenesis. Once the spikelet gets infected by the pathogen, the mycelium slowly moves within the earhead infecting the adjoining spikelets and produce partially infected grains (Dhaliwal et al. 1983).

Generally, endosperm and the dorsal side of the seed remain unaffected. Recently, Cashion and Luttrell (1988) have demonstrated that the pathogen does not invade the embryo and the mycelial growth is limited to the pericarp. Transmission electron microscope (TEM) study shows that the mycelium proliferates in the pericarp by disintegrating the middle layers of parenchymatous cells and prevents the fusion of the outer and inner layers of pericarp, with the seed coat. The mycelial mat forms a compact hymenium-like structure and gives rise to short, septate stalks that bear single teliospores (Roberson and Luttrell, 1987). Mycelial growth ruptures the connection between the pericarp tissue surrounding the vascular bundle in the bottom of adaxil groove in the pericarp and the nuclear projection along the length of the developing seed. The consequence is atrophy of the seed through disruption of normal flow of nutrients from the pericarp and it starves first the endosperm and then the embryo. The endosperm is shrunken to varying degrees and normally the embryo is not infected or damaged excepting under very severe infection.

SOIL BANK:

During harvesting and thrashing the KB infected grains release the teliospores and contaminate the soil and seed. Since the soilborne primary inoculum is the source for the annual recurrence of the disease, a procedure was developed to quantify the teliospore population in soil (Datnoff et al 1986). In has been observed that in many fields of Punjab the teliospore density is 5 × 10(^3) to 16 × 10(^3) per 250 g of soil. This indicates that teliospore availability is not a limiting factor in the recurrence of KB. The soil borne teliospores have dormancy and retain their viability for more than eighteen months at 5-cm depth. Year old teliospores germinate better in compost, grain extract medium and even in plain water in 2-3 weeks time. The teliospores in soil remain viable for more than 5 years. Nagarajan (1991) was of the view that the teliospores lose their viability at extreme low (below freezing) and high temperatures. The argument stems from the fact that the disease rarely occurs in the irrigated areas bordering the Indian Thar desert. The fringes of the desert, being dry and hot, reduce teliospores viability. Similarly KB does not occur at elevations above the snow line in the Himalaya, where thawing and snowing occur in a weave, several times during the winter months. Such extreme conditions are in close proximity of the KB endemic areas, and have remained free from the disease.

TELIOSPORE NATURE:

Teliospores are globose to subglobose in shape, 22-49 microns in size, reticulate with spines and are surrounded by a thick cover sheath (2-4 microns). Teliospore morphology shows that there are three distinct layers. The perisporium or sheath is a fragile, fractured structure and is easily identifiable under the electron microscope. The epispore is reticulate and has numerous curved spines (Khanna et al, 1966). The mature teliospore is diploid (2n) and at the time of germination of the nucleus divides meiotically and then mitotically to produce haploid primary sporidia. According to Fuentes and Duran (1986) meiosis occurs at germination followed by a series of mitotic divisions in teliospores, promycelia or both, which produce numerous haploid nuclei in the promycelia. Using transmission electron microscopy it has been noted that several mitotic divisions followed by meiosis occur in the teliospores. In these studies the mean F-DNA content of filiform primary sporidia was 0.115 arbitrary units. The mean F-DNA content of the binucleate teliospore initials was 0.217 arbitrary units, that of post fusion nuclei 0.473 arbitrary units. Apparently DNA replication in the teliospores initially occurred before nuclear fusion.

TELIOSPORE GERMINATION:

The teliospore enables the pathogen to survive during the hot dry summer months of May and June when maximum temperature exceeds 45 degrees C. Fresh teliospores have dormancy and can be broken by exposing them to 40-43 degrees C under direct sunlight for 18 days or more (Krishna and Singh 1982, 1983). Soaking the teliospore in peptone or wheat straw extract, benzaldehyde, furfuraldehyde, butyric acid are all reported to influence dormancy and the germinability of teliospores. Even after this only 50% of the teliospores germinate in plain water, compared to just 2% germination of fresh teliospores kept in darkness at 20 degrees C (Aujla et al 1986). If teliospores are buried deep in soil they retain germinability for two years. By keeping the teliospore at 15-20 degrees C for 10-15 days the germination can be enhanced and by subjecting the spores to various treatments, teliospore dormancy gets broken permitting a free and better germination (Smilanick et al. 1985). The stout promycelium measures 10-190 microns long and 6-13 microns broad and produces a cluster of 60-185 primary sporidia at the tip. These sensitive, short lived sporidia germinate in free water and produce a thick mycelial mat. Subsequently, from the cushion-like structure, crescent shaped allantoid spores or secondary sporidia and produced. The primary sporidia occasionally exhibit yeast-like tendencies, to bud and produce a crop of allantoid spores on wet leaf surfaces. Depending on temperature and availability of free water the pathogen follows different pathways, to produce crops of spores (Dhaliwal, 1989; Dhaliwal and Singh, 1989; and Smilanick et al 1989).