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A review of the impact of charcoal rot (Macrophomina phaseolina) on sunflower

Published online by Cambridge University Press:  01 June 2012

S. IJAZ,
H. A. SADAQAT and
M. N. KHAN
S. IJAZ*
Affiliation:
Centre of Agricultural Biochemistry and Biotechnology (CABB), University of Agriculture, Faisalabad, Pakistan
H. A. SADAQAT
Affiliation:
Department of Plant Breeding and Genetics, University of Agriculture, Faisalabad, Pakistan
M. N. KHAN
Affiliation:
Ayub Agriculture Research Institute (AARI), Faisalabad, Pakistan
*
*To whom all correspondence should be addressed. Email: siddraijazkhan@yahoo.com
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Summary

Charcoal rot, caused by Macrophomina phaseolina, is the most prevalent and important disease of crop plants such as sunflower. Although it is monotypic and no physiological races have been reported, it has high genetic variability resulting in a wide host range, which in turn means that crop rotation is not an effective strategy to combat the disease. The current paper reviews the adverse effects of this disease and summarizes the present state of knowledge about charcoal rot severity and its impact on crop production.

Information

Type
Crops and Soils Review
Information
The Journal of Agricultural Science , Volume 151 , Issue 2 , April 2013, pp. 222 - 227
Copyright
Copyright © Cambridge University Press 2012

INTRODUCTION

Macrophomina phaseolina (Tassi) Goid (there are numerous synonyms such as Tiarosporella phaseolina, Macrophoma phaseoli and Rhizoctonia lamellifera) is an anamorphic ascomycete of the family Botryosphaeriaceae and causes the disease charcoal rot on a broad range of plants in many areas of the world (Reichert & Hellinger Reference Reichert and Hellinger1947). The lack of a known teleomorph has stalled its taxonomy over the years (Kulkarni & Patil Reference Kulkarni and Patil1966; Crous et al. Reference Crous, Slippers, Wingfield, Rheeder, Marasas, Philips, Alves, Burgess, Barber and Groenewald2006); however, a thorough phylogenetic study of 113 members of the family Botryosphaeriaceae using ribosomal DNA sequences was able to separate the genera Macrophomina and Tiarosporella (Crous et al. Reference Crous, Slippers, Wingfield, Rheeder, Marasas, Philips, Alves, Burgess, Barber and Groenewald2006). Although M. phaseolina is generally known as a plant pathogen, it is also an opportunistic human pathogen (Tan et al. Reference Tan, Sigler, Gibas and Fong2008; Srinivasan et al. Reference Srinivasan, Wickes, Romanelli, Debelenko, Rubnitz, Sutton, Thompson, Fothergill, Rinaldi, Hayden and Shenep2009) and, so far, the strains that invade plants and humans appear to be very similar (Srinivasan et al. Reference Srinivasan, Wickes, Romanelli, Debelenko, Rubnitz, Sutton, Thompson, Fothergill, Rinaldi, Hayden and Shenep2009). M. phaseolina is very widespread across the world and poses a threat to crop production (Hoes Reference Hoes1985). It is one of the most destructive plant pathogens in the tropics and subtropics, causing disease in a wide range of host plants (Reuveni et al. Reference Reuveni, Nachmias and Krikun1983), with the most common diseases being charcoal rot, damping-off (Cowan Reference Cowan1999), dry rot, wilt, leaf blight and ashy stem blight. In addition, M. phaseolina from different crops are cross-pathogenic (Mishra & Sinha Reference Mishra and Sinha1982). The fungus is known to cause stalk rot or charcoal rot disease in more than 500 plant species worldwide, including grass species such as Avena sativa, Sorghum bicolor and Zea mays, legumes such as Arachis hypogaea, Cicer arietinum, Glycine max, Medicago sativa, Phaseolus spp. and Vigna unguiculata, and many other species of agricultural importance and of woody plants (Farr et al. Reference Farr, Bills, Chamuris and Rossman1989; Ali & Dennis Reference Ali and Dennis1992). It is seed-borne (Kunwar et al. Reference Kunwar, Singh, Machado and Sinclair1986), found both on the seed coat and cotyledons (Reuveni et al. Reference Reuveni, Nachmias and Krikun1983), and causes charcoal rot by infecting the roots. Infected seeds produce infected seedlings that can transmit the pathogen into the fruit via the peduncle and so infect the seeds within the fruit, and also augment the inoculum potential in the soil. Hussain et al. (Reference Hussain, Hassan and Khan1989) reported that M. phaseolina was one of the six most common seed contaminants affecting soybean grown in the Sindh province of Pakistan.

M. phaseolina grows well on sunflower seeds and has been shown to increase the content of oil and free fatty acids in the seeds, as well as discolouration of the oil (Ataga & Akueshi Reference Ataga and Akueshi1986). Sclerotia are the primary means of survival (Mirza Reference Mirza1984), but the fungus over-winters either as free sclerotia in the soil or in plant residue. Charcoal rot infection may alter soybean seed composition and influence nitrogen fixation. The alteration in seed composition depends on cultivar susceptibility to charcoal rot and also irrigation management (Bellaloui et al. Reference Bellaloui, Mengistu and Paris2008). Positive correlations have been reported between the inoculum level of M. phaseolina in the seedbed and disease severity (Khan Reference Khan2007). Mechanical injury, high plant density and insect attacks are considered to be predisposing factors for transmission of the disease (Ahmad et al. Reference Ahmad, Burney, Asad, Ghaffar and Shahzad1991).

CHARCOAL ROT, A SERIOUS DISEASE

The first report of the occurrence of charcoal rot on sunflower was from Sri Lanka, by Small (Reference Small1927), while in Pakistan, charcoal rot of sunflower was first reported in Faisalabad and later from other areas of Punjab, Sindh and North West Frontier provinces (Mirza & Beg Reference Mirza and Beg1983). Charcoal rot is of great economic importance in the world and has been found to reduce head weight and diameter, stem height and weight, and in particular, the stem girth and root weight of sunflower plants (Hoes Reference Hoes1985; Kolte Reference Kolte1985). A limited laboratory experiment showed that pre-emergence infections by charcoal rot reduced seedling emergence to 65–77% of seeds sown and post-emergence infection reduced plant populations by a further 8–30% of seeds sown, resulting in final proportions of seeds surviving of 0·48–0·60 (Shahda et al. Reference Shahda, Tarabeih, Michail and Hemeda1991). The development of charcoal rot disease in sunflower requires the presence of a virulent isolate of M. phaseolina accompanied by low moisture and high temperatures (Wyllie Reference Wyllie, Wyllie and Scott1988). The severity of infection depends on relative humidity, temperature, the nature of the isolate, climatic region and host cultivar (Ahmad Reference Ahmad1996). The sclerotia are the prime sources of inocula (Papavizas & Klag Reference Papavizas and Klag1975). Charcoal rot is a particularly complex disease to control due to its longevity in the soil and the increase of inocula densities due to field cropping history (Long et al. Reference Long, Todd, Sweeney, Granade and Johnson1994). The occurrence of sclerotia in plant trash allows the fungus to live in soil in the absence of a host for 2 or more years, depending on soil conditions (Wantanabe et al. Reference Wantanabe, Smith and Snyder1970). Seed, soil and plant remains are the sources of primary inoculum (Reuveni et al. Reference Reuveni, Nachmias and Krikun1983) and the severity of the disease is directly related to the number of live sclerotia in the soil. Under dry soil conditions, the fungus can remain viable as sclerotia for more than 10 months. The mycelium in the soil, however, is not considered to be a primary source of inoculum (Meyer et al. Reference Meyer, Sinclair and Khare1974).

The symptoms of charcoal rot disease do not become noticeable until the latter part of the growing season, from mid March to late April, even though M. phaseolina is known to infect the plant at the seedling stage. Underground symptoms start with development of lesions on the taproot and basal portion of the stems, causing infected plants to wilt and progressing to rapid drying of the leaves. Yield is considerably reduced in plants that wilt at any stage from flowering to near maturity (Prioletta & Bazzalo Reference Prioletta and Bazzalo1998); seed yield reductions of c. 30% in weight have been observed in sunflower in India (Raut Reference Raut1981). The disease also reduces mean seed weight, germination, seedling vigour index and oil contents, while protein and iodine contents increase.

In some crops, such as sunflower, losses can reach 60–90% in environments that favour infection (Khan Reference Khan2007). Outbreaks of epidemic proportions and yield losses ranging from 46 to 74% due to charcoal rot of cowpea induced by M. phaseolina have recently been observed in many bean-growing areas in Nigeria (Amusa et al. Reference Amusa, Okechukwu and Akinfenwa2007). In the United States, estimated yield lost to charcoal rot in soybean (2 million metric tonnes) can reach 1·56% (Wrather & Koenning Reference Wrather and Koenning2006).

GENETIC VARIATION OF M. PHASEOLINA

Genetic variability is a product of genetic recombination, mutation and natural selection, so the variation in genetic background is mediated by these factors. High levels of pathogenic variability and genetic diversity have been observed between M. phaseolina isolates from different geographical origins or even different hosts after characterization with different markers [Random Amplification of Polymorphic DNA (RAPDs), Restriction Fragment Length Polymorphism (RFLPs) and Amplified Fragment Length Polymorphism (AFLPs)] (Almeida et al. Reference Almeida, Abdelnoor, Arias, Carvalho, Filho, Marin, Benato, Pinto and Carvalho2003), although isolates from the same species and same location had related pathotypes. Another study showed that the variation in M. phaseolina may have a relationship with geographic origin (Harlton et al. Reference Harlton, Lévesque and Punja1995). The qualitative differences in M. phaseolina are related to the host specificity of the fungal isolate, which varies from crop to crop, i.e. it may show host-specific behaviour on one crop and not on the other. The in vitro cultural and pathogenic differences are highly variable and are very difficult to quantify for adequate classification (Clude & Rupe Reference Clude and Rupe1991).

The genetic variation within a fungal population has been correlated with many factors including the uniformity of its substrate and previous environmental experience. The degree of sexual reproduction within a population or species is also related to genetic variation (Kendrick Reference Kendrick1992). The unstable B chromosome may be one of the mechanisms for generating variation in fungi (Miao et al. Reference Miao, Covertand and VanEtten1991). M. phaseolina, a saprophyte and opportunistic pathogen, exhibits a high degree of genetic variation. The most appropriate approach for combating it is to use resistant varieties (Ahmad & Burney Reference Ahmad, Burney, Ooi, Lim and Teng1990). Variability in varietal resistance may be attributed to variation not only in the host but also in the pathogen. As large-scale variation is observed in the pathogen population (Horst Reference Horst1965), knowledge about the variation in host and pathogen is a prerequisite for successful breeding programmes (Prota-Puglia et al. Reference Prota-Puglia, Crino and Mosconi1996).

Although only one species is recognized within the genus Macrophomina (Sutton Reference Sutton1980), great variability in morphology has been observed among isolates from different hosts (Pearson et al. Reference Pearson, Leslie and Schwenk1987). The great variability of the fungus reflects its heterokaryotic character. The variation in host sensitivity to Macrophomina can depend on the host growth stage (Saumon et al. Reference Saumon, Herbach, Goore and Davet1984).

Identification of charcoal rot-resistant genotypes (Pastor-Corrales & Abawi Reference Pastor-Corrales and Abawi1988) verified that susceptibility to M. phaseolina is positively related to earliness. Resistance in sunflower is a dominant character (Fuhlbohm Reference Fuhlbohm2000); however, the response of genotypes from different seasons and their seed yield, as affected by charcoal rot infection, varies widely. The development of disease resistance is correlated with the accumulation of new polypeptides synthesized by the host (Broglie et al. Reference Broglie, Gaynor and Broglie1986). The new protein contents depend on host genotype, sensitivity to infection and the virulence genes of the pathogens (Hlinkova & Sykora Reference Hlinkova, Sykora, Kema, Niks and Daamen1996; Radwan Reference Radwan2000). Arias et al. (Reference Arias, Ray, Mengistu and Scheffler2011) developed 182 microsatellite markers for M. phaseolina and tested these on 24 isolates of M. phaseolina obtained from seven plant species to establish the genetic variation in this fungus. One hundred and twenty of the SSR markers were polymorphic and only 27 markers were monomorphic.

RELATIONSHIP WITH BIOTIC AND ABIOTIC FACTORS

M. phaseolina is a pathogen of a wide number of cultivated and wild species around the world. The expression of symptoms depends on environmental conditions: more severe symptoms are observed under warmer conditions. Pathogenicity is optimal between 28 and 35°C (Dhingra & Sinclair Reference Dhingra and Sinclair1978). Host water stress is another principal factor favouring development of the disease (Pearson et al. Reference Pearson, Schwenk, Crowe and Kelly1984; Mayek-Perez et al. Reference Mayek-Perez, Gracia-Espiosa, Lopez-Castaneda, Acosta-Gallegis and Simpson2002). The disease is most prevalent where high temperatures and low precipitation coincide with the reproductive stage of crop plants and may become a potential threat to sunflower production (Mirza & Beg Reference Mirza and Beg1983).

Although free sclerotia can survive in dry soil for several years, Sinclair (Reference Sinclair1982) found that in wet soil sclerotia did not survive for more than 2 years and mycelium not more than 7 days. In Pakistan, charcoal rot is related to maturity of plants under water stress. Favourable conditions for the growth and expansion of the pathogen may lead to plant death. The pathogen specialization to the host also seems to be related to stem nitrogen composition, and is promoted at low water availability (Pearson et al. Reference Pearson, Leslie and Schwenk1987). Infection by nematodes causes disruption and damage of vascular tissues and physiological changes, providing a favourable substrate for the development of the fungus and therefore increasing the severity of charcoal rot. Ross (Reference Ross1965) documented the interaction of Heterodera glycines Inchinohe (soybean cyst nematode) and M. phaseolina separately in disease complexes. The disruption of vascular tissues resulting from infection by H. glycines increased the susceptibility of the host to water stress (Ross Reference Ross1965). Stress-related nitrogenous compounds such as asparagines and prolines are utilized efficiently by M. phaseolina and this could explain the positive correlation between H. glycines and population of fungus (Pearson et al. Reference Pearson, Leslie and Schwenk1987). As a result of interaction with fungi, the populations of sedentary nematodes are suppressed (Powell Reference Powell1971).

PHYSIOLOGY AND CYTOLOGY OF M. PHASEOLINA

Physiological specialization in M. phaseolina is not well demonstrated and the fungus is known to have a high degree of variation in its morphological, cultural and pathological properties even when isolated from different parts of the same plant (Dhingra & Sinclair Reference Dhingra and Sinclair1978). M. phaseolina enters the host tissue either by exerting mechanical pressure from the growing germ tubes or by dissolving the cell wall through the secretion of toxins or enzymes. The fungus can penetrate intact wax membranes up to 5–10 μm. Degradation of cell walls by M. phaseolina is due to the enzymes polyglacturonase and cellulase. The development of intercellular mycelium and its close association with cell wall in the cortex are correlated with the concentration of polyglacturonase. Development of M. phaseolina in the vascular system of the plant is not in a systematic manner. Mature hyaline and pigmented hyphal cells of Macrophomina are uninucleate, but young, growing hyphal cells and hyphal tip cells are usually multinucleate (Knox-Davies Reference Knox-Davies1967). Hyphal fusion heterokaryosis after mitotic segregation and recombination may explain the occurrence of cultural types or physiological races reported (Punithalingam Reference Punithalingam1983). Double-stranded RNA (dsRNA) has also been reported in M. phaseolina with sizes ranging from c. 0·4 to 10 kbp and the number of dsRNA ranging from 1 to 10 (Pecina et al. Reference Pecina, Alvarado, Alanis, Almaraz and Vandemark2000). Variations exist in pathogenicity among M. phaseolina from different geographical regions (Dhingra & Sinclair Reference Dhingra and Sinclair1973). The phytotoxin produced in cultures of M. phaseolina is Botryodiplodin. Phaseolinone was not detected, which suggested that Botryodiplodin may be the phytotoxin that facilitates infection (Ramezani et al. Reference Ramezani, Shier, Abbas, Tonos, Baird and Sciumbato2007).

EFFECTS OF FUNGICIDES AND ANTIBIOTICS ON M. PHASEOLINA

Many studies have reported on chemotherapeutic approaches to eliminating/reducing seed-borne fungi (e.g. Shah et al. Reference Shah, Hussain, Ali and Khattak1992). Sinclair (Reference Sinclair, Raychaudhri and Verma1989) examined the effect of thermotherapy on the growth of seed-borne fungi in soybean by immersing infected seeds in heated palm, sunflower and soybean oil as a means of eliminating seed-borne fungi. Brooker et al. (Reference Brooker, Kuzimichev, Lass and Pavlis2007) screened six derivatives of coumarin, for their antifungal activity against M. phaseolina and Pythium species and observed that these derivatives have higher antifungal activities and stability as compared with either the original coumarin or sesamol compounds alone. In chemical control studies, methyl [1-[(butylamino)carbonyl]-1H-benzimidazol-2-yl]carbamate (Benlate T) was shown to be most effective against M. phaseolina isolated from sunflower (Raut & Bhombe Reference Raut and Bhombe1986). Shahda et al. (Reference Shahda, Tarabeih, Michail and Hemeda1991) studied the in vitro effect of certain fungicides such as Benlate T, 2-(4-thiazolyl)-1H-benzimidazole (Thiabendazole), N-trichtoromethylthio–cyclohexene-1,2-dicarboximide (Captan 75), 5,6-dihydro-2-methyl-N-phenyl-1, 4-oxathiin-3-carboxamide and tetramethylthiuram disulfide (Vitavax 200), 5,6-dihydro-2-methyl-N-phenyl-1,4-oxathiin-3-carboxamide and N-trichtoromethylthio–cyclohexene-1,2-dicarboximide (Vitavax 300), on mycelial growth of seed-borne fungi of sunflower and 5,6-dihydro-2-methyl-N-phenyl-1,4-oxathiin-3-carboxamide and tetramethylthiuram disulfide (Vitavax 200) was found to be most effective for M. phaseolina. Patil & Kamble (Reference Patil and Kamble2011) examined the effect of UV light on the hostile/antagonistic action of Trichoderma koningii against M. phaseolina, using five T. koningii mutants, and found that T. koningii 2 showed maximum antagonistic activity against the charcoal rot pathogen when tested by dual culture.

In conclusion, charcoal rot, caused by the ascomycete fungus M. phaseolina, is a major potential threat for crops such as sunflower and soybean. Charcoal rot epidemics are common under severe conditions such as water scarcity and other biotic and abiotic stresses. There are differences in the pathogenicity of M. phaseolina isolates from different geographical regions. There is an urgent need to develop crop cultivars resistant to this pathogen. Breeding of resistant germplasm can be achieved through conventional and non-conventional means.

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