Department of Biotechnology, Plant Tissue Culture and Molecular Biology Laboratory, Bhimtal Campus, Kumaun University, Nainital, Uttarakhand-263136, India
Received date: April 29, 2015; Accepted date: May 21, 2015; Published date: June 15, 2015
Citation: Sharma R, Tamta S (2015) A Review on Red Rot: The “Cancer” of Sugarcane. J Plant Pathol Microbiol S1:003. doi:10.4172/2157-7471.S1-003
Copyright: © 2015 Sharma R, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Sugarcane is an important agro industrial crop of the world. India being the largest consumer as well as the second largest producer of sugar, so, it requires sugarcane production on large scale. But diseases are the major concern for the sugarcane, responsible for its low yield. Among all the diseases, fungal disease named red rot of sugarcane is the most threatening disease of sugarcane, rightly called as ‘Cancer’ of sugarcane. It causes severe loss in yield and quality of the sugarcane. As the fungus Colletotrichum falcatum responsible for this disease is highly variable in nature, hence, it causes the frequent breakdown of resistant varieties. Keeping in view the seriousness of this disease, the present review summarizes the distribution, mode and source of infection, description of casual pathogen and disease management
Colletotrichum falcatum, Saccharum spp.; Cancer; Dissemination; Resistance
Saccharum spp. (Sugarcane) is an important cash crop cultivated in tropTical and sub- tropical regions of the world. It is valuable mainly because of its ability to store high concentrations of sucrose, or sugar, in the stem and more recently for the production of ethanol, which is an important renewable biofuel source [1,2]. Globally, sugarcane is an important source of commercial sugar accounting for almost twothirds of world sugar production . Brazil is the largest sugarcane producer, contributing with 40% of the world production, followed by India, China, Thailand, Pakistan, Mexico, Philippines, United States, Australia and Argentina . The list of top ten sugarcane producing countries with their estimated sugarcane production in the year 2011 is listed in Table 1.
|People's Republic of China||115,124|
TMT: Trillion Metric Tons
Table 1: Top ten sugarcane producers: 2011 (Source: Food and Agricultural Organization of United Nations: Economic And Social Department: The Statistical Division).
Sugarcane is cultivated in most of the states of India with total area coverage of 4.2 million hectare (M ha). It is the second most important agro industrial crop in India, next only to cotton . The sugarcane producing states of India and their contribution in sugarcane production is shown in Figure 1. India is the largest consumer of sugar in the world with annual consumption of about 19 million MT (Metric Tons) and the second largest producer of sugar next to Brazil, with production of sugar crossing 28 million MT in India in year 2009- 10  and with increasing population needs, sugarcane production requires enhancement . However various biotic and abiotic factors are responsible for its low yield, diseases are the major cause of concern. About hundred diseases of sugarcane have been reported from different parts of the world . Over 100 fungi, 10 bacteria, and 10 viruses and about 50 species of nematodes are pests of sugarcane in different parts of the world .
In India, the estimated loss in crop production due to fungal diseases is about 18-31% . Losses due to sugarcane diseases are shown in Figure 2. Red rot is the most common disease of sugarcane, caused by the fungus Colletotrichum falcatum Went. It causes severe loss in yield and quality of the susceptible cultivars in the Indian subcontinent [9,10]. It can reduce cane weight by up to 29% and loss in sugar recovery by 31% . Red rot pathogen hydrolysed the stored sucrose by producing the enzyme invertase which breaks the sucrose molecule into its components namely glucose and fructose. As a result the quantity of molasses increases . It is aptly called the “Cancer” of sugarcane .
Red rot is also the oldest mentioned disease of sugarcane dating back to the times of Buddha. The disease was first reported from Java, Indonesia, where it was known as “Sereh”  and generally known to cause by the fungus, C. falcatum Went. The perfect stage of the fungus was identified as Physalospora tucumanesis Speg.  and finally known as Glomerella tucumanesis Speg. . Barber Ca  recorded the first report of red rot occurrence in India. Since then a number of red rot epidemics have been reported, especially in eastern Uttar Pradesh, northern Bihar and pockets of Punjab. These epidemics have resulted in failure of some important Indian commercial sugarcane varieties [18-20].
Sources of infection
Red rot can infect mature stalks of sugarcane, leaf mid ribs and cause rot of planting material which results in substantial losses in crop yield and sugar quality . The fungus is sett-borne. The perpetuation of red rot is through infected setts/canes, diseased stubble/debris and by resting propagules in the soil. Annual recurrence of red rot in sugarcane is primarily due to infected seed cane and stubble through which the pathogen is carried over to subsequent crops [22,23]. The role of soil-borne inoculum in the recurrence of disease is perhaps negligible as the fungus is not a true soil borne organism and does not survive in soil for more than 5-6 months [24,25].
The pathogen attacks the cane plant from the very beginning, i.e., germination  and cause germination failure or cause death of germinated seedlings. In general, dormant mycelia present in the bud scales are responsible for post-germination infection of young emerging shoots .
Manifestation of red rot varies depending on the nature of infection, time of the season and the prevailing environment. Diagnostic symptoms are observed during monsoon or post monsoon period [28,29]. With the advent of pre-monsoon showers, symptoms of the disease start appearing, and with the onset of the monsoon when the weather is most suitable, full manifestation of the disease takes place .
The secondary transmission of the fungus during monsoon is mediated through irrigation, rain water, rain splash and results in the infection of mid-rib, lamina, leaf sheath and stalk, while in winter air currents aid in the spread of the pathogen [30,31]. The conidia produced over the rind wash down with water and cause infection through nodes. Dissemination of inoculum by means of wind appears more difficult because of the mucilaginous nature of the spore mass. But the occurrence of the disease in the upper portion of the canes provides an indication of an aerial mode of dispersal of the inoculum. Environmental conditions prevailing during the winter season do not favour the fungus to infect the crop and may not pose any serious threat to infect the cane crop  but leads to the development of incipient infections in the nodal region (buds, bud scales, root primordia, etc.). Such infections serve as primary infection when cane is used as seed . Borers also help in the secondary transmission of the pathogen .
Mode of infection
The pathogen mainly infects canes through nodes and main portal of entry are leaf scar, growth ring, root primordia and buds [33-35]. The pathogen can also enter the stalk through root lets, growth cracks and cut ends of the setts .
After the fungus invades the tissues of the stalk, the mycelium may spread from cell to cell leads to gum formation in moderately resistant genotypes. More rapid spread can occur through the vascular bundles. Infected internode tissues develop a rot with a characteristic red colour that often contains interspersed areas with normal colour known as “white spots” [36-39]. The disease cycle of red rot is shown in Figure 3.
Favourable conditions for disease development
• pH 5-6 .
• Drought conditions during the initial growth phase .
• High atmospheric humidity (90%).
• Water-logged conditions of the soil.
• Lack of cultural practices that result in the growth of weeds.
• Continuous cultivation of same variety in the field.
• Presence of susceptible varieties in the surroundings.
Sub division: Deuteromycotina
The key morphological identification features of C. falcatum fungus are: its mycelium which is both intracellular and intercellular, asexual fruiting bodies known as acervuli (minute, velvety and formed on the surface of the host part), often with setae (dark-pigmented, unbranched, thick-walled sterile hyphae usually pointed at the tip), having hyaline, linear or club shaped conidiophores producing elongated, single celled, thin walled, uninucleate, colourless, sickle shaped (Falcate), slimy conidia having granular protoplasm with a large oil globule, thick walled, greenish black chlamydospores and the presence of appressoria (thick-walled swellings at the end of a hypha or germ tube useful for attaching the fungus to the host surface before penetration of the tissue), presence or absence of the telomorph, colony colour and growth, production of pigments and growth rate which are mostly used for genetic characterization [9,10,44,45].
C. falcatum, a facultative saprophyte, known to produce a phytotoxic metabolite identified as an anthroquinone compound. It has been established that the toxic metabolite is host-specific and produces part of the disease symptoms [46,47]. Its sexual stage known as G. tucumanensis is responsible for the survival of the fungus on decaying leaves and formation of new virulent pathological races which are responsible for the frequent epidemics .
Ten races of C. falcatum have been reported in India based on host differentials . If a fairly large number of isolates of the fungus obtained from different cane varieties or geographic areas are studied on artificial culture media, considerable variation in the type of growth and colour of the fungus colony usually is seen. Some isolates or races are light gray and form a loose cottony colony, others are dark gray and form a restricted velvety colony while some are intermediate in those respects. If they are inoculated into stalks of sugarcane, they also differ in pathogenicity and their ability to infect and rot the stalks . The light race produced abundant spores and proved more virulent than the dark one. All the previous isolates of C. falcatum from India were dark type with sparse sporulation .
Expression of the disease may vary depending upon nature of infection and prevailing environmental conditions . In the early stages of infection, it is difficult to recognize the presence of the disease in the field as reddening of the internal tissues with interrupted red and white patches, the characteristic symptoms of the disease, develops on the stem only at later stages. Furthermore, latent infection occurs frequently, making visual diagnosis impossible .
The first symptoms of the disease are seen when the vegetative growth of the plant is stopped and sucrose formation begins, i.e., after rainy season. The pathogen, C. falcatum Went, can attack any part of the sugarcane plant; be it stalk, leaf, buds or roots. C. falcatum completes its life cycle on the sugarcane leaf and usually the damage to leaf does not pose a serious threat to cane or cause much harm to the plant . Discolouration of the leaves is the first symptom in the field. The spindle leaves (3rd and 4th leaf) display drying which withers away at the tips along the margins. This discolouration from tip to the base is continued till all the leaves of the crown wilt . Tiny reddish lesions occur on the upper surface of the lamina with minute red spots in both the directions of the upper surface of the midrib. Infection also resulted in change in the colour of the leaves that become straw coloured in the center and dark reddish brown at the margins with the development of black acervuli. The infected leaves may break at the lesions and hang down.
The most damaging phase of this disease occurs when the pathogen attacks the stalk. Depending on the age of the stalk, time of infection and susceptibility of the cane genotype, it produces different types of symptoms . Typical symptoms of red rot are observed in the internodes of a stalk by splitting it longitudinally. These include the reddening of the internal tissues which are usually elongated at right angles to the long axis of the stalk. Cross-wise white patches are the important diagnostic characters of the disease. The white spots may vary in size and number and sometimes they are so numerous as to give the tissue a mottled appearance . With the advancement of disease, the stalk becomes hollow and covered with white mycelial growth. Later on the rind shrinks longitudinally with the protrusion of minute black, velvety fruiting bodies. The infected cane emits acidic-sour smell while its juice emits alcoholic smell. As sucrose gets converted to glucose and alcohol in diseased cane, it does not set well upon boiling.
The factors responsible for determining host resistance against C. falcatum have not been fully understood. Two types of resistance against red rot pathogen have been recognized .
It refers to those structures or modification in the plant tissue, which mechanically restrict or prevent the entry or spread of the pathogen in the host tissues. Various parameters viz., thickness of epidermis, cuticle, bud scales, rind, relative abundance of vascular bundles under the rind and the presence of septa in vascular bundles prevents the rapid migration of spores in the plant tissue .
A brown gummy substance is formed in advance of the infection in resistant varieties which seals off further spread of the pathogen in adjoining tissues . On the contrary, gum formation in susceptible varieties takes place after tissue has been infected to a lesser extent. This has been termed as hypersensitive gumming reaction .
In resistant varieties it was observed that the level of total phenolics increased after infection and was maintained, while in susceptible varieties, the level of phenolic content dropped after an initial increase [51-53].
Srinivasan and Srivastava et al. [54,55] observed that higher activity of poly phenol oxidase (PPO) and flavone glycosides is linked with red rot resistance. Madan et al.  linked the red rot resistance to higher specific activity of Phenylalanine Ammonia lyase (PAL) and Tyrosine Ammonia lyase (TAL). Viswanathan et al.  correlated the role of phytoalexin 3- deoxyanthocyanin with red rot resistance.
As pathogen is highly variable in nature, the resistant sugarcane varieties gets prone to red rot within a short time period, therefore detailed investigation is required to understand the true basis of disease resistance at molecular level .
Management of red rot has been a challenging area of work for the pathologists and sugarcane breeders. The epiphytotic of the disease depends upon weather conditions, genotypes, presence of virulent pathogen and time for disease development. These factors must be studied in depth so as to achieve effective control of the disease. It has been observed that once the disease has appeared in the field it is impossible to control. Most of the recommended management practices hence are aimed at prophylactic measures to reduce pathogen build up in the field . In view of diversity in the kinds of pathogens, a single method would not be useful to mitigate the losses from red rot , hence Integrated Disease Management (IDM) should be practiced. The IDM chart is shown in Figure 4. The following methods in desirable combinations could be adopted for controlling the red rot disease.
Correct diagnosis of pathogens is the primary requirement in any sound disease management practice . Disease diagnosis and pathogen identification by conventional methods involves isolating the pathogen and characterizing it by inoculation tests . The variability of red rot pathogen was first studied by Edgerton and Moreland . The characterization of pathogen has primarily been based upon variation in colour, conidial size and shape, appressoria, colony characters, host association and sporulation [60-64]. But this phenotypic identification is time consuming, expertise specific and not always fully discriminative .
Over the past few decades, immunological methods have increasingly Received attention as an alternative or complement to conventional methods . Polyclonal antisera were developed against the C. falcatum proteins and ELISA, DIBA and Western blot methods were standardized for detection of C. falcatum in sugarcane . Hiremath and Naik  developed a protocol for rapid diagnosis of sugarcane red rot infection by using Dot Immunobinding assay (DIBA) technique. But there is a drawback associated with serological assays that there could be chances of false positives caused by crossreaction of antibodies with plant debris or unrelated organisms .
Molecular methods based on polymerase chain reaction (PCR) are frequently being used now a day for detecting fungal pathogens in plant tissues [69-73], due to their increased specificity and sensitivity in comparison to the traditional techniques. Variability in C. falcatum isolates have been characterized by using arbitrary marker system such as RAPD [74-77]. Kumar et al.  used inter simple sequence repeat (ISSR), universal rice primers (URPs) and RAPD markers to characterize variability among C. falcatum isolates. ITS primers were also used to study the variability among pathogen [78,79]. Nithya et al.  developed SCAR markers specific to races and isolates of C. falcatum.
A combination of molecular diagnostic techniques and conventional morphological characterization is a suitable and reliable approach for studying Colletotrichum species/isolates complexes [80,81]. But it is very much difficult to diagnose the dormant infections of the C. falcatum fungus in seed canes under field conditions as red colour develops on stem and leaves at a later stage . It is therefore, important to explore other possibilities for the management of red rot in sugarcane .
Effective control of red rot has been mainly through the use of resistant varieties. Even though genetics of inheritance of red rot resistance is not well established, considerable progress has been made in the production of red rot resistant varieties . In India, the breeding work is primarily focused on developing red rot resistant varieties . But as the pathogen is highly variable in nature, therefore, even if a disease resistant variety is released for cultivation, it gets susceptible to red rot disease within 8–10 years because of the development of new more virulent races of the pathogen [84,85].
From the last few decades, molecular diagnostic tools have increasingly been used as an alternative to traditional techniques . Molecular markers could be used as an effective means that can unfold the complex genetics of sugarcane and also aid the breeders in improving the genetic makeup of varieties [86-88]. So far, sugarcane diversity has been studied using ribosomal DNA , simple sequence repeats ; amplified fragment length polymorphism ; restriction fragment length polymorphism ; TRAP  and random amplified polymorphic DNA . Considerable efforts are going on to identify genes and develop markers associated with red rot resistance.
Quarantine regulations govern the introduction of plant material from high-risk areas. In India, seed cane is frequently taken from one state to another without any regulatory restriction . Unrestricted movement of seed material has been largely responsible for the spread of red rot in different regions. The recent introduction of the disease in Karnataka and Maharashtra was because seed material of highly susceptible varieties was brought from red rot endemic areas . Hence there is a need for restricting transport of cane from an infected zone to disease free zones. The seed material from outside state is procured only from research stations with proper phytosanitory certificate .
Prevention is better than cure hence, healthy cultural practices should be adopted while planting the sugarcane. Use of healthy seeds, crop rotation, field sanitation and efficient drainage have been recommended to reduce inoculum in the field and minimize losses due to the disease. The primary inoculum of the disease mainly comes through infected seed material  hence; disease free seed nursery should be established in each farm and farmer’s field. In this context, seed from heat treated crop or certified nursery will serve the purpose. In addition to this, sanitary measures must be adopted in the field. Crop debris, trash and stubble should be burnt prior to planting . Extremely dry and wet soils should be avoided. Ratooning should not be done in case of heavily infected plant crops. To minimise the soil borne inoculum, crop rotation should be adopted by growing some other crop for 2-3 years. Flow of irrigation water from diseased to healthy plants should be discouraged to avoid the spread of disease through water medium. Long setts should be used for planting. Three or four budded setts are very suitable seed setts for the control of soil born inoculums of redroot .
A number of fungitoxicants have been tried against the red rot but a little success is found in controlling this devastating disease. This may be because of impervious nature of rind, presence of fibrous nodes at the cut ends, low solubility of fungicides, lack of broad spectrum fungicides and presence of abundant nutrients in the sett [9,26]. Some reduction in red rot incidence has been reported when infected setts were treated with carbendazim and benomyl, which is not commercially produced now for 1-2 hours [96-98]. Chand et al.  also reported that Vitavax reduced the red rot incidence in sugarcane. Dip treatment of setts in Agallal (0.5%) for 15 min was found effective . Bleaching powder was effective in reducing red rot incidence . Soaking of sugarcane setts in 0.25% suspension of thiophanate methyl and its metabolite carbendazim for 24 h before planting was found to be effective in controlling debris-borne infection . In a test conducted by Subhani et al.  benomyl, folicar, radomil and tilet completely inhibited the growth of fungus (100% inhibition) while minimum mycelial growth inhibition was observed in case of nimrod. Treatment with topsin M helps in protecting canes from red rot disease and improving plant yield . In an experiment conducted by Bharadwaj and Sahu , bavistin showed complete inhibition of mycelial growth of the C. falcatum. Secondary infection of red rot was checked by spraying copper and dithiocarbamate fungicides , but negative results were obtained by Sinha and Misra .
Heat therapy has been used for controlling sett borne infection of red rot by various workers. Sinha et al. and Singh [107,108] reported complete elimination of sett-borne infection by hot air treatment (54°C for 8 h). Some workers have used heat and chemotherapy in combination by incorporating the chemical into the hot water tank for adequate control of red rot . Findings of various workers have proved that moist hot air therapy (MHAT) of seed cane at 54°C for 4 hr (R.H. 95-100) was most effective against red rot [110-113]. Ref.  reported that moist hot air treatment (54°C - 2 h) was more effective than hot water treatment (50°C-2 h) in reducing red rot. Aerated steam treatment at 52°C or the soaking of setts in cold running water for 48 h followed by hot-water treatment (50°C for 150-180 min) also helps in eliminating the pathogen from infected setts .
Red rot disease of sugarcane was observed to be biologically controlled through Trichoderma harzianum and T. viride . T. harzianum and Pseudomonas spp.. possess the ability to protect the crop from soil borne inoculum of red rot and the efficacy is because of the chitinase enzyme produced by them . The findings of ref.  clearly supported that ech42 gene of Trichoderma spp. is responsible for controlling the red rot incidence in sugarcane in an experiment conducted by Singh et al. , addition of SA (salicylic acid) has boosted the protection level significantly against red rot disease and helped T. harzianum for inducing systemic resistance in sugarcane.
Ocimum, Ginger, Onion and Garlic were found to inhibit the mycelial growth. It was also examined that the essential oils, viz. Peppermint oil, Mentha oil, Geranium oil, Patchouli oil and Palmaroza oil were effective in inhibiting the growth of mycelia of C. falcatum .
In sugarcane,  established PGPR (Plant growth promoting rhizobacteria) mediated ISR (Induced systemic resistance) against C. falcatum causing red rot disease. The study conducted by Viswanathan et al.  indicates a possible role of PR (pathogenesis related) proteins in conferring red rot resistance in sugarcane. The peptides MUC1 60 mer and Purothionins mixture significantly inhibited the mycelial growth and spore germination of C. falcatum .
It was showed in an experiment that leaf extracts of Curcuma domestica and Datura metel inhibited the conidial as well as mycelial growth. Smoke of dhup (incense) and tobacco also showed inhibition against conidial germination [122-124].
Red rot disease of sugarcane continues to be a serious threat to production of sugarcane all around the globe. Integrated disease management strategy is the best possible option in controlling this disease, rather than relying upon a single method. An understanding of the pathogen is a pre-requisite for disease management, which could be accomplished by molecular diagnostic tools for a rapid and precise detection of the pathogen in seed cane. Though limited information is available regarding the true basis of disease resistance, molecular tools are now available to identify suitable markers that can be relied upon for supporting the conventional breeding approaches. These biotechnological approaches should be supplemented with different other control measures like quarantine regulations, clean cultural practices, use of chemicals, biocontol agents and heat therapy. In addition to the existing control measures, novel strategies should be thought of to explore the possibility of inducing systemic resistance against the C. falcatum. Further with the identification of candidate defense genes, development of transgenic sugarcane with built-in resistance to red rot is to be looked into for the future.