The Epidemic Characteristics and Control Strategies of Sugarcane Red Rot

Jie LI Rongyue ZHANG Hongli SHAN Xiaoyan WANG Xiaoyan CANG Changmi WANG Zhiming LUO Jiong YIN Yingkun HUANG

Abstract Sugarcane red rot caused by Colletotrichum falcatum Went. is an important epidemical fungal disease. The outbreak of large-scale epidemics would cause huge losses to sugarcane production. At present, the pesticide control effect is not ideal. Moreover, due to long-term continuous cropping and changeable climate in recent years, favorable conditions for the occurrence of red rot have been created. The disease was often prevalent in various sugarcane areas, caused serious damage and seriously affected the sugarcane production. With the rapid spread of the disease worldwide, the control of sugarcane red rot has become the hot spot in the field of sugarcane production and research. In this paper, the epidemic characteristics of sugarcane red rot were analyzed in combination with the field investigation. To provide theoretical basis for prevention and control of red rot in China and effective control the widespread occurrence of the disease, combined with the latest research results at home and abroad, we proposed to select resistant varieties mainly, use biological control agents such as Trichoderma spp., Pseudomonas spp. and Bacillus spp. to treat the seed cane and soil, timely apply chemical pesticide in critical periods and strengthen scientific and effective comprehensive coordinated prevention and control measures such as field management against red rot.

Key words Sugarcane; Red rot; Epidemic characteristics; Control strategies

Received: January 25, 2020Accepted: March 9, 2020

Supported by Sugar Crop Research System (CARS-170303); the Yunling Industry and Technology Leading Talent Training Program "Prevention and Control of Sugarcane Pests" (2018LJRC56); the Yunnan Province Agriculture Research System (YNGZTX-4-92).

Jie LI (1989-), female, P. R. China, master, devoted to research about sugarcane diseases and pests control.

*Corresponding author. E-mail: huangyk64@163.com.

Sugarcane is an important cash crop, mainly used for the production of sucrose, ethanol, biofuels and fiber-related products［1-2]  . There are more than 100 countries in the world that grow sugarcane, and China has now developed into the third largest producer following Brazil and India［3]  . Red rot is the most serious sugarcane fungal disease, which is often called sugarcane "cancer" ［4]  . After sugarcane stems are damaged, the fungus secretes sucrose invertase, which reduces the gravity purity of sucrose juice, reduces sucrose content, and causes a severe lack of plants through seed canes carrying the disease［5]  . Colletotrichum falcatum Went varies frequently , often causing disease-resistant varieties to susceptibility, leading to the spread of red rot. The single control measures for this disease are not ideal. In order to scientifically prevent and control the disease, we systematically analyzed the epidemic characteristics of sugarcane red rot from the aspects of the occurrence, symptoms, pathogens, infectious pathways and occurrence conditions of sugarcane red rot in combination with field surveys and the latest research results at home and abroad. Furthermore, based on the actual production of sugarcane, taking into account planting management, scientific and effective comprehensive prevention and control countermeasures were proposed.

Occurrence

Sugarcane red rot, also known as red rot, can infect the stems, leaves, buds or roots of sugarcane［6]  . It mainly harms the cane stems and leaf midribs, and can occur throughout the growing season of sugarcane, which can lead to a 29.1% reduction in sugarcane yield and a loss of sucrose more than 30.8%［7]  . Sugarcane red rot occurred as early as 1893 in Java, Indonesia［8]  , and is widely distributed. It has been reported by 68 sugarcane growers worldwide［9]  , including Australia, Bangladesh, Pakistan, the United States, Thailand, India and China, which are severely harmed［10-12]  , and it has become the main restrictive factor for sugarcane production in India［10]  . The disease has been reported in sugarcane regions of various provinces in China［13-18]  . In recent years, investigations have found that the main cultivar ROC 1 in Shiping, Yunnan suffers from severe red rot which harms stumps, while Yuetang 93-159 and ROC 22 in Lincang and Menglian are generally infected by ret rot which harms cane stems, causing the sugarcane medulla to rot and become hollow and dry. Specifically, the disease area in Shiping sugarcane area is low-lying and accommodates stagnant water therein, and new alien insect species such as Chilo sacchariphagus Bojer and Tryporyza intacta Snellen, pokkah boeng, cane stem red rot and brown stripe disease occur simultaneously in Menglian sugarcane area, seriously reducing yield and reducing sugar.

Symptoms and Pathogens

Symptoms

When damaging the midribs of cane leaves, it initially produces small red spots, then red spots expanded up and down along the midribs to a spindle-shaped or long red-brown stripe parallel to the veins, which can run through the whole leaf at the longest, and has a distinct light halo at the outer periphery; and at the late period, the center of the spots changes from grass yellow to pale white, with dark red around it, and there are scattered black dots on the disease spot under humid conditions, which are acervulus of the pathogen. There are often multiple disease spots on a midrib, which often fracture at the late period, making the leaf break［5]  . In the early stage of infection of cane stems, the external symptoms are not obvious, but the internal tissues of the affected cane become red and expand up and down, and can penetrate several internodes. The discolored part is often mixed with round or oblong white plaques, which smells sour like amylofermentation. In the late stage of infection, the epidermis of the diseased stem is shrunk, dull, and covered with obvious scars and brown acervulus, and the medulla is hollow, and full of gray-white hyphae. The internal tissues of the cane stem are severely damaged and decomposed, which causes the upper leaves to lose water and wither, and even death of the whole plant in severe case. The damage to perennial ratoons can easily cause rot, affect germination, and often cause sugarcane to grow unevenly and a severe lack of plants, resulting in a reduction of effective stems and yield. If the seed cane is diseased, often the sugarcane buds cannot germinate and cause severe lack of plants［5]  .

Pathogens

The asexual stage of the sugarcane red rot pathogen is C. falcatum , and the sexual stage is Physalospora tucumanensis Speg［5]  . Conidia are nearly sickle-shaped, single-spore, light-colored, without diaphragm, containing granules and oil drops, and often have a large vacuole. When conidia are dense, they are pink or orange-red. The fungus grows best in oatmeal and Richards media; the optimal temperature for the growth of the mycelia is 25-30 ℃; the suitable pH is 6-8; the light condition has no obvious effect on the growth of the pathogen; and the lethal temperature of the conidia is 60 ℃ (10 min)［19]  . The most suitable carbon source is D-xylose, and the nitrogen source is sodium nitrate ［5]  .

Infection Pathways and Occurrence Conditions

Infection pathways

The pathogen mainly infects leaves and stem tissues through wounds such as borer holes, growth cracks, and mechanical wounds, among which the borer holes are the main invasion channels for pathogen spores, and sugarcane red rot occurs seriously in fields invaded by many borers［5,21]  . The pathogen overwinters in seedcane, diseased plants and soil with hyphae, conidia and chlamydospores［5]  . When conditions are appropriate, spores are transmitted to the surface of sugarcane plants through wind and rain, and the spores invade directly from the sugarcane epidermis or from the buds, leaf marks, cane stalks, leaf blades and mechanical wounds on the midribs, causing initial infection. The seed cane carrying the mycelia can directly spread and invade sprouting cane plants to cause initial infection［21]  , and the conidia or chlamydospores of pathogen on diseased leaves infect other plants repeatedly by wind and rain transmission［5]  . In severely damaged cane stems and cane plants, water ducts are blocked, cane leaves dry up, and finally, the entire plants stop growth and even die［21]  .

Occurrence conditions

The occurrence of sugarcane red rot is related to many factors such as climate, genotype, pathogenic strain and disease time. The incidence in seedlings is directly related to the seed cane carrying the pathogen［5]  . The disease is greatly affected by climatic conditions, and occurs easily when it is rains a lot. It is also closely related to the susceptibility of sugarcane varieties and the occurrence of borers, and often occurs seriously in sugarcane fields with severe damage caused by borers［21]  . After planting cane in winter and spring, the disease is often caused by low temperature and rain, slow germination, weak disease resistance and high humidity, which results in the lack of plants; and excessive humidity and acid in the soil are also conducive to disease occurrence［5]  . The disease generally happens seriously under the conditions such as many storms, high mechanical damage rate, or severe pests leading to many wormholes［5]  . The average temperature of 29.4-31.0 ℃ is most suitable for disease development［22-23]  , and a pH of 5-6［24]  , drought in early growth［25]  , high humidity (90%), water accumulation in the soil, many weeds and continuous planting of the same variety are all favorable to the disease［26]  .

Control Countermeasures

Selection of disease-resistant varieties

The use of disease-resistant varieties is the most effective and economical method for controlling red rot［27]  . Breeding of sugarcane for red rot resistance is very important in sugarcane improvement［28]  . India has conducted strict resistance screening of endemic races of red rot, and only moderate-resistant varieties have been obtained for commercial planting［29]  . Since it is difficult to diagnose dormant red rot in seedlings under field conditions, it is not feasible to control the disease by planting seedlings without the pathogen［30]  . Investigations revealed that ROC 1, ROC 22, ROC16, Taitang 89-1626, Yuetang 93-159, Yuetang 00-236, Guitang 15 and Guitang 42 are susceptible to the disease［5,15-16]  ; and Yuetang 55, Guitang 02-901, Guitang 29, Guitang 31, Yunzhe 99-596, Yunzhe 01-1413, Yunzhe 05-49, Yunzhe 05-51, Funong 15, Funong 38, Funong 39, Mintang 69-421 and Liucheng 05-136 are more resistant to the disease［5]  . Kumar et al. ［31] found that varieties SES 594, tropical species Baragua and Bo 91 were resistant to all red rot strains; and CoS 98247, Co 09022, CoS 96275, CoPb 10211, UP 9530［32]  , Co 93009, Co 94008［33] and Co 94004［34] were disease-resistant. Viswanathan［35] reported that varieties Bo 91, CoS 8436 and Co 98010 were resistant to the new pathogenic strain of India (Cf 94012).

Agricultural control

The agricultural control measures include establishing a three-level disease-free seed nursery to plant healthy seedlings, clearing the infection source in a timely manner to maintain rural hygiene and removing residual leaves of diseased plants in the field in time after harvesting sugarcane, strengthening field management and eliminating cane borers and other pests and field weeds in time to promote robust growth of sugarcane seedlings and enhance disease resistance［5]  , planting seed cane in winter and covering the field with plastic film when planting in early spring to promote germination and avoid germ invasion, implementing crop rotation and reducing years of ratoons［5]  , and preventing water accumulation in sugarcane fields.

Chemical prevention

It takes 8-10 years to develop varieties that are resistant to red rot［36-37]  , and chemical fungicides are still an effective method to control red rot［38]  . Many agents have been used to control the disease in the past, but the spray effect is not satisfactory after the occurrence of the disease［39]  . Practice has proven that selecting suitable agents to disinfect seedcane before planting sugar cane is one of the effective ways to reduce the incidence of the disease［20]  .

The seed cane can be sterilized by soaking in 1% copper sulfate solution for 2 h; and 1 000-1 500 times dilutions of 50% benomyl wettable powder and 75% chlorothalonil wettable powder can also be used to soak the seed cane at 52 ℃ for 20-30 min［5]  . Khan et al. ［40] respectively investigated the effects of soaking the seed cane with six fungicides for 24 h on the incidence of red rot and sugarcane yield. The results showed that thiophanate methyl had the best effect on the prevention and control of red rot and yield improvement. Malathi et al. ［41] carried out a comparative study of treating sugarcane seedcane with different fungicides, and the results showed that treating seedcane with 500 mg/L thiophanate methyl + trifloxystrobin· tebuconazole had significant effects on sugarcane survival and yield improvement, which were the same as those achieved by using 1 000 mg/L thiophanate methyl alone. It has also been reported that 500 mg/L thiophanate methyl combined with Pseudomonas was used to resist the infection of red rot, and the survival rate of sugarcane reached 81.67%［42]  .

Biological control

Prior to sugarcane planting, sugarcane seeds are treated with 2.5% Trichoderma harzianum (Th 38) culture filtrate for 15 min and 20 kg/hm2 of Trichoderma mixed culture (106 conidia/mL spore suspension, 2.5% Trichoderma culture filtrate) is applied into furrows formed in the soil, which can protect 75% of sugarcane from re-infection by red rot and improve germination and increase yield by 15-20 t/hm2［43]  .

Pseudomonas (2.5×108 to 3×108 CFU/g) is mixed with water at a ratio of 20 g/L to soak the seeds for 1 h, which are then incubated in the field overnight for 18 h and planted; or the mixture can be applied once at 2 months and once at 4 months after sugarcane planting at a rate of 25 kg/hm2. It is best to mix it with 250 kg of compost and applied to the base of sugarcane and covered with soil. The treatment with Pseudomonas can reduce the incidence of sugarcane red rot by 50%, and significantly increase the sugarcane germination rate, sugarcane yield and cane juice quality［44]  .

When sugarcane is planted for 4 and 5 months, 5 ml of Bacillus at a concentration of 1×108 CFU/ml is applied to the root soil of sugarcane once, which could effectively reduce the incidence of sugarcane red rot［45]  .

Heat treatment

Singh［46] reported that hot air treatment at 54 ℃ for 8 h could eliminate the infection of seed-borne diseases. Sugarcane seed treatment at 54 ℃ for 8 h (relative humidity 95%-100%) is the most effective against red rot［47]  . Anonymous［48] reported that the treatment with hot and humid air at 54 ℃ for 2 h was more effective in reducing red rot than with hot water at 50 ℃ for 2 h. Treatment of seedlings with aerated steam at 52 ℃ or hot water treatment at 50 ℃ for 150-180 min followed by soaking the seedlings in flowing cold water for 48 h could help eliminate the pathogen in susceptible seedlings［39]  . Edison et al. ［49] compared the effects of hot air treatment at 54 ℃ for 8 h, hot water treatment at 50 ℃ for 2 h and aerated steam treatment at 50 ℃ for 1 h. The results showed that the bud germination of all three treatments was affected. The incidence of red rot in the control was 22.2%, while the incidences of red rot in aerated steam treatment, hot air treatment and hot water treatment were 7.43%, 7.69%, and 19.75%, respectively. The results indicate that heat treatment cannot effectively eradicate red rot fungus. It is because the lethal temperature of conidia of red rot fungus is 60 ℃ for 10 min［19]  , and sugarcane buds cannot withstand such high temperatures. However, it has been reported that treatment of single sprouts with 0.1% carbendazim (Bavistin or Carbendazim) combined with hot water can completely control the disease［50]  .

Agricultural Biotechnology2020

References

［1］ MING R, MOORE PH, WU KK, et al. Sugarcane improvement through breeding and biotechnology［J] . Plant Breed Reviews, 2006(27):115-118.

［2]LAM E, SHINE JR, SILVA JD, et al. Improving sugarcane for biofuel: engineering for an even better feedstock［J] . Global Change Biology Bioenergy, 2009, 1(3):251-255.

［3]HUANG DJ, SUN JH. Research progress on sugarcane breeding［J] . Chinese Journal of Tropical Agriculture, 2012, 32(1): 46-49. (in Chinese)

［4]VIKASH P, SHUKLA DN. Morphological studies on red rot of sugarcane from Hardoi district of Uttar Pradesh［J] . International Journal of Agriculture Innovations and Research, 2017, 6(2):285-288.

［5]HUANG YK, LI WF. Color illustration of modern sugarcane pest and weed control［M] . Beijing: China Agricultural Press, 2016. (in Chinese)

［6]DUTTAMAJUMDAR SK. Red rot of sugarcane［M] . Lucknow India: Army Printing Press, 2008.

［7]HUSSNAIN Z, AFGHAN S. Impact of major cane diseases on sugarcane yield and sugar recovery［J] . Annual Report, 2006: 78-80.

［8]WENT FAFC. Het rood snot［J] . Archiefvoor De Java Suikerindustrie, 1893(1): 265-282.

［9]BHARTI YP, VISHWAKARMA SK, KUMAR A, et al. Physiological and pathological aspects of some new isolates of Colletotrichum falcatum causing red rot disease in Saccharum spp complex［J] . Acta Phytopathologica et Entomologica Hungarica, 2012, 47(1): 35-50.

［10]ALEXANDER KC, VISWANATHAN R. Diseases of sugarcane in India and its rapid diagnosis［M] . USA: SCI Tech Publishing LLC, 2002: 10-51.

［11]VISHWANATHAN R, SAMIYAPPAN R. Disease scenario and management of major sugarcane diseases in India［J] . Crop Protection, 2002(21): 1-10.

［12]VISWANATHAN R. Molecular basis of red rot resistance in sugarcane［J] . Functional Plant Science and Biotechnology, 2012(6): 40-50.

［13]WAN HE. Brief report on the damage of sugarcane red rot［J] . Hubei Plant Protection, 1994(3):18. (in Chinese)

［14]XU ZD, LIU JJ, HUANG HQ, et al. Occurrence and control of major diseases, pests and weeds of sugarcane in Hunan Province［J] . Sugarcane, 2000, 7(2): 16-18. (in Chinese)

［15]XIONG GR, LI ZP, ZHAO TT, et al. Sugarcane diseases and their occurrence in Hainan sugarcane area［J] . Chinese Journal of Tropical Crops, 2010, 31(9): 1589-1595. (in Chinese)

［16]LIN MJ, GONG HL, AN YX, et al. Preliminary study on occurrence of sugarcane red rot disease in Zhangjiang［J] . Sugarcane and Canesugar, 2011(1): 34-37. (in Chinese)

［17]HUO XJ, LI CS, LU RS. Investigation and identification of sugarcane diseases in Guangxi Province［J] . Journal of Anhui Agricultural Sciences, 2013, 41(10): 4368-4369. (in Chinese)

［18]LONG YH, LIU YY, WU XM, et al. Preliminary investigation of the fungal diseases on sugarcane in Guizhou and screening of fungicides against Cercospora longipes ［J] . Plant Protection, 2015, 41(4): 186-190. (in Chinese)

［19]LIANG YQ, LEI ZM, HE CP, et al. The biological characteristics of red rot disease of sugarcane caused by Colletotrichum falcatum ［J] . Chinese Journal of Tropical Crops, 2013, 34(5): 967-972. (in Chinese)

［20]WU WH, HU D, HE CP, et al. Utilization of carbon and nitrogen sources by sugarcane red rot and its indoor toxicity［J] . Sugar Crops of China, 2008(1): 14-17. (in Chinese)

［21]LI ZP, ZHANG SZ. Diagnosis altas of sugarcane diseases and insect pests in Hainan［M] . Beijing: China Agricultural Press，2014. (in Chinese)

［22]SINGH K, SINGH RP, LAL S. Effect of ambient temperature on red rot development in sugarcane［J] . Indian Phytopathology, 1988(41): 86-91.

［23]BENIWAL MS, SATYAVIR. Effect of atmospheric temperature on the development of red rot of sugarcane［J] . Indian Phytopathology, 1991(44): 333-338.

［24]SATYAVIR KA, KUMAR A, RAJ K. Fungal diseases of sugarcane［M] . 2002, New Delhi: Diseases of Field Crops Indus Publishing Company.

［25]YIN Z, HOY JW. Effect of stalk desiccation on sugarcane red rot［J] . Plant Disease, 1997, 81(11): 1247-1250.

［26]SHARMA R, TAMTA S. A review on red rot: The “cancer” of sugarcane［J] . Journal of Plant Pathology and Microbiology. 2015.

［27]SENGAR AS, THIND KS, KUMAR B, et al. In vitro selection at cellular level for red rot resistance in sugarcane ( Saccharum sp.) ［J] . Plant Growth Regulation, 2009, 58(2): 201-209.

［28]SINGH RK, SINGH RB, SINGH S, et al. Genes tagging and molecular diversity of red rot susceptible tolerant sugarcane hybrids using c-DNA and unigene derived markers［J] . World Journal of Microbiology and Biotechnology, 2012(28): 1669-1679.

［29]VISWANATHAN R, MOHANRAJ D, PADMANABAN P, et al. Synthesis of phytoalexins in sugarcane in response to infection by Colletotrichum falcatum Went［J] . Acta Phytopathological Et Entomologica Hungarica, 1996, 31(3): 229-237.

［30]VISWANATHAN R, SAMIYAPPAN R. Induced systemic resistance by fluorescent Pseudomonads against red rot disease of sugarcane caused by Colletotrichum falcatum ［J] . Crop Protection, 2002, 21(1): 1-10.

［31]KUMAR N, JHANG T, SATYAVIR, et al. Molecular and pathological characterization of Colletotrichum falcatum infecting subtropical Indian sugarcane［J] . Journal of Phytopathology, 2011,159 (4): 260-267.

［32]SHARMA R, TAMTA S. Red rot resistant gene characterization using RGAP markers among sugarcane cultivars resistant and susceptible to the red rot disease［J] . Biotech, 2017, 7(5): 306.

［33]KUMAR VG, VISWANATHAN R, MALATHI P, et al. Differential induction of 3-deoxyanthocyanidin phytoalexins in relation to Colletotrichum falcatum resistance in sugarcane. ［J]Sugar Tech, 2015, 17(3): 314-321.

［34]PRITTESH P, AMARESAN N, RUSHABH S, et al. Isolation and pathogenic variability of Colletotrichum falcatum causing red rot in sugarcane［J] . Journal of Plant Diseases and Protection, 2016(123): 273-277.

［35]VISWANATHAN R. Pathogen virulence in sugarcane red rot pathogen versus varieties in cultivation: Classical case of loss in virulence in the pathotype CF06 (Cf671) ［J] . Sugar Tech, 2017, 19(3): 293-299.

［36]GILL RS, MEETA M, THIND KS, et al. Identification of red rot resistant promising crosses［J] . Sugar Tech, 2007, 9(4): 321-324.

［37]SINGH G, SANDHU S K, MEETA M, et al. In vitro induction and characterization of somaclonal variation for red rot and other agronomic traits［J] . Euphytica, 2008, 160(1): 35-47.

［38]WU WH, WANG CX, LIANG YQ, et al. In vitro inhibitory effects of 11 fungicides on mycelial growth of sugarcane red rot pathogen［J] . Chinese Journal of Tropical Agriculture, 2015, 35(6): 37-41. (in Chinese)

［39]SINGH K, SINGH RP. Red rot diseases of sugarcane: major diseases［J] . Elsevier, Amsterdam, 1989:169-188.

［40]KHAN SH, SHAHID M, SAFUREHMAN, et al. Control of red rot disease of sugarcane through screening of varieties and seed dressing fungicides［J] . Pakistan Journal of Phytopathology, 2009, 21(1): 61-65.

［41]MALATHI P, VISWANATHAN R, SUNDAR AR. Mechanized means of sett treatment: An effective way of delivering fungicides for the management of red rot in sugarcane［J] . Sugar Tech. 2017, 19(2):176-182.

［42]MALATHI P, VISWANATHAN R, PADMANABAN P, et al. Compatibility of biocontrol agents with fungicides against red rot disease of sugarcane［J] . Sugar Tech, 2002, 4(3-4): 131-136.

［43]SINGH V, JOSHI BB, AWASTHI SK, et al. Eco-friendly management of red rot disease of sugarcane with Trichoderma strains［J] . Sugar Tech, 2008, 10(2): 158-161.

［44]SENTHIL N, RAGUCHANDER T, VISWANATHAN R, et al. Talc formulated fluorescent Pseudomonads for sugarcane red rot suppression and enhanced yield under field conditions［J] . Sugar Tech, 2003, 5(1-2): 37-43.

［45]HASSAN MN, AFGHAN S, HAFEEZ FY. Biological suppression of sugarcane red rot by Bacillus spp. under field conditions［J] . Journal of Plant Pathology, 2012, 94(2), 325-329.

［46]SINGH K. Hot air therapy against red rot of sugarcane［J] . Plant Disease Reporter, 1973(57): 220-222.

［47]AGNIHOTRI VP. Control of leaf scald of sugarcane by streptomycin and heat therapy［J] . Indian Sugar Crops Journal, 1984(10): 17-18.

［48]ANONYMOUS. Proceedings and Recommendations, all India coordinated project on sugarcane［M] . Lucknow: IISR. 1980.

［49]EDISON S, KSHIRSAGAR SS, ALEXANDER KC. Comparative efficacy of heat treatment viz., hot air, hot water and aerated steam for the control of red rot and smut［J] . SBI, Annual report, 1976: 51-52.

［50]RAO MA, SATYANARAYANA Y. Chemical control of sett-borne infection of red rot pathogen［M] . Lucknow: Sugarcane production constraints and strategies for research and management of red rot Part II, IISR, 1995: 323-330.

Editor: Yingzhi GUANGProofreader: Xinxiu ZHU