Abstract
Tremendous benefits have been derived from the use of fungicides but excessive use of chemical fungicides not only posing threat to human and animal life but also contaminates the prevailing environment. Damage by pathogenic fungi alone causes significant damage to crops like maize, rice, wheat, soybeans, and potatoes. Therefore, it becomes imperative that these diseases are checked and controlled, for which chemical pesticides are being sprayed on plants extensively. Considering the devastating damage and toxicity, the global focus has taken a drift from synthetic chemicals to nature-friendly biological control agents. The present study focuses on the use of biological control agents particularly Trichoderma in sugarcane during Pokkah boeng infection. In the present experiment, twenty promising Trichoderma strains were evaluated for plant growth promotion, lytic enzymes, and physiological and biocontrol activity. Out of the twenty, four potential Trichoderma strains were assessed in the pot experiment viz. T. harzianum strain T28, T41 and T49 and T. aureoviride strain T38. The T. harzianum (T28) showed efficient plant growth-promoting traits as it produced IAA (20.67 µg/ml), phosphorus solubilization (18.57 µg/ml), and cell wall degrading enzymes such as chitinase (24.98 µg/ml) and β-glucanase (29.98 µg/ml). The interference of biocontrol agent T. harzianum (T28) controlled the disease by 73.55%. Apart from this, the inoculation of Trichoderma (T28) enhanced growth attributes including germination percentage (26.61%), mean tiller number (8.28 tiller/pot), individual cane length (241.5 cm), single cane weight (1.13 kg) and the number of milleable canes (6.00 cane/pot). Improvements in physiological activities at different growth stages of the sugarcane crop were observed based on the photosynthetically active radiation (PAR) on the leaf surface, transpiration rate, stomatal conductance, and photosynthetic rate. Further, improvement in juice quality parameters was also observed as it recorded the highest 0brix, sucrose, and commercial cane sugar by 21.26%, 19.28%, and 13.50%, respectively, by applying T. harzianum strain T28. Thus, results proved that T. harzianum strain T28 may be an effective eco-friendly biocontrol tool for managing Pokkah boeng disease in sugarcane. This is the first report of the biocontrol potential of Trichoderma spp. against Fusarium proliferatum causing Pokkah boeng disease in sugarcane.
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References
Altomare C, Norvell WA, Bjbrkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65:2926–2933
Arya A, Sharma R, Sharma G, Kabdwal BC, Negi A, Mishra B (2017) Evaluation of fungal and bacterial antagonists for managing phytopathogen Fusarium moniliforme var. Subglutinans sheldon, causing Pokkah boeng disease of sugarcane. J Biol Control 31(4):217–222
Assigbetse K, Ciss I, Bakhoum N, Dieng L (2012) Effect of inoculation of Acacia senegal mature trees with mycorrhiza and rhizobia on soil properties and microbial community structure. In: Proceedings of the EGU general assembly conference abstracts, Vienna, Austria, pp 2012–8004
Azarmi R, Hajieghrari B, Giglou A (2011) Effect of Trichoderma isolates on tomato seedling growth response and nutrient uptake. Afr J Biotechnol 10:5850–5855. https://doi.org/10.5897/AJB10.1600
Bajinka O, Secka O (2017) Integration of molecular methods into microbiological diagnostics. Appl Microbiol 3:130. https://doi.org/10.4172/2471-9315.1000130
Benitez T, Delgado-Jarana J, Rincon AM, Rey M, Limon MC (1998) Biofungicides: Trichoderma as a biocontrol agent against phytopathogenic fungi. In: Pandalai SG (ed) Recent research developments microbiology. Research Signpost, Trivandrum. 2:129–150
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in-situ assay for indole acetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Brimner TA, Boland GJ (2003) A review of the non-target effects of fungi used to biologically control plant diseases. Agric Ecosyst Environ 100:3–16
Brotman Y, Kapuganti JG, Viterbo A (2010) Trichoderma. Curr Biol 20(9):390–391
Calvet C, Pera J, Barea JM (1989) Interactions of Trichoderma spp. with Glomus mosseae and two wilt pathogenic fungi. Agric Ecosyst Environ 29:59–65
Castro-Escarpulli G, Alonso-Aguilar NM, Sanchez GR, Bocanegra-Garcia V, Guo X, Juarez-Enriquez SR, Luna-Herrera J, Martinez CM, Guadalupe AAM (2015) Identification and typing methods for the study of bacterial infections: a brief review and mycobacterial as case of study. Arch Clin Microbiol 7:1–3
Contreras-Cornejo, Macias-Rodrigues HA, Cortes-Penagos L, Lopez-Bucio C (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592
Cook RJ, Baker KF (1989) The nature practice of biological control of plant pathogens. APS Press, St Paul
Dunaitsev IA, Kolombet LV, Zhigletsova SK, Bystrova EV, Besaeva SG, Klykova MV, Kondrashenko TN (2008) Phosphate releasing microorganisms with antagonistic activity against phytopathogenic microorganisms. Micol Phytopathol 42(3):264–269
Edgar RC (2004) Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
Elad Y, Chet L, Henis Y (1981) A selective medium for improving quantitative isolation of Trichoderma spp. from soil. Phytoparasitica 9(1):59–67
Elena B, Paolo A, Fabio P, Moreno T (2015) Use of Trichoderma spp. and arbuscular mycorrhizal fungi to increase soil beneficial population of bacteria in a nectarine commercial orchard: effect on root growth, nutrient acquisition and replanting disease. J Plant Nutr 39:1147–1155
Elmer WH (2002) Influence of inoculum density of Fusarium oxysporum f. sp. cyclaminis and sodium chloride on cyclamen and development of Fusarium wilt. Plant Dis 86:389–393
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125(1):1–5
Gordon TR (2017) Fusarium oxysporum and the Fusarium wilt syndrome. Annu Rev Phytopathol 55:23–39
Goswami G, Handique PJ, Suresh D (2014) Rhamnolipid biosurfactant against Fusarium sacchari-the causal organism of Pokkah boeng disease of sugarcane. J Basic Microbiol 54:548–557
Haran S, Schickler H, Chet I (1996) Molecular mechanisms of lytic enzymes involved in the biocontrol activity of Trichoderma harzianum. Microbiology 142(9):2321–2331
Harighi MJ, Zamani MR, Motallebi M (2007) Evaluation of antifungal activity of purified chitinase 42 from Trichoderma atroviride PTCC5220. Biotechnology 6(1):28–33
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56
Hermosa MR, Grondona I, Iturriaga EA, Diaz-Minguez JM, Castro C, Monte E (2000) Molecular characterization and identification of bio-control isolates of Trichoderma spp. Appl Environ Microbiol 66(5):1890–1898
Hoyos-carvajal L, Orduz S, Bisset J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51:409–416
Johnson LF, Curl EA (1972) Methods for research on the ecology of soil borne plant pathogens. Burgess Publishing Company, Minneapolis
Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars and L-tryptophan in exudates of vegetables growing on stone wool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Intract 19:250–256
Kapri A, Tewari L (2010) Phosphate solubilization potential and phosphatase activity of rhizospheric Trichoderma spp. Braz J Microbiol 41:787–795. https://doi.org/10.1590/S1517-8382201000500001
Karuppaiyan R, Ram B, Ramdiya S, Ali M, Meena MR (2015) The incidence of Pokkah boeng in indigenous and exotic sugarcane (Saccharum officinarum) clones. Indian J Agric Sci 85(4):596–601
Kotasthane A, Agrawal T, Kushwah R, Rahatkar OV (2015) In-vitro antagonism of Trichoderma spp. against Sclerotium rolfsii and Rhizoctonia solani and their response towards growth of cucumber, bottle gourd and bitter gourd. Eur J Plant Pathol 141:523–543
Kubicek CP, Mach RL, Peterbauer CK, Lorito M (2001) Trichoderma: from genes to biocontrol. J Plant Pathol 83(2):11–23
Kullnig-Gradinger CM, Szakacs G, Kubicek CP (2002) Phylogeny and evolution of the genus Trichoderma: a multigene approach. Mycol Res 106:757–767
Kumar K, Amaresan N, Bhagat S, Madhuri K, Srivastava RC (2012) Isolation and characterization of Trichoderma spp. for antagonistic activity against root rot and foliar pathogens. Indian J Microbiol 52(2):137–144
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lopez-bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123
Lorito M, Farkas V, Rebuffat S, Bodo B, Kucibek CP (1996) Cell wall synthesis is a major target of mycoparasite antagonism by Trichoderma harzianum. J Bacteriol 178:6382–6385
Lorito M, Harman GE, Mastouri F (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417
Matroudi S, Zamani MR, Motallebi M (2009) Antagonistic effects of three species of Trichoderma sp. on Sclerotinia sclerotium, the causal agent of canola stem rot. Egypt J Biol 11:37–44
Mccormick AJ, Cramer MD, Watt DA (2006) Sink strength regulates photosynthesis in sugarcane. New Phytol 171:759–770
Meady GP, Chen GCP (1977) Cane Sugar Handbook, vol 10. Wiley, New York, pp 882–885
Nogues S, Cotxarrera L, Alegre L, Trillas MI (2002) Limitations to photosynthesis in tomato leaves induced by Fusarium wilt. New Phytol 154:461–470
Nordahliawate SMS, Nur Ain Izzati MZ, Azmi AR, Salleh B (2008) Distribution, morphological characterization and pathogenicity of fusarium sacchari associated with Pokkah boeng disease of sugarcane in Peninsular Malaysia. Pertanika J Trop Agric Sci 31(2):279–286
Okorski A, Olszewski J, Pszczolkowska A, Kulik T (2008) Effect of fungal infection and the application of the biological agent Em 1 tm on the rate of photosynthesis and transpiration in pea (Pisum sativum L.) leaves. Pol J Nat Sci 23(1):35–47
Ranghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Mol Biol 50:665–693
Robert C, Bancal MO, Nicolas P, Lannou C, Ney B (2004) Analysis and modelling of effects of leaf rust and Septoria tritici blotch on wheat growth. J Exp Bot 55:1079–1094
Rogers SO, Benedich, (1988) Extraction of DNA from plant tissues. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Kluwer Academic Publishers, Botson, pp 1–10
Rossello-Mora R, Kampfer P (2003) Defining microbial diversity-the species concept for prokaryotic and eukaryotic microorganisms. Microb Divers Bioprospect. https://doi.org/10.1128/978155581777.ch3
Saini R, Pande SK, Yadav JK, Baboo D, Shainy P, Yadav GK (2018) Epidemiology and management of Fusarium oxysporum causing leaf rot disease in Aloe vera. Int J Chem Stud 6(6):2279–2282
Saravanakumar K, Shanmuga AV, Kathiresan K (2013) Effect of Trichoderma on soil phosphate solubilization and growth improvement of Avicennia marina. Aquat Bot 104:101–105
Sharma K, Mishra AK, Misra RS (2009) Morphological, biochemical and molecular characterization of Trichoderma harzianum isolates for their efficacy as bio-control agents. J Phytopathol 157:51–56
Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43
Shukla SK, Singh PN, Chauhan RS, Yadav RL (2012) Recycling of organic wastes amended with Trichoderma and Gluconacetobacter for sustenance in soil health and sugarcane ratoon yield in Udic Ustochrept. Commun Soil Sci Plant Anal 43:1073–1097
Singh A, Chauhan SS, Singh A, Singh SB (2006) Deterioration in sugarcane due to Pokkah boeng disease. Sugar Tech 8:187–190
Singh BN, Singh A, Singh GS, Dwivedi P (2015) Potential role of Trichoderma asperellum T42 strain in growth of pea plant for sustainable agriculture. J Pure Appl Microbiol 9:1069–1074. https://doi.org/10.13140/RG.2.1.4845.3201
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tarafdar JC, Bareja M, Panwar J (2003) Efficiency of some phosphatase producing soil-fungi. Indian J Microbiol 43:27–32
Tiwari R, Shukla SK, Jaiswal VP, Sharma L, Joshi D, Chandra K, Gaur A, Srivastava A, Tiwari RK (2021) Biocontrol potential of Trichoderma spp., against Fusarium spp., the incitants of Pokkah boeng disease of sugarcane under in-vitro conditions. Indian Phytopathol. https://doi.org/10.1007/s42360-021-00344-0
Vassilev N, Medina A, Azcon R, Vasslev M (2006) Microbial solubilization of rock phosphate media containing agro-industrial wastes and effect of the resulting products on plant growth and P uptake. Plant Soil 287:77–84
Yadav RL, Shukla SK, Suman A, Singh PN (2009) Trichoderma inoculation and trash management effects on soil microbial biomass, soil respiration, nutrient uptake and yield of ratoon sugarcane under subtropical conditions. Biol Fertil Soils 45:461–468. https://doi.org/10.1007/s00374-009-0352-4
Yedidia II, Benhamou N, Chet II (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070
Zeilinger S, Galhaup C, Payer K, Woo SL, Mach RL, Feket C, Lorito M, Kubicek CP (1999) Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet Biol 26(2):131–140
Zhang FG (2015) The effects and mechanisms of puta five Trichoderma harzianum mutant and ITS bio-organic fertilizer on growth of cucumber. Nanjing Agricultural University, Nanjing, pp 15–18
Zhou J, Wang M, Sun Y, Gu Z, Wang R, Saydin A, Guo S (2017) Nitrate increased cucumber tolerance to Fusarium wilt by regulating fungal toxin production and distribution. Toxins 9:100
Zhou X, Jia H, Ge X, Wu F (2018) Effects of vanillin on the community structures and abundances of Fusarium and Trichoderma spp. in cucumber seedling rhizosphere. J Plant Interact 13:45–50
Acknowledgements
We express our sincere thanks to the Director, ICAR-Indian Institute of Sugarcane Research, Lucknow (U.P.), for continuous support and for providing us necessary facilities to conduct the studies. We also express our gratitude to AMITY Institute of Biotechnology, Amity University Uttar Pradesh, Lucknow Campus, Lucknow (U.P.) for providing the necessary support to take up research work.
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Tiwari, R., Chandra, K., Shukla, S.K. et al. Interference of bio-control Trichoderma to enhance physical and physiological strength of sugarcane during Pokkah boeng infection. World J Microbiol Biotechnol 38, 139 (2022). https://doi.org/10.1007/s11274-022-03319-z
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DOI: https://doi.org/10.1007/s11274-022-03319-z