Antifungal Metabolites of Streptomyces chrestomyceticus STR-2 Inhibits Magnaporthe oryzae, the Incitant of Rice Blast

Current Microbiology - Tập 80 - Trang 1-15 - 2023
R. Rahila1, S. Harish1, K. Kalpana1, G. Anand2, M. Arulsamy1, R. Kalaivanan1
1Department of Plant Pathology, Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, India
2Department of Plant Breeding and Genetics, Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, India

Tóm tắt

Rice, a staple food crop worldwide, suffers devastating yield losses as a result of blast disease caused by Magnaporthe oryzae Cav. The adverse effects of chemicals on the environment are rising concerns for sustainable and eco-friendly approaches. The use of antagonistic microbes for the management of rice blast appears to be a sustainable solution to this challenge. Herein, we isolated 20 Streptomyces strains from rice rhizosphere, among which the isolate STR-2 exhibited maximum inhibition of mycelial growth of M. oryzae accounting for 50% reduction over control. The isolate STR-2 was identified as S. chrestomyceticus through 16S rRNA gene sequencing. In vitro tests demonstrated its ability to produce antifungal and bioactive compounds and also synthesize siderophore, IAA, and phosphate-solubilizing agents, thereby promoting plant growth upon inoculation on rice seeds. GC–MS analysis showed the presence of volatiles, antifungal, antimicrobial, and antioxidant compounds with different retention times. The crude antibiotic extract of 0.5% of S. chrestomyceticus STR-2 reduced the mycelial growth of M. oryzae over the control. Application of talc-based formulation of Streptomyces chrestomyceticus STR-2 resulted in the least disease incidence (15.89%) with the highest disease reduction of 65.26% over untreated control under field condition. These findings indicate the potential of S. chrestomyceticus as a potential bio-inoculant against rice blast disease.

Tài liệu tham khảo

Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x Ashkani S, Rafii MY, Shabanimofrad M, Miah G, Sahebi M, Azizi P, Tanweer FA, Akhtar MS, Nasehi A (2015) Molecular breeding strategy and challenges towards improvement of blast disease resistance in rice crop. Front Plant Sci 6:886. https://doi.org/10.3389/fpls.2015.00886 Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195. https://doi.org/10.1038/nrmicro2032 Kato H (2001) Rice blast disease. Pestic Outlook 12(1):23–25. https://doi.org/10.1039/B100803J Harish S, Parthasarathy S, Durgadevi D, Anandhi K, Raguchander T (2019) Plant growth-promoting rhizobacteria: harnessing its potential for sustainable plant disease management. In: Kumar A, Meena VS (eds) Plant growth promoting rhizobacteria for agricultural sustainability. Springer, Singapore, pp 151–187. https://doi.org/10.1007/978-981-13-7553-8_8 Harish S, Kavino M, Kumar N, Saravanakumar D, Soorianathasundaram K, Samiyappan R (2008) Biohardening with plant growth promoting rhizosphere and endophytic bacteria induces systemic resistance against banana bunchy top virus. Appl Soil Ecol 39(2):187–200. https://doi.org/10.1016/j.apsoil.2007.12.006 Reddy KRK, Jyothi G, Sowjanya C, Kusumanjali K, Malathi N, Reddy KRN (2016) Plant growth-promoting actinomycetes: Mass production, delivery systems, and commercialization. In: Plant growth promoting actinobacteria. Springer, Singapore, pp 287–298. https://doi.org/10.1007/978-981-10-0707-1_19 Vurukonda SSKP, Giovanardi D, Stefani E (2018) Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int J Mol Sci 19:952. https://doi.org/10.3390/ijms19040952 Law JW, Ser HL, Khan TM, Chuah LH, Pusparajah P, Chan KG, Goh BH, Lee LH (2017) The potential of Streptomyces as biocontrol agents against the rice blast fungus, Magnaporthe oryzae (Pyricularia oryzae). Front Microbiol 8:3. https://doi.org/10.3389/fmicb.2017.00003 Copping LG, Duke SO (2007) Natural products that have been used commercially as crop protection agents. Pest Manage Sci 63:524–554. https://doi.org/10.1002/ps.1378 Harsonowati W, Astuti RI, Wahyudi AT (2017) Leaf blast disease reduction by rice-phyllosphere actinomycetes producing bioactive compounds. Gen J Plant Pathol 83:98–108. https://doi.org/10.1007/s10327-017-0700-4 Xiong ZQ, Tu XR, Wei SJ, Huang L, Li XH, Lu H, Tu GQ (2013) In vitro antifungal activity of antifungalmycin 702, a new polyene macrolide antibiotic, against the rice blast fungus Magnaporthe grisea. Biotechnol Lett 35(9):1475–1479. https://doi.org/10.1007/s10529-013-1229-z Tamura T, Shinzato N, Ito M, Ueno M (2019) Microbial secondary metabolite induction of abnormal appressoria formation mediates control of rice blast disease caused by Magnaporthe oryzae. J Phytopathol 167(3):156–162. https://doi.org/10.1111/jph.12782 Taridaporn B, Lapanun S, Supothina S, Rachtawee P, Chunhametha S, Suriyachadkun C, Boonruangprapa T, Auncharoen P, Chutrakul C, Vichai V (2016) Polycyclic tetrahydroxanthones from Streptomyces chrestomyceticus BCC 24770. Tetrahedron 72(5):775–778. https://doi.org/10.1016/j.tet.2015.12.045 Mior ZA, Tong PE, Mohammadpourlima M, Yun WM (2017) Morphological and molecular characterizations of rice blast fungus, Magnaporthe oryzae. Pak J Agric Sci 54:765–772. https://doi.org/10.21162/PAKJAS/17.3786 Srivastava D, Shamim MD, Kumar D, Pandey P, Khan NA, Singh KN (2014) Morphological and molecular characterization of Pyricularia oryzae causing blast disease in rice (Oryza sativa) from North India. Int J Sci Res Publ 4:1–9 Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. for bigger datasets. Mol Biol Evol 33:1870–1874 Garcha S, Katyal P, Sharma V (2016) Microbial diversity in soil under different land use systems in sub-mountainous zone of Punjab. J Indian Soc Soil Sci 64(3):271–275. https://doi.org/10.5958/0974-0228.2016.00038.4 Parte A, Whitman WB, Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI (2012) Bergey’s manual of systematic bacteriology: volume 5: the actinobacteria. Springer, New York Boukaew S, Prasertsan P (2014) Suppression of rice sheath blight disease using a heat stable culture filtrate from Streptomyces philanthi RM-1-138. Crop Prot 61:1–10. https://doi.org/10.1016/j.cropro.2014.02.012 Masand M, Sivakala KK, Menghani E, Thinesh T, Anandham R, Sharma G, Sivakumar N, Jebakumar SRD, Jose PA (2018) Biosynthetic potential of bioactive Streptomycetes isolated from arid region of the Thar desert, Rajasthan (India). Front Microbiol 9:687. https://doi.org/10.3389/fmicb.2018.00687 Li Q, Jiang Y, Ning P, Zheng L, Huang J, Li G, Jiang D, Hsiang T (2011) Suppression of Magnaporthe oryzae by culture filtrates of Streptomyces globisporus JK-1. Biol Control 58(2):139–148. https://doi.org/10.1016/j.biocontrol.2011.04.013 Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U (2016) Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbiol Res 192:260–270. https://doi.org/10.1016/j.micres.2016.08.005 Manigundan K, Joseph J, Ayswarya S, Vignesh A, Vijayalakshmi G, Soytong K, Gopikrishnan V, Radhakrishnan M (2020) Identification of biostimulant and microbicide compounds from Streptomyces sp. UC1A-3 for plant growth promotion and disease control. Int J Agric Technol 16:1125–1144 Tang YW, Bonner J (1948) The enzymatic inactivation of indole acetic acid; the physiology of the enzyme. Am J Bot 35:570–578. https://doi.org/10.2307/2438053 Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9 Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x Gopalakrishnan S, Humayu P, Vadlamudi S, Vijayabharathi R, Bhimineni RK, Rupela O (2012) Plant growth-promoting traits of Streptomyces with biocontrol potential isolated from herbal vermicompost. Biocontrol Sci Technol 22(10):1199–1210. https://doi.org/10.1080/09583157.2012.719151 Adhilakshmi M, Latha P, Paranidharan V, Balachandar D, Ganesamurthy K, Velazhahan R (2014) Biological control of stem rot of groundnut (Arachis hypogaea L.) caused by Sclerotium rolfsii Sacc. with actinomycetes. Arch Phytopathol Plant Prot 47(3):298–311. https://doi.org/10.1080/03235408.2013.809224 Hasan NA, Rafii MY, Rahim HA, Ali NS, Mazlan N, Abdullah S (2016) Morphological and molecular characterization of fungal pathogen, Magnaphorthe oryzae. AIP Conf Proc. https://doi.org/10.1063/1.4940263 Zarandi ME, Bonjar GHS, Dehkaei FP, Moosavi SAA, Farokhi PR, Aghighi S (2009) Biological control of rice blast (Magnaporthe oryzae) by use of Streptomyces sindeneusis isolate 263 in greenhouse. Am J Appl Sci 6(1):194–199. https://doi.org/10.3844/ajas.2009.194.199 Aruna J, Kumar SV, Rambabu R, Ramesh S, Yashaswini C, Bhaskar B, Madhavi KR, Balachndran SM, Ravindrababu V, Prasad MS (2016) Morphological characterization of five different isolates of Pyricularia oryzae causing rice blast disease. Progress Res 11:3377–3380 Salim FM, Sharmili SA, Anbumalarmathi J, Umamaheswari K (2017) Isolation, molecular characterization and identification of antibiotic producing actinomycetes from soil samples. J Appl Pharm Sci 7:69–75. https://doi.org/10.7324/JAPS.2017.70909 Boukaew SA, Plubrukam PP (2013) Effect of volatile substances from Streptomyces philanthi RM-1-138 on growth of Rhizoctonia solani on rice leaf. Biol Control 58:471–482. https://doi.org/10.1007/s10526-013-9510-6 Aldesuquy HS, Mansour FA, Abo-Hamed SA (1998) Effect of the culture filtrates of Streptomyces on growth and productivity of wheat plants. Folia Microbiol 43(5):465–470. https://doi.org/10.1007/BF02820792 Chen YD, Zhou QD, Gao Z, Xie J, Luo Y (2018) Growth promotion and disease suppression ability of a Streptomyces sp. CB-75 from banana rhizosphere soil. Front Microbiol 8:2704. https://doi.org/10.3389/fmicb.2017.02704 Saleh M (2018) Evaluation of endophytes isolated from rice leaves for their antifungal activities against Pyricularia oryzae causative blast disease. Egypt J Phytopathol 46:193–214. https://doi.org/10.21608/ejp.2018.87788 Awla HK, Kadir J, Othman R, Rashid TS, Wong MY (2016) Bioactive compounds produced by Streptomyces sp. isolate UPMRS4 and antifungal activity against Pyricularia oryzae. Am J Plant Sci 7:1077. https://doi.org/10.4236/ajps.2016.77103 Newitt JT, Prudence SMM, Hutchings MI, Worsley SF (2019) Biocontrol of cereal crop diseases using Streptomycetes. Pathogens 8:78. https://doi.org/10.3390/pathogens8020078 Mun BG, Lee WH, Kang SM, Lee SU, Lee SM, Lee DY, Shahid M, Yun BW, Lee IJ (2020) Streptomyces sp. LH 4 promotes plant growth and resistance against Sclerotinia sclerotiorum in cucumber via modulation of enzymatic and defense pathways. Plant Soil. https://doi.org/10.1007/s11104-019-04411-4 Prabavathy VR, Mathivanan N, Murugesan K (2006) Control of blast and sheath blight diseases of rice using antifungal metabolites produced by Streptomyces sp. PM5. Biol Control 39:313–319. https://doi.org/10.1016/j.biocontrol.2006.07.011 Chaiharn M, Theantana T, Pathom-Aree W (2020) Evaluation of biocontrol activities of Streptomyces spp. against rice blast disease fungi. Pathogens 9:126. https://doi.org/10.3390/pathogens9020126 Awla HK, Kadir J, Othman R, Rashid TS, Hamid S, Wong MY (2017) Plant growth-promoting abilities and biocontrol efficacy of Streptomyces sp. UPMRS4 against Pyricularia oryzae. Biol Control 112:55–63. https://doi.org/10.1016/j.biocontrol.2017.05.011 Xu T, Li Y, Zeng X, Yang X, Yang Y, Yuan S, Hu X, Zeng J, Wang Z, Liu Q (2017) Isolation and evaluation of endophytic Streptomyces endus OsiSh-2 with potential application for biocontrol of rice blast disease. J Sci Food Agric 97:1149–1157. https://doi.org/10.1002/jsfa.7841 Xu T, Cao L, Zeng J, Franco CMM, Yang Y, Hu X, Liu Y, Wang X, Gao Y, Bu Z (2019) The antifungal action mode of the rice endophyte Streptomyces hygroscopicus OsiSh-2 as a potential biocontrol agent against the rice blast pathogen. Pest Biochem Physiol 160:58–69. https://doi.org/10.1016/j.pestbp.2019.06.015 Gao Y, Zeng XD, Ren B, Zeng JR, Xu T, Yang YZ, Hu XC, Zhu ZY, Shi LM, Zhou GY (2020) Antagonistic activity against rice blast disease and elicitation of host-defence response capability of an endophytic Streptomyces albidoflavus OsiLf-2. Plant Pathol 69:259. https://doi.org/10.1111/ppa.13118 Ilsan NA (2017) Antifungal activity of phyllosphere actinobacteria against Pyricularia oryzae. In: 2nd international seminar on global health (ISGH), pp 308–315 Awla HK (2021) Effect of Streptomyces xantholiticus on rice blast disease reduction and enzyme activity. Polytechnic J 11(1):112–117. https://doi.org/10.25156/ptj.v11n1y2021.pp112-117 Liu Y, Chen N, Gao Y, Bu Z, Niu S, Wang Y, Liu X, Zhu Y (2021) Physiological, biochemical and proteomic insight into the response system of Streptomyces hygroscopicus OsiSh-2 to rice blast fungus toxins. Appl Soil Ecol 167:104058. https://doi.org/10.1016/j.apsoil.2021.104058 Liu W, Wang J, Li S, Zhang H, Meng L, Liu L, Ping W, Du C (2022) Genomic and biocontrol potential of the crude lipopeptide by Streptomyces bikiniensis HD-087 against Magnaporthe oryzae. Front Microbiol. https://doi.org/10.3389/fmicb.2022.888645