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Defence responses in rice plants in prior and simultaneous applications of Cladosporium sp. during leaf blast suppression

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Abstract

An alternative method to control rice blast (Magnaporthe oryzae) is to include biological agent in the disease management strategy. The objective of this study was to assess the leaf blast-suppressing effects of rice phylloplane fungi. One Cladosporium sp. phylloplane fungus was shown to possess biocontrolling traits based on its morphological characteristics and an analysis of its 18S ribosomal DNA. Experiments aimed at determining the optimal time to apply the bioagent and the mechanisms involved in its rice blast-suppressing activities were performed under controlled greenhouse conditions. We used foliar spraying to apply the Cladosporium sp. 48 h prior to applying the pathogen, and we found that this increased the enzymatic activity. Furthermore, in vitro tests performed using isolate C24 showed that it possessed the ability to secrete endoxylanases and endoglucanases. When Cladosporium sp. was applied either prior to or simultaneous with the pathogen, we observed a significant increase in defence enzyme activity, and rice blast was suppressed by 84.0 and 78.6 %, respectively. However, some enzymes showed higher activity at 24 h while others did so at 48 h after the challenge inoculation. Cladosporium sp. is a biological agent that is capable of suppressing rice leaf blast by activating biochemical defence mechanisms in rice plants. It is highly adapted to natural field conditions and should be included in further studies aimed at developing strategies to support ecologically sustainable disease management and reduce environmental pollution by the judicious use of fungicidal sprays.

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References

  • Aidemark M, Tjellström H, Sandelius AS, Stålbrand H, Andreasson E, Rasmusson AG, Widell S (2010) Trichoderma viride cellulase induces resistance to the antibiotic pore-forming peptide alamethicin associated with changes in the plasma membrane lipid composition of tobacco BY-2 cells. BMC Plant Biol 10:274

    Article  CAS  Google Scholar 

  • Ashizawa T, Zenbayashi K, Sonoda R (2005) Effects of preinoculation with an avirulent isolate of Pyricularia grisea on infection and development of leaf blast lesions caused by virulent isolates on near-isogenic lines of Sasanishiki rice. J Gen Plant Pathol 71:345–350

    Article  Google Scholar 

  • Attaran E, Zeier TE, Griebel T, Zeier J (2009) Systemic acquired resistance in Arabidopsis is independent of methyl salicylate production and jasmonate signaling. Plant Cell 21:954–971

    Article  CAS  Google Scholar 

  • Axelrod B, Cheesbrough TM, Laakso S (1981) Lipoxygenase from soybean. Methods Enzymol 71:441–451

    Article  CAS  Google Scholar 

  • Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401

    Article  CAS  Google Scholar 

  • Chen C, Lian B, Hu J, Zhai H, Wang X, Venu R, Liu E, Wang Z, Chen M, Wang B (2013) Genome comparison of two Magnaporthe oryzae field isolates reveals genome variations and potential virulence effectors. BMC Genomics 14:887

    Article  Google Scholar 

  • Filippi MCC, Silva GB, Prabhu AS (2007) Indução de resistência à brusone em folhas de arroz por isolado avirulento de Magnaporthe oryzae. Fitopatol Bras 32:387–392

    Article  Google Scholar 

  • Filippi MCC, Silva GB, Silva-Lobo VL, Côrtes MVCB, Moraes AJG, Prabhu AS (2011) Leaf blast (Magnaporthe oryzae) suppression and growth promotion by rhizobacteria on aerobic rice in Brazil. Biol Control 58:160–166

    Article  Google Scholar 

  • Jackson AJ, Walters D, Marshall G (1997) Antagonistic interactions between the foliar pathogen Botrytis fabae and isolates of Cladosporium tenuissimum in vitro and Cladosporium cladosporioides on faba beans. Biol Control 8:97–106

    Article  Google Scholar 

  • Keesey J (1987) Biochemica information. Indianapolis, Boehringer Manhein Biochemicals

    Google Scholar 

  • Köhl J, Scheer C, Holb IJ, Masny S, Molhock W (2015) Toward an integrated use of biological control by Cladosporium cladosporioides H39 in apple scab (Venturia inaequalis) management. Plant Dis 99:535–543

    Article  Google Scholar 

  • Manandhar HK, Jorgensen HJL, Mathur SB, Smedegaard-Petersen V (1998) Resistance to rice blast induced by ferric chloride, di-potassium hydrogen phosphate and salicylic acid. Crop Prot 17:323–329

    Article  CAS  Google Scholar 

  • Manly BFJ (2007) Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall/ CRC, Boca Raton

    Google Scholar 

  • McDougall P (2013) R&D trends for chemical crop protection products and the position of the European market. A consultancy study undertaken for ECPA, Phillips McDougall Ltd, United Kingdom

    Google Scholar 

  • Miller GL (1959) Use of dinitrosalicylic acid reagent for the determination of reducing sugar. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Nawrocka J, Małolepsza U (2013) Diversity in plant systemic resistance induced by Trichoderma. Biol Control 67:149–156

    Article  Google Scholar 

  • Naznin HA, Kiyohara D, Kimura M, Mitsuo M, Shimizu M, Hyakumachi M (2014) Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS One 9:1–10

    Article  Google Scholar 

  • Notteghem JL (1981) Cooperative experiment on horizontal resistance to rice blast. In: BLAST and upland rice: report and recommendations from the meeting for international collaboration in upland rice improvement. International Rice Research Institute, Los Baños, pp. 43–51

    Google Scholar 

  • Pan SQ, Ye XS, Kuc J (1991) Association of a β-1,3-glucanase activity and isoform pattern with systemic resistance to blue mold in tobacco induced by stem injection with Peronospora tabacina or leaf inoculation with Tobacco mosaic virus. Physiol Mol Plant Pathol 39:25–39

    Article  CAS  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopatol 52:347–375

    Article  CAS  Google Scholar 

  • Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, Verhagen BWM, Léon-Kloosterziel K, Hase S, De Vos M, Oosten VV, Pozo M, Spoel S, Van Der Ent S, Koornneef A, Chalfun-Junior A, Resende MLV, Van Loon LC (2005) Indução de resistência sistêmica por rizobactérias e comunicação na rota de sinalização para uma defesa refinada. Rev Anu Patol Plantas 13:277–295

    Google Scholar 

  • Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    Article  CAS  Google Scholar 

  • Pontecorvo G, Roper JA, Hemmons LM, MaC Donald KD, Bufton AWJ (1953) The genetics of Aspergillus nidulans. Adv Genet 5:141–238

    CAS  Google Scholar 

  • Prabhu AS, Filippi MC, Silva GB, Silva-Lobo VL, Morais OP (2009) An unprecedented outbreak of rice blast on a newly released cultivar BRS Colosso in Brazil. In: Wang GL, Valent B (eds) Advances in genetics, genomics and control of rice blast. Springer Science, Netherlands, pp. 257–267

    Chapter  Google Scholar 

  • Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2002) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049–1055

    Article  CAS  Google Scholar 

  • Ruegger MJS, Tauk-Tornisielo SM (2004) Atividade de celulase de fungos isolados do solo da Estação Ecológica de Juréia-Itatins, São Paulo, Brasil. Revista Brasil Bot 27:205–211

    Article  CAS  Google Scholar 

  • Sakagami Y, Sano A, Hara O, Mikawa T, Marumo S (1995) Cladosporol, β-1,3-glucan biosynthesis inhibitor, isolated by the fungus Cladosporium cladosporioides. Tetrahedron Lett 36:1469–1472

    Article  CAS  Google Scholar 

  • Sena APA, Chaibub AA, Côrtes MVCB, Silva GB, Silva-Lobo VL, Prabhu AS, Filippi MCC, Araujo LG (2013) Increased enzymatic activity in rice leaf blast suppression by crude extract of Epicoccum sp. Trop Plant Pathol 38:387–397

    Article  Google Scholar 

  • Shaner G, Finney RF (1977) The effects of nitrogen fertilization on the expression slow-mildewing in Knox wheat. Phytopathology 67:1051–1055

    Article  CAS  Google Scholar 

  • Sharma HSS (1987) Polysaccharide-degrading enzymes associated with fungal spoilage of bleached flax rove. Trans Br Mycol Soc 88:122–125

    Article  CAS  Google Scholar 

  • Shoresh M, Mastouri F, Harman GE (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    Article  CAS  Google Scholar 

  • Smith JA, Métraux JP (1991) Pseudomonas syringae pv. syringae induces systemic resistance to Pyricularia oryzae in rice. Physiol Mol Plant Pathol 39:451–461

    Article  Google Scholar 

  • Tsukamoto H, Tsutsumi F, Onodera K, Yamada M, Fujimori T (1999) Biological control of rice leaf blast with Exserohilum monoceras, a pathogen of Echinochloa species. Jpn J Phytopathol 65:543–548

    Article  Google Scholar 

  • Van Der Ent S, Saskia CM, Wees V, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588

    Article  CAS  Google Scholar 

  • Verberne MC, Hoekstra J, Bol J, Linthorst HJM (2003) Signaling of systemic acquired resistance in tobacco depends on ethylene perception. Plant J 35:27–32

    Article  CAS  Google Scholar 

  • Wang YL, Liu SY, Mao XQ, Zhang Z, Jiang H, Chai RY, Qiu HP, Wang JY, Du XF, Li B, Sun GC (2013) Identification and characterization of rhizosphere fungal strain MF-91 antagonistic to rice blast and sheath blight pathogens. J Appl Microbiol 114:1480–1490

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp. 315–322

    Google Scholar 

  • Zhan G, Tian Y, Wang F, Chen X, Guo J, Jiao M, Huang L, Kang Z (2014) A novel fungal hyperparasite of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One 9:1–8

    Google Scholar 

  • Zolan M, Pukkila P (1986) Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6:195–200

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the Goiás State Research Support Foundation (FAPEG) and Goiás Federal University (UFG) for providing financial support for this research, the Coordination for the Improvement of Higher Education Personnel (CAPES) for financial support to the first author, the Multiuse Microscopic Laboratory (LabMic) of UFG for the SEM analysis and Dr. Anne Sitarama Prabhu for critically reading the manuscript.

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Correspondence to Marta Cristina Corsi de Filippi.

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Responsible Editor:Yi-ping Chen

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Chaibub, A.A., de Carvalho, J.C.B., de Sousa Silva, C. et al. Defence responses in rice plants in prior and simultaneous applications of Cladosporium sp. during leaf blast suppression. Environ Sci Pollut Res 23, 21554–21564 (2016). https://doi.org/10.1007/s11356-016-7379-5

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  • DOI: https://doi.org/10.1007/s11356-016-7379-5

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