Abstract
The inclusion of biological control in the integrated management of rice blast (Magnaporthe oryzae) is an alternative to reduce pesticides application. C24G, classified, as Cladosporium cladosporioides was isolated from the phylloplane of the rice plant, therefore, adapted to natural conditions of the original habitat. This study aimed to compare four application methods of C24G in rice plants to suppress leaf blast together with the increase in enzymatic activity and expression of defense genes. It was conducted by four assays (1: seed and soil, 2: soil drenching, 3: foliar spray pulverization—preventive and 4: foliar spray pulverization—curative) for choosing the best application method. The best methods identified were further investigated for the activity of Chitinase (CHI), β-1,3-Glucanase (GLU), Lipoxygenase (LOX), Phenylalanine ammonia-lyase (PAL), and Peroxidase (POX) and the expression of Gns1, JIOsPR10, LOX-RLL, and PR1b genes by Real-time PCR. The preventive foliar spray pulverization suppressed up to 83.78% of leaf blast severity, increasing enzymes (CHI, GLU, LOX, and PAL) activity and genes (JIOsPR10, LOX-RLL, and PR1b) expression. We conclude that Cladosporium cladosporioides isolated C24G is a potential biological agent. To prove its potential as a component of sustainable blast management, it should be tested under field conditions. The application of C24G isolate in rice fields can reduce the number of fungicides spraying, generating greater rentability and decreasing environmental contaminations.
Similar content being viewed by others
References
Agrawal GK, Rakwal R, Jwa NS (2000) Rice (Oryzasativa L.) OsPR1b gene is phytohormonally regulated in close interaction with light signals. Biochem Biophys Res Commun. https://doi.org/10.1006/bbrc.2000.3781
Bensch K, Groenewald JZ, Dijksterhuis J, Starink-Willemse M, Andersen B, Summerell BA, Shin HD, Dugan FM, Schroers HJ, Braun U, Crous PW (2010) Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Stud Mycol. https://doi.org/10.3114/sim.2010.67.01
Brunner K, Zeilinger S, Ciliento R, Woo SL, Lorito M, Kubicek CP, Mach RL (2005) Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and induction of plant systemic disease resistance. Appl Environ Microbiol. https://doi.org/10.1128/AEM.71.7.3959-3965.2005
Burketova L, Trda L, Ott PG, Valentova O (2015) Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2015.01.004
Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S (2009) AmiGO: online access to ontology and annotation data. Bioinformatics. https://doi.org/10.1093/bioinformatics/btn615
Castroagudín VL, Ceresini PC, Oliveira SC, Reges JT, Maciel JL, Bonato AL, Dorigan AF, McDonald BA (2015) Resistance to QoI fungicides is widespread in Brazilian populations of the wheat blast pathogen Magnaporthe oryzae. Phytopathology. https://doi.org/10.1094/PHYTO-06-14-0184-R
Chaibub AA, Carvalho JCB, Silva CS, Collevatti RG, Gonçalves FJ, Côrtes MVCB, Filippi MCC, Faria FP, Lopes DCB, Araújo LG (2016) Defence responses in rice plants in prior and simultaneous applications of Cladosporium sp. during leaf blast suppression. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-016-7379-5
Chung EJ, Hossain MT, Khan A, Kim KH, Jeon CO, Chung YR (2015) Bacillus oryzicola sp. nov., an endophytic bacterium isolated from the roots of rice with antimicrobial, plant growth promoting, and systemic resistance inducing activities in rice. Plant Pathol J. 25:256. https://doi.org/10.5423/PPJ.OA.12.2014.0136
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. https://doi.org/10.1016/j.biocontrol.2011.04.016
Francesco A, Martini C, Mari M (2016) Biological control of postharvest diseases by microbial antagonists: how many mechanisms of action? Eur J Plant Pathol. https://doi.org/10.1007/s10658-016-0867-0
Gene Ontology Consortium (2001) Creating the gene ontology resource: design and implementation. Genome Res. https://doi.org/10.1101/gr.180801
Hamayun M, Khan SA, Ahmad N, Tang D, Kang S, Na C, Sohn E, Hwang Y, Shin D, Lee B, Kim J, Lee I (2009) Cladosporium sphaerospermum as a new plant growth-promoting endophyte from the roots of Glycine max (L.) Merr. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-009-9982-9
Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, Hussain J, Sohn EY, Lee IJ (2010) Gibberellin production and plant growth promotion from pure cultures of Cladosporium sp MH-6 isolated from cucumber (Cucumis sativus L). Mycologia. https://doi.org/10.3852/09-261
Hao ZN, Wang LP, Tao RX (2009) Expression patterns of defence genes and antioxidant defence responses in a rice variety that is resistant to leaf blast but susceptible to neck blast. Physiol Mol Plant Pathol. https://doi.org/10.1016/j.pmpp.2009.11.003
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology. https://doi.org/10.1099/mic.0.052274-0
Huang CH, Vallad GE (2018) Soil applications of acibenzolar-S-methyl induce defense gene expression in tomato plants against bacterial spot. Eur J Plant Pathol. https://doi.org/10.1007/s10658-017-1336-0
Jwa N, Agrawal GK, Rakwal R, Park C, Agrawal VP (2001) Molecular cloning and characterization of a novel jasmonate inducible Pathogenesis-Related Class 10 Protein Gene, JIOsPR10, from Rice (Oryzasativa L.) seedling leaves. Biochem Biophys Res Commun. https://doi.org/10.1006/bbrc.2001.5507
Kawahara Y, Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice. https://doi.org/10.1186/1939-8433-6-4
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. https://doi.org/10.1094/PDIS-08-14-0836-RE
Law JWF, 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). https://doi.org/10.3389/fmicb.2017.00003
Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol. https://doi.org/10.1007/s10526-017-9801-4
Levy NO, Harel YM, Haile ZM, Elad Y, Rav-David E, Jurkevitch E, Katan J (2015) Induced resistance to foliar diseases by soil solarization and Trichoderma harzianum. Plant Pathol. https://doi.org/10.1111/ppa.12255
Liu Z, Zhang S, Sun N, Liu H, Zhao Y, Liang Y, Zhang L, Han Y (2015) Functional diversity of jasmonates in rice. Rice. https://doi.org/10.1186/s12284-015-0042-9
Nalley L, Tsiboe F, Durand-Morat A, Shew A, Thoma G (2016) Economic and environmental impact of rice blast pathogen (Magnaporthe oryzae) alleviation in the United States. PLoS ONE. https://doi.org/10.1371/journal.pone.0167295
Nishizawa Y, Saruta M, Nakazono K, Nishio Z, Soma M, Yoshida T (2003) Characterization of transgenic rice plants over-expressing the stress-inducible β-glucanase gene Gns1. Plant Mol Biol. https://doi.org/10.1023/A:1020714426540
Notteghem JL (1981) Cooperative experiment on horizontal resistance to rice blast. 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
Pagliaccia D, Urak RZ, Wong F, Douhan LI, Greer CA, Vidalakis G, Douhan GW (2018) Genetic structure of the rice blast pathogen (Magnaporthe oryzae) over a decade in North Central California rice fields. Microb Ecol. https://doi.org/10.1007/s00248-017-1029-4
Paul D, Park KS (2013) Identification of volatiles produced by Cladosporium cladosporioides CL-1, a fungal biocontrol agent that promotes plant growth. Sensors. https://doi.org/10.3390/s131013969
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, VanWees SCM, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopatol. https://doi.org/10.1146/annurev-phyto-082712-102340
Pooja K, Katoch A (2014) Past, present and future of rice blast management. Plant Sci Today. https://doi.org/10.14719/pst.2014.1.3.24
Prabhu AS, Filippi MCC, 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, Netherlands, pp 257–267
Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Herrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance throught jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol. https://doi.org/10.1007/s10658-011-9782-6
Selisana SM, Yanoria MJ, Quime B, Chaipanya C, Lu G, Opulencia R, Wang GZ, Mitchell T, Correll J, Talbot NJ, Leung H, Zhou B (2017) Avirulence (AVR) Gene-Based diagnosis complements existing pathogen surveillance tools for effective deployment of resistance (R) genes against rice blast disease. Phytopathology. https://doi.org/10.1094/PHYTO-12-16-0451-R
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. https://doi.org/10.1590/S1982-56762013005000028
Shaner G, Finney RF (1977) The effects of nitrogen fertilization on the expression slow-mildewing in Knox wheat. Phytopathology. https://doi.org/10.1094/Phyto-67-1051
Shoresh M, Mastouri F, Harman GE (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol. https://doi.org/10.1146/annurev-phyto-073009-114450
Simmons CR, Litts JC, Huang N, Rodriguez RL (1992) Structure of a rice β-glucanase gene regulated by ethylene, cytokinin, wounding, salicylic acid and fungal elicitors. Plant Mol Biol. https://doi.org/10.1007/BF00018454
Spadaro D, Gullino ML (2004) State of the art and future prospects of the biological control of postharvest fruit diseases. Int J Food Microbiol. https://doi.org/10.1016/S0168-1605(03)00380-5
Sperandio EM, Vale HMM, Reis MS, Cortes MVCB, Lanna AC, Filippi MCC (2017) Evaluation of rhizobacteria in upland rice in Brazil: growth promotion and interaction of induced defense responses against leaf blast (Magnaporthe oryzae). Acta Physiol Plant. https://doi.org/10.1007/s11738-017-2547-x
Suprapta DN (2012) Potential of microbial antagonists as biocontrol agents against plant fungal pathogens. JISSAAS 18(2):1–8
Torres DE, Rojas-Martínez RI, Zavaleta-Mejía E, Guevara-Fefer P, Márquez-Guzmán GJ, Pérez-Martínez C (2017) Cladosporium cladosporioides and Cladosporium pseudocladosporioides as potential new fungal antagonists of Puccinia horiana Henn, the causal agent of chrysanthemum white rust. PLoS ONE. https://doi.org/10.1371/journal.pone.0170782
Vitti A, Sofo A, Scopa A, Nuzzaci M (2015) Sustainable agricultural practices in disease defence of traditional crops in Southern Italy: the case study of tomato cherry protected by Trichoderma harzianum T-22 against Cucumber Mosaic Virus (CMV). In: Vastola A (ed) The sustainability of agro-food and natural resource systems in the Mediterranean Basin. Springer, Cham, pp 133–143
Vlot AC, Dempsey DMA, Klessing DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopatol. https://doi.org/10.1146/annurev.phyto.050908.135202
Wang B, Ebbole DJ, Wang Z (2017) The arms race between Magnaporthe oryzae and rice: diversity and interaction of Avr and R genes. J Integr Agric. https://doi.org/10.1016/S2095-3119(17)61746-5
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. https://doi.org/10.1371/journal.pone.0111484
Zhang YP, Jiang H, Wang L, Zhou J, Zhu DF (2015) A comparative study of stress-related gene expression under single stress and intercross stress in rice. Genet Mol Res. https://doi.org/10.4238/2015.April.17.20
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chaibub, A.A., de Sousa, T.P., de Araújo, L.G. et al. Cladosporium cladosporioides C24G Modulates Gene Expression and Enzymatic Activity During Leaf Blast Suppression in Rice Plants. J Plant Growth Regul 39, 1140–1152 (2020). https://doi.org/10.1007/s00344-019-10052-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-019-10052-9