Cladosporium cladosporioides C24G Modulates Gene Expression and Enzymatic Activity During Leaf Blast Suppression in Rice Plants

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. 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

    Article  PubMed  Google Scholar 

  2. 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

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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

    Article  PubMed  Google Scholar 

  7. 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

    Article  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. 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

    Article  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. Gene Ontology Consortium (2001) Creating the gene ontology resource: design and implementation. Genome Res. https://doi.org/10.1101/gr.180801

    Article  Google Scholar 

  12. 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

    Article  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

    Article  PubMed  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. 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

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. 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

    Google Scholar 

  27. 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

    Article  PubMed  Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. 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

    Google Scholar 

  32. 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

    Article  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    Article  Google Scholar 

  35. 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

    Article  Google Scholar 

  36. 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

    Article  PubMed  Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. Suprapta DN (2012) Potential of microbial antagonists as biocontrol agents against plant fungal pathogens. JISSAAS 18(2):1–8

    Google Scholar 

  41. 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

    Article  PubMed  PubMed Central  Google Scholar 

  42. 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

    Google Scholar 

  43. 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

    Article  Google Scholar 

  44. 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

    Article  PubMed  PubMed Central  Google Scholar 

  45. 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

    Article  PubMed  PubMed Central  Google Scholar 

  46. 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

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marta Cristina Corsi de Filippi.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

Keywords

  • Biocontrol
  • Oryza sativa
  • Induced resistance
  • Real-time PCR
  • PR proteins