European Journal of Plant Pathology

, Volume 153, Issue 4, pp 1185–1202 | Cite as

Induction of resistance to Bambusa pervariabilis×Dendrocalamopsis grandis blight by protein AP-toxin and response of culturable microorganisms

  • Shujiang Li
  • Qianqian He
  • Qi Peng
  • Hanmingyue Zhu
  • Shuhan Li
  • Tianhui ZhuEmail author


The protein Arthrinium phaeospermum toxin (AP-toxin) was isolated from Arthrinium phaeospermum, which is the pathogen of bamboo blight. The present study demonstrated that disease resistance against bamboo blight (caused by A. phaeospermum) in Bambusa pervariabilis×Dendrocalamopsis grandis varieties could be induced by the application of inactivated protein AP-toxin (40 μg/mL, treated at 60 °C) to branches. Culturable microorganisms from three varieties of bamboo showed responses to various epiphytic and endophytic species and numbers after the application of inactivated protein AP-toxin. The plate dilution and tissue separation methods were used to separate the epiphytic and endophytic microorganisms of the three bamboo varieties from twigs collected at four different time points, and morphological characterization and molecular biology techniques were used to identify the fungi, bacteria and actinomyces species and record the quantities. The results showed that the numbers and species of epiphytic and endophytic microorganisms were significantly correlated with the disease index, treatment method (Treated: only AP-toxin, Treated+Infected: AP-toxin+A. phaeospermum, Infected: sterilized water+ A. phaeospermum, Control: only sterilized water) and resistance of the varieties. Moreover, the species of epiphytic bacteria were highly correlated to the resistance of the varieties. The above fingings indicate that the inactivated protein AP-toxin can be used as an inducible factor to change the response of a culturable microorganism and thereby improve the resistance of bamboo.


Bambusa pervariabilis×Dendrocalamopsis grandis blight Disease resistance Induced effect Microbial response Protein AP-toxin 



This research was supported by the National Natural Science Foundation of China (31700568), the China Postdoctoral Science Foundation (2016 M602705) and College Students’ innovation and entrepreneurship training program of Sichuan Province (201810626117).


  1. Avdiushko, S. A., Ye, X. S., & Kuc, J. (1993). Detection of several enzymatic activities in leaf prints of cucumber plants. Physiological and Molecular Plant Pathology, 42(6), 441–454.CrossRefGoogle Scholar
  2. Bredbrook, J. R., & Mattews, R. E. F. (1973). Change in the flow of early products of photosynthetic carbon fixation associated with reoplication of TXMV. Virology, 53(1), 84–91.CrossRefGoogle Scholar
  3. Cai, X. Z., Zheng, Z., & Song, F. M. (1996). Effect of salicylic acid on the induction of resistance to rice seedling blast. Acta Phytopathologica Sinica, 26(1), 7–12.Google Scholar
  4. Dean, R. A., & Kuc, J. (1987). Rapid lignification in response to wounding and infection as a mechanism for induced systemic protection in cucumber. Physiological and Molecular Plant Pathology, 31(1), 69–81.CrossRefGoogle Scholar
  5. Dimki, I., Zivkovi, S., Beri, T., Lvanovi, Z., Gavrilovi, V., Stankovi, S., & Fira, D. (2013). Characterization and evaluation of two Bacillus strains, SS-12.6 and SS-13.1, as potential agents for the control of phytopathogenic bacteria and fungi. Biological Control, 65(3), 312–321.CrossRefGoogle Scholar
  6. Fang, Z. D. (1998). The research method of plant disease. Beijing: China Agriculture Press.Google Scholar
  7. Feng, B., Chen, Y., Zhao, C., Zhao, X., Bai, X., & Du, Y. (2006). Isolation of a novel Ser/Thr protein kinase gene from oligochitosan-induced tobacco and its role in resis-tance against tobacco mosaic virus. Plant Physiology and Biochemistry, 44(10), 596–603.CrossRefGoogle Scholar
  8. Freitas, J. R. D., & Germida, J. J. (1990). Plant growth promoting rhizobacteria for winter wheat. Canadian Journal of Microbiology, 36(36), 265–272.CrossRefGoogle Scholar
  9. Hagedorn, C., Gould, W. D., & Bardinelli, T. R. (1989). Rhizobacteria of cotton and their repression of seedling disease pathogens. Applied and Environmental Microbiology, 55(11), 2793–2797.Google Scholar
  10. Han, S., & Zhu, T. H. (2009). Isolation, purification and structure of Cp-I toxin from Cryphonectria parasitica. Mycosystema, 28(4), 535–540.Google Scholar
  11. Han, S., Zhu, T. H., Li, S. J., & Li, F. L. (2011). Effect of Cryphonectria parasitica toxin on lipid peroxidation and ultrastructure in two Chinese chestnut cultivars. African Journal of Biotechnology, 10(65), 14404–14409.CrossRefGoogle Scholar
  12. He, Q.Q., Liu Y.X., Fang X.M., Zhu T.H., Qiao T.M., Han S., Li S.J. (2018). Screening of induced factor of Bambusa pervariabilis × Dendrocalamopisis grandis against Arthrinium phaeospermum and its duration. Plant Protection,
  13. Huang, Z. C., & Zhu, T. H. (2007). Effective fungicide screening against pathogen of hybrid bamboo blight in lab. Forest Pest and Disease, 26(3), 35–38.Google Scholar
  14. Hyun, J. S., Chandra, P. N., Xin, D. J., Sook, K. Y., & Sik, Y. B. (2013). Biocontrol activity of Bacillus amyloliquefaciens CNU114001 against fungal plant diseases. Mycobiology, 41(4), 234–242.CrossRefGoogle Scholar
  15. Keller, N. P., Butchko, R., Sarr, A., & Phillips, T. D. (1994). A visual pattern of mycotoxin production in maize kernels by Aspergillus spp. Phytopathology, 84(5), 483–488.CrossRefGoogle Scholar
  16. Li, S.J. (2013). Protein toxin produced from Arthrinium phaeospermum causing blight in Bambusa pervariabilis × Dendrocalamopsis grandis and its accurate pathogenic mechanism. Doctoral Dissertation, Sichuan Agricultural University, China.Google Scholar
  17. Li, S. J., & Zhu, T. H. (2013). Biochemical response and induced resistance against anthracnose (Colletotrichum camelliae) of camellia (Camellia pitardii) by chitosan oligosaccharide application. Forest Pathology, 43(1), 67–76.Google Scholar
  18. Li, S. J., & Zhu, T. H. (2014). Purification of the toxin protein pc from Arthrinium phaeospermum and its effect on the defence enzymes of Bambusa pervariabilis×Dendrocalamopsis grandis varieties. Forest Pathology, 44(2), 96–106.CrossRefGoogle Scholar
  19. Li, M., Tan, G. J., Li, Y., Ding, K. J., Chan, Z. L., & Ling, Y. (2009). Relationships between the contents of phenolics, soluble proteins in plants of kiwifruit cultivars and their resistance to kiwifruit bacterial canker by Pseudomonas syringae pv. actinidiae. Plant Protection, 35(1), 37–41.Google Scholar
  20. Li, S. J., Zhu, T. H., Li, F. L., Qiao, T. M., & Han, S. (2010). Selection of an antagonistic bacterium against Arthrinium phaeospermum and analysis of its antibacterial substance. Chinese Journal of Biological Control, 26(S1), 55–61.Google Scholar
  21. Li, S. J., Peng, Y., Zhu, T. H., Zhu, H. M. Y., Mao, C., & Qiao, T. M. (2012). Diversity of epiphytic fungi on the diseased and healthy leaves of Bambusa. African Journal of Microbiology Research, 6(49), 7556–7563.CrossRefGoogle Scholar
  22. Li, S. J., Liang, M., Zhu, T. H., & Yang, C. Q. (2013a). Selection of an antagonistic bacterium against Arthriuium phaeospermum and its antibacterial protein analysis. Journal of Nanjing Forestry University (Natural Sciences Edition), 37(6), 27–32.Google Scholar
  23. Li, S. J., Zhu, T. H., Zhu, H. M. Y., Liang, M., Qiao, T. M., Han, S., & Che, G. N. (2013b). Purification of protein AP-toxin from Arthrinium phaeospermum causing blight in Bambusa pervariabilis×Dendrocalamopsis grandis and its metabolic effects on four bamboo varieties. Phytopathology, 103(2), 135–145.CrossRefGoogle Scholar
  24. Liu, Y.G. (2002). Study on identification of toxin from Cercospora sojina and the pathogenesis as well as induced resistance. Doctoral Dissertation, Northeast Agricultural University, China.Google Scholar
  25. Loh, J., Pierson, E. A., Lii, L. S. P., Stacey, G., & Chatterjee, A. (2002). Quorum sensing in plant-associated bacteria. Current Opinion in Plant Biology, 5(4), 285–290.CrossRefGoogle Scholar
  26. Ma, X. J., & Zhu, D. H. (2003). Functional roles of the plant superoxide dismutase. Hereditas, 25(2), 225–231.Google Scholar
  27. Maechesi, J. R., Sato, T., Weightman, A. J., Martin, T. A., Fry, J. C., Hiom, S. J., & Wade, W. G. (1998). Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Applied and Environmental Microbiology, 84(2), 795–799.Google Scholar
  28. Martin, D. F., Priest, F. G., Todd, C., & Goodfellow, M. (1980). Distribution of beta-glucanases within the genus Bacillus. Applied and Environmental Microbiology, 40(6), 1136–1138.Google Scholar
  29. Mayumi, E., Hajime, A., Takashi, T., Hiroshi, O., & Motoichiro, K. (2009). Induced resistance in tomato plants to the toxin-dependent necrotrophic pathogen Alternaria alternate. Physiological and Molecular Plant Pathology, 73(4–5), 67–77.Google Scholar
  30. Okuno, T., Nakyama, M., Okajima, N., & Furusawa, I. (2009). Systemic resistance to downy mildew and appearance of acid soluble proteins in cucumber leaves treated with biotic and abiotic inducers. Annals of the Phytopathological Society of Japan, 57(2), 203–211.CrossRefGoogle Scholar
  31. Peng, Y., Mao, C., Zhu, T. H., & Liu, Y. (2015). Foliar bacterial diversity of Bambusa pervariabilis×Dendrocalamopsis daii. Journal of Northeast Forestry University, 43(6), 67–71.Google Scholar
  32. Ran, L. X., Gu, W. Z., & Wu, G. J. (2004). Role of salicylic acid in induction of resistance against bacterial wilt in Eucalyptus urophylla and changes of peroxidase and polyphenol oxidase. Forest Research, 17(1), 12–18.Google Scholar
  33. Roberts, M. R., & Paul, N. D. (2006). Seduced by the dark side: Integrating molecular and ecological perspectives on the influence of light onplant defense against pests and pathogens. New Phytologist, 170(4), 677–699.CrossRefGoogle Scholar
  34. Shahin, E. A., & Spivey, R. (1986). Asingle dominant gene for Fusarium wilt resistance in protoplast-derived tomato plants. Theoretical and Applied Genetics, 73(2), 164–169.CrossRefGoogle Scholar
  35. Swift, S., Throup, J. P., Williams, P., Salmond, G. P. C., & Stewart, G. S. A. B. (1996). Quorum sensing :A population-density component in the determination of bacterial phenotype. Trends in Biochemical Sciences, 21(6), 214–219.CrossRefGoogle Scholar
  36. Tsukada, K., Ishizaka, M., Fujisawa, Y., Iwasaki, Y., Yamaguchi, T., Minami, E., & Shibuya, N. (2002). Rice receptor for chitin oligosaccharide elic-itor does not couple to heterotrimeric G-protein: Elicitor responses of suspension cultured rice cells from Daikoku dwarf (d1) mutants lacking a functional G-protein a-subunit. Physiologia Plantarum, 116(3), 373–382.CrossRefGoogle Scholar
  37. Walters, D. R., Newton, A. C., & Lyon, G. D. (2005). Induced resistance: Helping plants to help themselves. Biologist, 52, 28–33.Google Scholar
  38. Wan, Z. X., Zhu, J. J., & Qiang, S. (2001). The pathogenic mechanism of toxin of Alternaria alternate (Fr.) Keissler to Eupatorium adenophorum spreng. Journal of Plant Resources & Environment, 10(3), 47–50.Google Scholar
  39. Wang, J. W., & Xue, Y. L. (1982). Studies on plant phenylalanine ammonia-lyase (PAL)-II. The role of PAL in the resistance of potato late blight. Acta Phytophysiologia Sinica, 8(1), 35–42.Google Scholar
  40. Weller, D. M. (1988). Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology, 26(1), 379–407.CrossRefGoogle Scholar
  41. Will, M. E., & Sylvia, D. M. (1990). Interaction of rhizosphere bacteria, fertilizer and vesicular arbuscular mycorrhizal fungi with sea oats. Applied and Environmental Microbiology, 56(7), 2073–2079.Google Scholar
  42. Withers, H., Swift, S., & Williams, P. (2001). Quorum sensing as an integral component of gene regulatory networks in gram-negative bacteria. Current Opinion in Microbiology, 4(2), 186–193.CrossRefGoogle Scholar
  43. Yang, Z. Z., & Ye, J. R. (2004). Identification on pathogen of hybrid bamboo blight. Journal of Sichuan Agricultural University, 22(3), 225–227.Google Scholar
  44. Zhang, R. S., Wang, X. Y., Luo, C. P., Liu, Y. F., & Chen, Z. Y. (2013). Identification of the lipopeptides from Bacillus amyloliquefaciens Lx-11 and biocontrol efficacy of surfactin against bacterial leaf streak. Scientia Agricultura Sinica, 46(10), 2014–2021.Google Scholar
  45. Zhao, M. M., Liu, Z. P., & Hu, J. (2003). The effects of Verticillium dahliae toxin on some enzyme activities of eggplant. Acta Agriculturae Boreali-Sinica, 18(2), 70–73.Google Scholar
  46. Zhu, T. H., Huang, Z. C., Gao, Q. Z., Li, F. L., Luo, L. J., & Li, X. D. (2009). Pathogen and occurrence regularity of Bambusa pervariabilis×Dendrocalamopsis grandis blight. Forest Pest and Disease, 28(2), 10–12.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Shujiang Li
    • 1
  • Qianqian He
    • 1
  • Qi Peng
    • 1
  • Hanmingyue Zhu
    • 2
  • Shuhan Li
    • 1
  • Tianhui Zhu
    • 1
    Email author
  1. 1.College of ForestrySichuan Agricultural UniversityChengduChina
  2. 2.College of Landscape ArchitectureSichuan Agricultural UniversityChengduChina

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