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European Journal of Plant Pathology

, Volume 147, Issue 1, pp 43–53 | Cite as

Trichoderma harzianum-induced resistance against Fusarium oxysporum involves regulation of nuclear DNA content, cell viability and cell cycle-related genes expression in cucumber roots

  • Shuang-Chen Chen
  • Hong-Jiao Zhao
  • Zhong-Hong Wang
  • Cai-Xia Zheng
  • Pu-Yan Zhao
  • Zhi-Hua Guan
  • Hai-Yang Qin
  • Ai-Rong Liu
  • Xiao-Min Lin
  • Golam-Jalal Ahammed
Article

Abstract

Fusarium wilt, one of the destructive diseases of cucumber can be effectively controlled by using biocontrol agents such as Trichoderma harzianum. However, the mechanisms controlling T. harzianum-induced enhanced resistance remain largely unknown in cucumber plants. Here we screened the potent T. harzianum isolate TH58 that could effectively control F. oxysporum (FO). Glasshouse efficacy trials also showed that TH58 decreased disease incidence by 69.7 %. FO induced ROS over accumulation, while TH58 inoculation suppressed ROS over accumulation and improved root cell viability under F. oxysporum infection. TH58 inoculation could reverse the FO-induced cell division block and regulate the proportional distribution of nuclear DNA content through inducing 2C fraction. Moreover, the expression levels of cell cycle-related genes such as CDKA, CDKB, CycA, CycB, CycD3;1 and CycD3;2 in TH58 - pre-inoculated seedlings were up-regulated compared with those infected with FO alone. Taken together, these results suggest that T. harzianum improved plant resistance against Fusarium wilt disease via alterations in nuclear DNA content and cell cycle-related genes expression that might maintain a lower ROS accumulation and higher root cell viability in cucumber seedlings.

Keywords

Trichoderma harzianum Cell viability Cucumber Fusarium wilt disease Cell division Endoreduplication 

Notes

Acknowledgments

This work was supported by National Natural Science Foundation of China (31471867, 31560554, 31260478, 31550110201), Flexible Talent Introduction Project of Agricultural and Animal Husbandry College of Tibet University (201406) and Outstanding Young Teacher Project in Henan Province (2011GGJS-075, 2012GGJS-078).

References

  1. Aleandri, M. P., Chilosi, G., Bruni, N., Tomassini, A., Vettraino, A. M., & Vannini, A. (2015). Use of nursery potting mixes amended with local Trichoderma strains with multiple complementary mechanisms to control soil-borne diseases. Crop Protection, 67, 269–278.Google Scholar
  2. Barow, M., & Meister, A. (2003). Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant, Cell & Environment, 26, 571–584.CrossRefGoogle Scholar
  3. Baxter, A., Mittler, R., & Suzuki, N. (2015). ROS as key players in plant stress signaling. Journal of Experimental Botany, 65, 1229–1240.CrossRefGoogle Scholar
  4. Bertin, N. (2005). Analysis of the tomato fruit growth response to temperature and plant fruit load in relation to cell division, cell expansion and DNA endoreduplication. Annals of Botany, 95, 439–447.CrossRefPubMedGoogle Scholar
  5. Blaya, J., López-Mondéjar, R., Lloret, E., Pascual, J. A., & Ros, M. (2013). Changes induced by Trichoderma harzianum in suppressive compost controlling Fusarium wilt. Pesticide Biochemistry and Physiology, 107, 112–119.CrossRefPubMedGoogle Scholar
  6. Booth, C. (1971). The genus Fusarium. Commonwealth Mycological Institute: Surrey, UK.Google Scholar
  7. Cools, T., & De Veylder, L. (2009). DNA stress checkpoint control and plant development. Current Opinion in Plant Biology, 12, 23–28.CrossRefPubMedGoogle Scholar
  8. Cordero-Ramirez, J. D., Lopez-Rivera, R., Figueroa-Lopez, A. M., Mancera-Lopez, M. E., Martinez-Alvarez, J. C., Apodaca-Sanchez, M. A., et al. (2013). Native soil bacteria isolates in Mexico exhibit a promising antagonistic effect against Fusarium oxysporum f. Sp radicis-lycopersici. Journal of Basic Microbiology, 53, 838–847.PubMedGoogle Scholar
  9. Dewitte, W., & Murray, J. A. H. (2003). The plant cell cycle. Annual Review of Plant Biology, 54, 235–264.CrossRefPubMedGoogle Scholar
  10. Ding, J., Zhang, Y., Zhang, H., Li, X., Sun, Z., Liao, Y., et al. (2014). Effects of Fusarium oxysporum on rhizosphere microbial communities of two cucumber genotypes with contrasting Fusarium wilt resistance under hydroponic condition. European Journal of Plant Pathology, 140, 643–653.CrossRefGoogle Scholar
  11. Ding, Z., Li, M., Sun, F., Xi, P., Sun, L., Zhang, L., & Jiang, Z. D. (2015). Mitogen-activated protein kinases are associated with the regulation of physiological traits and virulence in Fusarium oxysporum f. sp. cubense. PloS One, 10, e0122634.Google Scholar
  12. Dmitrovic, S., Simonovic, A., Mitic, N., Savic, J., Cingel, A., Filipovic, B., et al. (2015). Hairy root exudates of allelopathic weed Chenopodium murale L. Induce oxidative stress and down-regulate core cell cycle genes in Arabidopsis and wheat seedlings. Plant Growth Regulation, 75, 365–382.CrossRefGoogle Scholar
  13. Doulis, A. G., Debian, N., Kingston-Smith, A. H., & Foyer, C. H. (1997). Differential localization of antioxidants in maize leaves. Plant Physiology, 114, 1031–1037.CrossRefPubMedPubMedCentralGoogle Scholar
  14. El Komy, M. H., Saleh, A. A., Eranthodi, A., & Molan, Y. Y. (2015). Characterization of novel Trichoderma asperellum isolates to select effective biocontrol agents against tomato Fusarium wilt. Plant Pathology Journal, 31, 50–60.CrossRefPubMedGoogle Scholar
  15. Elstner, E. F., & Heupel, A. (1976). Oxygen activation by isolated chloroplasts from Euglena gracilis. Isolation and properties of a fluorescent compound that catalyzes monovalent oxygen reduction. Archives of Biochemistry and Biophysics, 173, 614–622.CrossRefPubMedGoogle Scholar
  16. Engler, J. D., & Gheysen, G. (2013). Nematode-induced endoreduplication in plant host cells: why and how? Molecular Plant-Microbe Interactions, 26, 17–24.CrossRefGoogle Scholar
  17. Ezaki, B., Gardner, R. C., Ezaki, Y., & Matsumoto, H. (2000). Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiology, 122, 657–665.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Ferrigo, D., Raiola, A., Piccolo, E., Scopel, C., & Causin, R. (2014). Trichoderma harzianum T22 induces in maize systemic resistance against Fusarium verticillioides. Journal of Plant Pathology, 96, 133–142.Google Scholar
  19. Galbraith, D. W., Harkins, K. R., Maddox, J. M., Ayres, N. M., Sharma, D. P., & Firoozabady, E. (1983). Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science, 220, 1049–1051.CrossRefPubMedGoogle Scholar
  20. Gilissen, L. J. W., van Staveren, M. J., Creemers-Molenaar, J., & Verhoeven, H. A. (1993). Development of polysomaty in seedlings and plants of Cucumis sativus L. Plant Science, 91, 171–179.CrossRefGoogle Scholar
  21. Greilhuber, J. (2008). Cytochemistry and C-values: the less-well-known world of nuclear DNA amounts. Annals of Botany, 101, 791–804.CrossRefPubMedGoogle Scholar
  22. Hano, C. Addi, M., Fliniaux, O., Lamine, B., Eric, D., François, M., Frédéric, L., & Lainé E. (2008). Molecular characterization of cell death induced by a compatible interaction between Fusarium oxysporum f. Sp. linii and flax (Linum usitatissimum) cells. Plant Physiology and Biochemistry, 46, 590–600.Google Scholar
  23. Innocenti, G., Roberti, R., & Piattoni, F. (2015). Biocontrol ability of Trichoderma harzianum strain T22 against Fusarium wilt disease on water-stressed lettuce plants. BioControl, 60, 573–581.CrossRefGoogle Scholar
  24. Inzé, D., & De Veylder, L. (2006). Cell cycle regulation in plant development. Annual Review of Genetics, 40, 77–105.CrossRefPubMedGoogle Scholar
  25. Isack, Y., Benichis, M., Gillet, D., & Gamliel, A. (2014). A selective agar medium for isolation, enumeration and morphological identification of Fusarium proliferatum. Phytoparasitica, 42, 1–7.CrossRefGoogle Scholar
  26. Ito, S., Ihara, T., Hideyuki, T., Tanaka, S., Ikeda, T., Kajihara, H., Dissanayake C., Abdel-Motaal F. F., & El-Sayed M. A. (2007). α-Tomatine, the major saponin in tomato, induces programmed cell death mediated by reactive oxygen species in the fungal pathogen Fusarium oxysporum. FEBS Letters, 581, 3217–3222.Google Scholar
  27. Larkin, R. P., & Fravel, D. R. (2002). Effects of varying environmental conditions on biological control of Fusarium wilt of tomato by nonpathogenic Fusarium spp. Biological Control, 92, 160–1166.Google Scholar
  28. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods, 25, 402–408.CrossRefPubMedGoogle Scholar
  29. Liu, A. R., Chen, S. C., Jin, W. J., Yu, B. B., Wang, F. H., & He, C. X. (2012). Effects of Trichoderma harzianum on secondary metabolites in cucumber roots infected with Fusarium oxysporum. Chinese Journal of Biological Control, 4, 545–551 (in Chinese).Google Scholar
  30. López-Bucio, J., Pelagio-Flores, R., & Herrera-Estrella, A. (2015). Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Scientia Horticulturae, 196, 109–123.Google Scholar
  31. Martinez-Medina, A., Pascual, J. A., Perez-Alfocea, F., Albacete, A., & Roldan, A. (2010). Trichoderma harzianum and Glomus intraradices modify the hormone disruption induced by Fusarium oxysporum infection in melon plants. Phytopathology, 100, 682–688.CrossRefPubMedGoogle Scholar
  32. Marzano, M., Gallo, A., & Altomare C. (2013). Improvement of biocontrol efficacy of Trichoderma harzianum vs. Fusarium oxysporum f. Sp. lycopersici through UV-induced tolerance to fusaric acid. Biological Control, 67, 397–408.Google Scholar
  33. Menges, M., Samland, A. K., Planchais, S., & Murray, J. A. H. (2006). The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell, 18, 893–906.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Petrov, V., Hille, J., Mueller-Roeber, B., & Gechev, T. S. (2015). ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science, 6, 69.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Porceddu, A., Stals, H., Reichheld, J. P., Segers, G., De Veylder, L., Barroco, R. P., et al. (2001). A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plants. The Journal of Biological Chemistry, 276, 36354–36360.CrossRefPubMedGoogle Scholar
  36. Reichheld, J. P., Vernoux, T., Lardon, F., Montagu, M. V., & Inzé, D. (1999). Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant Journal, 17, 647–656.CrossRefGoogle Scholar
  37. Repetto, O., Massa, N., Gianinazzi-Pearson, V., Dumas-Gaudot, E., & Berta, G. (2007). Cadmium effects on populations of root nuclei in two pea genotypes inoculated or not with the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza, 17, 111–120.CrossRefPubMedGoogle Scholar
  38. Rewers, M., & Sliwinska, E. (2014). Endoreduplication in the germinating embryo and young seedling is related to the type of seedling establishment but is not coupled with superoxide radical accumulation. Journal of Experimental Botany, 65, 4385–4396.CrossRefPubMedGoogle Scholar
  39. Rymen, B., Fiorani, F., Kartal, F., Vandepoele, K., Inzé, D., & Beemster, G. T. S. (2007). Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiology, 143, 1429–1438.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Saravanakumar, K., Yu, C. J., Dou, K., Wang, M., Li, Y., & Chen, J. (2016). Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. Sp. Cucumerinum. Biological Control, 94, 37–46.CrossRefGoogle Scholar
  41. Schuster, A., & Schmoll, M. (2010). Biology and biotechnology of Trichoderma. Applied Microbiology and Biotechnology, 87, 787–799.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Scott, J. C., Gordon, T. R., Kirkpatrick, S. C., Koike, S. T., Matheron, M. E., Ochoa, O. E., et al. (2012). Crop rotation and genetic resistance reduce risk of damage from Fusarium wilt in lettuce. California Agriculture, 66, 20–24.CrossRefGoogle Scholar
  43. Shadel, G. S., & Horvath, T. L. (2015). Mitochondrial ROS signaling in organismal homeostasis. Cell, 163, 560–569.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sliwinska, E., & Lukaszewska E. (2005). Polysomaty in growing in vitro sugar-beet (Beta vulgaris L.) seedlings of different ploidy level. Plant Science, 168, 1067–1074.Google Scholar
  45. Srivastava, R., Khalid, A., Singh, U. S., & Sharma, A. K. (2010). Evaluation of arbuscular mycorrhizal fungus, fluorescent Pseudomonas and Trichoderma harzianum formulation against Fusarium oxysporum f. Sp lycopersici for the management of tomato wilt. Biological Control, 53, 24–31.CrossRefGoogle Scholar
  46. Suzuki, K., Nishiuchi, T., Nakayama, Y., Ito, M., & Shinshi, H. (2006). Elicitor-induced down-regulation of cell cycle-related genes in tobacco cells. Plant, Cell & Environment, 29, 183–191.CrossRefGoogle Scholar
  47. Tan, J. Y., Shao, X. H., Chen, L. H., Chen, L. N., & Xu, H. L. (2012). Effect of formulations of Trichoderma harzianum SQR-T037 on the induction of resistance against Fusarium wilt in cucumber. Journal of Agricultural and Food Chemistry, 10, 1205–1209.Google Scholar
  48. Tsukagoshi, H. (2012). Defective root growth triggered by oxidative stress is controlled through the expression of cell cycle-related genes. Plant Science, 197, 30–39.CrossRefPubMedGoogle Scholar
  49. Verma, M., Brar, S. K., Tyagi, R. D., Surampalli, R. Y., & Valero, J. R. (2007). Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochemical Engineering Journal, 37, 1–20.CrossRefGoogle Scholar
  50. Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Woo, S. L., & Lorito, M. (2008). Trichoderma–plant–pathogen interactions. Soil Biology & Biochemistry, 40, 1–10.Google Scholar
  51. West, G., Inzé, D., & Beemster, G. T. S. (2004). Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiology, 135, 1050–1058.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Willekens, H., Chamnongpol, S., Davey, M., Schraudner, M., Langebartels, C., Van Montagu, M., et al. (1997). Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO Journal, 16, 4806–4816.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Xia, X. J., Zhou, Y. H., Ding, J., Shi, K., Asami, T., Chen, Z. X., et al. (2011). Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytologist, 191, 706–720.CrossRefPubMedGoogle Scholar
  54. Xiong, W., Li, Z. G., Liu, H. J., Xue, C., Zhang, R. F., Wu, H. S., et al. (2015). The effect of long-term continuous cropping of black pepper on soil bacterial communities as determined by 454 pyrosequencing. PloS One, 10, e0136946.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Yin, K., Ueda, M., Takagi, H., Kajihara, T., Aki, S. S., Nobusawa, T., et al. (2014). A dual-color marker system for in vivo visualization of cell cycle progression in Arabidopsis. Plant Journal, 80, 541–552.CrossRefPubMedGoogle Scholar
  56. Yu, J. Q., & Komada, H. (1999). Hinoki bark, a substrate with antipathogen properties that suppress root diseases of tomato. Scientia Horticulturae, 81, 13–24.CrossRefGoogle Scholar
  57. Zhang, F. G., Yang, X. M., Ran, W., & Shen, Q. R. (2014). Fusarium oxysporum induces the production of proteins and volatile organic compounds by Trichoderma harzianum T-E5. FEMS Microbiology Letters, 359, 116–123.CrossRefPubMedGoogle Scholar
  58. Zhang, Y., Gu, M., Shi, K., Zhou, Y. H., & Yu, J. Q. (2010). Effects of aqueous root extracts and hydrophobic root exudates of cucumber (Cucumis sativus L.) on nuclei DNA content and expression of cell cycle-related genes in cucumber radicles. Plant and Soil, 327, 455–463.CrossRefGoogle Scholar
  59. Zhao, F. Y., Hu, F., Zhang, S. Y., Wang, K., Zhang, C. R., & Liu, T. (2013). MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environmental Science and Pollution Research, 20, 5449–5460.CrossRefPubMedGoogle Scholar
  60. Zuo, C. W., Li, C. Y., Li, B., Wei, Y. R., Hu, C. H., Yang, Q. S., et al. (2015). The toxic mechanism and bioactive components of Chinese leek root exudates acting against Fusarium oxysporum f. Sp. cubense tropical race 4. European Journal of Plant Pathology, 143, 447–460.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2016

Authors and Affiliations

  • Shuang-Chen Chen
    • 1
    • 2
  • Hong-Jiao Zhao
    • 1
  • Zhong-Hong Wang
    • 2
  • Cai-Xia Zheng
    • 1
  • Pu-Yan Zhao
    • 3
  • Zhi-Hua Guan
    • 2
  • Hai-Yang Qin
    • 1
  • Ai-Rong Liu
    • 1
  • Xiao-Min Lin
    • 1
  • Golam-Jalal Ahammed
    • 4
  1. 1.College of ForestryHenan University of Science and TechnologyLuoyangPeople’s Republic of China
  2. 2.Department of Plant Science, Agricultural and Animal Husbandry CollegeTibet UniversityLinzhiPeople’s Republic of China
  3. 3.College of HorticultureSouth China Agricultural UniversityGuangzhouPeople’s Republic of China
  4. 4.Department of HorticultureZhejiang UniversityHangzhouPeople’s Republic of China

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