Skip to main content
SpringerLink
Log in

Temporal dynamics of the survival of Verticillium dahliae microsclerotia with or without melanin in soils amended with biocontrol agents

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Verticillium dahliae is a soilborne pathogen that causes wilt in many economically important crops. It produces melanized microsclerotia for its long-term survival in soil. Accurate quantification of viable microsclerotia in soil prior to planting is essential for predicting the risk of wilt. Melanin is believed to help microsclerotia resist to or tolerate abiotic stresses. We studied the temporal dynamics of both melanized and melanin-deficient microsclerotia of V. dahliae in four types of soils with or without addition of two biocontrol products (one based on Trichoderma viride; and the other based on two Bacillus strains: B. subtilis and B. amyloliquefaciens). Of the four soil types, two were from wheat and maize (non-host to V. dahliae) fields and the other two from sites with history of continuous cropping of cotton and pepper (both susceptible to V. dahliae). Results showed that the survival of microsclerotia in soils over time can be satisfactorily described by a negative exponential decline model. Microsclerotium mortality was much greater in the soils from wheat and maize field than from cotton and pepper, irrespective of biocontrol agents. Similarly, mortality of melanin-deficient microsclerotia was much greater than melanized microsclerotia. Both biocontrol products resulted in additional mortality of microsclerotia, especially Bacillus spp. There were significant interactions between soil origin, microsclerotium type and biocontrol treatment in affecting microsclerotium mortality. These results demonstrated that melanin contributes to the long-time survival of microsclerotia in soil and suggested that combination of biocontrol with rotation with non-host crops can be effective in reducing the number of viable microsclerotia of V. dahliae in soil.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahlem, H., Mohammed, E., Badoc, A., & Ahmed, L. (2012). Effect of pH, temperature and water activity on the inhibition of Botrytis cinerea by Bacillus amyloliquefaciens isolates. African Journal of Biotechnology, 11, 2210–2217.

    Google Scholar 

  • Bell, A. A., Puhalla, J. E., Tolmsoff, W. J., & Stipanovic, R. D. (1976). Use of mutants to establish (+)-scytalone as an intermediate in melanin biosynthesis by Verticillium dahliae. Canadian Journal of Microbiology, 22, 787–799.

    CAS  PubMed  Google Scholar 

  • Bisutti, I. L., Pelz, J., Büttner, C., & Stephan, D. (2017). Field assessment on the influence of RhizoVital® 42 fl. and Trichostar® on strawberries in the presence of soil-borne diseases. Crop Protection, 96, 195–203.

    CAS  Google Scholar 

  • Burpee, L. L. (1990). The influence of abiotic factors on biological control of soilborne plant pathogenic fungi. Canadian Jounal of Plant Pathology, 12, 08–317.

    Google Scholar 

  • Chen, L., Yang, X., Raza, W., Li, J., Liu, Y., Qiu, M., & Shen, Q. (2011a). Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Applied Microbiology and Biotechnology, 89, 1653–1663.

  • Chen, L., Yang, X., Raza, W., Luo, J., Zhang, F., & Shen, Q. (2011b). Solid-state fermentation of agro-industrial wastes to produce bioorganic fertilizer for the biocontrol of Fusarium wilt of cucumber in continuously cropped soil. Bioresource Technology, 102, 3900–3910.

    CAS  PubMed  Google Scholar 

  • Chowdhury, S. P., Dietel, K., Rändler, M., Schmid, M., Junge, H., Borriss, R., & Grosch, R. (2013). Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS ONE, 8, e68818.

    PubMed  PubMed Central  Google Scholar 

  • Cook, R. J. (1988). Biological control and holistic plant-health care in agriculture. American Journal of Alternative Agriculture, 3, 51–62.

    Google Scholar 

  • Cunniffe, N. J., & Gilligan, C. A. (2011). A theoretical framework for biological control of soil-borne plant pathogens: Identifying effective strategies. Journal of Theoretical Biology, 278, 32–43.

    PubMed  Google Scholar 

  • Davis, J. R., Pavek, J. J., Corsini, D. L., Sorensen, L. H., Schneider, A. T., Everson, D. O., & Huisman, O. C. (1994). Influence of continuous cropping of several potato clones on the epidemiology of Verticillium wilt of potato. Phytopathology, 84, 207–214.

    Google Scholar 

  • Davis, J. R., Huisman, O. C., Westermann, D. T., Hafez, S. L., Everson, D. O., Sorensen, L. H., & Schneider, A. T. (1996). Effects of green manures on Verticillium wilt of potato. Phytopathology, 86, 444–453.

    Google Scholar 

  • Dubey, S. C., Bhavani, R., & Singh, B. (2011). Integration of soil application and seed treatment formulations of Trichoderma species for management of wet root rot of mungbean caused by Rhizoctonia solani. Pest Management Science, 67, 1163–1168.

    CAS  PubMed  Google Scholar 

  • Duressa, D., Anchieta, A., Chen, D., Klimes, A., Garcia-Pedrajas, M. D., Dobinson, K. F., & Klosterman, S. J. (2013). RNA-seq analyses of gene expression in the microsclerotia of Verticillium dahliae. BMC genomics, 14(1), 607.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan, R., Klosterman, S. J., Wang, C. H., Subbarao, K. V., Xu, X. M., Shang, W. J., & Hu, X. P. (2017). Vayg1 is required for microsclerotium formation and melanin production in Verticillium dahliae. ‎Fungal Genetics and Biology, 98, 1–11.

    CAS  PubMed  Google Scholar 

  • Fradin, E. F., & Thomma, B. P. H. J. (2006). Physiology and molecular aspects of I wilt diseases caused by V. dahliae and V. albo-atrum. Molecular Plant Pathology, 7, 71–86.

    CAS  PubMed  Google Scholar 

  • Freeman, S., Minz, D., Kolesnik, I., Barbul, O., Zveibil, A., Maymon, M., Nitzani, Y., Kirshner, B., Rav-David, D., Bilu, A., Dag, A., Shafir, S., & Elad, Y. (2004). Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. European Journal of Plant Pathology, 110,361–370.

  • Hawke, M. A. (1994. Studies on the survival of microsclerotia of Verticillium dahliae. Ph. D. Theses, 2357.

  • Hu, X. P., Bai, Y. W., Chen, T., Hu, D. F., Yang, J. R., & Xu, X. (2013). An optimized method for in vitro production of Verticillium dahliae microsclerotia. European Journal of Plant Pathology, 136, 225–229.

    Google Scholar 

  • Hu, D. F., Wang, C. S., Tao, F., Cui, Q., Xu, X. M., Shang, W. J., & Hu, X. P. (2014). Whole genome wide expression profiles on germination of Verticillium dahliae microsclerotia. PLos One, 9, e100046.

    PubMed  PubMed Central  Google Scholar 

  • Hu, X. P., Gurung, S., Short, Dylan, P. G., Sandoya, G. V., Shang, W. J., Hayes, R. J., Davis, R., Michael., & Subbarao, K. V. (2015). Nondefoliating and defoliating strains from cotton correlate with races 1 and 2 of Verticillium dahliae. Plant Disease, 99, 1713–1720.

  • Hu, P., Wu, L., Hollister, E. B., Wang, A. S., Somenahally, A. C., Hons, F. M., & Gentry, T. J. (2019). Fungal community structural and microbial functional pattern changes after soil amendments by oilseed meals of Jatropha curcas and Camelina sativa: a microcosm study. Frontiers in Microbiology, 10, 537.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, J., Ebach, M. C., & Triantafilis, J. (2017). Cladistic analysis of Chinese soil taxonomy. Geoderma Regional, 10, 11–20.

    Google Scholar 

  • Inderbitzin, P., & Subbarao, K. V. (2014). Verticillium systematics and evolution: how confusion impedes Verticillium wilt management and how to resolve it. Phytopathology, 104, 564–574.

    PubMed  Google Scholar 

  • Inderbitzin, P., Ward, J., Barbella, A., Solares, N., Izyumin, D., Burman, P., Chellemi, D., & Subbarao, K. V. (2017). Soil microbiomes associated with Verticillium wilt-suppressive broccoli and chitin amendments are enriched with potential biocontrol agents. Phytopathology, 108, 31–43.

    PubMed  Google Scholar 

  • Jabnoun-Khiareddine, H., Daami-Remadi, M., Ayed, F., & Mahjoub, E., M (2009). Biological control of tomato Verticillium wilt by using indigenous Trichoderma spp. The African Journal of Plant Science and Biotechnology, 3, 26–36.

  • Jilani, G., Mahmood, S., Chaudhry, A. N., Hassan, I., & Akram, M. (2008). Allelochemicals: sources, toxicity and microbial transformation in soil-a review. Annals of Microbiology, 58, 351–357.

    CAS  Google Scholar 

  • Klosterman, S. J., Atallah, Z. K., Vallad, G. E., & Subbarao, K. V. (2009). Diversity, pathogenicity, and management of Verticillium species. Annual Review of Phytopathology, 47, 39–62.

    CAS  PubMed  Google Scholar 

  • Kong, C. H., Wang, P., Gu, Y., Xu, X. H., & Wang, M. L. (2008). Fate and impact on microorganisms of rice allelochemicals in paddy soil. Journal of Agricultural and Food Chemistry, 56, 5043–5049.

    CAS  PubMed  Google Scholar 

  • Kredics, L., Antal, Z., Manczinger, L., Szekeres, A., Kevei, F., & Nagy, E. (2003). Influence of environmental parameters on Trichoderma strains with biocontrol potential. Food Technology and Biotechnology, 41, 37–42.

    Google Scholar 

  • Larkin, R. P. (2008). Relative effects of biological amendments and crop rotations on soil microbial communities and soilborne diseases of potato. Soil Biology and Biochemistry, 40, 1341–1351.

    CAS  Google Scholar 

  • Liu, J., Li, X., Jia, Z., Zhang, T., & Wang, X. (2017). Effect of benzoic acid on soil microbial communities associated with soilborne peanut diseases. Applied Soil Ecology, 110, 34–42.

    Google Scholar 

  • Liua, X., & Herbert, S. J. (2002). Fifteen years of research examining cultivation of continuous soybean in northeast China: A review. Field Crops Research, 79, 1–7.

    Google Scholar 

  • Manici, L. M., & Caputo, F. (2010). Soil fungal communities as indicators for replanting new peach orchards in intensively cultivated areas. European Journal of Agronomy, 33, 188–196.

    Google Scholar 

  • Martin, F. N., & Bull, C. T. (2002). Biological approaches for control of root pathogens of strawberry. Phytopathology, 92, 1356–1362.

    CAS  PubMed  Google Scholar 

  • Mazzola, M., & Manici, L. M. (2012). Apple replant disease: role of microbial ecology in cause and control. Annual Review of Phytopathology, 50, 45–65.

    CAS  PubMed  Google Scholar 

  • Morán-Diez, M. E., Carrero-Carrón, I., Rubio, M. B., Jiménez-Díaz, R. M., Monte, E., & Hermosa, R. (2019). Transcriptomic analysis of Trichoderma atroviride overgrowing plant-wilting Verticillium dahliae reveals the role of a new M14 metallocarboxypeptidase CPA1 in biocontrol. Frontiers in Microbiology, 10.

  • Nayyar, A., Hamel, C., Lafond, G., Gossen, B. D., Hanson, K., & Germida, J. (2009). Soil microbial quality associated with yield reduction in continuous-pea. Applied Soil Ecology, 43, 115–121.

    Google Scholar 

  • Nosanchuk, J. D., & Casadevall, A. (2003). The contribution of melanin to microbial pathogenesis. Cellular Microbiology, 5, 203–223.

    CAS  PubMed  Google Scholar 

  • Paz, Z., García-Pedrajas, M. D., Andrews, D. L., Klosterman, S. J., Baeza-Montañez, L., & Gold, S. E. (2011). One step construction of Agrobacterium-Recombination-ready plasmids (OSCAR), an efficient and robust tool for ATMT based gene deletion construction in fungi. Fungal Genetics and Bology, 48, 677–684.

    CAS  Google Scholar 

  • Pegg, G. F., & Brady, B. L. (2002). Verticillium Wilts. New York: CABI Publishing.

    Google Scholar 

  • Porras, M., Barrau, C., Arroyo, F. T., Santos, B., Blanco, C., & Romero, F. (2007). Reduction of Phytophthora cactorum in strawberry fields by Trichoderma spp. and soil solarization. Plant Disease, 91, 142–146.

    CAS  PubMed  Google Scholar 

  • Shang, W., Chen, T., Bai, Y., Yang, J., & Hu, X. (2013). Germination condition and lethal temperature for microsclerotia of Verticillium dahliae. Mycosystema, 32, 986–992.

    Google Scholar 

  • Short, D. P., Sandoya, G., Vallad, G. E., Koike, S. T., Xiao, C. L., Wu, B. M., & Subbarao, K. V. (2015). Dynamics of Verticillium species microsclerotia in field soils in response to fumigation, cropping patterns, and flooding. Phytopathology, 105, 638–645.

    PubMed  Google Scholar 

  • Subbarao, K. V., & Hubbard, J. C. (1996). Interactive effects of broccoli residue and temperature on Verticillium dahliae microsclerotia in soil and on wilt in cauliflower. Phytopathology, 86, 1303–1310.

    Google Scholar 

  • Weir, T. L., Park, S.-W., & Vivanco, J. M. (2004). Biochemical and physiological mechanisms mediated by allelochemicals. Current Opinion in Plant Biology, 7, 472–479.

    CAS  PubMed  Google Scholar 

  • Wu, S. F., Zhang, H., & Wu, P. T. (2002). Vertical and horizontal regularity of change in soil physical properties in Yangling. Research of Soil and Water Conservation, 9, 25–27.

    Google Scholar 

  • Wu, B. M., & Subbarao, K. V. (2014). A model for multiseasonal spread of Verticillium wilt of lettuce. Phytopathology, 104, 908–917.

    CAS  PubMed  Google Scholar 

  • Wu, F. Z., & Wang, X. Z. (2006). Effect of p-hydroxybenzoic and cinnamic acids on soil fungi (Fusarium oxysporum f.sp. cucumerinum) growth and microbial population. Allelopathy Journal, 18, 129–139.

    Google Scholar 

  • Xiao, C. L., Subbarao, K. V., Schulbach, K. F., & Koike, S. T. (1998). Effects of crop rotation and irrigation on Verticillium dahliae microsclerotia in soil and wilt in cauliflower. Phytopathology, 88, 1046–1055.

    CAS  PubMed  Google Scholar 

  • Xu, X. M., & Jeger, M. J. (2013a). Combined use of two biocontrol agents with different biocontrol mechanisms most likely results in less than expected efficacy in controlling foliar pathogens under fluctuating conditions: a modeling study. Phytopathology, 103, 108–116.

    PubMed  Google Scholar 

  • Xu, X. M., & Jeger, M. J. (2013b). Synergy may result from combined use of two biocontrol agents for controlling foliar pathogens under spatial heterogeneous conditions: a simulation study. Phytopathology, 103, 768–775.

    PubMed  Google Scholar 

  • Yu, D., Fang, Y., Tang, C., Klosterman, S. J., Tian, C., & Wang, Y. (2019). Genomewide transcriptome profiles reveal how bacillus subtilis lipopeptides inhibit microsclerotia formation in Verticillium dahliae. Molecular Plant-Microbe Interactions, 32(5), 622–634.

    CAS  PubMed  Google Scholar 

  • Zhang, Y. L., Wang, Y., Hu, Q., Sun, H. Y., L., & Xu, H. (2011). Study on the soil physics in Shaanxi province in China. Agricultural Research in the Arid Areas, 29, 75–79.

  • Zhu, S., & Morel, J. B. (2018). Molecular mechanisms underlying microbial disease control in intercropping. Molecular Plant-Microbe Interactions, 32(1), 20–24.

    PubMed  Google Scholar 

Download references

Acknowledgements

The study was sponsored by NSFC (31371888) and the National Key Research and Development Program of China (2018YFE0112500). We thank Fungal Genetics Stock Center (www.fgsc.net) for providing the plasmid DNA of pOSCAR and pA-Hyg-OSCAR used for target deletion of genes in V. dahliae.

Author information

Author notes

  1. Rong Fan

    Present address: College of Agronomy, Guizhou University, Guiyang, 550025, Guizhou, China

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Rong Fan, Xue Gong, Liqiang Gao, Wenjing Shang & Xiaoping Hu

  2. NIAB East Malling Research (EMR), West Malling, ME19 6BJ, UK

    Xiangming Xu

Authors
  1. Rong Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xue Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liqiang Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenjing Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaoping Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiangming Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenjing Shang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This article does not contain any research involving human or animal participants.

Informed consent

Not applicable.

Electronic supplementary material

Figure S1

(DOC 334 kb)

Figure S2

(DOC 584 kb)

Table S1

(DOC 40 kb)

Table S2

(DOC 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, R., Gong, X., Gao, L. et al. Temporal dynamics of the survival of Verticillium dahliae microsclerotia with or without melanin in soils amended with biocontrol agents. Eur J Plant Pathol 157, 521–531 (2020). https://doi.org/10.1007/s10658-020-02014-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-02014-9

Keywords

Search

Navigation