Advertisement

Role of endophytes in early seedling growth of plants: a test using systemic fungicide seed treatment

  • M. M. Vasanthakumari
  • Jambagi Shridhar
  • R. J. Madhura
  • Mohanasundaram Nandhitha
  • Chinnasamy Kasthuri
  • B Janardhana
  • Karaba N. Nataraja
  • Gudasalamani Ravikanth
  • Ramanan Uma Shaanker
Original Article
  • 16 Downloads

Abstract

Systemic fungicide seed treatments are routinely used in conventional agriculture to control soil and seed-borne diseases, but little is known about their unintended adverse effects on non-target beneficial fungal endophytes that are known to be involved in plant growth and development. This study evaluated the seed treatment effect of a broad spectrum systemic fungicide, carbendazim (bavistin) on symbiotic association of fungal endophytes in rice and on early seedling growth of rice, green gram, soybean, and cowpea. Seeds were surface sterilized with sodium hypochlorite followed by 0.2% bavistin treatment. Growth of fungal endophytes was significantly affected by the seed treatment with fungicide in rice seedlings, while shoot and root growth was suppressed in all the crops. Quantitative real time PCR showed that the level of expression of two basal transcriptional regulator genes, OsBTF3 and OsNF-YC1 that are required for seed germination and seedling growth significantly decreased in bavistin treated rice seedlings. Re-inoculation of consortia of fungal endophytes onto bavistin treated rice seedlings significantly recovered seedling growth and development. These results suggest that fungicide treatment of seeds affects early seedling growth and has negative impact on beneficial fungal endophytes that are involved in plant growth and development. This study provides information on possible ill effects of fungicide on beneficial fungal endophytes that play key roles in early seedling growth of plants and also open up the prospect to additional research on different crops in vitro and field conditions to determine the consequences of fungicide effects and optimise fungicide application strategies to develop sustainable disease control methods.

Keywords

Fungal endophytes Seedling growth Seed treatment Bavistin Fungicide 

Notes

Acknowledgements

The authors would like to thank DBT, India funded project “Chemical Ecology of the North East Region (NER) of the India: A collaborative programme Linking NER and Bangalore Researchers” for financial support DBT-NER/Agri/24/2013, and Poornima A, and Santhosh Kumar J U for technical assistance. This work is partially supported by Indian Council of Agricultural Research (ICAR-CAAST- F.No./NAHEP/CAAST/2018-19), Government of India, New Delhi.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

40502_2018_404_MOESM1_ESM.doc (664 kb)
Supplementary material 1 (DOC 663 kb)

References

  1. Arnold, A. E., Maynard, Z., Gilbert, G. S., Coley, P. D., & Kursar, T. A. (2000). Are tropical fungal endophytes hyperdiverse? Ecology Letters, 3, 267–274.CrossRefGoogle Scholar
  2. Arx, J. (1981). The genera of fungi sporulating in pure culture. Vaduz: J Cramer.Google Scholar
  3. Bagga, P. S., & Sharma, V. K. (2006). Evaluation of fungicides as seedling treatment for controlling bakanae/foot-rot (Fusarium moniliforme) disease in basmati rice. Indian Phytopathology, 59, 305–308.Google Scholar
  4. Buysens, C., De Boulois, H. D., & Declerck, S. (2015). Do fungicides used to control Rhizoctonia solani impact the non-target arbuscular mycorrhizal fungus Rhizophagus irregularis? Mycorrhiza, 25, 277–288.CrossRefGoogle Scholar
  5. Dhingra, O., & Sinclair, J. (1985). Culture media and their formulas. In O. Dhingra & J. Sinclair (Eds.), Basic plant pathology methods (pp. 285–315). Boca Raton: CRC Press.Google Scholar
  6. Domsch, K., & Gams, W. (1972). Fungi in agriculture soils. London: Longman Group Ltd.Google Scholar
  7. Dubey, S. C., & Singh, B. (2010). Seed treatment and foliar application of insecticides and fungicides for management of cercospora leaf spots and yellow mosaic of mungbean (Vigna radiata). International Journal of Pest Management, 56, 309–314.CrossRefGoogle Scholar
  8. Ellis, M. (1976). More dematiaceous Hypomycetes. Kew Surrey: Commonwealth Mycological Institute.Google Scholar
  9. Finch, S., Pennell, C., Kerby, J., & Cave, V. (2015). Mice find endophyte-infected seed of tall fescue unpalatable—implications for the aviation industry. Grass & Forage Science, 71, 659–666.CrossRefGoogle Scholar
  10. Gahlot, S., Joshi, A., Singh, P., Tuteja, R., Dua, M., Jogawat, A., et al. (2015). Isolation of genes conferring salt tolerance from Piriformospora indica by random overexpression in Escherichia coli. World Journal of Microbiology & Biotechnology, 31, 1195–1209.CrossRefGoogle Scholar
  11. Gan, Y., Siddique, K., MacLeod, W., & Jayakumar, P. (2006). Management options for minimizing the damage by ascochyta blight (Ascochyta rabiei) in chickpea (Cicer arietinum L.). Field Crops Research, 97, 121–134.CrossRefGoogle Scholar
  12. Garcia, P. C., Rivero, R. M., Ruiz, J. M., & Romero, L. (2003). The role of fungicides in the physiology of higher plants: Implications for defense responses. Botanical Review, 69, 162–172.CrossRefGoogle Scholar
  13. Hou, X., Zhou, J., Liu, C., Liu, L., Shen, L., & Yu, H. (2014). Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nature Communications, 5, 4601.CrossRefGoogle Scholar
  14. Karlsson, I., Friberg, H., Steinberg, C., & Persson, P. (2014). Fungicide effects on fungal community composition in the wheat phyllosphere. PLoS ONE, 9, e111786.CrossRefGoogle Scholar
  15. Khan, A. R., Ullah, I., Waqas, M., Shahzad, R., Hong, S. J., Park, G. S., et al. (2015). Plant growth-promoting potential of endophytic fungi isolated from Solanum nigrum leaves. World Journal of Microbiology & Biotechnology, 31, 1461–1466.CrossRefGoogle Scholar
  16. Kumimoto, R. W., Zhang, Y., Siefers, N., & Holt, B. F. (2010). NF–YC3, NF–YC4 and NF–YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant Journal, 63, 379–391.CrossRefGoogle Scholar
  17. Lambert, E., Rodenhiser, H., & Flor, H. (1926). The effectiveness of various fungicides in controlling the covered smuts of small grains. Phytopathology, 16, 393–411.Google Scholar
  18. Liu, X., Hu, P., Huang, M., Tang, Y., Li, Y., Li, L., et al. (2016). The NF-YC–RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nature Communications, 7, 12768.CrossRefGoogle Scholar
  19. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25, 402–408.CrossRefGoogle Scholar
  20. Márquez, L. M., Redman, R. S., Rodriguez, R. J., & Roossinck, M. J. (2007). A virus in a fungus in a plant: Three-way symbiosis required for thermal tolerance. Science, 315, 513–515.CrossRefGoogle Scholar
  21. Mueller, D., Hartman, G., & Pedersen, W. (1999). Development of sclerotia and apothecia of Sclerotinia sclerotiorum from infected soybean seed and its control by fungicide seed treatment. Plant Disease, 83, 1113–1115.CrossRefGoogle Scholar
  22. Munkvold, G., & O’mara, J. (2002). Laboratory and growth chamber evaluation of fungicidal seed treatments for maize seedling blight caused by Fusarium species. Plant Disease, 86, 143–150.CrossRefGoogle Scholar
  23. Nettles, R., Watkins, J., Ricks, K., Boyer, M., Licht, M., Atwood, L. M., et al. (2016). Influence of pesticide seed treatments on rhizosphere fungal and bacterial communities and leaf fungal endophyte communities in maize and soybean. Applied Soil Ecology, 102, 61–69.CrossRefGoogle Scholar
  24. Palmeros-Suárez, P. A., Massange-Sánchez, J. A., Martínez-Gallardo, N. A., Montero-Vargas, J. M., Gómez-Leyva, J. F., & Délano-Frier, J. P. (2015). The overexpression of an Amaranthus hypochondriacus NF-YC gene modifies growth and confers water deficit stress resistance in Arabidopsis. Plant Science, 240, 25–40.CrossRefGoogle Scholar
  25. Penuelas, J., Rico, L., Ogaya, R., Jump, A., & Terradas, J. (2012). Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biology, 14, 565–575.CrossRefGoogle Scholar
  26. Prior, R., Mittelbach, M., & Begerow, D. (2017). Impact of three different fungicides on fungal epi-and endophytic communities of common bean (Phaseolus vulgaris) and broad bean (Vicia faba). Journal of Environmental Science and Health, Part B, 52, 376–386.CrossRefGoogle Scholar
  27. Rodriguez, R. J., Redman, R. S., & Henson, J. M. (2004). The role of fungal symbioses in the adaptation of plants to high stress environments. Mitigation and Adaptation Strategies for Global Change, 9, 261–272.CrossRefGoogle Scholar
  28. Sajeevan, R. S., Shivanna, M. B., & Nataraja, K. N. (2014). An efficient protocol for total RNA isolation from healthy and stressed tissues of mulberry (Morus sp.) and other species. American Journal Plant Science, 5, 2057–2065.CrossRefGoogle Scholar
  29. Schulz, B., Guske, S., Dammann, U., & Boyle, C. (1998). Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis, 25, 213–227.Google Scholar
  30. Sharma-Poudyal, D., Duveiller, E., & Sharma, R. (2005). Effects of seed treatment and foliar fungicides on Helminthosporium leaf blight and on performance of wheat in warmer growing conditions. Journal of Phytopathology, 153, 401–408.CrossRefGoogle Scholar
  31. Suryanarayanan, T. (1992). Light-incubation: A neglected procedure in mycology. Mycologist, 6, 144.CrossRefGoogle Scholar
  32. Sutton, B. (1980). The Coelomycetes, Fungi Imperfecti with acervuli, pycnidia and stromata. Kew: Commonwealth Mycological Institute.Google Scholar
  33. Tanweer, A. (1982). Effect of a new fungicide on the viability of rice and sorghum seeds. Pestology, 6, 9–10.Google Scholar
  34. Taylor, A., & Harman, G. (1990). Concepts and technologies of selected seed treatments. Annual review of Phytopathology, 28, 321–339.CrossRefGoogle Scholar
  35. Van Nghiep, H., & Gaur, A. (2005). Efficacy of seed treatment in improving seed quality in rice (Oryza sativa L.). Omonrice, 13, 42–51.Google Scholar
  36. Wang, Y., Zhang, X., Lu, S., Wang, M., Wang, L., Wang, W., et al. (2012). Inhibition of a basal transcription factor 3-like gene Osj10gBTF3 in rice results in significant plant miniaturization and typical pollen abortion. Plant and Cell Physiology, 53, 2073–2089.CrossRefGoogle Scholar
  37. Wang, W., Xu, M., Wang, Y., & Jamil, M. (2014). Basal transcription factor 3 plays an important role in seed germination and seedling growth of rice. BioMed Research International, 2014, 465739.PubMedPubMedCentralGoogle Scholar
  38. Waqas, M., Khan, A. L., Kamran, M., Hamayun, M., Kang, S.-M., Kim, Y.-H., et al. (2012). Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules, 17, 10754–10773.CrossRefGoogle Scholar
  39. Waqas, M., Khan, A. L., Hamayun, M., Shahzad, R., Kim, Y.-H., Choi, K.-S., et al. (2015). Endophytic infection alleviates biotic stress in sunflower through regulation of defence hormones, antioxidants and functional amino acids. European Journal of Plant Pathology, 141, 803–824.CrossRefGoogle Scholar
  40. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18, 315–322.Google Scholar
  41. Wiewióra, B., Żurek, G., & Żurek, M. (2015). Endophyte-mediated disease resistance in wild populations of perennial ryegrass (Lolium perenne). Fungal Ecology, 15, 1–8.CrossRefGoogle Scholar
  42. Yang, C., Hamel, C., Vujanovic, V., & Gan, Y. (2011). Fungicide: modes of action and possible impact on non-target microorganisms. International Scholarly Research Notices: Ecology.  https://doi.org/10.5402/2011/130289.CrossRefGoogle Scholar
  43. Zhang, Q., Zhang, J., Yang, L., Zhang, L., Jiang, D., Chen, W., et al. (2014). Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biological Control, 72, 98–108.CrossRefGoogle Scholar
  44. Zhang, Y., Di Wang, H., & Zhang, C. Q. (2016). Management of benzimidazole fungicide resistance in eggplant brown rot (Phomopsis vexans) with pyraclostrobin. Phytoparasitica, 44, 313–324.CrossRefGoogle Scholar

Copyright information

© Indian Society for Plant Physiology 2018

Authors and Affiliations

  • M. M. Vasanthakumari
    • 1
  • Jambagi Shridhar
    • 1
  • R. J. Madhura
    • 1
  • Mohanasundaram Nandhitha
    • 1
  • Chinnasamy Kasthuri
    • 1
  • B Janardhana
    • 1
    • 2
  • Karaba N. Nataraja
    • 2
  • Gudasalamani Ravikanth
    • 3
  • Ramanan Uma Shaanker
    • 1
    • 2
    • 3
  1. 1.School of Ecology and ConservationUniversity of Agricultural Sciences, GKVKBengaluruIndia
  2. 2.Department of Crop PhysiologyUniversity of Agricultural Sciences, GKVKBengaluruIndia
  3. 3.Ashoka Trust for Research in Ecology and the EnvironmentBengaluruIndia

Personalised recommendations