Effect of Trichoderma spp. and Bacillus subtilis in tomato growth factors and induction of resistance to greenhouse whitefly, Trialeurodes vaporariorum (Hem.: Aleyrodidae)

Document Type : Research Paper

Authors

1 Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia, Iran

2 Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

Abstract

One of the effective methods to reduce pest damage is to induce resistance in plants. This study investigated the impact of inducing resistance using indigenous isolates of Trichoderma spp. and a commercial product (Trichorun), as well as indigenous isolates of Bacillus subtilis (Ehrenberg) and a commercial product (Serenade), along with chemical compounds like Salicylic acid and Humic acid on the host preference and oviposition of the greenhouse whitefly Trialeurodes vaporariorum (Westwood), as well as on plant growth factors. Four tests were conducted to assess the effects of these treatments on the growth factors of tomato (Vadaro 1012), total phenol levels, host preference and oviposition of whitefly in the greenhouse conditions (25 ± 2°C, 60-70% RH, 16:8 h light: dark). The results indicated that the root treatment of the plants with the native strain of Trichoderma harzianum (Rifai) and the treatment of the combination of Trichorun with Serenade have the best performance in plant growth with a significant increase in the root volume, fresh and dry weight of the root and aerial parts of tomato compared to the control. Compared to control, Serenade treatment showed the best results in measuring total phenol, host preference and oviposition of whitefly in the greenhouse with a significant decrease in the average number of insects attracted to the leaf underside, and egg laying rate in the selective test and emerged adult insects in F1generation in the non-selective test.  The findings of this research showed that root inoculation with native isolates of T. harzianum fungus and B. subtilis bacteria increased tomato growth factors, induced resistance to greenhouse whitefly and reduction of host preference and oviposition of whitefly.

Keywords

References

Abdul, R. W., Barkat, H., & Sharma, H. C. (2015). Induced resistance in groundnut by
jasmonic acid and salicylic acid through alteration of trichome density and oviposition by
Helicoverpa armigera (Lepidoptera: Noctuidae). AoB Plants, 5, 1-9.  DOI: https://doi.org/10.1093/aobpla/plt053
Aldaghi, M., Allahyari, H., Hosseini-Naveh, V., & Behboodi, K. (2021). Effect of Trichoderma harzianum Tr6 in inducing resistance against greenhouse whitefly, Trialeurodes vaporariorum (Hem.: Aleyodidae) in Tomato. Plant Protection, 44(3), 107-119. DOI: https://doi.org/10.22055/ ppr.2021.17128 (In Farsi)
Alınç, T., Cusumano, A., Peri, E., Torta, L., & Colazza, S. (2021). Trichoderma harzianum Strain T22 modulates direct defense of tomato plants in response to Nezara viridula feeding activity. Journal of Chemical Ecology, 47(4), 455-462. DOI: https://doi.org/10.1007/s10886-021-01260-3
Alizadeh, H. R., Behboudi, K., Ahmadzadeh, M., Javan-Nikkhah, M., Zamioudis, C., Pieterse, C. M. J., & Bakker, P. H. M. (2013). Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14. Biological Control, 65, 14-23. DOI: https://doi.org/10.1016/j.biocontrol.2013.01.009
Altomare, C., Norvell, W. A., Bjo¨rkman, T., & Harman, G. E. (1999). Solubilization of Phosphates and Micronutrients by the Plant-Growth-Promoting and Biocontrol Fungus Trichoderma harzianum Rifai 1295-22. Applied and Environmental Microbiology, 65(7), 2926-2933. DOI: https://doi.org/10.1128/AEM.65.7.2926-2933.1999
Ayoubi, N., Zafari, D., & Mirabolfathy, M. (2012). Combination of Trichoderma species and Bradyrhizobium japonicum in control of Phytophthora sojae and soybean growth. Journal of Crop Protection, 1(1), 67-79. DOI:  https://doi.org/20.1001.1.22519041.2012.1.1.4.5
Bagheri, S., Kocheily, F., Mosadegh, M. S., & Shishehbor, P. (2012). Investigation on
population changes of jasmine whitefly Aleuroclava jasmini (Takahashi) (Homo.:
Aleyrodidae) in citrus orchards of Dezful city. 20th Iranian Plant Protection Congress. 25-28 August, Shiraz. pp. 666. (In Farsi)
Baldwin, I. T., & Schultz, J. C. (1983). Rapid changes in tree leaf chemistry induced by
damage: evidence for communication between plants. Science, 221, 277-279. DOI: https://doi.org/10.1126/science.221.4607.277
Battaglia, D., Bossi, S., Cascone, P., Digilio, M. C., Prieto, J. D., Fanti, P., Guerrieri, E., Iodice, L., Lingua, G., Lorito, M., & Maffei, M. E. (2013). Tomato below ground–above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Molecular Plant-Microbe Interactions, 26(10), 1249-1256. DOI: https://doi.org/10.1094/MPMI-02-13-0059-R
Bawa, G., Feng, L., Yan, L., Du, Y., Shang, J., Sun, X., Wang, X., Yu, L., Liu, C., Yang, W., & Du, J.  (2019). Pre-treatment of salicylic acid enhances resistance of soybean seedlings to Fusarium solani. Plant Molecular Biology, 101(3), 315-323. DOI: https://doi.org/10.1007/s11103-019-00906-x. 
Blake, C., Christensen, M. N., & Kovács, Á. T. (2021). Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Molecular Plant-Microbe Interactions, 34(1), 15-25. DOI:  https://doi.org/10.1094/MPMI-08-20-0225-CR
Carillo, P., Woo, L. S., Comite, E., El-Nakhel, C., Rouphael, Y., Fusco, G. M., Borzacchiello, A., Lanzuise, S., & Vinale, F. (2020). Application of Trichoderma harzianum, 6-Pentyl-α-pyrone and plant biopolymer formulations modulate plant metabolism and fruit quality of plum tomatoes. Plants, 9, 771. DOI:  https://doi.org/10.3390/plants9060771
Coppola, M., Diretto, G., Digilio, M. C., Woo, S. L., Giuliano, G., Molisso, D., Pennacchio, F., Lorito, M., & Rao, R. (2019). Transcriptome and metabolome reprogramming in tomato plants by Trichoderma harzianum strain T22 primes and enhances defense responses against aphids. Frontiers in Physiology, 10, 745-754. DOI:  https://doi.org/10.3389/fphys.2019.00745
Farrokhi, S. (2016). Localization of commercial production of Encarsia formosa (Hym., Aphelinidae), the parasitoid of greenhouse whitefly. The final report of the research project of the Iranian Research Institute of Plant Protection. Frost number, 50720, 25 p. (In Farsi)
Felton, G. W., Korth, K. L., Bi, J. L., Wesley, S. V., Huhman, D. V., Mathews, M. C., &
Murphy, J. B. (1999). Inverse relationship between systemic resistance of plants to
microorganisms and to insect herbivory. Current Biology, 9, 317-320. DOI: https://doi.org/10.1016/S0960-9822(99)80140-7
Ghamari, M., Hosseininaveh, V., Talebi, K., Nozari, J., & Allahyari, H. (2020). Biochemical characterization of the induced immune system of pistachio (Pistacia vera) by Salicylic Acid. International Journal of Fruit Science, 20(2), 117-132. DOI: https://doi.org/10.1080/15538362.2019.1586025
Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species-opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2, 43-56. DOI: https://doi.org/10.1038/nrmicro797
Hashem, A., Tabassum, B., & Abd-Allah, E. F. (2019). Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi Journal of Biological Sciences, 26(6), 1291-1297. DOI:  https://doi.org/10.1016/j.sjbs.2019.05.004
Jafarbeigi, F., Samih, M. A., Alaei, H., & Shirani, H. (2020). Induced tomato resistance against Bemisia tabaci triggered by salicylic acid, β-aminobutyric acid, and Trichoderma. Neotropical Entomology, 49(3), 456-467. DOI:  https://doi.org/10.1007/s13744-020-00771-0
Kafi, M., Babalar, M., Nikbakht, A., Ebrahimzadeh, H., Etemadi, N., & Samavat, S. (2009). Effect of humic acid spray on nutrients uptake, protein content and postharvest life of Gerbera jamesonii L. cv. Malibu. Iranian Journal of Horticultural Science, 8, 238-248. (In Farsi) http://ijhs.ut.ac.ir/?_action=articleInfo&article=19944&vol=1976
Khalid, A. S., Mohamad Roof, M. N., Rebecca, H. H., & Idris, A. B. (2015). Aphid-induced
defences in chilli affect preferences of the whitefly, Bemisia tabaci (Hemiptera:
Aleyrodidae). Scientific Reports, 5(13), 1-9. DOI: https://doi.org/10.1038/srep13697
Kumar, S., Arutselvan, A. R., Masurkar, P., Singh, U. B., Tripathi, R., Bhupenchandra, I., Minkina, T., & Keswani, C. (2024). Bacillus subtilis-Mediated Induction of Disease Resistance and Promotion of Plant Growth of Vegetable Crops. In Mageshwaran, V., Singh, U. B., Saxena, A. K., & Singh, H. B. (Eds). Applications of Bacillus and Bacillus Derived Genera in Agriculture, Biotechnology and Beyond. Springer Nature Singapore. pp. 165-211. DOI: https://doi.org/10.1007/978-981-99-8195-3_9
Liorens, E., García-Agustín, P., & Lapeña, L. (2017). Advances in induced resistance by natural compounds: towards new options for woody crop protection. Science Agriculture, 74, 90-100. DOI: https://doi.org/10.1590/1678-992X-2016-0012
Maketon, M., Apisitsantikul, J., & Siriraweekul, C. (2008). Greenhouse evaluation of Bacillus subtilis AP-01 and Trichoderma harzianum AP-001 in controlling tobacco diseases. Brazil Journal of Microbiology, 39, 296-300. DOI: https://doi.org/10.1590/S1517-838220080002000018
McLean, K. L., Hunt, J. S., Stewart, A., Wite, D., Porter, I. J., & Villalta, O. (2012).
Compatibility of a Trichoderma atroviride biocontrol agent with management practices of
Allium crops. Crop Protection, 33, 94-100. DOI: https://doi.org/10.1016/j.cropro.2011.11.018
Menjivar, R. D., Cabrera, J. A., Kranz, J., & Sikora, R. A. (2012). Induction of metabolite organic compounds by mutualistic endophytic fungi to reduce the greenhouse whitefly Trialeurodes vaporariorum (Westwood) infection on tomato. Plant and Soil, 352(1), 233-241. DOI:  https://doi.org/10.3390/agriculture10120587
Pourtaghi, E., Talaei-Hassanloui, R., Nasibi, F., & Fotouhifar, K. B. (2020). Endophytic colonization of tomato by Beauveria bassiana for control of the greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Acta Biologica, 27, 149-160.  DOI: https://doi.org/10.18276/ab.2020. 27-14
Radwan, M. A., Farrag, S. A. A., Abu-Elamayem, M. M., & Ahmed, N. S. (2012). Biological control of the root-knot nematode, Meloidogyne incognita on tomato using bioproducts of microbial origin. Applied Soil Ecology, 56, 58-62. DOI: https://doi.org/10.1016/j.apsoil.2012.02.008
Rani, P. U., & Yasur, J. (2009). Physiological changes in groundnut plants induced by
pathogenic infection of Cercosporidium personatun Deighton. Allelopathy Journal, 23(2), 369-378.
Rokhzadi, A., Asgazadeh, A., Darvish, F., Nour-Mohammed, G., & Majidi, E. (2008). Influence of plant growth promoting rhizobacteria on dry matter accumulation and yield of chickpea (Cicer
arietinum L.) under field conditions. American Eurasian Journal of Agriculture Environmental Science, 3, 253-257.
Rudresh, D. L., Shivaprakash, M. K., & Prasad, R. D. (2005). Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Applied Soil Ecology, 28, 139-146. DOI: https://doi.org/10.1016/j.apsoil.2004.07.005
Rumyantsev, S. D., Alexeeve, V. Y., Sorokan, A. V., Burkhanova, G. F., Cherepanova, E. A., Garafutdinov, R. R., Maksimov, I. V., & Vesolova, S. V. (2023). Additive effect of the composition of endophytic bacteria bacillus subtilis on systemic resistance of wheat against greenbug aphid Schizaphis graminum due to lipopeptides. Life, 13(1), 214. DOI: https://doi.org/10.3390/life13010214
Sharon, E., Bar-Eyal, M., Chet, I., Herrera-Estrella, A., Kleifeld, O., & Spiegel, Y. (2001). Biological control of root knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology, 91, 687-693. DOI: https://doi.org/10.1094/PHYTO.2001.91.7.687
Sikora, R. A., Schäfer, K., & Dababat, A. A. (2007). Modes of action associated with microbially induce in planta suppression of plant-parasitic nematodes. Australasian Plant Pathology, 36, 124-134. https://link.springer.com/article/10.1071/AP07008
Tahir, H. A., Gu, Q., Wu, H., Raza, W., Hanif, A., Wu, L., Colman, M. V., & Gao, X. (2017). Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Frontiers in Microbiology, 8, 171-180. DOI: https://doi.org/10.3389/fmicb.2017.00171
Valenzuela-Soto, J. H., Estrada-Hernández, M. G., Ibarra-Laclette, E., & Délano-Frier, J. P. (2010). Inoculation of tomato plants (Solanum lycopersicum) with growth-promoting Bacillus subtilis retards whitefly Bemisia tabaci development. Planta, 231(2), 397-410. DOI: https://doi.org/10.1007/s00425-009-1061-9.
van Lenteren, J. C., Szabo, P., & Huisman, P. W. T. (1992). The parasite-host relationship between Encarsia formosa Gahan (Hymenoptera, Aphelinidae) and Trialeurodes vaporariorum (Westwood) (Homoptera, Aleyrodidae). Journal of Applied Entomology, 114(5), 392-399. DOI: https://doi.org/10.1111/j.1439-0418.1992.tb01142.x
van Lenteren, J. C. (2000). A greenhouse without pesticides: fact or fantasy? Crop Protection, 19(6), 375-384. DOI: https://doi.org/10.1016/S0261-2194(00)00038-7
Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Woo, S., & Lorito, M. (2008). Trichoderma–plant–pathogen interactions. Soil Biology and Biochemistry, 40(1), 1-10. DOI: https://doi.org/10.1016/j.soilbio.2007.07.002
Walling, L. (2008). Avoiding effective defences: Strategies employed by phloem-feeding
insects. Plant Physiology, 146, 859-866. https://doi.org/10.1104/pp.107.113142
Whipps, J. M. (2001). Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany, 52, 487-511. DOI: https://doi.org/10.1093/jexbot/52.suppl_1.487
Worrall, D., Holroyd, G. H., Moore, J. P., Glowacz, M., Croft, P., Taylor, J. E., Paul, N. D., & Roberts, M. R. (2012). Treating seeds with activators of plant defence generates long‐lasting priming of resistance to pests and pathogens. New Phytologist, 193(3), 770-778. DOI: https://doi.org/10.1111/j.1469-137.2011.03987.x
Wu, J., & Baldwin, I. T. (2010). New insights into plant responses to the attack from insect
herbivores. Annual Review of Genetics, 44, 1-24. DOI:  https://www.annualreviews.org/doi/10.1146/annurev-genet-102209-163500
Zaim, S., Bekkar, A. A., & Belabid, L. (2018). Efficacy of Bacillus subtilis and Trichoderma harzianum combination on chickpea Fusarium wilt caused by F. oxysporum f. sp. ciceris. Archives of Phytopathology and Plant Protection, 51(3-4), 217-226. DOI: https://doi.org/10.1080/03235408.2018.1447896
Plant Pest Research
Volume 14, Issue 2
September 2024
Pages 1-15

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History

  • Receive Date: 14 May 2024
  • Revise Date: 31 July 2024
  • Accept Date: 01 August 2024

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