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Research Article

Trichoderma harzianum-induced defense in sunflower (Helianthus annuus L.) against Plasmopara halstedii with changes in metabolite profiling of roots

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Pages 1403-1418 | Received 21 Feb 2021, Accepted 29 Jul 2021, Published online: 06 Aug 2021

References

  • Abdelrahman, M., Abdel-Motaal, F., El-Sayed, M., Jogaiah, S., Shigyoa, M., Ito, S. I., & Tran, L. S. P. (2016). Dissection of Trichoderma longibrachiatum-induced defense in onion (Allium cepa L.) against Fusarium oxysporum f. sp. cepa by target metabolite profiling. Plant Science, 246, 128–138. https://doi.org/10.1016/j.plantsci.2016.02.008
  • Ahmad, J., Bagheri, R., Bashir, H., Baig, M. A., Al-Huqail, A., Ibrahim, M. M., & Qureshi, M. I. (2018). Organ-specific phytochemical profiling and antioxidant analysis of Parthenium hysterophorus L. BioMed Research International, 2018, Article 9535232. https://doi.org/10.1155/2018/9535232
  • Albourie, J. M., Tourvieille, J., & de Labrouhe, D. T. (1998). Resistance to metalaxyl in isolates of the sunflower pathogen Plasmopara halstedii. European Journal of Plant Pathology, 104(3), 235–242. https://doi.org/10.1023/A:1008691123239
  • Ayaz, F., Küçükboyacı, N., & Demirci, B. (2017). Essential oil composition and antimicrobial activity of Aster subulatus Michx. from Turkey. Record of Natural Products, 11(4), 389–394.
  • Batovska, D. I., Todorova, I. T., Parushev, S. P., Nedelcheva, D. V., Bankova, V. S., Popov, S. S., Ivanova, I. I., & Batowski, S. A. (2009). Biomarkers for the prediction of the susceptibility of grapevine leaves to downy mildew. Journal of Plant Physiology, 166(7), 781–785. https://doi.org/10.1016/j.jplph.2008.08.008
  • Bollina, V., Kumaraswamy, G. K., Kushalappa, A. C., Choo, T. M., Dion, Y., Rioux, S., Faubert, D., & Hamzehzarghani, H. (2010). Mass spectrometry-based metabolomics application to identify quantitative resistance-related metabolites in barley against Fusarium head blight. Molecular Plant Pathology, 11(6), 769–782. https://doi.org/10.1111/j.1364-3703.2010.00643.x
  • Chen, F., Tholl, D., Bohlmann, J., & Pichersky, E. (2011). The family of terpene synthase in plants: A mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant Journal, 66(1), 212–229. https://doi.org/10.1111/j.1365-313X.2011.04520.x
  • Choi, G. J., Jang, K. S., Choi, Y. H., Yu, J. H., & Kim, J. C. (2010). Antifungal activity of lower alkyl fatty acid esters against powdery mildews. Plant Pathology Journal, 26(4), 360–366. https://doi.org/10.5423/PPJ.2010.26.4.360
  • Ciuperca, O. T., Tebrencu, C. E., Iacob, E., Cretu, M. R., Chiriac, M., & Ionescu, E. (2016). Phytochemical screening and chromatographic fingerprint studies on ethanolic extracts of Arnica montana L. Analele Ştiinţifice ale Universităţii *Al. I. Cuza” din Iaşi (serie IIa), Biologie vegetală, 62(2), 53–60.
  • Conforti, F., Menichini, F., Loizzo, M. R., Statti, G. A., Rapisarda, A., Menichini, F., & Houghton, P. J. (2008). Antioxidant, a-amylase inhibitory and brine-shrimp toxicity studies on Centaurea centaurium L. methanolic root extract. Natural Product Research, 22(16), 1457–1466. https://doi.org/10.1080/14786410802098071
  • Dahmani, M. M., Laoufi, R., Selama, O., & Arab, K. (2018). Gas chromatography coupled to mass spectrometry characterization, anti-inflammatory effect, wound-healing potential, and hair growth-promoting activity of Algerian Carthamus caeruleus L (Asteraceae). Indian Journal of Pharmacology, 50(3), 123–129. https://doi.org/10.4103/ijp.IJP_65_17
  • Delen, N., Onoğur, E., & Yıldız, M. (1985). Sensitivity levels to metalaxyl in six Plasmopara helianthi Novot. Isolates. The Journal of Turkish Phytopathology, 14(1), 31–36.
  • Demirtaş, I., & Şahin, A. (2013). Bioactive volatile content of the stem and root of Centaurea carduiformis DC. subsp. carduiformis var. carduiformis. Journal of Chemistry, 2013, Article 125286. https://doi.org/10.1155/2013/125286
  • Eyol, P. C., Sarikahya, N. B., Karakoc, A. G., Gokce, A., Demirci, F., Kirmizigul, S., & Goren, N. (2017). Fatty acid composition and biological activities of Tanacetum zahlbruckneri (Náb.) Grierson growing in Turkey. Records of Natural Products, 11(4), 401–405.
  • Georgiev, M., Georgiev, V., Penchev, P., Antonova, D., Pavlov, A., Ilieva, M., & Popov, S. (2010). Volatile metabolic profiles of cell suspension cultures of Lavandula vera, Nicotiana tabacum and Helianthus annuus, cultivated under different regimes. Engineering in Life Sciences, 10(2), 148–157. https://doi.org/10.1002/elsc.200900090
  • Goel, D., Goel, R., Singh, V., Ali, M., Mallavarapu, G. R., & Kumar, S. (2007). Composition of the essential oil from the root of Artemisia annua. Journal of Natural Medicines, 61(4), 458–461. https://doi.org/10.1007/s11418-007-0175-2
  • Gulya, T., Draper, M., Harbour, J., Holen, C., Knodel, J., Lamely, A., & Manson, P. (1999). Metalaxyl resistance in sunflower downy mildew in Nort America. Proceedings of the 21st. NSA Sunflower Research Workshop, pp. 118–123, Bismarck, ND.
  • Gunnaiah, R., Kushalappa, A. C., Duggavathi, R., Fox, S., & Somers, D. J. (2012). Integrated metabolo proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS One, 7(7), Article e40695. https://doi.org/10.1371/journal.pone.0040695
  • Hansjakob, A., Riederer, M., & Hildebrandt, U. (2011). Wax matters: Absence of very-long-chain aldehydes from the leaf cuticular wax of the glossy11 mutant of maize compromises the prepenetration processes of Blumeria graminis. Plant Pathology, 60(6), 1151–1161. https://doi.org/10.1111/j.1365-3059.2011.02467.x
  • Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species-opportunistic a virulent plant symbionts. Nature Reviews Microbiology, 2(1), 43–56. https://doi.org/10.1038/nrmicro797
  • Hasegawa, K., Knegt, E., & Bruinsma, J. (1983). Caprolactam, a light-promoted growth inhibitor in sunflower seedlings. Phytochemistry, 22(11), 2611–2612. https://doi.org/10.1016/0031-9422(83)80177-0
  • Hazarhun, G., & Özer, N. (2016). Control of sunflower downy mildew (Plasmopara halstedii with antagonist fungi. Communications in Agricultural and Applied Biological Sciences, 81(2), 91–97.
  • Hichri, F., Omri, A., Hossan, A. S. M., Flamini, G., & Jannet, H. B. (2018). Chemical composition and biological evaluation of the Tunisian Achillea cretica L. essential oils. Journal of Essential Oil Research, 30(2), 105–112. https://doi.org/10.1080/10412905.2017.1391720
  • Lafon, S., Penaud, A., Walser, P., De Guenin, M. C., Molinero, V., Mestres, R., & Tourvieille, D. (1996). Le Mildiou du tournesol toujours sous surveillance. Pytoma, 484, 35–36.
  • Lawson, S. K., Sharp, L. G., Powers, C. N., McFeeters, R. L., Satyal, P., & Setzer, W. N. (2019). Essential oil compositions and antifungal activity of Sunflower (Helianthus) species growing in North Alabama. Applied Sciences, 9(15), Article 3179. https://doi.org/10.3390/app9153179
  • Mayo-Prieto, S., Marra, R., Vinale, F., Rodríguez-González, A., Woo, S. I., Lorito, M., Gutiérrez, S., & Casquero, P. A. (2019). Effect of Trichoderma velutinum and Rhizoctonia solani on the metabolome of bean plants (Phaseolus vulgaris L. International Journal of Molecular Sciences, 20(3), Article 549. https://doi.org/10.3390/ijms20030549
  • Mithun, N. M., Shashidhara, S., & Vivek Kumar, R. (2011). Eclipta alba (L.), A Review on its phytochemical and pharmacological profile. Pharmacologyonline (Section: Newsletter), 1, 345–357.
  • Mohebat, R., & Bidoki, M. Z. (2018). Comparative chemical analysis of volatile compounds of Echinops ilicifolius using hydrodistillation and headspace solid-phase microextraction and the antibacterial activities of its essential oil. Royal Society Open Science, 5(2), Article 171424. https://doi.org/10.1098/rsos.171424
  • Molinero-Ruiz, M. L., Cordón-Torres, M. M., Martínez-Aguilar, J., Melero-Vara, J. M., & Domínguez, J. (2008). Resistance to metalaxyl and to metalaxyl-M in populations of Plasmopara halstedii causing downy mildew in sunflower. Canadian Journal of Plant Pathology, 30(1), 97–105. https://doi.org/10.1080/07060660809507500
  • Mottaki, Z., Rezayian, M., Niknam, V., Ebrahimzadeh, H., & Mirmasoumi, M. (2019). Using hairy roots for production of secondary metabolites in Artemisia. Plant Biotechnology Reports, 13(3), 263–271. https://doi.org/10.1007/s11816-019-00534-3
  • Muhammad, R., Amna, S., & Arshad, J. (2020). GC-MS analysis of Sonchus asper root extract for identification of fungicidal compounds against Rhizoctonia solani. Pakistan Journal of Weed Science Research, 26(3), 267. https://doi.org/10.28941/pjwsr.v26i3.858.
  • Nagaraju, A., Murali, M., Sudisha, J., Amruthesh, K. N., & Mahadeva, S. (2012a). Beneficial microbes promote plant growth and induce systemic resistance in sunflower against downy mildew disease caused by Plasmopara halstedii Murthy. Current Botany, 3(5), 12–18.
  • Nagaraju, A., Sudisha, J., & Mahadeva, S. (2012b). Seed priming with Trichoderma harzianum isolates enhances plant growth and induces resistance against Plasmopara halstedii an incitant of sunflower downy mildew disease. Australasian Plant Pathology, 41(6), 609–620. https://doi.org/10.1007/s13313-012-0165-z
  • NandeeshKumar, P., RamachandraKini, K., Prakash, H., Niranjana, S., R, S., & Shekar Shetty, H. (2008). Induction of resistance against downy mildew on sunflower by rhizobacteria. Journal of Plant Interactions, 3(4), 255–262. https://doi.org/10.1080/17429140802245697
  • Nawrocka, J., & Małolepsza, U. (2013). Diversity in plant systemic resistance induced by Trichoderma. Biological Control, 67(2), 149–156. https://doi.org/10.1016/j.biocontrol.2013.07.005
  • Nawrocka, J., Małolepsza, U., Szymczak, K., & Szczech, M. (2018). Involvement of metabolic components, volatile compounds, PR proteins, and mechanical strengthening in multilayer protection of cucumber plants against Rhizoctonia solani activated by Trichoderma atroviride TRS25. Protoplasma, 255(1), 359–373. https://doi.org/10.1007/s00709-017-1157-1
  • Nazaruk, J., & Kalemba, D. (2009). Chemical composition of the essential oils from the roots of Erigeron acris L. and Erigeron annuus (L.) Pers. Molecules, 14(7), 2458–2465. https://doi.org/10.3390/molecules14072458
  • Ogunwande, I. A., Flamini, G., Cioni, P. L., Omikorede, O., Azeez, R. A., Ayodele, A. A., & Kamil, Y. O. (2010). Aromatic plants growing in Nigeria: Essential oil constituents of Cassia alata (Linn.) Roxb. and Helianthus annuus L. Records of Natural Products, 4(4), 211–217.
  • Oros, G., & Viranyi, F. (1984). Resistance of Plasmopara halstedii to metalaxyl in the greenhouse. Temperate Downy Mildew Newsletter, 3, 22–23.
  • Özer, N. (2011). Screening for fungal antagonists to control black mold disease and to induce the accumulation of antifungal compounds in onion after seed treatment. Biocontrol, 56(2), 237–247. https://doi.org/10.1007/s10526-010-9326-6
  • Özer, N., & Arın, L. (2014). Evaluation of fungal antagonists to control black mold disease under field conditions and to induce the accumulation of antifungal compounds in onion following seed and set treatment. Crop Protection, 65, 21–28. https://doi.org/10.1016/j.cropro.2014.06.027
  • Özer, N., Koç, M., & Der, B. (2009). The sensitivity of Aspergillus niger and Fusarium oxysporum f sp cepae to fungistasis in onion growing soils. Journal of Plant Pathology, 91(2), 401–410.
  • Özer, N., Sabudak, T., Özer, C., Gindro, K., Schnee, S., & Solak, E. (2017). Investigations on the role of cuticular wax in resistance to powdery mildew in grapevine. Journal of General Plant Pathology, 83(5), 316–328. https://doi.org/10.1007/s10327-017-0728-5
  • Parween, D., Sahu, B. B., Kumari, M., & Pudake, R. N. (2019). Plant metabolites involved in plant–pathogen interactions. In A. Varma, S. Tripathi, & R. Prasad (Eds.), Plant biotic interactions (pp. 61–84). Springer Nature.
  • Polatoglu, K., Demirci, F., Demirci, B., Gören, N., & Baser, K. H. C. (2012). Essential oil composition and antimicrobial activities of Tanacetum chiliophyllum (Fisch. & Mey.) Schultz Bip. var. monocephalum Grierson from Turkey. Records of Natural Products, 6(2), 184–188.
  • Şahin, S., & Elhussein, E. A. A. (2018). Valorization of a biomass: Phytochemicals in oilseed by-products. Phytochemistry Reviews, 17(4), 657–668. https://doi.org/10.1007/s11101-018-9552-6
  • Sakr, N. (2014). Evolution of new Plasmopara halstedii races under the selection pressure with resistant sunflower plants: A review. Hellenic Plant Protection Journal, 7(1), 1–13.
  • Sakr, N., Ducher, M., Tourvieille, J., Walser, P., Vear, F., & De Labrouhe, D. T. (2008). Variation in form and size of Plasmopara halstedii (sunflower downy mildew) zoosporangia. Mycological Progress, 7(4), 257–265. https://doi.org/10.1007/s11557-008-0568-y
  • Shah, J. (2005). Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annual Review of Phytopathology, 43(1), 229–260. https://doi.org/10.1146/annurev.phyto.43.040204.135951
  • Sharma, R. K., & Katiyar, D. (2013). Recent advances in the development of coumarin derivatives as antifungal agents. In K. Singh, & N. Srivastava (Eds.), Recent trends in human and animal mycology (pp. 235–263). Springer.
  • Shigemori, H. (2019). Bioactive compounds involved in the life cycle of higher plants. In A. Douglas Kinghorn, H. Falk, S. Gibbons, J. Kobayashi, Y. Asakawa, & J. K. Liu (Eds.), Progress in the chemistry of organic natural products (pp. 385–408). Springer.
  • Shoresh, M., Harman, G. E., & Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, 48(1), 21–43. https://doi.org/10.1146/annurev-phyto-073009-114450
  • Singh, B. N., Singh, A., Singh, S. P., & Sing, H. B. (2011). Trichoderma harzianum-mediated reprogramming of oxidative stress response in root apoplast of sunflower enhances defence against Rhizoctonia solani. European Journal of Plant Pathology, 131(1), 121–134. https://doi.org/10.1007/s10658-011-9792-4
  • Skala, E., Rijo, P., Garcia, C., Sitarek, P., Kalemba, D., Toma, M., Szemraj, J., Pytel, D., Wysokińska, H., & Uliwiński, T. (2016). The essential oils of Rhaponticum carthamoides hairy roots and roots of soil-grown plants: Chemical composition and antimicrobial, anti-inflammatory, and antioxidant activities. Oxidative Medicine and Cellular Longevity, 2016, Article 8505384. https://doi.org/10.1155/2016/8505384
  • Spring, O., Bachofer, M., Thines, M., Riethmüller, A., Göker, M., & Oberwinkler, F. (2006). Intraspecific relationship of Plasmopara halstedii isolates differing in pathogenicity and geographic origin based on ITS sequence data. European Journal of Plant Pathology, 114(3), 309–315. https://doi.org/10.1007/s10658-005-5996-9
  • Stringlis, I. A., Yu, K., Feussnerb, K., de Jonge, B., Van Bentuma, S., Van Verk, M. C., Berendsen, R. L., Bakker, P. A. H. M., Feussner, I., & Pieterse, C. M. J. (2018). MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proceedings of the National Academy of Sciences, 115(22), E5213–E5222. https://doi.org/10.1073/pnas.1722335115
  • Tsuba, M., Katagiri, C., Takeuchi, Y., Takada, Y., & Yamaoka, N. (2002). Chemical factors of the leaf surface involved in the morphogenesis of Blumeria graminis. Physiological and Molecular Plant Pathology, 60(2), 51–57. https://doi.org/10.1006/pmpp.2002.0376
  • Ur-Rashid, M., Alamzeb, M., Ali, S., Khan, A. A., Igoli, J. O., Ferro, V. A., Gray, A. I., & Khan, M. R. (2015). A new ceramide along with eight known compounds from the roots of Artemisia incisa Pamp. Records of Natural Products, 9(3), 294–304.
  • Viranyi, F., & Spring, O. (2011). Advanced in sunflower downy mildew research. European Journal of Plant Pathology, 129(2), 207–220. https://doi.org/10.1007/s10658-010-9683-0
  • Yokotani-Tomita, K., Kato, J., Kosemura, S., Yamamura, S., Kushima, M., Kakutata, H., & Hasegawa, K. (1997). Light-induced auxin-inhibiting substance from sunflower seedlings. Phytochemistry, 46(3), 503–506. https://doi.org/10.1016/S0031-9422(97)00307-5
  • Zhao, M. P., Liu, Q. Z., Liu, Q., & Liu, Z. L. (2017). Identification of larvicidal constituents of the essential oil of Echinops grijsii roots against the three species of mosquitoes. Molecules, 132(4), 470–474. https://doi.org/10.1016/j.exppara.2012.09.010

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