Saccharin and its parental compound probenazole (PBZ) are plant activators of effective defense responses to (hemi) biotrophic pathogens. Here, we demonstrate that pretreatment of wheat seedlings with saccharin or PBZ results in a significant reduction of powdery mildew caused by Blumeria graminis f. sp. tritici. Transcriptional analysis revealed the expression of 15 defense-related genes including PR genes, WCI genes, LOX, AOS, NPR1, PAL and WRKY genes in wheat seedlings exposed to either saccharin or PBZ. Moreover, the saccharin- and PBZ-enhanced expression of those genes during fungal infection further proved a close correlation with increased resistance in wheat.
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Bassoli A, Merlini L (2003) Sweeteners. In: Caballero B, Finglas P, Toldra F (eds) Encyclopedia of food sciences and nutrition, 2nd edn. Academic Press & Elsevier Science, London, pp 5688–5695
Bektas Y, Eulgem T (2015) Synthetic plant defense elicitors. Front Plant Sci 5:804
Boyle C, Walters D (2005) Induction of systemic protection against rust infection in broad bean by saccharin: effects on plant growth and development. New Phytol 167:607–612
Boyle C, Walters DR (2006) Saccharin-induced protection against powdery mildew in barley: effects on growth and phenylpropanoid metabolism. Plant Pathol 55:82–91
De Vleesschauwer D, Gheysen G, Höfte M (2013) Hormone defense networking in rice: tales from a different world. Trends Plant Sci 18:555–565
Desmond OJ, Edgar CI, Manners JM, Maclean DJ, Schenk PM, Kazan K (2006) Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum. Physiol Mol Plant Pathol 67:171–179
Desmond OJ, Manners JM, Schenk PM, Maclean DJ, Kazan K (2008) Gene expression analysis of the wheat response to infection by Fusarium pseudograminearum. Physiol Mol Plant Pathol 73:40–47
Ding L, Xu H, Yi H, Yang L, Kong Z, Zhang L, Zhang L, Xue S, Ma Z (2011) Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS One 6:e19008
Fujioka K, Gotoh H, Noumi T, Yoshida A, Noutoshi Y, Inagaki Y, Yamamoto M, Ichinose Y, Shiraishi T, Toyoda K (2015) Protection induced by volatile limonene against anthracnose disease in Arabidopsis thaliana. J Gen Plant Pathol 81:415–419
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Gorlach J, Volrath S, Hengy GKG, Beckhove U, Kogel K, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–643
Iwai T, Seo S, Mitsuhara I, Ohashi Y (2007) Probenazole-induced accumulation of salicylic acid confers resistance to Magnaporthe grisea in adult rice plants. Plant Cell Physiol 48:915–924
Koganezawa H, Sato T, Sasaya T (1998) Effect of probenazole and saccharin on symptom appearance TMV in tobacco. Ann Phytopathol Soc Jpn 64:80–84
Kouzai Y, Kimura M, Yamanaka Y, Watanabe M, Matsui H, Yamamoto M, Ichinose Y, Toyoda K, Onda Y, Mochida K, Noutoshi Y (2016) Expression profiling of marker genes responsive to the defence-associated phytohormones salicylic acid, jasmonic acid and ethylene in Brachypodium distachyon. BMC Plant Biol 16:59
Lawrence JF (2003) Saccharin. In: Caballero B, Finglas P, Toldra F (eds) Encyclopedia of food sciences and nutrition, 2nd edn. Academic Press & Elsevier Science, London, pp 5033–5035
Li HP, Fischer R, Liao YC (2001) Molecular evidence for induction of phenylalanine ammonia-lyase during Puccinia graminis infection and elicitation in wheat. Can J Plant Pathol 23:286–291
Liu H, Costa L, Kazan K, Schenk PM (2016) Development of marker genes for jasmonic acid signaling in shoots and roots of wheat. Plant Signal Behav 11:1–8
Lu Z, Gaudet D, Puchalski B, Despins T, Frick M, Laroche A (2006) Inducers of resistance reduce common bunt infection in wheat seedlings while differentially regulating defence-gene expression. Physiol Mol Plant Pathol 67:138–148
Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe Interact 19:1127–1137
Molina A, Görlach J, Volrath S, Ryals J (1999) Wheat genes encoding two types of PR-1 proteins are pathogen inducible, but do not respond to activators of systemic acquired resistance. Mol Plant Microbe Interact 12:53–58
Nakashita H, Yoshioka K, Yasuda M, Nitta T, Arai Y, Yoshida S, Yamaguchi I (2002) Probenazole induces systemic acquired resistance in tobacco through salicylic acid accumulation. Physiol Mol Plant Pathol 61:197–203
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655
Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521
Sahu R, Sharaff M, Pradhan M, Sethi A, Bandyopadhyay T, Mishra VK (2016) Elucidation of defense-related signaling responses to spot blotch infection in bread wheat (Triticum aestivum L.). Plant J 86:35–49
Seo S, Nakaho K, Hong SW, Takahashi H, Shigemori H, Mitsuhara I (2016) l-histidine induces resistance in plants to the bacterial pathogen Ralstonia solanacearum partially through the activation of ethylene signaling. Plant Cell Physiol 57:1932–1942
Srivastava P, George S, Marois JJ, Wright DL, Walker DR (2011) Saccharin-induced systemic acquired resistance against rust (Phakopsora pachyrhizi) infection in soybean: effects on growth and development. Crop Prot 30:726–732
Tamaoki D, Seo S, Yamada S, Kano A, Miyamoto A, Shishido H, Miyoshi S, Taniguchi S, Akimitsu K, Gomi K (2013) Jasmonic acid and salicylic acid activate a common defense system in rice. Plant Signal Behav 8:e24260
Uchiyama M, Abe H, Sato R, Shimura M, Watanabe T (1973) Fate of 3-allyloxy-1, 2-benzisothiazole 1, 1-dioxide (Oryzemate®) in rice plant. Agric Biol Chem 37:737–745
Wang F, Wu W, Wang D, Yang W, Sun J (2016) Characterization and genetic analysis of a novel light-dependent lesion mimic mutant, lm3, showing adult-plant resistance to powdery mildew in common wheat. PLoS ONE 11:e0155358
Yamaguchi I (1982) Fungicides for the control of rice blast disease. J Pestic Sci 7:307–316
Yoshioka K, Nakashita H, Klessig DF, Yamaguchi I (2001) Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant J 25:149–157
Yu G, Muehlbauer GJ (2001) Benzothiadiazole-induced gene expression in wheat spikes does not provide resistance to Fusarium head blight. Physiol Mol Plant Pathol 59:129–136
Zhao L, Phuong LT, Luan MT, Fitrianti AN, Matsui H, Nakagami H, Noutoshi Y, Yamamoto M, Ichinose Y, Shiraishi T, Toyoda K (2019) A class III peroxidase PRX34 is a component of disease resistance in Arabidopsis. J Gen Plant Pathol 85:405–412
LTP thanks the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) for financial support during her doctoral program. This research was supported in part by the Grants-in-Aid for Scientific Research (18K05645) from the Japan Society for Promotion of Science (JSPS).
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Supplementary file2 Fig. S1 Effect of saccharin doses and application methods on growth of 10-day-old seedlings of susceptible wheat (Triticum aestivum cv. Nourin No. 61). Seedlings were sprayed with water (as a control) or saccharin (0, 0.1, 1, 3 and 5 mM) solutions amended with 0.01% (v/v) Silwet L-77 as a surfactant (a) or by drenching soil in pots with 2, 5 and 10 ml of solution (b). Wheat seedlings (aerial parts) were harvested to assess growth 10 days after treatment. Plant height and fresh mass did not differ significantly among doses or application methods (c) (Tukey’s test, p > 0.05). Data are means ± SD of plant height (cm) and fresh mass (g/seedling) from 20 seedlings. However, necrosis appeared on the tip of the first leaf of wheat plants (in circle, when saccharin was applied at high doses [3–5 mM]). The experiment was repeated twice with similar results; representative results are shown. Fig. S2 Foliar sprays of saccharin on 10-day-old wheat seedlings reduced disease development of B. graminis. Ten-day-old wheat seedlings were sprayed with 0, 0.1 or 1 mM saccharin amended with 0.01% (v/v) Silwet L-77, then inoculated 2 days later in a chamber containing wheat plants heavily infected with B. graminis. Pustules on adaxial side of leaves were counted (b) and symptoms photographed at 7 days post inoculation (a). Means (±SD) from 15–20 leaves are shown. Different letters indicate significant differences among treatments using Tukey’s test analysis (p < 0.05). The experiment was repeated twice with similar results; representative results are shown. (PPTX 14759 kb)
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Phuong, L.T., Zhao, L., Fitrianti, A.N. et al. The plant activator saccharin induces resistance to wheat powdery mildew by activating multiple defense-related genes. J Gen Plant Pathol 86, 107–113 (2020). https://doi.org/10.1007/s10327-019-00900-7
- Blumeria graminis f. sp. tritici
- Induced resistance
- Plant activator
- Probenazole (PBZ)