Research Papers

Spireoside Controls Blast Disease by Disrupting Membrane Integrity of Magnaporthe oryzae

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  • State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Rice Research Institute, Sichuan Agricultural University, Chengdu 611130, China
First author contact:#These authors contributed equally to this work

Received date: 2024-08-27

  Accepted date: 2024-10-11

  Online published: 2024-10-15

Abstract

The application of fungicides is an effective strategy for controlling plant diseases. Among these agents, plant-derived antifungal metabolites are particularly promising due to their eco-friendly and sustainable nature. Plant secondary metabolites typically exhibit broad-spectrum antifungal activity without selective toxicity against pathogens. However, only a small fraction of antifungal metabolites have been identified from the tens of thousands of known plant secondary metabolites. In this study, we conducted a metabolomic analysis on both blast-resistant (Digu) and -susceptible (Lijiangxintuanheigu) rice varieties to uncover novel metabolites that enhance blast resistance. We found that 24 and 48 h post-inoculation with Magnaporthe oryzae were critical time points for metabolomic profiling, based on the infected status of M. oryzae in rice and the observed differences in shikimate accumulation between the two varieties. Following metabolomic analysis, we identified nine flavonoids that were differentially accumulated and are considered potential candidates for disease control. Among these, apigenin-7-glucoside, rhamnetin, and spireoside were found to be effective in controlling blast disease, with spireoside demonstrating the most pronounced efficacy. We discovered that spireoside controlled blast disease by inhibiting both spore germination and appressorium formation in M. oryzae, primarily through disrupting cell membrane integrity. However, spireoside did not induce rice immunity. Furthermore, spireoside was also effective in controlling sheath blight disease. Thus, spireoside shows considerable promise as a candidate for the development of a fungicide for controlling plant diseases.

Cite this article

Xu Liting, He Kaiwei, Guo Chunyu, Quan Cantao, Ma Yahuan, Zhang Wei, Ren Lifen, Wang Long, Song Li, Ouyang Qing, Yin Junjie, Zhu Xiaobo, Tang Yongyan, He Min, Chen Xuewei, Li Weitao . Spireoside Controls Blast Disease by Disrupting Membrane Integrity of Magnaporthe oryzae[J]. Rice Science, 2025 , 32(1) : 107 -117 . DOI: 10.1016/j.rsci.2024.10.005

References

[1] Akatsuka T, Kodama O, Sekido H, et al. 1985. Novel phytoalexins (oryzalexins A, B and C) isolated from rice blast leaves infected with Pyricularia oryzae: Part I. Isolation, characterization and biological activities of oryzalexins. Agric Biol Chem, 49(6): 1689-1694.
[2] An X Y, Zhang H, Li J L, et al. 2022. The level of endogenous JA is critical for activation of SA- and JA-defensive signaling pathway in japonica rice cultivar Ziyu44 upon Magnaporthe oryzae infection. J Plant Pathol, 104(2): 619-629.
[3] An Y L, Chen X H, Huang Y M, et al. 1999. A study on repression effects of some anthraquinoneson fungus phytop athogens. J Southwest For Coll, 19(2): 122-125. (in Chinese with English abstract)
[4] Bai J R, Wu Y P, Liu X Y, et al. 2015. Antibacterial activity of shikimic acid from pine needles of Cedrus deodara against Staphylococcus aureus through damage to cell membrane. Int J Mol Sci, 16(11): 27145-27155.
[5] Bao J D, Chen M L, Zhong Z H, et al. 2017. PacBio sequencing reveals transposable elements as a key contributor to genomic plasticity and virulence variation in Magnaporthe oryzae. Mol Plant, 10(11): 1465-1468.
[6] Carvalho M F N N. 2022. Synthesis and biological activity of antimicrobial agents. Antibiotics, 11(3): 337.
[7] Deleu M, Paquot M, Nylander T. 2005. Fengycin interaction with lipid monolayers at the air-aqueous interface: Implications for the effect of fengycin on biological membranes. J Colloid Interface Sci, 283(2): 358-365.
[8] Du Fall L A, Solomon P S. 2011. Role of cereal secondary metabolites involved in mediating the outcome of plant-pathogen interactions. Metabolites, 1(1): 64-78.
[9] Durmaz L, Kiziltas H, Karagecili H, et al. 2023. Potential antioxidant, anticholinergic, antidiabetic and antiglaucoma activities and molecular docking of spiraeoside as a secondary metabolite of onion (Allium cepa). Saudi Pharm J, 31(10): 101760.
[10] Fukuoka S, Saka N, Koga H, et al. 2009. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science, 325: 998-1001.
[11] Gao X W, Wang Y C, Sun J H, et al. 2020. Field efficacy trials of tea saponin & berberine 7.5% SL against rice blast. Pestic Sci Adm, 41(8): 39-45. (in Chinese with English abstract)
[12] González-Jaramillo L M, Aranda F J, Teruel J A, et al. 2017. Antimycotic activity of fengycin C biosurfactant and its interaction with phosphatidylcholine model membranes. Colloid Surf B: Biointerfaces, 156: 114-122.
[13] Guo Z Q, Liu X Y, Wang N, et al. 2023. Membrane component ergosterol builds a platform for promoting effector secretion and virulence in Magnaporthe oryzae. New Phytol, 237(3): 930-943.
[14] Hafeez R, Guo J N, Ahmed T, et al. 2024. Integrative transcriptomic and metabolomic analyses reveals the toxicity and mechanistic insights of bioformulated chitosan nanoparticles against Magnaporthe oryzae. Chemosphere, 356: 141904.
[15] Hasegawa M, Mitsuhara I, Seo S, et al. 2014. Analysis on blast fungus-responsive characters of a flavonoid phytoalexin sakuranetin; accumulation in infected rice leaves, antifungal activity and detoxification by fungus. Molecules, 19(8): 11404-11418.
[16] He M, Xu Y P, Chen J H, et al. 2018. MoSnt2-dependent deacetylation of histone H3 mediates MoTor-dependent autophagy and plant infection by the rice blast fungus Magnaporthe oryzae. Autophagy, 14(9): 1543-1561.
[17] Hiruma K, Onozawa-Komori M, Takahashi F, et al. 2010. Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell, 22(7): 2429-2443.
[18] Kai K, Wang R, Bi W L, et al. 2021. Chlorogenic acid induces ROS-dependent apoptosis in Fusarium fujikuroi and decreases the postharvest rot of cherry tomato. World J Microbiol Biotechnol, 37(6): 93.
[19] Katanić J, Boroja T, Stanković N, et al. 2015. Bioactivity, stability and phenolic characterization of Filipendula ulmaria (L.) Maxim. Food Funct, 6(4): 1164-1175.
[20] Kato H, Kodama O, Akatsuka T. 1993. Oryzalexin E, a diterpene phytoalexin from UV-irradiated rice leaves. Phytochemistry, 33(1): 79-81.
[21] Kato H, Kodama O, Akatsuka T. 1994. Oryzalexin F, a diterpene phytoalexin from UV-irradiated rice leaves. Phytochemistry, 36(2): 299-301.
[22] Kodama O, Li W X, Tamogami S, et al. 1992. Oryzalexin S, a novel stemarane-type diterpene rice phytoalexin. Biosci Biotechnol Biochem, 56(6): 1002-1003.
[23] Koga J, Ogawa N, Yamauchi T, et al. 1997. Functional moiety for the antifungal activity of phytocassane E, a diterpene phytoalexin from rice. Phytochemistry, 44(2): 249-253.
[24] Kühnau J. 1976. The flavonoids. A class of semi-essential food components: Their role in human nutrition. World Rev Nutr Diet, 24: 117-191.
[25] Lee J, Lee D G. 2015. Antimicrobial peptides (AMPs) with dual mechanisms: Membrane disruption and apoptosis. J Microbiol Biotechnol, 25(6): 759-764.
[26] Li A P, Zhao Z M, Zhang S Y, et al. 2021. Fungicidal activity and mechanism of action of glabridin from Glycyrrhiza glabra L. Int J Mol Sci, 22(20): 10966.
[27] Li W T, Zhu Z W, Chern M, et al. 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell, 170(1): 114-126.e15.
[28] Li W T, Chern M, Yin J J, et al. 2019. Recent advances in broad- spectrum resistance to the rice blast disease. Curr Opin Plant Biol, 50: 114-120.
[29] Mabrouk S B, Reis M, Sousa M L, et al. 2020. The marine seagrass Halophila stipulacea as a source of bioactive metabolites against obesity and biofouling. Mar Drugs, 18(2): 88.
[30] Maeda H, Dudareva N. 2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol, 63: 73-105.
[31] Murota K, Mitsukuni Y, Ichikawa M, et al. 2004. Quercetin-4?- glucoside is more potent than quercetin-3-glucoside in protection of rat intestinal mucosa homogenates against iron ion-induced lipid peroxidation. J Agric Food Chem, 52(7): 1907-1912.
[32] Ngo M T, Han J W, Yoon S, et al. 2019. Discovery of new triterpenoid saponins isolated from Maesa japonica with antifungal activity against rice blast fungus Magnaporthe oryzae. J Agric Food Chem, 67(27): 7706-7715.
[33] Nile A, Gansukh E, Park G S, et al. 2021. Novel insights on the multi-functional properties of flavonol glucosides from red onion (Allium cepa L) solid waste: In vitro and in silico approach. Food Chem, 335: 127650.
[34] Norvienyeku J, Lin L L, Waheed A, et al. 2021. Bayogenin 3-O- cellobioside confers non-cultivar-specific defence against the rice blast fungus Pyricularia oryzae. Plant Biotechnol J, 19(3): 589-601.
[35] Ogi K, Sumitani H. 2019. Elucidation of an α-glucosidase inhibitor from the peel of Allium cepa by principal component analysis. Biosci Biotechnol Biochem, 83(4): 751-754.
[36] Piyo A, Udomsilp J, Khang-Khun P, et al. 2009. Antifungal activity of essential oils from basil (Ocimum basilicum Linn.) and sweet fennel (Ocimum gratissimum Linn.): Alternative strategies to control pathogenic fungi in organic rice. Asian J Food Agro-Ind, 2: S2-S9.
[37] Qi Z Q, Xue Y F, Zhang M, et al. 2015. Effect of osthol on the invasion of Magnaporthe oryzae. Jiangsu J Agric Sci, 31(6): 1265-1269. (in Chinese with English abstract)
[38] Riedlmeier M, Ghirardo A, Wenig M, et al. 2017. Monoterpenes support systemic acquired resistance within and between plants. Plant Cell, 29(6): 1440-1459.
[39] Sato H, Feix J B. 2006. Peptide-membrane interactions and mechanisms of membrane destruction by amphipathic alpha-helical antimicrobial peptides. Biochim Biophys Acta, 1758(9): 1245-1256.
[40] Savina T, Lisun V, Feduraev P, et al. 2023. Variation in phenolic compounds, antioxidant and antibacterial activities of extracts from different plant organs of meadowsweet (Filipendula ulmaria (L.) Maxim.). Molecules, 28(8): 3512.
[41] Schlaeppi K, Abou-Mansour E, Buchala A, et al. 2010. Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant J, 62(5): 840-851.
[42] Sekido H, Endo T, Suga R, et al. 1986. Oryzalexin D (3,7-dihydroxy- (+)-sandaracopimaradiene), a new phytoalexin isolated from blast- infected rice leaves. J Pestic Sci, 11(3): 369-372.
[43] Sharma A, Kashyap D, Sak K, et al. 2018. Therapeutic charm of quercetin and its derivatives: A review of research and patents. Pharm Pat Anal, 7(1): 15-32.
[44] Sianglum W, Saeloh D, Tongtawe P, et al. 2018. Early effects of rhodomyrtone on membrane integrity in methicillin-resistant Staphylococcus aureus. Microb Drug Resist, 24(7): 882-889.
[45] Stotz H U, Sawada Y, Shimada Y, et al. 2011. Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate- derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant J, 67(1): 81-93.
[46] Vasconcelos-Cardoso M, Batista-Almeida D, Rios-Barros L V, et al. 2022. Cellular and molecular mechanisms underlying plasma membrane functionality and integrity. J Cell Sci, 135(13): jcs259806.
[47] Wang J H, Lou J F, Luo C, et al. 2012. Phenolic compounds from Halimodendron halodendron (Pall.) voss and their antimicrobial and antioxidant activities. Int J Mol Sci, 13(9): 11349-11364.
[48] Want E J, Masson P, Michopoulos F, et al. 2013. Global metabolic profiling of animal and human tissues via UPLC-MS. Nat Protoc, 8(1): 17-32.
[49] Wu S C, Yang Z Q, Liu F, et al. 2019. Antibacterial effect and mode of action of flavonoids from licorice against methicillin- resistant Staphylococcus aureus. Front Microbiol, 10: 2489.
[50] Zeng H L, He K W, He Q, et al. 2024. Exogenous indole-3-acetic acid suppresses rice infection of Magnaporthe oryzae by affecting plant resistance and fungal growth. Phytopathology, 114(5): 1050-1056.
[51] Zhang B, Dong C J, Shang Q M, et al. 2013. New insights into membrane-active action in plasma membrane of fungal hyphae by the lipopeptide antibiotic bacillomycin L. Biochim Biophys Acta, 1828(9): 2230-2237.
[52] Zhang M L. 2016. Effects of the extraction of Ginkgo biloba L. leaves and quercetin on control of postharvest blue mould in kiwifruit. Shaanxi, China: Northwest A & F University. (in Chinese with English abstract)
[53] Zhang Q, Liu F Y, Zeng M, et al. 2022. Antifungal activity of sodium new houttuyfonate against Aspergillus fumigatus in vitro and in vivo. Front Microbiol, 13: 856272.
[54] Zhao Y T, Wang X E, Zheng B L, et al. 2022. Current situation and prospects of screening research of plant-derived fungicides. Biol Disaster Sci, 45(4): 400-404. (in Chinese with English abstract)
[55] Zhong L Y, Lin Y J, Wang C, et al. 2022. Chemical profile, antimicrobial and antioxidant activity assessment of the crude extract and its main flavonoids from Tartary buckwheat sprouts. Molecules, 27(2): 374.
[56] Zhu Z W, Yin J J, Chern M, et al. 2020. New insights into bsr-d1- mediated broad-spectrum resistance to rice blast. Mol Plant Pathol, 21(7): 951-960.
[57] Zhu Z W, Xiong J, Shi H, et al. 2023. Magnaporthe oryzae effector MoSPAB1 directly activates rice Bsr-d1 expression to facilitate pathogenesis. Nat Commun, 14: 8399.
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