Research Paper

In Vitro Antifungal Activity of Dihydrochelerythrine and Proteomic Analysis in Ustilaginoidea virens

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  • 1Northeast Forestry University, Harbin 150040, China
    2Institute of Plant Protection, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, China
First author contact:#These authors contributed equally to this work
Zhao Min (82191513@163.com);
Cui Daizong (siyu19831114@163.com);
Zheng Baojiang (zbjnefu@126.com)

Received date: 2022-07-01

  Accepted date: 2022-11-09

  Online published: 2022-11-09

Abstract

Dihydrochelerythrine (DHCHE) is an isoquinoline compound, which has distinct antifungal activity and can induce apoptosis. The antifungal activity of DHCHE against five rice pathogenic fungi was studied in vitro. At the concentration of 7.5 mg/L, DHCHE exhibited the highest efficacy among tested compounds in inhibiting mycelium growth, with an inhibition rate of 68.8% in Ustilaginoidea virens, which was approximately 2.4 times of that of validamycin (28.7%). After exposure to DHCHE, transmission electron micrographs revealed spores showed incomplete organelles, malformed cell walls and nuclear membranes, as well as irregular lipid spheres. Reactive oxygen species accumulation in treated spores was markedly higher than that in control spores. DHCHE induced cell damage increased in a dose-dependent manner, as indicated by the decrease in mitochondrial membrane potential and initiation of apoptosis. The differences of expression levels of Fip1, ACP1, PMS2 and COX13 that are important for oxidative phosphorylation and mismatch repair pathway were significant, which may be some of the reasons for the induction of apoptosis in DHCHE-treated U. virens. The protein levels of Fip1, ACP1, PMS2 and COX13 agreed with protein fold change ratio from parallel reaction monitoring Gene Ontology terms and Kyoto Encyclopedia of Genes and Genomes pathway of differentially expressed proteins were further analyzed. These findings will help to elucidate the mechanisms associated with antifungal and pro-apoptotic effects of DHCHE on U. virens, thereby aiding the potential development of novel pesticides.

Cite this article

Wei Qinghui, Cui Daizong, Zheng Baojiang, Zhao Min . In Vitro Antifungal Activity of Dihydrochelerythrine and Proteomic Analysis in Ustilaginoidea virens[J]. Rice Science, 2023 , 30(3) : 257 -266 . DOI: 10.1016/j.rsci.2023.03.009

References

[1] An P P, Yang X B, Yu J, Qi J R, Ren X Y, Kong Q J. 2019. α-terpineol and terpene-4-ol, the critical components of tea tree oil, exert antifungal activities in vitro and in vivo against Aspergillus niger in grapes by inducing morphous damage and metabolic changes of fungus. Food Control, 98: 42-53.
[2] Branen J K, Chiou T J, Engeseth N J. 2001. Overexpression of acyl carrier protein-1 alters fatty acid composition of leaf tissue in Arabidopsis. Plant Physiol, 127(1): 222-229.
[3] Cao F J, Yang R, Lv C, Ma Q, Lei M, Geng H L, Zhou L. 2015. Pseudocyanides of sanguinarine and chelerythrine and their series of structurally simple analogues as new anticancer lead compounds: Cytotoxic activity, structure-activity relationship and apoptosis induction. Eur J Pharm Sci, 67: 45-54.
[4] Chen Q L, Tang H L, Zha Z Q, Yin H P, Wang Y, Wang Y F, Li H T, Yue L. 2017. β-d-glucan from Antrodia camphorata ameliorates LPS-induced inflammation and ROS production in human hepatocytes. Int J Biol Macromol, 104: 768-777.
[5] Egan J M, Kaur A, Raja H A, Kellogg J J, Oberlies N H, Cech N B. 2016. Antimicrobial fungal endophytes from the botanical medicine goldenseal (Hydrastis canadensis). Phytochem Lett, 17: 219-225.
[6] Forbes K P, Addepalli B, Hunt A G. 2006. An Arabidopsis Fip1 homolog interacts with RNA and provides conceptual links with a number of other polyadenylation factor subunits. J Biol Chem, 281(1): 176-186.
[7] Ghorbanpour M, Omidvari M, Abbaszadeh-Dahaji P, Omidvar R, Kariman K. 2018. Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol Control, 117: 147-157.
[8] Guo W W, Gao Y X, Yu Z M, Xiao Y H, Zhang Z G, Zhang H F. 2019. The adenylate cyclase UvAc1 and phosphodiesterase UvPdeH control the intracellular cAMP level, development, and pathogenicity of the rice false smut fungus Ustilaginoidea virens. Fungal Genet Biol, 129: 65-73.
[9] Helmling S, Zhelkovsky A, Moore C L. 2001. Fip1 regulates the activity of poly(A) polymerase through multiple interactions. Mol Cell Biol, 21(6): 2026-2037.
[10] Hou F, Cui M H. 2014. Expression and clinical significance of hMLH1 and hPMS2 in colon cancer and concomitant polyps. Chin J Curr Adv Gen Surg, 17(7): 531-534. (in Chinese with English abstract)
[11] Jang B C, Park J G, Song D K, Baek W K, Yoo S K, Jung K H, Park G Y, Lee T Y, Suh S I. 2009. Sanguinarine induces apoptosis in A549 human lung cancer cells primarily via cellular glutathione depletion. Toxicol Vitro, 23(2): 281-287.
[12] Lauridsen P E, Rasmussen L J, Desler C. 2019. Mitochondrial oxidative phosphorylation capacity of cryopreserved cells. Mitochondrion, 47: 47-53.
[13] Liu G X. 2012. Effects on lipid synthesis of ACP1 and ACP2 genes on Chlamydomonas reinhardtii. Wuhan, China: Hubei University. (in Chinese with English abstract)
[14] Liu Y J, Li X J, Yuan H, Liu X, Gao Y X, Gong M, Zhou Z R. 2017. Fusing the acyl carrier protein enhances the solubility and thermostability of the recombinant proteins in Escherichia coli. China Biotechnol, 37(7): 115-123. (in Chinese with English abstract)
[15] Lu W. 2018. Mitochondrial oxidative phosphorylation deficiency inhibits the differentiation of brown adipocytes and related mechanism. Suzhou, China: Soochow University. (in Chinese with English abstract)
[16] Marampon F, Gravina G L, Ju X M, Vetuschi A, Sferra R, Casimiro M C, Pompili S, Festuccia C, Colapietro A, Gaudio E, di Cesare E, Tombolini V, Pestell R G. 2016. Cyclin D1 silencing suppresses tumorigenicity, impairs DNA double strand break repair and thus radiosensitizes androgen-independent prostate cancer cells to DNA damage. Oncotarget, 7: 64526.
[17] Navarro V, Delgado G. 1999. Two antimicrobial alkaloids from Bocconia arborea. J Ethnopharmacol, 66(2): 223-226.
[18] Norris A M, Woodruff R D, D’Agostino R B, Clodfelter J E, Scarpinato K D. 2007. Elevated levels of the mismatch repair protein PMS2 are associated with prostate cancer. Prostate, 67(2): 214-225.
[19] Perrone G G, Tan S X, Dawes I W. 2008. Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta, 1783(7): 1354-1368.
[20] Sun J, Zhou J, Wang Z H, He W N, Zhang D J, Tong Q Q, Su X R. 2015. Multi-omics based changes in response to cadmium toxicity in Bacillus licheniformis A. RSC Adv, 5(10): 7330-7339.
[21] Téllez-Robledo B, Manzano C, Saez A, Navarro-Neila S, Silva- Navas J, de Lorenzo L, González-García M P, Toribio R, Hunt A G, Baigorri R, Casimiro I, Brady S M, Castellano M M,Del Pozo J C. 2019. The polyadenylation factor FIP1 is important for plant development and root responses to abiotic stresses. Plant J, 99(6): 1203-1219.
[22] Thomas J. 2009. Characterization of the Escherichia coli acyl carrier protein phosphodiesterase. Illinois, USA: University of Illinois at Urbana-Champaign.
[23] Vrba J, Dolezel P, Vicar J, Modriansky M, Ulrichová J. 2008. Chelerythrine and dihydrochelerythrine induce G1 phase arrest and bimodal cell death in human leukemia HL-60 cells. Toxicol Vitro, 22(4): 1008-1017.
[24] Wei Q H, Zhao M, Li X Y. 2017. Extraction of chelerythrine and its effects on pathogenic fungus spore germination. Pharmacogn Mag, 13(52): 600-606.
[25] Wen S Q, Jeyakkumar P, Avula S R, Zhang L, Zhou C H. 2016. Discovery of novel berberine imidazoles as safe antimicrobial agents by down regulating ROS generation. Bioorg Med Chem Lett, 26(12): 2768-2773.
[26] Xin W J, Mao Y S, Lu F, Li T, Wang J X, Duan Y B, Zhou M G. 2020. In vitro fungicidal activity and in planta control efficacy of coumoxystrobin against Magnaporthe oryzae. Pestic Biochem Physiol, 162: 78-85.
[27] Yakovlev A Y, Borovskii G B, Voinikov V K, Grabelnych O I, Pobezhimova T P, Antipina A I. 2002. An effect of water-soluble proteins of fungi differed in frost-hardy on the energetic activity of isolated plant mitochondria. J Therm Biol, 27(3): 239-244.
[28] Yang R, Gao Z F, Zhao J Y, Li W B, Zhou L, Miao F. 2015. New class of 2-aryl-6-chloro-3,4-dihydroisoquinolinium salts as potential antifungal agents for plant protection: Synthesis, bioactivity and structure-activity relationships. J Agric Food Chem, 63(7): 1906-1914.
[29] Yuan J, Guan L J, Cong B, Zhang Z J, Wang L Z. 2005. Determination of antimicrobial activity of matrine alkaloids. J Pestic, 44(2): 4. (in Chinese with English abstract)
[30] Zhao Z M, Shang X F, Lawoe R K, Liu Y Q, Zhou R, Sun Y, Yan Y F, Li J C, Yang G Z, Yang C J. 2019. Anti-phytopathogenic activity and the possible mechanisms of action of isoquinoline alkaloid sanguinarine. Pestic Biochem Physiol, 159: 51-58.
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