
Three Genes Related to Trehalose Metabolism Affect Sclerotial Development of Rhizoctonia solani AG-1 IA, Causal Agent of Rice Sheath Blight
Received date: 2021-07-12
Accepted date: 2021-09-17
Online published: 2022-03-10
Trehalose metabolism is related to the sclerotial development of Rhizoctonia solani AG-1 IA, the causal agent of rice sheath blight (RSB). Here, we further elucidated the functions of three genes Rstre, Rstps1 and Rstpp that encode three key enzymes trehalase (TRE), alpha, alpha-trehalose- phosphate synthase (TPS1) and trehalose 6-phosphate phosphatase (TPP) in the sclerotial development of R. solani AG-1 IA. Due to the lack of a stable genetic transformation system for R. solani, the heterologous expression of these three genes in Pichia pastoris GS115 was performed. The results showed that reactive oxygen species (ROS) contents and enzyme activities in R. solani decreased significantly in the treatments of the fermentation broths of Rstps1 and Rstpp transformants, and that in the treatment of the fermentation broth of Rstre transformant visibly increased. Furthermore, the fermentation broths of the transformants of all the three genes were added to potato dextrose agar (PDA) medium for the cultivation of R. solani, as a result, the dry weight of sclerotia in each PDA plate containing the fermentation broths of Rstps1 and Rstpp transformants significantly increased compared with the control, and that of Rstre transformant obviously decreased. Finally, 178 proteins were found to interact with RSTPS1, and 16 of them were associated with ROS. Taken together, the findings suggest that all these three genes related to trehalose metabolism play important roles in the sclerotial development of R. solani AG-1 IA, and can be used as new targets for the development of novel high-efficiency fungicides for the controlling of RSB.
Wang Chenjiaozi, Zhao Mei, Shu Canwei, Zhou Erxun . Three Genes Related to Trehalose Metabolism Affect Sclerotial Development of Rhizoctonia solani AG-1 IA, Causal Agent of Rice Sheath Blight[J]. Rice Science, 2022 , 29(3) : 268 -276 . DOI: 10.1016/j.rsci.2021.09.004
| [1] | Benaroudj N, Lee D H, Goldberg A L. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem, 276: 24261-24267. |
| [2] | Bookout A L, Cummins C L, Mangelsdorf D J, Pesola J M, Kramer M F. 2006. High-throughput real-time quantitative reverse transcription PCR. Curr Protoc Mol Biol, 15(8): 15.8. 1-15.8.21. |
| [3] | da Costa Morato Nery D, da Silva C G, Mariani D, Fernandes P N, Pereira M D, Panek A D, Eleutherio E C A. 2008. The role of trehalose and its transporter in protection against reactive oxygen species. Biochim Biophys Acta, 1780: 1408-1411. |
| [4] | Domingo D D, Bawingan P A, Bharathan S, Bharathan N. 2014. Molecular screening and characterization of dsRNA from wild- type and mutant strains of Rhizoctonia solani Kühn isolates. Philipp J Sci, 143: 61-72. |
| [5] | Fan K Q, Jin L Q, Zheng Y G. 2009. The enzymatic properties of trehalase and its exploitation as a target of new pesticides. Chem Bioeng, 26(4): 7-11. |
| [6] | Fang Y Z, Yang S, Wu G Y. 2002. Free radicals, antioxidants, and nutrition. Nutrition, 18: 872-879. |
| [7] | Feng S J, Shu C W, Wang C J Z, Jiang S F, Zhou E X. 2017. Survival of Rhizoctonia solani AG-1 IA, the causal agent of rice sheath blight, under different environmental conditions. J Phytopathol, 165(1): 44-52. |
| [8] | Georgiou C D, Tairis N, Sotiropoulou A. 2000. Hydroxyl radical scavengers inhibit sclerotial differentiation and growth in Sclerotinia sclerotiorum and Rhizoctonia solani. Mycol Res, 104: 1191-1196. |
| [9] | Georgiou C D, Patsoukis N, Papapostolou I, Zervoudakis G. 2006. Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr Comp Biol, 46: 691-712. |
| [10] | Harlow E, Lane D. 1988. Antibodies:A Laboratory Manual. New York, USA: Cold Spring Harbor Laboratory Publishing. |
| [11] | Hottiger T, Schmutz P, Wiemken A. 1987. Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol, 169: 5518-5522. |
| [12] | Jin K, Peng G X, Liu Y C, Xia Y X. 2015. The acid trehalase, ATM1, contributes to the in vivo growth and virulence of the entomopathogenic fungus, Metarhizium acridum. Fungal Genet Biol, 77: 61-67. |
| [13] | Lara-Ortíz T, Riveros-Rosas H, Aguirre J. 2003. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol, 50(4): 1241-1255. |
| [14] | Leite F C B, da Rocha Leite D V, Pereira L F, de Barros Pita W, de Morais Junior M A. 2016. High intracellular trehalase activity prevents the storage of trehalose in the yeast Dekkera bruxellensis. Lett Appl Microbiol, 63: 210-214. |
| [15] | Lu L, Shu C W, Liu C, Wang C J Z, Zhou E X. 2016. The impacts of natural antioxidants on sclerotial differentiation and development in Rhizoctonia solani AG-1 IA. Eur J Plant Pathol, 146(4): 729-740. |
| [16] | Luo Y, Li W M, Wang W. 2008. Trehalose: Protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot, 63: 378-384. |
| [17] | Pan L, Zhang X Q, Wang J P, Ma X, Zhou M L, Huang L K, Nie G, Wang P X, Yang Z F, Li J. 2016. Transcriptional profiles of drought- related genes in modulating metabolic processes and antioxidant defenses in Lolium multiflorum. Front Plant Sci, 7: 519. |
| [18] | Pedreño Y, González-Párraga P, Martínez-Esparza M, Sentandreu R, Valentín E, Argüelles J C. 2007. Disruption of the Candida albicans ATC1 gene encoding a cell-linked acid trehalase decreases hypha formation and infectivity without affecting resistance to oxidative stress. Microbiology, 153: 1372-1381. |
| [19] | Richards A B, Krakowka S, Dexter L B, Schmid H, Wolterbeek A P M, Waalkens-Berendsen D H, Shigoyuki A, Kurimoto M. 2002. Trehalose: A review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem Toxicol, 40: 871-898. |
| [20] | Shu C W, Sun S, Chen J L, Chen J Y, Zhou E X. 2014. Comparison of different methods for total RNA extraction from sclerotia of Rhizoctonia solani. Electron J Biotechnol, 17(1): 50-54. |
| [21] | Shu C W, Chen J L, Sun S, Zhang M L, Wang C J Z, Zhou E X. 2015. Two distinct classes of protein related to GTB and RRM are critical in the sclerotial metamorphosis process of Rhizoctonia solani AG-1 IA. Funct Integr Genomics, 15(4): 449-459. |
| [22] | Shu C W, Zhao M, Anderson J P, Garg G, Singh K B, Zheng W B, Wang C J Z, Yang M, Zhou E X. 2019. Transcriptome analysis reveals molecular mechanisms of sclerotial development in the rice sheath blight pathogen, Rhizoctonia solani AG1-IA. Funct Integr Genomics, 19: 743-758. |
| [23] | Suzuki S, Koga M, Niizeki N, Furuya A, Matsuo K, Tanahashi Y, Tsuchida E, Nohara F, Okamoto T, Nagaya K, Azuma H. 2013. Evaluation of glycated hemoglobin and fetal hemoglobin- adjusted HbA1c measurements in infants. Pediatr Diabetes, 14(4): 267-272. |
| [24] | Svanström A, Melin P. 2013. Intracellular trehalase activity is required for development, germination and heat-stress resistance of Aspergillus niger conidia. Res Microbiol, 164: 91-99. |
| [25] | Theerakulpisut P, Gunnula W. 2012. Exogenous sorbitol and trehalose mitigated salt stress damage in salt-sensitive but not salt-tolerant rice seedlings. Asian J Crop Sci, 4: 165-170. |
| [26] | Tournu H, Fiori A, van Dijck P. 2013. Relevance of trehalose in pathogenicity: Some general rules, yet many exceptions. PLoS Pathog, 9(8): e1003447. |
| [27] | Wang C J Z, Pi L, Jiang S F, Yang M, Shu C W, Zhou E X. 2018. ROS and trehalose regulate sclerotial development in Rhizoctonia solani AG-1 IA. Fungal Biol, 122(5): 322-332. |
| [28] | Wibberg D, Jelonek L, Rupp O, Kröber M, Goesmann A, Grosch R, Pühler A, Schlüter A. 2014. Transcriptome analysis of the phytopathogenic fungus Rhizoctonia solani AG1-IB 7/3/14 applying high-throughput sequencing of expressed sequence tags (ESTs). Fungal Biol, 118: 800-813. |
| [29] | Xu L J, Zhao W, Cao C, Wang J, Wang Q, Wang Q G. 2015. Research progress of Jinggangmycin. Chin Agric Sci Bull, 31: 191-198. (in Chinese with English abstract) |
| [30] | Zou Y P, Ma L J, Dong H T, Tao F, Feng X J, Yuan D Z, Fan D S, Hu X P. 2017. PstTPS1, the trehalose-6-phosphate synthase gene of Puccinia striiformis f. sp. tritici, involves in cold stress response and hyphae development. Physiol Mol Plant Pathol, 100: 201-208. |
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