UPLC-QTOF-MS metabolomics analysis revealed the contributions of metabolites to the pathogenesis of Rhizoctonia solani strain AG-1-IA

PLOS ONE, Nov 2019

To explore the pathogenesis of Rhizoctonia solani and its phytotoxin phenylacetic acid (PAA) on maize leaves and sheaths, treated leaf and sheath tissues were analyzed and interpreted by ultra-performance liquid chromatography-mass spectrometry combined with chemometrics. The PAA treatment had similar effects to those of R. solani on maize leaves regarding the metabolism of traumatin, phytosphingosine, vitexin 2'' O-beta-D-glucoside, rutin and DIBOA-glucoside, which were up-regulated, while the synthesis of OPC-8:0 and 12-OPDA, precursors for the synthesis of jasmonic acid, a plant defense signaling molecule, was down-regulated under both treatments. However, there were also discrepancies in the influences exhibited by R. solani and PAA as the metabolic concentration of zeaxanthin diglucoside in the R. solani infected leaf group decreased. Conversely, in the PAA-treated leaf group, the synthesis of zeaxanthin diglucoside was enhanced. Moreover, although the synthesis of 12 metabolites were suppressed in both the R. solani- and PAA-treated leaf tissues, the inhibitory effect of R. solani was stronger than that of PAA. An increased expression of quercitrin and quercetin 3-O-glucoside was observed in maize sheaths treated by R. solani, while their concentrations were not changed significantly in the PAA-treated sheaths. Furthermore, a significant decrease in the concentration of L-Glutamate, which plays important roles in plant resistance to necrotrophic pathogens, only occurred in the R. solani-treated sheath tissues. The differentiated metabolite levels may be the partial reason of why maize sheaths were more susceptible to R. solani than leaves and may explain the underlying mechanisms of R. solani pathogenesis.

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UPLC-QTOF-MS metabolomics analysis revealed the contributions of metabolites to the pathogenesis of Rhizoctonia solani strain AG-1-IA

February UPLC-QTOF-MS metabolomics analysis revealed the contributions of metabolites to the pathogenesis of Rhizoctonia solani strain AG-1-IA Wenjin Hu 0 1 Xinli Pan 1 Fengfeng Li 0 1 Wubei Dong 0 1 0 Department of Plant Pathology, College of Plant Science and Technology and the Key Lab of Crop Disease Monitoring & Safety Control in Hubei Province, Huazhong Agricultural University , Wuhan, Hubei Province , China , 2 Department of Biochemical and Chemical Engineering, Technische Universit aE?t Dortmund , Dortmund , Germany 1 Editor: Zonghua Wang, Fujian Agriculture and Forestry University , CHINA To explore the pathogenesis of Rhizoctonia solani and its phytotoxin phenylacetic acid (PAA) on maize leaves and sheaths, treated leaf and sheath tissues were analyzed and interpreted by ultra-performance liquid chromatography-mass spectrometry combined with chemometrics. The PAA treatment had similar effects to those of R. solani on maize leaves regarding the metabolism of traumatin, phytosphingosine, vitexin 2'' O-beta-D-glucoside, rutin and DIBOA-glucoside, which were up-regulated, while the synthesis of OPC-8:0 and 12-OPDA, precursors for the synthesis of jasmonic acid, a plant defense signaling molecule, was down-regulated under both treatments. However, there were also discrepancies in the influences exhibited by R. solani and PAA as the metabolic concentration of zeaxanthin diglucoside in the R. solani infected leaf group decreased. Conversely, in the PAA-treated leaf group, the synthesis of zeaxanthin diglucoside was enhanced. Moreover, although the synthesis of 12 metabolites were suppressed in both the R. solani- and PAA-treated leaf tissues, the inhibitory effect of R. solani was stronger than that of PAA. An increased expression of quercitrin and quercetin 3-O-glucoside was observed in maize sheaths treated by R. solani, while their concentrations were not changed significantly in the PAA-treated sheaths. Furthermore, a significant decrease in the concentration of L-Glutamate, which plays important roles in plant resistance to necrotrophic pathogens, only occurred in the R. solanitreated sheath tissues. The differentiated metabolite levels may be the partial reason of why maize sheaths were more susceptible to R. solani than leaves and may explain the underlying mechanisms of R. solani pathogenesis. - Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by the National Major Project for Transgenic Organism Breeding (2016ZX08003-001) and the Hubei Provincial Technology Innovation Program (2016ABA093). Competing interests: The authors have declared that no competing interests exist. Introduction As one of the most important crops, maize has been cultivated widely around the world. In addition to providing food for people, maize is also used to produce bioenergy [ 1 ]. Maize production is reduced by various factors [ 2, 3 ]. Plant pathogens may cause severe yield losses. Rhizoctonia solani, a plant pathogen, is a necrotrophic fungus that has a wide range of plant hosts [4]. R. solani infection on plants primarily occurs on roots and lower stems. During the infection of R. solani, enzymes and small molecular toxins are released to damage host plants [ 5 ]. The known toxins isolated from R. solani are phenylacetic acid (PAA) and its derivatives [ 6 ]. However, the roles of PAA and its derivatives in the pathogenesis of R. solani on maize are not yet understood. Another secreted toxin was found to be a polysaccharide with a currently unknown structure [ 7 ]. There are a few reports about the interactions between maize and R. solani. When maize was infected by R. solani, modulations of gene expression involved in transcription, regulation, signal transduction, cellular transport, protein processing, metabolism, and defense were discussed [ 8, 9 ]. A novel PCR removal approach developed by our group was applied to isolate regulated genes in the maize leaf after the R. solani infection [10]. No research has been reported investigating the metabolomics of maize infected by R. solani. Metabolomics is becoming a popular tool for studies in crops and pathogens. In maize, metabolic profiling-related studies have mostly been on environmental stresses and genetic modifications. Genetically modified and non-modified maize plants were compared and characterized by NMR metabolic profiles [ 11 ]. Metabolic variations related to osmolytes and branched amino acids were studied in the genetically modified maize [ 12 ]. Functional evaluation of the gene hda101 was conducted in mutant maize plants by metabolic profiling, which confirmed its role in cell cycle control [ 13 ]. Accumulations of phenylalanine and tyrosine were found in maize mutants that were deficient for two glutamine synthetase isoenzymes using an NMR-based profiling technique [ 14 ]. When maize was treated with salt and profiled with NMR, the impact (...truncated)


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Wenjin Hu, Xinli Pan, Fengfeng Li, Wubei Dong. UPLC-QTOF-MS metabolomics analysis revealed the contributions of metabolites to the pathogenesis of Rhizoctonia solani strain AG-1-IA, PLOS ONE, 2018, Volume 13, Issue 2, DOI: 10.1371/journal.pone.0192486