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The Endophytic Fungus Phomopsis liquidambari Increases Nodulation and N2 Fixation in Arachis hypogaea by Enhancing Hydrogen Peroxide and Nitric Oxide Signalling

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Abstract

The continuous cropping obstacles in monoculture fields are a major production constraint for peanuts. Application of the endophytic fungus Phomopsis liquidambari has increased peanut yields, and nodulation and N2 fixation increases have been considered as important factors for P. liquidambari infection-improved peanut yield. However, the mechanisms involved in this process remain unknown. This work showed that compared with only Bradyrhizobium inoculation, co-inoculation with P. liquidambari significantly elevated endogenous H2O2 and NO levels in peanut roots. Pre-treatment of seedlings with specific scavengers of H2O2 (CAT) and NO (cPTIO) blocked P. liquidambari-induced nodulation and N2 fixation. CAT not only suppressed the P. liquidambari-induced nodulation and N2 fixation, but also suppressed the enhanced H2O2 and NO generation. Nevertheless, the cPTIO did not significantly inhibit the induced H2O2 biosynthesis, implying that H2O2 acted upstream of NO production. These results were confirmed by observations that exogenous H2O2 and sodium nitroprusside (SNP) reversed the inhibition of P. liquidambari-increased nodulation and N2 fixation by the specific scavengers. The transcriptional activities of the symbiosis-related genes SymRK and CCaMK of peanut–Bradyrhizobium interactions also increased significantly in response to P. liquidambari, H2O2 and SNP treatments. The pot experiment further confirmed that the P. liquidambari infection-enhanced H2O2 and NO signalling pathways were significantly related to the increase in peanut nodulation and N2 fixation. This is the first report that endophytic fungus P. liquidambari can increase peanut–Bradyrhizobium interactions via enhanced H2O2/NO-dependent signalling crosstalk, which is conducive to the alleviation of continuous cropping obstacles via an increase in nodulation and N2 fixation.

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Acknowledgements

We would like to acknowledge the National Natural Science Foundation of China (NSFC No. 31370507), the Ph.D. Programs Foundation of Ministry of Education of China (No. 20133207110001), the Major Natural Science Research Programs of Jiangsu Higher Education Institutions (No. 13KJA180003), the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions of China, and the Graduate Education Innovation Project of Jiangsu Province (KYZZ15_0215). We also express our great thanks to the anonymous reviewers and editorial staff for their time and attention.

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Correspondence to Chuan-Chao Dai.

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Xie, XG., Fu, WQ., Zhang, FM. et al. The Endophytic Fungus Phomopsis liquidambari Increases Nodulation and N2 Fixation in Arachis hypogaea by Enhancing Hydrogen Peroxide and Nitric Oxide Signalling. Microb Ecol 74, 427–440 (2017). https://doi.org/10.1007/s00248-017-0944-8

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