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Generalist endophyte Phomopsis liquidambaris colonization of Oryza sativa L. promotes plant growth under nitrogen starvation

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Rice- Phomopsis liquidambaris mutualistic interaction, under low nitrogen conditions, leads to increased plant growth and nitrogen uptake, as a consequence of host transcriptional reprogramming.

Abstract

Fungal endophytes establish symbiotic relationships with host plants, which results in a mutual growth benefit. However, little is known about the plant genetic response underpinning endophyte colonization. Phomopsis liquidambaris usually lives as an endophyte in a wide range of asymptomatic hosts and promotes biotic and abiotic stress resistance. In this study, we show that under low nitrogen conditions P. liquidambaris promotes rice growth in a hydroponic system, which is free of other microorganisms. In order to gain insights into the mechanisms of plant colonization by P. liquidambaris under low nitrogen conditions, we compared root and shoot transcriptome profiles of root-inoculated rice at different colonization stages. We determined that genes related to plant growth promotion, such as gibberellin and auxin related genes, were up-regulated at all developmental stages both locally and systemically. The largest group of up-regulated genes (in both roots and shoots) were related to flavonoid biosynthesis, which is involved in plant growth as well as antimicrobial compounds. Furthermore, genes encoding plant defense-related endopeptidase inhibitors were strongly up-regulated at the early stage of colonization. Together, these results provide new insights into the molecular mechanisms of plant-microbe mutualism and the promotion of plant growth by a fungal endophyte under nitrogen-deficient conditions.

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Availability of data and material

The RNA sequencing data generated in this work have been deposited to the NCBI’s Sequence Read Archive under BioProject PRJNA737734 (http://www.ncbi.nlm.nih.gov/bioproject/737734).

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Acknowledgements

We thank Dr. Theresa Catania and Dr. Madeleine Berger (University of York, UK) for proof reading the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (NSFC 32071638); Program for Jiangsu Excellent Scientific and Technological Innovation Team (17CXTD00014); and a project funded by the Priority Academic Program Development (PAPD) of the Jiangsu Higher Education Institutions of China.

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JZ designed experiments. JZ, PWH and XL performed experiments. JZ analyzed data. JZ and FEV wrote the manuscript. CCD supervised the work.

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Correspondence to Chuan-Chao Dai.

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Zhou, J., Huang, PW., Li, X. et al. Generalist endophyte Phomopsis liquidambaris colonization of Oryza sativa L. promotes plant growth under nitrogen starvation. Plant Mol Biol 109, 703–715 (2022). https://doi.org/10.1007/s11103-022-01268-7

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  • DOI: https://doi.org/10.1007/s11103-022-01268-7

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