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Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth

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Abstract

Arbuscular mycorrhizal (AM) fungi establish symbiotic associations with many plant species, transferring significant amounts of soil nutrients such as phosphorus to plants and receiving photosynthetically fixed carbon in return. Functioning of AM symbiosis is thus based on interaction between two living partners. The importance of dead AM fungal biomass (necromass) in ecosystem processes remains unclear. Here, we applied either living biomass or necromass (0.0004 potting substrate weight percent) of monoxenically produced AM fungus (Rhizophagus irregularis) into previously sterilized potting substrate planted with Andropogon gerardii. Plant biomass production significantly improved in both treatments as compared to non-amended controls. Living AM fungus, in contrast to the necromass, specifically improved plant acquisition of nutrients normally supplied to the plants by AM fungal networks, such as phosphorus and zinc. There was, however, no difference between the two amendment treatments with respect to plant uptake of other nutrients such as nitrogen and/or magnesium, indicating that the effect on plants of the AM fungal necromass was not primarily nutritional. Plant growth stimulation by the necromass could thus be either due to AM fungal metabolites directly affecting the plants, indirectly due to changes in soil/root microbiomes or due to physicochemical modifications of the potting substrate. In the necromass, we identified several potentially bioactive molecules. We also provide experimental evidence for significant differences in underground microbiomes depending on the amendment with living or dead AM fungal biomass. This research thus provides the first glimpse into possible mechanisms responsible for observed plant growth stimulation by the AM fungal necromass.

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Acknowledgments

The authors are thankful to M. Hujslová, O. Beskid, D. Püschel and other members of the Laboratory of Fungal Biology for their laboratory support and technical assistance. Czech Science Foundation (projects P504-12-1665 and 18-04892S) and the Czech Ministry of Education, Youth and Sports (project LK11224) funded the research. Further support was provided by the long-term development programs RVO 61388971 and RVO 67985831.

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MG and JJ designed and established the experiment. MR, HH and MG prepared the mycorrhizal inoculum (either living or dead). HH and PB helped with harvesting, sample processing and conducting the molecular analyses. JB analysed elemental composition of plant biomass. STF analysed the composition of fungal cell walls by infrared spectroscopy. MR contributed data on elemental composition of the AM fungal biomass. MG conducted the bioinformatics on the sequencing data. PŠ ran the multivariate statistics. JJ prepared samples of AM fungal biomass for biochemical analyses. TŘ performed the identification of fungal metabolites (PIMs) by mass spectrometry and contributed to writing. KS conducted the chitinases digestion assay including subsequent analyses of chitin oligomers and contributed to writing. JJ wrote the first draft of the manuscript. All authors approved the final version of the manuscript before submission.

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Correspondence to Jan Jansa.

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Jansa, J., Šmilauer, P., Borovička, J. et al. Dead Rhizophagus irregularis biomass mysteriously stimulates plant growth. Mycorrhiza 30, 63–77 (2020). https://doi.org/10.1007/s00572-020-00937-z

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  • DOI: https://doi.org/10.1007/s00572-020-00937-z

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