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Fungal endophyte colonization patterns alter over time in the novel association between Lolium perenne and Epichloë Endophyte AR37

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posted on 2023-05-10, 07:44 authored by Flavia Forte, Jan Schmid, Paul Dijkwel, Istvan Nagy, David HumeDavid Hume, Richard JohnsonRichard Johnson, Wayne SimpsonWayne Simpson, Shaun Monk, Ningxin Zhang, Tina Sehrish, Torben Asp
Infection of the pasture grass Lolium perenne with the seed-transmitted fungal endophyte Epichloë festucae enhances its resilience to biotic and abiotic stress. Agricultural benefits of endophyte infection can be increased by generating novel symbiotic associations through inoculating L. perenne with selected Epichloë strains. Natural symbioses have coevolved over long periods. Thus, artificial symbioses will probably not have static properties, but symbionts will coadapt over time improving the fitness of the association. Here we report for the first time on temporal changes in a novel association of Epichloë strain AR37 and the L. perenne cultivar Grasslands Samson. Over nine generations, a seed maintenance program had increased the endophyte seed transmission rates to > 95% (from an initial 76%). We observed an approximately fivefold decline in endophyte biomass concentration in vegetative tissues over time (between generations 2 and 9). This indicates strong selection pressure toward reducing endophyte-related fitness costs by reducing endophyte biomass, without compromising the frequency of endophyte transmission to seed. We observed no obvious changes in tillering and only minor transcriptomic changes in infected plants over time. Functional analysis of 40 plant genes, showing continuously decreasing expression over time, suggests that adaptation of host metabolism and defense mechanisms are important for increasing the fitness of this association, and possibly fitness of such symbioses in general. Our results indicate that fitness of novel associations is likely to improve over time and that monitoring changes in novel associations can assist in identifying key features of endophyte-mediated enhancement of host fitness.

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© 2020 Forte, Schmid, Dijkwel, Nagy, Hume, Johnson, Simpson, Monk, Zhang, Sehrish and Asp. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Publication date

2020-10-29

Project number

  • Non revenue

Language

  • English

Does this contain Māori information or data?

  • No

Publisher

Frontiers Media

Journal title

Frontiers in Plant Science

ISSN

1664-462X

Citation

Forte, F. P., Schmid, J., Dijkwel, P. P., Nagy, I., Hume, D. E., Johnson, R. D., … Asp, T. (2020). Fungal endophyte colonization patterns alter over time in the novel association between Lolium perenne and Epichloë Endophyte AR37. Frontiers in Plant Science, 11, 570026. doi:10.3389/fpls.2020.570026

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