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Ectomycorrhizal symbiosis prepares its host locally and systemically for abiotic cue signaling.

Authors :
de Freitas Pereira, Maíra
Cohen, David
Auer, Lucas
Aubry, Nathalie
Bogeat‐Triboulot, Marie‐Béatrice
Buré, Cyril
Engle, Nancy L.
Jolivet, Yves
Kohler, Annegret
Novák, Ondřej
Pavlović, Iva
Priault, Pierrick
Tschaplinski, Timothy J.
Hummel, Irène
Vaultier, Marie‐Noëlle
Veneault‐Fourrey, Claire
Source :
Plant Journal. Dec2023, Vol. 116 Issue 6, p1784-1803. 20p.
Publication Year :
2023

Abstract

SUMMARY: Tree growth and survival are dependent on their ability to perceive signals, integrate them, and trigger timely and fitted molecular and growth responses. While ectomycorrhizal symbiosis is a predominant tree‐microbe interaction in forest ecosystems, little is known about how and to what extent it helps trees cope with environmental changes. We hypothesized that the presence of Laccaria bicolor influences abiotic cue perception by Populus trichocarpa and the ensuing signaling cascade. We submitted ectomycorrhizal or non‐ectomycorrhizal P. trichocarpa cuttings to short‐term cessation of watering or ozone fumigation to focus on signaling networks before the onset of any physiological damage. Poplar gene expression, metabolite levels, and hormone levels were measured in several organs (roots, leaves, mycorrhizas) and integrated into networks. We discriminated the signal responses modified or maintained by ectomycorrhization. Ectomycorrhizas buffered hormonal changes in response to short‐term environmental variations systemically prepared the root system for further fungal colonization and alleviated part of the root abscisic acid (ABA) signaling. The presence of ectomycorrhizas in the roots also modified the leaf multi‐omics landscape and ozone responses, most likely through rewiring of the molecular drivers of photosynthesis and the calcium signaling pathway. In conclusion, P. trichocarpa‐L. bicolor symbiosis results in a systemic remodeling of the host's signaling networks in response to abiotic changes. In addition, ectomycorrhizal, hormonal, metabolic, and transcriptomic blueprints are maintained in response to abiotic cues, suggesting that ectomycorrhizas are less responsive than non‐mycorrhizal roots to abiotic challenges. Significance Statement: Current research on tree physiology primarily focuses on tree responses to abiotic stress, with little emphasis on root‐associated mutualistic fungi. Our results provide insights into how and to what extent the presence of ectomycorrhizas modifies host responses to abiotic changes: symbiosis has local and systemic impacts on host signaling pathways. A better understanding of the molecular mechanisms underpinning root‐microbe mutualistic interactions under abiotic stress will allow for robust modeling of tree adaptation to environmental challenges. [ABSTRACT FROM AUTHOR]

Details

Language :
English
ISSN :
09607412
Volume :
116
Issue :
6
Database :
Academic Search Index
Journal :
Plant Journal
Publication Type :
Academic Journal
Accession number :
174157735
Full Text :
https://doi.org/10.1111/tpj.16465