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Orchids and their mycorrhizal fungi: an insufficiently explored relationship

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Abstract

Orchids are associated with diverse fungal taxa, including nonmycorrhizal endophytic fungi as well as mycorrhizal fungi. The orchid mycorrhizal (OM) symbiosis is an excellent model for investigating the biological interactions between plants and fungi due to their high dependency on these symbionts for growth and survival. To capture the complexity of OM interactions, significant genomic, numerous transcriptomic, and proteomic studies have been performed, unraveling partly the role of each partner. On the other hand, several papers studied the bioactive metabolites from each partner but rarely interpreted their significance in this symbiotic relationship. In this review, we focus from a biochemical viewpoint on the OM dynamics and its molecular interactions. The ecological functions of OM in plant development and stress resistance are described first, summarizing recent literature. Secondly, because only few studies have specifically looked on OM molecular interactions, the signaling pathways and compounds allowing the establishment/maintenance of mycorrhizal association involved in arbuscular mycorrhiza (AM) are discussed in parallel with OM. Based on mechanistic similarities between OM and AM, and recent findings on orchids’ endophytes, a putative model representing the different molecular strategies that OM fungi might employ to establish this association is proposed. It is hypothesized here that (i) orchids would excrete plant molecule signals such as strigolactones and flavonoids but also other secondary metabolites; (ii) in response, OM fungi would secrete mycorrhizal factors (Myc factors) or similar compounds to activate the common symbiosis genes (CSGs); (iii) overcome the defense mechanism by evasion of the pathogen-associated molecular patterns (PAMPs)-triggered immunity and by secretion of effectors such as small inhibitor proteins; and (iv) finally, secrete phytohormones to help the colonization or disrupt the crosstalk of plant defense phytohormones. To challenge this putative model, targeted and untargeted metabolomics studies with special attention to each partner’s contribution are finally encouraged and some technical approaches are proposed.

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Abbreviations

ABA:

Abscisic acid

ABC:

Adenosine triphosphate-binding cassette

AM:

Arbuscular mycorrhizal

BLAST:

Basic local alignment search tool

C:

Carbon

COs:

Chitooligosaccharides

CSGs:

Common symbiosis genes

EM:

Ericoid mycorrhizal

ET:

Ethylene

ETI:

Effector-triggered immunity

GAs:

Gibberellins

IAA:

Indole-3-acetic acid

IMS:

Imaging mass spectrometry

ITS:

Internal transcribed spacer

JA:

Jasmonate

LCOs:

Lipo-chitooligosaccharides

MALDI:

Matrix-assisted laser desorption ionization

MiSSP:

Mycorrhizal-induced small-secreted protein

Myc factors:

Mycorrhizal factors

N:

Nitrogen

Nod factors:

Noduling factors

OM:

Orchid mycorrhizal

P:

Phosphorus

PAMPs:

Pathogen-associated molecular patterns

PCA:

Principal component analysis

PDRs:

Pleiotropic drug resistance

PRRs:

Pattern-recognition receptors

PTI:

PAMP-triggered immunity

QS:

Quorum sensing

ROS:

Reactive oxygen species

SA:

Salicylic acid

TCM:

Traditional Chinese medicine

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Acknowledgments

We thank Ludivine Riffault-Valois, Aurélie Urbain, Laurence Gondet (Faculty of Pharmacy, University of Strasbourg), and Megan Krumpoch for their critical reading and revision of the manuscript.

Funding

This research was financially supported by Guerlain to contribute in the understanding and preservation of orchids.

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Correspondence to Quentin Favre-Godal.

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Favre-Godal, Q., Gourguillon, L., Lordel-Madeleine, S. et al. Orchids and their mycorrhizal fungi: an insufficiently explored relationship. Mycorrhiza 30, 5–22 (2020). https://doi.org/10.1007/s00572-020-00934-2

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  • DOI: https://doi.org/10.1007/s00572-020-00934-2

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