Metabolomic adjustments in the orchid mycorrhizal fungus Tulasnella calospora during symbiosis with Serapias vomeracea

Abstract

 All orchids rely on mycorrhizal fungi for organic carbon, at least during early development. Orchid seed germination leads in fact to the formation of a protocorm, a heterotrophic postembryonic structure colonized by intracellular fungal coils, thought to be the site for nutrients transfer. The molecular mechanisms underlying mycorrhizal interactions and metabolic changes induced by this peculiar symbiosis in both partners remain mostly unknown.  We studied plant-fungus interactions in the mycorrhizal association between the Mediterranean orchid Serapias vomeracea and the basidiomycete Tulasnella calospora using non-targeted metabolomics. Plant and fungal metabolomes obtained from symbiotic structures were compared with those obtained under asymbiotic conditions.  Symbiosis induced profound metabolomic alterations in both partners. In particular, structural and signaling lipid compounds sharply increased in the external fungal mycelium growing near the symbiotic protocorms, whereas chito-oligosaccharides were identified uniquely in symbiotic protocorms.  This work represents the first description of metabolic changes occurring in orchid mycorrhiza. These results-supported by transcriptomic data-provide novel insights on the mechanisms underlying the orchid mycorrhizal association and open intriguing questions on the role of fungal lipids in this symbiosis.

Novel Microdialysis Technique Reveals a Dramatic Shift in Metabolite Secretion during the Early Stages of the Interaction between the Ectomycorrhizal Fungus Pisolithus microcarpus and Its Host Eucalyptus grandis

“…Interaction between the two organisms resulted in a dramatic alteration to the metabolites secreted by the fungus, with those metabolites having a high abundance in fungus-only conditions being almost completely replaced with a new set of metabolites. In a metabolomics study with orchid mycorrhizal fungi, Ghirardo et al [ 42 ] similarly found a substantial number of metabolites that were associated with symbiotic tissues but not found in free-living controls, and vice versa. Other studies considering the transcriptomic response of tree hosts to ECM fungi at an early pre-symbiotic time point found a significant enrichment in gene expression associated with alterations to metabolic compound processes in the plant or up-regulation of genes in secretion or general metabolism pathways [ 8 , 31 , 43 ].…”

A Transcriptomic Approach Provides Insights on the Mycorrhizal Symbiosis of the Mediterranean Orchid Limodorum abortivum in Nature

“…Although the last few years have seen an increase in the use of omics approaches to investigate the molecular basis of orchid mycorrhizal symbioses [23,45], information is still patchy mainly due to the complexity of this symbiosis, that involves different developmental stages as well as orchid and fungal symbionts with a range of lifestyles. The absence of Limodorum abortivum genome sequence did not make feasible the alignment of transcript short reads directly to a reference genome, thus putatively leading to an incomplete identification of genes.…”

“…Transcriptomic [15][16][17] and proteomic [18][19][20] approaches have revealed the upregulation of several plant membrane transporters in mycorrhizal protocorms, including amino acid transporters and bidirectional sugar transporters of the SWEET (Sugars Will Eventually be Exported Transporters) family [15,21,22]. Interestingly, a recent metabolomic study revealed that the external mycelium of the mycorrhizal fungus Tulasnella calospora growing near the host protocorms showed significant metabolic changes, mainly in lipid metabolism [23].…”

The Plant Growth-Promoting Fungus MF23 (Mycena sp.) Increases Production of Dendrobium officinale (Orchidaceae) by Affecting Nitrogen Uptake and NH4+ Assimilation

“…Plants mainly obtain N nutrition by absorbing and , but organic N is the major source transferred to orchid hosts from fungi ( Cameron et al, 2006 ; Kuga et al, 2014 ; Ghirardo et al, 2020 ). In addition, SvAAPs, SvLHT , and SvOPTs were more abundant in mycorrhizal protocorms ( Fochi et al, 2017b ).…”