The Mycoheterotrophic Symbiosis Between Orchids and Mycorrhizal Fungi Possesses Major Components Shared with Mutualistic Plant-Mycorrhizal Symbioses

Abstract

Achlorophylous and early developmental stages of chorolophylous orchids are highly dependent on carbon and other nutrients provided by mycorrhizal fungi, in a nutritional mode termed mycoheterotrophy. Previous findings have implied that some common properties at least partially underlie the mycorrhizal symbioses of mycoheterotrophic orchids and that of autotrophic arbuscular mycorrhizal (AM) plants; however, information about the molecular mechanisms of the relationship between orchids and their mycorrhizal fungi is limited. In this study, we characterized the molecular basis of an orchid-mycorrhizal (OM) symbiosis by analyzing the transcriptome of Bletilla striata at an early developmental stage associated with the mycorrhizal fungus Tulasnella sp. The essential components required for the establishment of mutual symbioses with AM fungi or rhizobia in most terrestrial plants were identified from the B. striata gene set. A cross-species gene complementation analysis showed one of the component genes, calcium and calmodulin-dependent protein kinase gene CCaMK in B. striata, retains functional characteristics of that in AM plants. The expression analysis revealed the activation of homologs of AM-related genes during the OM symbiosis. Our results suggest that orchids possess, at least partly, the molecular mechanisms common to AM plants.

Bletilla striata (Orchidaceae) Seed Coat Restricts the Invasion of Fungal Hyphae at the Initial Stage of Fungal Colonization

“…Symbiotic fungal hyphae penetrate orchid seeds either through the suspensor [10,11,12] or through epidermal hairs [13] and then form dense coils of mycelium called pelotons. The symbiotic protocorms limit the fungal growth to cortical cells at the suspensor side of the embryo, and the pelotons are not found in the apical meristem [14,15]. It is generally accepted that orchid cells obtain nutrients including carbon compounds thorough the symbiotic cells, predominantly during peloton degradation [16].…”

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

“…Transcriptomics is the most common approach to indirectly investigate metabolic changes in symbiotic organisms because it reveals the contributions of both partners through changes in their gene expression. This approach was successfully used to investigate orchid mycorrhizal (OM) protocorms, symbiotic structures that contain a mixture of plant and fungal molecules that cannot be separated before molecular or biochemical analyses (Zhao et al, 2013;Fochi et al, 2017a;Miura et al, 2018). However, although gene regulation is indicative of activation or repression of distinct biosynthetic pathways, transcriptional regulation of genes encoding enzymes does not necessarily reflect the final enzymatic activity, and there may be no direct association between metabolites and transcripts (Cavill et al, 2016).…”

Symbiotic and Asymbiotic Germination of Dendrobium officinale (Orchidaceae) Respond Differently to Exogenous Gibberellins

“…Orchid seeds are too tiny to perform genetic manipulations and this has inevitably limited the studies on their mechanisms of symbiotic germination, yet recent breakthroughs on arbuscular mycorrhiza have laid the foundation for investigating the SG of orchid seeds [ 16 ]. Recent studies show that the mycoheterotrophic symbiosis between orchids and mycorrhizal fungi possesses major components shared with mutualistic plant–mycorrhizal symbioses [ 17 ]. Many studies have revealed that plant hormones, especially gibberellins, are important factors affecting seed germination [ 10 ], and they are also critical for the establishment of mycorrhizal symbiosis [ 18 , 19 ].…”