Stimulation of asymbiotic sporulation in arbuscular mycorrhizal fungi by fatty acids

Kameoka, Hiromu; Tsutsui, Ippo; Saito, Katsuichi; Kikuchi, Yuta; Handa, Yoshihiro; Ezawa, Tatsuhiro; Hayashi, Hideo; Kawaguchi, Masayoshi; Akiyama, Kazuo

doi:10.1038/s41564-019-0485-7

Cited by 69 publications

(64 citation statements)

References 40 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Although myristate initiates AM fungal growth and sporulation, the size of myristate-induced spores remains small compared with that of symbiotically generated spores. Similar results were obtained with palmitoleic acid-induced spores (7). As smaller spores show low germination rates and infectivity (38), spore maturation in the absence of the host represents an exciting future challenge for the pure culture of AM fungi.…”

Section: Discussionsupporting

confidence: 86%

“…1 F , M , and P ). In the presence of palmitoleic acid (C16:1 Δ9) in the medium, extensive hyphal branching and secondary spore formation was observed as reported by Kameoka et al (7), although this was not associated with an increase in biomass (Fig. 1A and SI Appendix , Fig.…”

Section: Resultssupporting

confidence: 72%

“…Based on lipid profile analyses of plant mutants defective in arbuscule formation, 16:0 β-MAG or its related chemicals are transferred to AM fungi from the host under symbiotic conditions (1–3, 14, 15). Recently, palmitoleic acid, a monounsaturated C16 fatty acid, has been shown to induce hyphal branching and fertile spores in the absence of a host (7). However, fatty acids and β-MAGs except for myristate were ineffective in biomass production in our culture conditions.…”

Section: Discussionmentioning

confidence: 99%

“…One report showed that the co-cultivation of the AM fungus Glomus intraradices with strains of Paenibacillus validus separated from each other with dialysis membranes induced secondary spore formation of the AM fungus (6). Another study reported that some fatty acids, including palmitoleic acid and ( S )-12-methyltetradecanoic acid, induced fertile secondary spores in asymbiotic cultures of AM fungi (7). These results suggest that AM fungi may be cultured independently from host plants under artificial conditions.…”

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi

Sugiura

Akiyama

Tanaka

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

19Arbuscular mycorrhiza (AM) is one of the most widespread mutualistic symbioses, which is 20 formed between the majority of land plants and soil-borne fungi belonging to Glomeromycotina. 21 AM fungi are obligate symbionts that cannot complete their natural life cycle without a host. 22 Recent evidence suggests that lipids synthesized by a host are transferred to AM fungi that 23 possess no fatty acid synthase genes in their genome and that mutations in lipid biosynthesis-24 related genes of the host lead the symbiotic interaction to fail (1-3). We hypothesized that lipids 25 derived from plants are crucial for AM fungal growth and reproduction. In this study, we 26 evaluated whether AM fungi can grow on medium supplied with fatty acids under asymbiotic 27 conditions without the host. Myristate led to an extensive hyphal growth of Rhizophagus 28 irregularis and an increase in biomass production. Other examined fatty acids showed no effect 29 on biomass production. Myristate also induced secondary spore formation. The myristate-30 induced spores can germinate, colonize carrot hairy roots, and form the next generation of 31 mature daughter spores. A fluorescently labeled fatty acid probe was taken up by branched 32 hyphae of AM fungi. Tracer experiments using 13 C-labeled myristic acid showed that myristate 33 and its metabolites were utilized for the synthesis of triacylglycerol and cell wall components 34 of AM fungi. Furthermore, myristate activated ATP generation in the fungal hyphae. Here we 35 demonstrate that myristate is utilized as a carbon and energy source for biomass production and 36 3 sporulation under asymbiotic conditions. 37 38 Introduction 39 Arbuscular mycorrhizal (AM) fungi belonging to the subphylum Glomeromycotina (4) form 40 symbiotic associations with over 70% of land plant species (5). AM fungi provide hosts with 41 minerals taken up via hyphal networks in soil and in return receive carbon sources, such as 42 sugars and lipids derived from plant photosynthates. This is regarded as an obligate symbiotic 43 relationship, where the life cycle of AM fungi is completed through colonization with their host. 44Only a few reports have been published on AM fungal culture without hosts. One report showed 45 that the co-cultivation of the AM fungus Glomus intraradices with strains of Paenibacillus 46 validus separated from each other with dialysis membranes induced secondary spore formation 47 of the AM fungus (6). Another study reported that some fatty acids, including palmitoleic acid 48 and (S)-12-methyltetradecanoic acid, induced fertile secondary spores in asymbiotic cultures of 49 AM fungi (7). These results suggest that AM fungi may be cultured independently from host 50 plants under artificial conditions. In nature, the life cycle of AM fungi proceeds as follows. 51Resting spores of AM fungi germinate, and then germ tubes emerge from the spores and 52 elongate into the soil. After colonization into plant roots, AM fungi form a highly branched 53 hyphal structure, called an arbuscule, in ...

show abstract

Section: Discussionsupporting

confidence: 86%

Section: Resultssupporting

confidence: 72%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi

Sugiura

Akiyama

Tanaka

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The RAM2 gene product produces sn2-acyl-glycerol form glycerol-3-phosphate and acyl-CoA, with preference for 16:0-CoA [3]. Recently, methyl-myristic acid (methyl-14:0) was shown to induce spore formation of R. irregularis [9]. Furthermore, myristic acid (14:0) supplementation to the medium was sufficient to support hyphal growth in axenic culture, 14:0 was taken up by the fungus and metabolized [10].…”

Section: Introductionmentioning

confidence: 99%

Palmitvaccenic acid (Δ11-cis-hexadecenoic acid) is synthesized by an OLE1-like desaturase in the arbuscular mycorrhiza fungusRhizophagus irregularis

Brands

Cahoon

Dörmann

2020

Preprint

View full text Add to dashboard Cite

Arbuscular mycorrhiza (AM) fungi deliver mineral nutrients to the plant host in exchange for reduced carbon in the form of sugars and lipids. Colonization with AM fungi upregulates a specific host lipid synthesis pathway resulting in the production of fatty acids. The fungus Rhizophagus irregularis accumulates predominantly palmitic acid (16:0) and the unusual palmitvaccenic acid (16:1 Δ 11cis). Here, we present the isolation and characterization of RiOLE1-LIKE, the desaturase involved in palmitvaccenic acid synthesis, by heterologous expression in yeast and plants. Results are in line with the scenario that RiOLE1-LIKE encodes an acyl-CoA desaturase with substrate specificity for C15-C18 acyl groups, in particular C16. Phylogenetic analysis of RiOLE1-LIKE related sequences revealed that this gene is conserved in AM fungi from the Glomales and Diversisporales, but is absent from non-symbiotic Mortierellaceae and Mucoromycotina fungi, suggesting that 16:1 Δ 11cis provides a specific function during AM colonization. Δ 11cis is absent from plants. It accounts for 46 -78 mol% of total fatty acids in spores of AMF of the Glomales including the families Acaulosporaceae, Glomaceae and Gigasporaceae, albeit some species of Glomaceae (Glomus leptotichum, Glomus occultum) and Gigasporacea (Gigaspora albida, Gigaspora gigantea, Gigaspora margarita, Gigaspora rosea) contain no or traces of 16:1 Δ 11cis . In addition to 16:1 Δ 11cis , Rhizophagus irregularis, Glomus claroideum and Gigaspora roseae spores and hyphae contain 0.2 -3.3 mol% of 16:1 Δ 9cis (palmitoleic acid; 16:1 ω 7cis ). Glomaceae species lacking 16:1 Δ 11cis (Glomus leptotichum, Glomus occultum) instead contain considerable amounts (11 -55 %) of 16:1 Δ 9cis . Spores of Gigaspora spp. with low amounts of 16:1 Δ 11cis contain high contents (38 -48 %) of 18:1 Δ 9cis (oleic acid) and 8 -15 % of 20:1 Δ 11cis (gondoic acid) [12]. Oleic acid and gondoic acid are present in low amounts in spores of R. irregualris and other Glomaceae [11,12]. Experimental Phylogenetic analysis For retrieving the desaturase sequences from R. irregularis, the four characterized Mortierella alpina desaturase sequences were retrieved from UniProtKB (uniprot.org) and used in BLASTp searches at the EnsemblFungi database (fungi.ensembl.org). For phylogenetic analysis of desaturases in symbiotic and non-symbiotic Mucoromycota, RiOLE1 and RiOLE1-LIKE sequences were used in BLASTn searches to identify orthologs in Gigasprora rosea, Rhizophagus cerebriforme and Rhizophagus diaphanus genomes available at MycoCosm [25]. Rhizophagus clarus, Mortierella circinelloides, Rhizophagus microsporus, Mortierella elongata and Lobosporangium transversale genomes at EnsemblFungi were surveyed for RiOLE1 and RiOLE1-LIKE orthologs using BLASTp. The sequences for phylogenetic analyses were aligned using MUSCLE implemented in MEGA 7, and the alignments used to create a maximum-likelihood tree with the WAG +F nucleotide substitution model. Gamma distributed rates with invariant sites (G+I) and 1000 bootstrap iterat...

show abstract

DES2 is a fatty acid Δ11 desaturase capable of synthesizing palmitvaccenic acid in the arbuscular mycorrhizal fungus Rhizophagus irregularis

et al. 2020

View full text Add to dashboard Cite

Edited by Ulf-Ingo Fl€ uggeArbuscular mycorrhizal (AM) fungi are oleaginous organisms, and the most abundant fatty acyl moiety usually found in their lipids is palmitvaccenic acid (16:1 D11cis ). However, it is not known how this uncommon fatty acid species is made. Here, we have cloned two homologues of lepidopteran fatty acylcoenzyme A D11 desaturases from the AM fungus Rhizophagus irregularis. Both enzymes, DES1 and DES2, are expressed in intraradical mycelium and can complement the unsaturated fatty acid-requiring auxotrophic growth phenotype of the Saccharomyces cerevisiae ole1D mutant. DES1 expression leads almost exclusively to oleic acid (18:1 D9cis ) production, whereas DES2 expression results in the production of 16:1 D11cis and vaccenic acid (18:1 D11cis ). DES2 therefore encodes a D11 desaturase that is likely to be responsible for the synthesis of 16:1 D11cis in R. irregularis.

show abstract

Stimulation of asymbiotic sporulation in arbuscular mycorrhizal fungi by fatty acids

Cited by 69 publications

References 40 publications

Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi

Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi

Palmitvaccenic acid (Δ11-cis-hexadecenoic acid) is synthesized by an OLE1-like desaturase in the arbuscular mycorrhiza fungusRhizophagus irregularis

DES2 is a fatty acid Δ11 desaturase capable of synthesizing palmitvaccenic acid in the arbuscular mycorrhizal fungus Rhizophagus irregularis

Contact Info

Product

Resources

About