Biosynthesis and Secretion of Indole-3-Acetic Acid and Its Morphological Effects on Tricholoma vaccinum-Spruce Ectomycorrhiza

Abstract

bFungus-derived indole-3-acetic acid (IAA), which is involved in development of ectomycorrhiza, affects both partners, i.e., the tree and the fungus. The biosynthesis pathway, excretion from fungal hyphae, the induction of branching in fungal cultures, and enhanced Hartig net formation in mycorrhiza were shown. Gene expression studies, incorporation of labeled compounds into IAA, heterologous expression of a transporter, and bioinformatics were applied to study the effect of IAA on fungal morphogenesis and on ectomycorrhiza. Tricholoma vaccinum produces IAA from tryptophan via indole-3-pyruvate, with the last step of this biosynthetic pathway being catalyzed by an aldehyde dehydrogenase. The gene ald1 was found to be highly expressed in ectomycorrhiza and induced by indole-3-acetaldehyde. The export of IAA from fungal cells is supported by the multidrug and toxic extrusion (MATE) transporter Mte1 found in T. vaccinum. The addition of IAA and its precursors induced elongated cells and hyphal ramification of mycorrhizal fungi; in contrast, in saprobic fungi such as Schizophyllum commune, IAA did not induce morphogenetic changes. Mycorrhiza responded by increasing its Hartig net formation. The IAA of fungal origin acts as a diffusible signal, influencing root colonization and increasing Hartig net formation in ectomycorrhiza. F ungi, mainly basidiomycetes, form a mutually beneficial symbiotic association, commonly known as ectomycorrhiza, with the roots of woody plants (1). After establishing contact with the host, the fungus initially grows around the roots to form a mass of mycelium called the fungal mantle. From there, some hyphae penetrate the roots to grow between cortical cells to form the Hartig net, which acts as a surface for the exchange of nutrients and signals between the two symbiotic partners (1). Variation in host specificity occurs within ectomycorrhizal fungi: some have a broad host range, whereas others form host-specific ectomycorrhiza. In contrast to ectomycorrhizal fungi such as Pisolithus tinctorius and Paxillus involutus, Tricholoma species often show host specificity; their fruiting bodies are found only below compatible host trees. For example, Tricholoma vaccinum fruiting bodies occur only near spruce, which is the compatible host (2). Under laboratory conditions, Tricholoma species form ectomycorrhiza with nonhost trees, but the mycorrhization process in such lowcompatibility interactions requires more time and features spotty Hartig net formation (3). Thus, T. vaccinum, a slow-growing, latestage, and highly host-specific mycorrhizal fungus was chosen for the investigation of fungus-derived phytohormone effects on both partners. These interactions were expected to show the importance of indole-3-acetic acid (IAA) in the establishment and functioning of the symbiosis. We hypothesized that a long period of incubation might be necessary to observe changes in the morphogenetic responses that are not easily visualized with fast-growing, early-stage mycorrhiza. In order to generalize our findin...

Indole-3-acetic acid in plant–pathogen interactions: a key molecule for in planta bacterial virulence and fitness

“…The hypothetical MATE transporter is encoded to mediate IAA efflux. Very recently, the MATE transporter Mte1 of the ectomycorrhizal fungus Tricholoma vaccinum was shown to export IAA during its compatible interaction with the host, positively regulating ectomycorrhiza formation and morphology [52]. Interestingly, some multidrug resistance-like genes of Arabidopsis have also been shown to transport IAA [14].…”

“…Trp is mostly used as a precursor of IAA, essentially by the IAM or IPA pathway [50]. While the pivotal role of this phytohormone in development of hyperplastic symptoms caused by Ustilago maydis and P. savastanoi on their hosts [51], or for rhizobia and ectomycorrhizal fungi in supporting their beneficial interaction with plants is very clear [52], its physiological role in the presence of IAA produced by plant pathogenic necrotrophic fungi such as Colletotrichum and Fusarium spp. is less intuitive [53,54].…”

Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions

“…Uncultured bacteria are also quite common in hostassociated environments, and mixed cultures can offer a chance to study host−microbe interactions (Stewart 2012, Krause et al 2015. For example, cocultures of algae and bacteria revealed that 2 specific bacterial strains (originally identified as Roseobacter sp.…”

Hydrophobins in the Life Cycle of the Ectomycorrhizal Basidiomycete Tricholoma vaccinum

“…Plant-derived phytohormones were shown to increase growth and hyphal ramification in T . vaccinum , and the fungus is able to produce indole-3-acetic acid [8, 15]. …”