Plants are the foundation of terrestrial ecosystems and their colonization of land was likely facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following that founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Through analysis of 271 transcriptomes and 122 plant genomes, we demonstrate that the common symbiosis signalling pathway controlling the association with arbuscular mycorrhizal fungi and with nitrogen-fixing bacteria specifically co-evolved with intracellular endosymbioses, including ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. In contrast, species forming exclusively extracellular symbioses like ectomycorrhizae or associations with cyanobacteria have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million years of plant diversification.
Most plants entertain mutualistic interactions known as arbuscular mycorrhiza (AM) with soil fungi (Glomeromycota) which provide them with mineral nutrients in exchange for reduced carbon from the plant. Mycorrhizal roots represent strong carbon sinks in which hexoses are transferred from the plant host to the fungus. However, most of the carbon in AM fungi is stored in the form of lipids. The absence of the type I fatty acid synthase (FAS-I) complex from the AM fungal model species Rhizophagus irregularis suggests that lipids may also have a role in nutrition of the fungal partner. This hypothesis is supported by the concerted induction of host genes involved in lipid metabolism. We explore the possible roles of lipids in the light of recent literature on AM symbiosis. Carbohydrates in AM Fungal NutritionAM fungi are strictly biotrophic, in other words they depend on their host to complete their life cycle. Although the basis of biotrophy is poorly understood, it has been suggested that it is due to the dependency of AM fungi on some essential nutritional factor(s) from the host [1]. Direct uptake measurements revealed that intraradical mycelium (IRM) can take up carbohydrates, whereas extraradical mycelium (ERM) did not acquire significant amounts of carbohydrates [2,3]. Perhaps this is because AM fungal genes involved in nutrient uptake are expressed only in the host, which would explain their biotrophy. Tracer studies on mycorrhizal roots, and respirometric analysis on isolated intraradical hyphae have established glucose as a central substrate for AM fungi [3][4][5], and indeed a monosaccharide transporter has been identified in the fungal partner [6]. Mycorrhizal roots represent strong carbon sinks [2,4,7], suggesting that they attract sucrose from photosynthetic source tissues. Sucrose is thought to be cleaved in the vicinity of the fungus by invertases and sucrose synthase [8], resulting in monosaccharides (glucose and fructose) that are released to the fungus and taken up by its IRM [5,6]. However, in the fungal storage compartments -the spores and the vesicles -carbon is stored primarily in the form of lipids, with minor amounts of the glucose polymer glycogen. We discuss here salient issues relating to carbohydrate and lipid metabolism in AM fungi and their significance for fungal nutrition during symbiosis. Lipid Metabolism in AM Fungi -Open Questions and SurprisesAlthough the aforementioned carbon fluxes in AM fungi have been firmly established, several questions remain open. AM fungi store and transport most of their carbon in the form of lipids [9][10][11][12]. However, AM fungi cannot produce the basic fatty acid (FA) palmitate (C16) in the absence of their host (as shown in two distantly related species, Rhizophagus irregularis and Gigaspora rosea), while FA elongation and desaturation can occur independently of the plant [13]. This and similar results suggested that AM fungi can only synthesize C16 in the IRM [3,13]. Taken together, the available evidence suggests that AM fungi take up sugars (...
Symbiosis with arbuscular mycorrhizal fungi (AMF) improves plant nutrition in most land plants, and its contribution to the colonization of land by plants has been hypothesized. Here, we identify a conserved transcriptomic response to AMF among land plants, including the activation of lipid metabolism. Using gain of function, we show the transfer of lipids from the liverwort Marchantia paleacea to AMF and its direct regulation by the transcription factor WRINKLED (WRI). Arbuscules, the nutrient-exchange structures, were not formed in loss-of-function wri mutants in M. paleacea, leading to aborted mutualism. Our results show the orthology of the symbiotic transfer of lipids across land plants and demonstrate that mutualism with arbuscular mycorrhizal fungi was present in the most recent ancestor of land plants 450 million years ago.
Arbuscular mycorrhiza (AM) is a mutual symbiosis that involves a complex symbiotic interface over which nutrients are exchanged between the plant host and the AM fungus. Dozens of genes in the host are required for the establishment and functioning of the interaction, among them nutrient transporters that mediate the uptake of mineral nutrients delivered by the fungal arbuscules. We have isolated in a genetic mutant screen a petunia (Petunia hybrida) GIBBERELLIC ACID INSENSITIVE, REPRESSOR of GIBBERELLIC ACID INSENSITIVE, and SCARECROW (GRAS)-type transcription factor, ATYPICAL ARBUSCULE (ATA), that acts as the central regulator of AM-related genes and is required for the morphogenesis of arbuscules. Forced mycorrhizal inoculations from neighboring wild-type plants revealed an additional role of ATA in restricting mycorrhizal colonization of the root meristem. The lack of ATA, which represents the ortholog of REQUIRED FOR ARBUSCULAR MYCORRHIZA1 in Medicago truncatula, renders the interaction completely ineffective, hence demonstrating the central role of AM-related genes for arbuscule development and function.
BackgroundDevelopment of arbuscular mycorrhiza (AM) requires a fundamental reprogramming of root cells for symbiosis. This involves the induction of hundreds of genes in the host. A recently identified GRAS-type transcription factor in Petunia hybrida, ATA/RAM1, is required for the induction of host genes during AM, and for morphogenesis of the fungal endosymbiont. To better understand the role of RAM1 in symbiosis, we set out to identify all genes that depend on activation by RAM1 in mycorrhizal roots.ResultsWe have carried out a transcript profiling experiment by RNAseq of mycorrhizal plants vs. non-mycorrhizal controls in wild type and ram1 mutants. The results show that the expression of early genes required for AM, such as the strigolactone biosynthetic genes and the common symbiosis signalling genes, is independent of RAM1. In contrast, genes that are involved at later stages of symbiosis, for example for nutrient exchange in cortex cells, require RAM1 for induction. RAM1 itself is highly induced in mycorrhizal roots together with many other transcription factors, in particular GRAS proteins.ConclusionSince RAM1 has previously been shown to be directly activated by the common symbiosis signalling pathway through CYCLOPS, we conclude that it acts as an early transcriptional switch that induces many AM-related genes, among them genes that are essential for the development of arbuscules, such as STR, STR2, RAM2, and PT4, besides hundreds of additional RAM1-dependent genes the role of which in symbiosis remains to be explored. Taken together, these results indicate that the defect in the morphogenesis of the fungal arbuscules in ram1 mutants may be an indirect consequence of functional defects in the host, which interfere with nutrient exchange and possibly other functions on which the fungus depends.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3988-8) contains supplementary material, which is available to authorized users.
Plants engage in mutualistic interactions with microbes that improve their mineral nutrient supply. The most wide-spread symbiotic association is arbuscular mycorrhiza (AM), in which fungi of the order Glomeromycota invade roots and colonize the cellular lumen of cortical cells. The establishment of this interaction requires a dedicated molecular-genetic program and a cellular machinery of the plant host. This program is partially shared with the root nodule symbiosis (RNS), which involves prokaryotic partners collectively referred to as rhizobia. Both, AM and RNS are endosymbioses that involve intracellular accommodation of the microbial partner in the cells of the plant host. Since plant cells are surrounded by sturdy cell walls, root penetration and cell invasion requires mechanisms to overcome this barrier while maintaining the cytoplasm of the two partners separate during development of the symbiotic association. Here, we discuss the diverse functions of the cell wall compartment in establishment and functioning of plant symbioses with the emphasis on AM and RNS, and we describe the stages of the AM association between the model organisms Petunia hybrida and Rhizophagus irregularis.
In flowering plants, strigolactones (SLs) have dual functions as hormones that regulate growth and development, and as rhizosphere signaling molecules that induce symbiosis with arbuscular mycorrhizal (AM) fungi. Here, we report the identification of bryosymbiol (BSB), an SL from the bryophyte Marchantia paleacea. BSB is also found in vascular plants, indicating its origin in the common ancestor of land plants. BSB synthesis is enhanced at AM symbiosis permissive conditions and BSB deficient mutants are impaired in AM symbiosis. In contrast, the absence of BSB synthesis has little effect on the growth and gene expression. We show that the introduction of the SL receptor of Arabidopsis renders M. paleacea cells BSB-responsive. These results suggest that BSB is not perceived by M. paleacea cells due to the lack of cognate SL receptors. We propose that SLs originated as AM symbiosis-inducing rhizosphere signaling molecules and were later recruited as plant hormone.
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