Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis.
TL;DR: An overview of the molecular program for AM symbiosis is provided and an exciting coalescence of genome mining, lipid profiling, and tracer studies collectively has led to the conclusion that AM fungi are fatty acid auxotrophs and that plants provide their fungal endosymbionts with fatty acids.
Abstract: Plants have lived in close association with arbuscular mycorrhizal (AM) fungi for over 400 million years. Today, this endosymbiosis occurs broadly in the plant kingdom where it has a pronounced impact on plant mineral nutrition. The symbiosis develops deep within the root cortex with minimal alterations in the external appearance of the colonized root; however, the absence of macroscopic alterations belies the extensive signaling, cellular remodeling, and metabolic alterations that occur to enable accommodation of the fungal endosymbiont. Recent research has revealed the involvement of a novel N-acetyl glucosamine transporter and an alpha/beta-fold hydrolase receptor at the earliest stages of AM symbiosis. Calcium channels required for symbiosis signaling have been identified, and connections between the symbiosis signaling pathway and key transcriptional regulators that direct AM-specific gene expression have been established. Phylogenomics has revealed the existence of genes conserved for AM symbiosis, providing clues as to how plant cells fine-tune their biology to enable symbiosis, and an exciting coalescence of genome mining, lipid profiling, and tracer studies collectively has led to the conclusion that AM fungi are fatty acid auxotrophs and that plants provide their fungal endosymbionts with fatty acids. Here, we provide an overview of the molecular program for AM symbiosis and discuss these recent advances.
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01 Jan 2004
TL;DR: DMI3, a Medicago truncatula gene that acts immediately downstream of calcium spiking in this signaling pathway and is required for both nodulation and mycorrhizal infection, has high sequence similarity to genes encoding calcium and calmodulin-dependent protein kinases (CCaMKs).
Abstract: Legumes can enter into symbiotic relationships with both nitrogen-fixing bacteria (rhizobia) and mycorrhizal fungi. Nodulation by rhizobia results from a signal transduction pathway induced in legume roots by rhizobial Nod factors. DMI3 ,a Medicago truncatula gene that acts immediately downstream of calcium spiking in this signaling pathway and is required for both nodulation and mycorrhizal infection, has high sequence similarity to genes encoding calcium and calmodulin-dependent protein kinases (CCaMKs). This indicates that calcium spiking is likely an essential component of the signaling cascade leading to nodule development and mycorrhizal infection, and sheds light on the biological role of plant CCaMKs.
679 citations
TL;DR: New developments in the industry for AM-related products for agriculture, horticulture, and landscaping are discussed, and future potential and limits toward the use of AM fungi for plant production are highlighted.
Abstract: Arbuscular mycorrhiza (AM) is the most common symbiotic association of plants with microbes AM fungi occur in the majority of natural habitats and they provide a range of important ecological services, in particular by improving plant nutrition, stress resistance and tolerance, soil structure and fertility AM fungi also interact with most crop plants including cereals, vegetables, and fruit trees, therefore, they receive increasing attention for their potential use in sustainable agriculture Basic research of the past decade has revealed the existence of a dedicated recognition and signaling pathway that is required for AM Furthermore, recent evidence provided new insight into the exchange of nutritional benefits between the symbiotic partners The great potential for application of AM has given rise to a thriving industry for AM-related products for agriculture, horticulture, and landscaping Here, we discuss new developments in these fields, and we highlight future potential and limits toward the use of AM fungi for plant production
299 citations
Cites background from "Plant Signaling and Metabolic Pathw..."
...Phosphate delivery is among the most important benefits for the host in AM symbiosis (Karandashov and Bucher, 2005), and the collective information suggests that the arbuscules are the site of transfer of phosphate from the fungus to the plant (MacLean et al., 2017)....
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TL;DR: Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.
Abstract: Plants host a mesmerizing diversity of microbes inside and around their roots, known as the microbiome. The microbiome is composed mostly of fungi, bacteria, oomycetes, and archaea that can be either pathogenic or beneficial for plant health and fitness. To grow healthy, plants need to surveil soil niches around the roots for the detection of pathogenic microbes, and in parallel maximize the services of beneficial microbes in nutrients uptake and growth promotion. Plants employ a palette of mechanisms to modulate their microbiome including structural modifications, the exudation of secondary metabolites and the coordinated action of different defence responses. Here, we review the current understanding on the composition and activity of the root microbiome and how different plant molecules can shape the structure of the root-associated microbial communities. Examples are given on interactions that occur in the rhizosphere between plants and soilborne fungi. We also present some well-established examples of microbiome harnessing to highlight how plants can maximize their fitness by selecting their microbiome. Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.
293 citations
Cornell University1, Kanazawa University2, University of Zurich3, University of Cambridge4, University of Toulouse5, University of Arizona6, University of Marburg7, University of Leeds8, Polytechnic University of Valencia9, University of Göttingen10, University of Düsseldorf11, University of Bristol12, Boyce Thompson Institute for Plant Research13, University of California, Davis14, Wageningen University and Research Centre15, University of Bonn16, Hiroshima University17, University of Freiburg18, Laval University19, Smithsonian Institution20, University of Münster21, University of Alberta22, Rikkyo University23
TL;DR: High-quality genomes of Anthoceros hornworts are provided and candidate genes involved in cyanobacterial symbiosis are identified and found that LCIB, a Chlamydomonas CCM gene, is present in hornwort but absent in other plant lineages, implying a possible conserved role in CCM function.
Abstract: Hornworts comprise a bryophyte lineage that diverged from other extant land plants >400 million years ago and bears unique biological features, including a distinct sporophyte architecture, cyanobacterial symbiosis and a pyrenoid-based carbon-concentrating mechanism (CCM). Here, we provide three high-quality genomes of Anthoceros hornworts. Phylogenomic analyses place hornworts as a sister clade to liverworts plus mosses with high support. The Anthoceros genomes lack repeat-dense centromeres as well as whole-genome duplication, and contain a limited transcription factor repertoire. Several genes involved in angiosperm meristem and stomatal function are conserved in Anthoceros and upregulated during sporophyte development, suggesting possible homologies at the genetic level. We identified candidate genes involved in cyanobacterial symbiosis and found that LCIB, a Chlamydomonas CCM gene, is present in hornworts but absent in other plant lineages, implying a possible conserved role in CCM function. We anticipate that these hornwort genomes will serve as essential references for future hornwort research and comparative studies across land plants.
180 citations
TL;DR: Novel studies highlighted the importance of plant and fungal genotypes for the outcome of the symbiosis, and first insights into the regulatory mechanisms of root colonization in accordance with nutrient transfer and status were obtained.
Abstract: Contents Summary 1031 I. Introduction 1031 II. Interkingdom communication enabling symbiosis 1032 III. Nutritional and regulatory roles for key metabolites in the AM symbiosis 1035 IV. The plant-fungus genotype combination determines the outcome of the symbiosis 1039 V. Perspectives 1039 Acknowledgements 1041 References 1041 SUMMARY: The evolutionary and ecological success of the arbuscular mycorrhizal (AM) symbiosis relies on an efficient and multifactorial communication system for partner recognition, and on a fine-tuned and reciprocal metabolic regulation of each symbiont to reach an optimal functional integration. Besides strigolactones, N-acetylglucosamine-derivatives released by the plant were recently suggested to trigger fungal reprogramming at the pre-contact stage. Remarkably, N-acetylglucosamine-based diffusible molecules also are symbiotic signals produced by AM fungi (AMF) and clues on the mechanisms of their perception by the plant are emerging. AMF genomes and transcriptomes contain a battery of putative effector genes that may have conserved and AMF- or host plant-specific functions. Nutrient exchange is the key feature of AM symbiosis. A mechanism of phosphate transport inside fungal hyphae has been suggested, and first insights into the regulatory mechanisms of root colonization in accordance with nutrient transfer and status were obtained. The recent discovery of the dependency of AMF on fatty acid transfer from the host has offered a convincing explanation for their obligate biotrophism. Novel studies highlighted the importance of plant and fungal genotypes for the outcome of the symbiosis. These findings open new perspectives for fundamental research and application of AMF in agriculture.
131 citations
References
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TL;DR: Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
Abstract: Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
1,982 citations
"Plant Signaling and Metabolic Pathw..." refers background in this paper
...Current data suggest that the molecular dialogue is initiated by strigolactones, a group of carotenoid-based phytohormones produced by the plant, that also regulate many aspects of plant development (Akiyama et al., 2005; Gomez-Roldan et al., 2008; Lopez-Obando et al., 2015)....
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TL;DR: Evidence is presented that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigOLactone application restores the wild-type branching phenotype to ccd8 mutants, and that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack striglactone response.
Abstract: A carotenoid-derived hormonal signal that inhibits shoot branching in plants has long escaped identification. Strigolactones are compounds thought to be derived from carotenoids and are known to trigger the germination of parasitic plant seeds and stimulate symbiotic fungi. Here we present evidence that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigolactone application restores the wild-type branching phenotype to ccd8 mutants. Moreover, we show that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack strigolactone response, and are not deficient in strigolactones. These responses are conserved in Arabidopsis. In agreement with the expected properties of the hormonal signal, exogenous strigolactone can be transported in shoots and act at low concentrations. We suggest that endogenous strigolactones or related compounds inhibit shoot branching in plants. Furthermore, ccd8 mutants demonstrate the diverse effects of strigolactones in shoot branching, mycorrhizal symbiosis and parasitic weed interaction.
1,873 citations
TL;DR: A survey of 659 papers mostly published since 1987 was conducted to compile a checklist of mycorrhizal occurrence among 3,617 species (263 families) of land plants and a plant phylogeny was then used to map the mycor rhizal information to examine evolutionary patterns.
Abstract: A survey of 659 papers mostly published since 1987 was conducted to compile a checklist of mycorrhizal occurrence among 3,617 species (263 families) of land plants. A plant phylogeny was then used to map the mycorrhizal information to examine evolutionary patterns. Several findings from this survey enhance our understanding of the roles of mycorrhizas in the origin and subsequent diversification of land plants. First, 80 and 92% of surveyed land plant species and families are mycorrhizal. Second, arbuscular mycorrhiza (AM) is the predominant and ancestral type of mycorrhiza in land plants. Its occurrence in a vast majority of land plants and early-diverging lineages of liverworts suggests that the origin of AM probably coincided with the origin of land plants. Third, ectomycorrhiza (ECM) and its derived types independently evolved from AM many times through parallel evolution. Coevolution between plant and fungal partners in ECM and its derived types has probably contributed to diversification of both plant hosts and fungal symbionts. Fourth, mycoheterotrophy and loss of the mycorrhizal condition also evolved many times independently in land plants through parallel evolution.
1,653 citations
TL;DR: It is hypothesised that roots gradually evolved from rhizomes to provide more suitable habitats for mycorrhizal fungi and provide plants with complex branching and leaves with water and nutrients.
Abstract: Summary Here, the coevolution of mycorrhizal fungi and roots is assessed in the light of evidence now available, from palaeobotanical and morphological studies and the analysis of DNA-based phylogenies. The first bryophyte-like land plants, in the early Devonian (400 million years ago), had endophytic associations resembling vesicular‐ arbuscular mycorrhizas (VAM) even before roots evolved. Mycorrhizal evolution would have progressed from endophytic hyphae towards balanced associations where partners were interdependent due to the exchange of limiting energy and nutrient resources. Most mycorrhizas are mutualistic, but in some cases the trend for increasing plant control of fungi culminates in the exploitative mycorrhizas of achlorophyllous, mycoheterotrophic plants. Ectomycorrhizal, ericoid and orchid mycorrhizas, as well as nonmycorrhizal roots, evolved during the period of rapid angiosperm radiation in the Cretaceous. It is hypothesised that roots gradually evolved from rhizomes to provide more suitable habitats for mycorrhizal fungi and provide plants with complex branching and leaves with water and nutrients. Selection pressures have caused the morphological divergence of roots with different types of mycorrizas. Root cortex thickness and exodermis suberization are greatest in obligately mycorrhizal plants, while nonmycorrhizal plants tend to have fine roots, with more roots hairs and relatively advanced chemical defences. Major coevolutionary trends and the relative success of plants with different root types are discussed.
1,308 citations
"Plant Signaling and Metabolic Pathw..." refers background in this paper
...…land plants including liverworts, hornworts, lycophytes, and ferns reveals that AM symbiosis predates the development of true root systems (Brundrett, 2002; Field et al., 2012), while the broad occurrenceofAM inextantplant families isconsistentwithasingle early origin andwith retention of…...
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TL;DR: CERK1 is a plasma membrane protein containing three LysM motifs in the extracellular domain and an intracellular Ser/Thr kinase domain with autophosphorylation/myelin basic protein kinase activity, suggesting that CERK 1 plays a critical role in fungal MAMP perception in plants.
Abstract: Chitin is a major component of fungal cell walls and serves as a microbe-associated molecular pattern (MAMP) for the detection of various potential pathogens in innate immune systems of both plants and animals. We recently showed that chitin elicitor-binding protein (CEBiP), plasma membrane glycoprotein with LysM motifs, functions as a cell surface receptor for chitin elicitor in rice. The predicted structure of CEBiP does not contain any intracellular domains, suggesting that an additional component(s) is required for signaling through the plasma membrane into the cytoplasm. Here, we identified a receptor-like kinase, designated CERK1, which is essential for chitin elicitor signaling in Arabidopsis. The KO mutants for CERK1 completely lost the ability to respond to the chitin elicitor, including MAPK activation, reactive oxygen species generation, and gene expression. Disease resistance of the KO mutant against an incompatible fungus, Alternaria brassicicola, was partly impaired. Complementation with the WT CERK1 gene showed cerk1 mutations were responsible for the mutant phenotypes. CERK1 is a plasma membrane protein containing three LysM motifs in the extracellular domain and an intracellular Ser/Thr kinase domain with autophosphorylation/myelin basic protein kinase activity, suggesting that CERK1 plays a critical role in fungal MAMP perception in plants.
1,222 citations
"Plant Signaling and Metabolic Pathw..." refers background in this paper
...OsCERK1 and its homolog in ArabidopsisAtCERK1 were identified originally in the context of their roles in defenserelated chitin perception (Miya et al., 2007; Shimizu et al., 2010), revealingasurprisingdualityofOsCERK1 inmediatingbothchitintriggered immunity to restrict the growth of fungal…...
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...OsCERK1 and its homolog in ArabidopsisAtCERK1 were identified originally in the context of their roles in defenserelated chitin perception (Miya et al., 2007; Shimizu et al., 2010), revealingasurprisingdualityofOsCERK1 inmediatingbothchitintriggered immunity to restrict the growth of fungal pathogens yet also being necessary to promote the colonization of AM fungi during symbiosis....
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