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Journal ArticleDOI

A Versatile Monosaccharide Transporter That Operates in the Arbuscular Mycorrhizal Fungus Glomus sp Is Crucial for the Symbiotic Relationship with Plants

01 Oct 2011-The Plant Cell (American Society of Plant Biologists)-Vol. 23, Iss: 10, pp 3812-3823
TL;DR: It is found that the external mycelium of AM fungi is able to take up sugars in a proton-dependent manner, implying that the sugar uptake system operating in this symbiosis is more complex than previously anticipated.
Abstract: For more than 400 million years, plants have maintained a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi. This evolutionary success can be traced to the role of these fungi in providing plants with mineral nutrients, particularly phosphate. In return, photosynthates are given to the fungus, which support its obligate biotrophic lifestyle. Although the mechanisms involved in phosphate transfer have been extensively studied, less is known about the reciprocal transfer of carbon. Here, we present the high-affinity Monosaccharide Transporter2 (MST2) from Glomus sp with a broad substrate spectrum that functions at several symbiotic root locations. Plant cell wall sugars can efficiently outcompete the Glc uptake capacity of MST2, suggesting they can serve as alternative carbon sources. MST2 expression closely correlates with that of the mycorrhiza-specific Phosphate Transporter4 (PT4). Furthermore, reduction of MST2 expression using host-induced gene silencing resulted in impaired mycorrhiza formation, malformed arbuscules, and reduced PT4 expression. These findings highlight the symbiotic role of MST2 and support the hypothesis that the exchange of carbon for phosphate is tightly linked. Unexpectedly, we found that the external mycelium of AM fungi is able to take up sugars in a proton-dependent manner. These results imply that the sugar uptake system operating in this symbiosis is more complex than previously anticipated.

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Citations
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Journal ArticleDOI
TL;DR: This review aims to capture the most exciting developments in this area by evaluating the roles of key sucrose metabolic enzymes in development, abiotic stress responses, and plant-microbe interactions and the coupling between sucrose metabolism and sugar signaling from extra- to intracellular spaces.
Abstract: Sucrose metabolism plays pivotal roles in development, stress response, and yield formation, mainly by generating a range of sugars as metabolites to fuel growth and synthesize essential compounds (including protein, cellulose, and starch) and as signals to regulate expression of microRNAs, transcription factors, and other genes and for crosstalk with hormonal, oxidative, and defense signaling. This review aims to capture the most exciting developments in this area by evaluating (a) the roles of key sucrose metabolic enzymes in development, abiotic stress responses, and plant–microbe interactions; (b) the coupling between sucrose metabolism and sugar signaling from extra- to intracellular spaces; (c) the different mechanisms by which sucrose metabolic enzymes could perform their signaling roles; and (d ) progress on engineering sugar metabolism and transport for high yield and disease resistance. Finally, the review outlines future directions for research on sugar metabolism and signaling to better understand and improve plant performance.

878 citations

Journal ArticleDOI
TL;DR: Current knowledge about the phloem transport mechanisms is summarized and the effects of several abiotic (water and salt stress, mineral deficiency, CO2, light, temperature, air, and soil pollutants) and biotic andmutualistic and pathogenic microbes, viruses, aphids, and parasitic plants are reviewed.
Abstract: Source-to-sink transport of sugar is one of the major determinants of plant growth and relies on the efficient and controlled distribution of sucrose (and some other sugars such as raffinose and polyols) across plant organs through the phloem. However, sugar transport through the phloem can be affected by many environmental factors that alter source/sink relationships. In this paper, we summarize current knowledge about the phloem transport mechanisms and review the effects of several abiotic (water and salt stress, mineral deficiency, CO2, light, temperature, air, and soil pollutants) and biotic (mutualistic and pathogenic microbes, viruses, aphids, and parasitic plants) factors. Concerning abiotic constraints, alteration of the distribution of sugar among sinks is often reported, with some sinks as roots favored in case of mineral deficiency. Many of these constraints impair the transport function of the phloem but the exact mechanisms are far from being completely known. Phloem integrity can be disrupted (e.g., by callose deposition) and under certain conditions, phloem transport is affected, earlier than photosynthesis. Photosynthesis inhibition could result from the increase in sugar concentration due to phloem transport decrease. Biotic interactions (aphids, fungi, viruses…) also affect crop plant productivity. Recent breakthroughs have identified some of the sugar transporters involved in these interactions on the host and pathogen sides. The different data are discussed in relation to the phloem transport pathways. When possible, the link with current knowledge on the pathways at the molecular level will be highlighted.

852 citations


Cites background from "A Versatile Monosaccharide Transpor..."

  • ...Mycorrhizal fungus Glomus high-affinity MST2 has been identified as a major player in sugar uptake with a critical function in the establishment of symbiosis (Helber et al., 2011; Doidy et al., 2012)....

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Journal ArticleDOI
TL;DR: The genome of Rhizophagus irregularis provides insight into genes involved in obligate biotrophy and mycorrhizal symbioses and the evolution of an ancient asexual organism, and is of fundamental importance to the field of genome evolution.
Abstract: The mutualistic symbiosis involving Glomeromycota, a distinctive phylum of early diverging Fungi, is widely hypothesized to have promoted the evolution of land plants during the middle Paleozoic. These arbuscular mycorrhizal fungi (AMF) perform vital functions in the phosphorus cycle that are fundamental to sustainable crop plant productivity. The unusual biological features of AMF have long fascinated evolutionary biologists. The coenocytic hyphae host a community of hundreds of nuclei and reproduce clonally through large multinucleated spores. It has been suggested that the AMF maintain a stable assemblage of several different genomes during the life cycle, but this genomic organization has been questioned. Here we introduce the 153-Mb haploid genome of Rhizophagus irregularis and its repertoire of 28,232 genes. The observed low level of genome polymorphism (0.43 SNP per kb) is not consistent with the occurrence of multiple, highly diverged genomes. The expansion of mating-related genes suggests the existence of cryptic sex-related processes. A comparison of gene categories confirms that R. irregularis is close to the Mucoromycotina. The AMF obligate biotrophy is not explained by genome erosion or any related loss of metabolic complexity in central metabolism, but is marked by a lack of genes encoding plant cell wall-degrading enzymes and of genes involved in toxin and thiamine synthesis. A battery of mycorrhiza-induced secreted proteins is expressed in symbiotic tissues. The present comprehensive repertoire of R. irregularis genes provides a basis for future research on symbiosis-related mechanisms in Glomeromycota.

621 citations


Cites background from "A Versatile Monosaccharide Transpor..."

  • ...No secreted invertase or sucrose transporter was identified, implying that this fungus likely relies on the host plant to provide monosaccharides as a carbon source (27)....

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Journal ArticleDOI
TL;DR: An elegant study has unveiled a new and unexpected mechanism for specific protein localization to the periarbuscular membrane, which relies on the timing of gene expression to synchronize protein biosynthesis with a redirection of secretion.
Abstract: The default mineral nutrient acquisition strategy of land plants is the symbiosis with arbuscular mycorrhiza (AM) fungi. Research into the cell and developmental biology of AM revealed fascinating insights into the plasticity of plant cell development and of interorganismic communication. It is driven by the prospect of increased exploitation of AM benefits for sustainable agriculture. The plant cell developmental program for intracellular accommodation of AM fungi is activated by a genetically defined signaling pathway involving calcium spiking in the nucleus as second messenger. Calcium spiking is triggered by chitooligosaccharides released by AM fungi that are probably perceived via LysM domain receptor kinases. Fungal infection and calcium spiking are spatiotemporally coordinated, and only cells committed to accommodating the fungus undergo high-frequency spiking. Delivery of mineral nutrients by AM fungi occurs at tree-shaped hyphal structures, the arbuscules, in plant cortical cells. Nutrients are taken up at a plant-derived periarbuscular membrane, which surrounds fungal hyphae and carries a specific transporter composition that is of direct importance for symbiotic efficiency. An elegant study has unveiled a new and unexpected mechanism for specific protein localization to the periarbuscular membrane, which relies on the timing of gene expression to synchronize protein biosynthesis with a redirection of secretion. The control of AM development by phytohormones is currently subject to active investigation and has led to the rediscovery of strigolactones. Nearly all tested phytohormones regulate AM development, and major insights into the mechanisms of this regulation are expected in the near future.

427 citations


Cites background from "A Versatile Monosaccharide Transpor..."

  • ...…knockdown of a Medicago sucrose synthase gene expressed in arbusculated cells, as well as host-induced gene silencing of the fungal monosaccharide transporter MST2, caused the formation of stunted arbuscules reminiscent of those formed in the pt4 mutant (Baier et al. 2010, Helber et al. 2011)....

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Journal ArticleDOI
TL;DR: It is found that the C supply of the host plant triggers the uptake and transport of N in the symbiosis, and that the increase in N transport is orchestrated by changes in fungal gene expression.
Abstract: The arbuscular mycorrhizal (AM) symbiosis, formed between the majority of land plants and ubiquitous soil fungi of the phylum Glomeromycota, is responsible for massive nutrient transfer and global carbon sequestration. AM fungi take up nutrients from the soil and exchange them against photosynthetically fixed carbon (C) from the host. Recent studies have demonstrated that reciprocal reward strategies by plant and fungal partners guarantee a “fair trade” of phosphorus against C between partners [Kiers ET, et al. (2011) Science 333:880–882], but whether a similar reward mechanism also controls nitrogen (N) flux in the AM symbiosis is not known. Using mycorrhizal root organ cultures, we manipulated the C supply to the host and fungus and followed the uptake and transport of N sources in the AM symbiosis, the enzymatic activities of arginase and urease, and fungal gene expression in the extraradical and intraradical mycelium. We found that the C supply of the host plant triggers the uptake and transport of N in the symbiosis, and that the increase in N transport is orchestrated by changes in fungal gene expression. N transport in the symbiosis is stimulated only when the C is delivered by the host across the mycorrhizal interface, not when C is supplied directly to the fungal extraradical mycelium in the form of acetate. These findings support the importance of C flux from the root to the fungus as a key trigger for N uptake and transport and provide insight into the N transport regulation in the AM symbiosis.

350 citations


Cites background from "A Versatile Monosaccharide Transpor..."

  • ..., and of PT4, a mycorrhizaspecific plant P transporter, are correlated (23)....

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References
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Journal ArticleDOI
TL;DR: Version 4 of MEGA software expands on the existing facilities for editing DNA sequence data from autosequencers, mining Web-databases, performing automatic and manual sequence alignment, analyzing sequence alignments to estimate evolutionary distances, inferring phylogenetic trees, and testing evolutionary hypotheses.
Abstract: We announce the release of the fourth version of MEGA software, which expands on the existing facilities for editing DNA sequence data from autosequencers, mining Web-databases, performing automatic and manual sequence alignment, analyzing sequence alignments to estimate evolutionary distances, inferring phylogenetic trees, and testing evolutionary hypotheses. Version 4 includes a unique facility to generate captions, written in figure legend format, in order to provide natural language descriptions of the models and methods used in the analyses. This facility aims to promote a better understanding of the underlying assumptions used in analyses, and of the results generated. Another new feature is the Maximum Composite Likelihood (MCL) method for estimating evolutionary distances between all pairs of sequences simultaneously, with and without incorporating rate variation among sites and substitution pattern heterogeneities among lineages. This MCL method also can be used to estimate transition/transversion bias and nucleotide substitution pattern without knowledge of the phylogenetic tree. This new version is a native 32-bit Windows application with multi-threading and multi-user supports, and it is also available to run in a Linux desktop environment (via the Wine compatibility layer) and on Intel-based Macintosh computers under the Parallels program. The current version of MEGA is available free of charge at (http://www.megasoftware.net).

29,021 citations


"A Versatile Monosaccharide Transpor..." refers methods in this paper

  • ...Phylogenetic Analysis Phylogenetic analyses were conducted using Mega 4.0 software and ClustalW for the alignment and the neighbor-joining method for the construction of the phylogeny (Tamura et al., 2007)....

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Journal ArticleDOI
TL;DR: The GATEWAY conversion technology has provided a fast and reliable alternative to the cloning of sequences into large acceptor plasmids for transformation of a wide range of plant species.

3,473 citations


"A Versatile Monosaccharide Transpor..." refers methods in this paper

  • ...For MST2 silencing via the plant host, 300 bp of theMST2 cDNA, starting from the ATG, was amplified using the primers RNAiMST2-F1_and RNAiMST2_R1 and recombined in the Gateway binary RNAi vector pK7GWIWG2D(II) (Karimi et al., 2002)....

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  • ...Host-Induced Gene Silencing (HIGS) For MST2 silencing via the plant host, 300 bp of theMST2 cDNA, starting from the ATG, was amplified using the primers RNAiMST2-F1_and RNAiMST2_R1 and recombined in the Gateway binary RNAi vector pK7GWIWG2D(II) (Karimi et al., 2002)....

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Journal ArticleDOI
TL;DR: P is an important plant macronutrient, making up about 0.2% of a plant's dry weight, and is a component of key molecules such as nucleic acids, phospholipids, and ATP, and, consequently, plants cannot grow without a reliable supply of this nutrient.
Abstract: P is an important plant macronutrient, making up about 0.2% of a plant's dry weight. It is a component of key molecules such as nucleic acids, phospholipids, and ATP, and, consequently, plants cannot grow without a reliable supply of this nutrient. Pi is also involved in controlling key enzyme

1,860 citations


"A Versatile Monosaccharide Transpor..." refers background in this paper

  • ...Indications of the use of Xyl as a carbon source in the AM symbiosis are found in the work of Schliemann et al. (2008), who described an increased content of xylitol in M. truncatula mycorrhizal roots from 35 days after inoculation (DAI) onward, although at very low levels....

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Journal ArticleDOI
12 Aug 2011-Science
TL;DR: It is concluded that, unlike many other mutualisms, the symbiont cannot be “enslaved,” and the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.
Abstract: Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be "enslaved." Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.

1,346 citations

Journal ArticleDOI
TL;DR: The discovery of arbuscules in Aglaophyton major, an Early Devonian land plant, provides unequivocal evidence that mycorrhizae were established >400 million years ago and indicates that nutrient transfer mutualism may have been in existence when plants invaded the land.
Abstract: The discovery of arbuscules in Aglaophyton major, an Early Devonian land plant, provides unequivocal evidence that mycorrhizae were established >400 million years ago. Nonseptate hyphac and arbuscules occur in a specialized meristematic region of the cortex that continually provided new cells for fungal infection. Arbuscules are morphologically identical to those of living arbuscular mycorrhizae in consisting of a basal trunk and repeatedly branched bush-like tuft within the plant cell. Although interpretations of the evolution of mycorrhizal mutualisms continue to be speculative, the existence of arbuscules in the Early Devonian indicates that nutrient transfer mutualism may have been in existence when plants invaded the land.

1,078 citations


"A Versatile Monosaccharide Transpor..." refers background in this paper

  • ...Arbuscular mycorrhizal (AM) fungi are obligate biotrophs that form one of the most widespread and ancient mutualistic symbioses with plant roots (Remy et al., 1994)....

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