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1.
New Phytol ; 232(5): 2207-2219, 2021 12.
Article in English | MEDLINE | ID: mdl-34449891

ABSTRACT

Soil fungi establish mutualistic interactions with the roots of most vascular land plants. Arbuscular mycorrhizal (AM) fungi are among the most extensively characterised mycobionts to date. Current approaches to quantifying the extent of root colonisation and the abundance of hyphal structures in mutant roots rely on staining and human scoring involving simple yet repetitive tasks which are prone to variation between experimenters. We developed Automatic Mycorrhiza Finder (AMFinder) which allows for automatic computer vision-based identification and quantification of AM fungal colonisation and intraradical hyphal structures on ink-stained root images using convolutional neural networks. AMFinder delivered high-confidence predictions on image datasets of roots of multiple plant hosts (Nicotiana benthamiana, Medicago truncatula, Lotus japonicus, Oryza sativa) and captured the altered colonisation in ram1-1, str, and smax1 mutants. A streamlined protocol for sample preparation and imaging allowed us to quantify mycobionts from the genera Rhizophagus, Claroideoglomus, Rhizoglomus and Funneliformis via flatbed scanning or digital microscopy, including dynamic increases in colonisation in whole root systems over time. AMFinder adapts to a wide array of experimental conditions. It enables accurate, reproducible analyses of plant root systems and will support better documentation of AM fungal colonisation analyses. AMFinder can be accessed at https://github.com/SchornacklabSLCU/amfinder.


Subject(s)
Deep Learning , Glomeromycota , Lotus , Mycorrhizae , Fungi , Plant Roots , Symbiosis
2.
PLoS Biol ; 19(7): e3001326, 2021 07.
Article in English | MEDLINE | ID: mdl-34260583

ABSTRACT

Arbuscular mycorrhiza (AM) are mutualistic interactions formed between soil fungi and plant roots. AM symbiosis is a fundamental and widespread trait in plants with the potential to sustainably enhance future crop yields. However, improving AM fungal association in crop species requires a fundamental understanding of host colonisation dynamics across varying agronomic and ecological contexts. To this end, we demonstrate the use of betalain pigments as in vivo visual markers for the occurrence and distribution of AM fungal colonisation by Rhizophagus irregularis in Medicago truncatula and Nicotiana benthamiana roots. Using established and novel AM-responsive promoters, we assembled multigene reporter constructs that enable the AM-controlled expression of the core betalain synthesis genes. We show that betalain colouration is specifically induced in root tissues and cells where fungal colonisation has occurred. In a rhizotron setup, we also demonstrate that betalain staining allows for the noninvasive tracing of fungal colonisation along the root system over time. We present MycoRed, a useful innovative method that will expand and complement currently used fungal visualisation techniques to advance knowledge in the field of AM symbiosis.


Subject(s)
Betalains/metabolism , Mycorrhizae/growth & development , Genes, Fungal , Genetic Markers , Medicago truncatula/microbiology , Mycorrhizae/genetics , Mycorrhizae/metabolism , Plant Roots/microbiology , Promoter Regions, Genetic , Symbiosis/genetics , Nicotiana/genetics , Nicotiana/microbiology
3.
Plant Physiol ; 186(1): 581-598, 2021 05 27.
Article in English | MEDLINE | ID: mdl-33619553

ABSTRACT

Legumes form a symbiosis with rhizobia that convert atmospheric nitrogen (N2) to ammonia and provide it to the plant in return for a carbon and nutrient supply. Nodules, developed as part of the symbiosis, harbor rhizobia that are enclosed in a plant-derived symbiosome membrane (SM) to form an organelle-like structure called the symbiosome. In mature nodules exchanges between the symbionts occur across the SM. Here we characterize Yellow Stripe-like 7 (GmYSL7), a Yellow stripe-like family member localized on the SM in soybean (Glycine max) nodules. It is expressed specifically in infected cells with expression peaking soon after nitrogenase becomes active. Unlike most YSL family members, GmYSL7 does not transport metals complexed with phytosiderophores. Rather, it transports oligopeptides of between four and 12 amino acids. Silencing GmYSL7 reduces nitrogenase activity and blocks infected cell development so that symbiosomes contain only a single bacteroid. This indicates the substrate of YSL7 is required for proper nodule development, either by promoting symbiosome development directly or by preventing inhibition of development by the plant. RNAseq of nodules where GmYSL7 was silenced suggests that the plant initiates a defense response against rhizobia with genes encoding proteins involved in amino acid export downregulated and some transcripts associated with metal homeostasis altered. These changes may result from the decrease in nitrogen fixation upon GmYSL7 silencing and suggest that the peptide(s) transported by GmYSL7 monitor the functional state of the bacteroids and regulate nodule metabolism and transport processes accordingly. Further work to identify the physiological substrate for GmYSL7 will allow clarification of this role.


Subject(s)
Glycine max/genetics , Membrane Transport Proteins/genetics , Nitrogen Fixation , Plant Proteins/genetics , Rhizobium/physiology , Biological Transport , Membrane Transport Proteins/metabolism , Plant Proteins/metabolism , Glycine max/metabolism , Glycine max/microbiology , Symbiosis
4.
Curr Biol ; 30(21): 4165-4176.e5, 2020 11 02.
Article in English | MEDLINE | ID: mdl-32888486

ABSTRACT

The cell wall is the primary interface between plant cells and their immediate environment and must balance multiple functionalities, including the regulation of growth, the entry of beneficial microbes, and protection against pathogens. Here, we demonstrate how API, a SCAR2 protein component of the SCAR/WAVE complex, controls the root cell wall architecture important for pathogenic oomycete and symbiotic bacterial interactions in legumes. A mutation in API results in root resistance to the pathogen Phytophthora palmivora and colonization defects by symbiotic rhizobia. Although api mutant plants do not exhibit significant overall growth and development defects, their root cells display delayed actin and endomembrane trafficking dynamics and selectively secrete less of the cell wall polysaccharide xyloglucan. Changes associated with a loss of API establish a cell wall architecture with altered biochemical properties that hinder P. palmivora infection progress. Thus, developmental stage-dependent modifications of the cell wall, driven by SCAR/WAVE, are important in balancing cell wall developmental functions and microbial invasion.


Subject(s)
Cell Wall/metabolism , Disease Resistance/genetics , Phytophthora/pathogenicity , Plant Diseases/genetics , Plant Proteins/genetics , Actins/metabolism , Gene Expression Regulation, Plant , Host-Pathogen Interactions/genetics , Medicago truncatula , Mutation , Plant Diseases/microbiology , Plant Proteins/metabolism , Plant Roots/metabolism , Plant Roots/microbiology , Plants, Genetically Modified , Rhizobium/cytology , Rhizobium/metabolism , Symbiosis/genetics
5.
New Phytol ; 228(2): 667-681, 2020 10.
Article in English | MEDLINE | ID: mdl-32533710

ABSTRACT

Legumes establish symbiotic relationships with soil bacteria (rhizobia), housed in nodules on roots. The plant supplies carbon substrates and other nutrients to the bacteria in exchange for fixed nitrogen. The exchange occurs across a plant-derived symbiosome membrane (SM), which encloses rhizobia to form a symbiosome. Iron supplied by the plant is crucial for rhizobial enzyme nitrogenase that catalyses nitrogen fixation, but the SM iron transporter has not been identified. We use yeast complementation, real-time PCR and proteomics to study putative soybean (Glycine max) iron transporters GmVTL1a and GmVTL1b and have characterized the role of GmVTL1a using complementation in plant mutants, hairy root transformation and microscopy. GmVTL1a and GmVTL1b are members of the vacuolar iron transporter family and homologous to Lotus japonicus SEN1 (LjSEN1), which is essential for nitrogen fixation. GmVTL1a expression is enhanced in nodule infected cells and both proteins are localized to the SM. GmVTL1a transports iron in yeast and restores nitrogen fixation when expressed in the Ljsen1 mutant. Three GmVTL1a amino acid substitutions that block nitrogen fixation in Ljsen1 plants reduce iron transport in yeast. We conclude GmVTL1a is responsible for transport of iron across the SM to bacteroids and plays a crucial role in the nitrogen-fixing symbiosis.


Subject(s)
Glycine max , Nitrogen Fixation , Iron , Plant Proteins/genetics , Plant Proteins/metabolism , Root Nodules, Plant/metabolism , Glycine max/genetics , Glycine max/metabolism , Symbiosis
6.
Plant Physiol ; 180(3): 1598-1613, 2019 07.
Article in English | MEDLINE | ID: mdl-31015300

ABSTRACT

In nature, plants interact with numerous beneficial or pathogenic soil-borne microorganisms. Plants have developed various defense strategies to expel pathogenic microbes, some of which function soon after pathogen infection. We used Medicago truncatula and its oomycete pathogen Aphanomyces euteiches to elucidate early responses of the infected root. A. euteiches causes root rot disease in legumes and is a limiting factor in legume production. Transcript profiling of seedlings and adult plant roots inoculated with A. euteiches zoospores for 2 h revealed specific upregulation of a gene encoding a putative sesquiterpene synthase (M. truncatula TERPENE SYNTHASE 10 [MtTPS10]) in both developmental stages. MtTPS10 was specifically expressed in roots upon oomycete infection. Heterologous expression of MtTPS10 in yeast led to production of a blend of sesquiterpenes and sesquiterpene alcohols, with NMR identifying a major peak corresponding to himalachol. Moreover, plants carrying a tobacco (Nicotiana tabacum) retrotransposon Tnt1 insertion in MtTPS10 lacked the emission of sesquiterpenes upon A. euteiches infection, supporting the assumption that the identified gene encodes a multiproduct sesquiterpene synthase. Mttps10 plants and plants with reduced MtTPS10 transcript levels created by expression of an MtTPS10-artificial microRNA in roots were more susceptible to A. euteiches infection than were the corresponding wild-type plants and roots transformed with the empty vector, respectively. Sesquiterpenes produced by expression of MtTPS10 in yeast also inhibited mycelial growth and A. euteiches zoospore germination. These data suggest that sesquiterpene production in roots by MtTPS10 plays a previously unrecognized role in the defense response of M. truncatula against A. euteiches.


Subject(s)
Alkyl and Aryl Transferases/genetics , Disease Resistance/genetics , Medicago truncatula/genetics , Plant Diseases/genetics , Plant Proteins/genetics , Plant Roots/genetics , Alkyl and Aryl Transferases/metabolism , Aphanomyces/physiology , Gene Expression Profiling/methods , Gene Expression Regulation, Enzymologic , Gene Expression Regulation, Plant , Host-Pathogen Interactions , Medicago truncatula/enzymology , Medicago truncatula/microbiology , Plant Diseases/microbiology , Plant Proteins/metabolism , Plant Roots/enzymology , Plant Roots/microbiology , Sesquiterpenes/metabolism
7.
Plant J ; 93(2): 297-310, 2018 01.
Article in English | MEDLINE | ID: mdl-29171909

ABSTRACT

Phytophthora palmivora is a devastating oomycete plant pathogen. We found that P. palmivora induces disease in Lotus japonicus and used this interaction to identify cellular and molecular events in response to this oomycete, which has a broad host range. Transcript quantification revealed that Lys12 was highly and rapidly induced during P. palmivora infection. Mutants of Lys12 displayed accelerated disease progression, earlier plant death and a lower level of defence gene expression than the wild type, while the defence program after chitin, laminarin, oligogalacturonide or flg22 treatment and the root symbioses with nitrogen-fixing rhizobia and arbuscular mycorrhiza were similar to the wild type. On the microbial side, we found that P. palmivora encodes an active chitin synthase-like protein, and mycelial growth is impaired after treatment with a chitin-synthase inhibitor. However, wheat germ agglutinin-detectable N-acetyl-glucosamine (GlcNAc) epitopes were not identified when the oomycete was grown in vitro or while infecting the roots. This indicates that conventional GlcNAc-mers are unlikely to be produced and/or accumulate in P. palmivora cell walls and that LYS12 might perceive an unknown carbohydrate. The impact of Lys12 on progression of root rot disease, together with the finding that similar genes are present in other P. palmivora hosts, suggests that LYS12 might mediate a common early response to this pathogen.


Subject(s)
Host-Pathogen Interactions , Lotus/immunology , Phytophthora/physiology , Plant Diseases/immunology , Plant Proteins/metabolism , Signal Transduction , Chitin Synthase/genetics , Chitin Synthase/metabolism , Lotus/cytology , Lotus/microbiology , Lotus/parasitology , Mycorrhizae/physiology , Phytophthora/cytology , Plant Diseases/microbiology , Plant Diseases/parasitology , Plant Proteins/genetics , Plant Roots/immunology , Plant Roots/microbiology , Plant Roots/parasitology , Rhizobium/physiology , Symbiosis
8.
J Exp Bot ; 68(21-22): 5871-5881, 2017 12 16.
Article in English | MEDLINE | ID: mdl-29186498

ABSTRACT

The roots of most land plants are colonized by symbiotic arbuscular mycorrhiza (AM) fungi. To facilitate this symbiosis, plant genomes encode a set of genes required for microbial perception and accommodation. However, the extent to which infection by filamentous root pathogens also relies on some of these genes remains an open question. Here, we used genome-wide association mapping to identify genes contributing to colonization of Medicago truncatula roots by the pathogenic oomycete Phytophthora palmivora. Single-nucleotide polymorphism (SNP) markers most significantly associated with plant colonization response were identified upstream of RAD1, which encodes a GRAS transcription regulator first negatively implicated in root nodule symbiosis and recently identified as a positive regulator of AM symbiosis. RAD1 transcript levels are up-regulated both in response to AM fungus and, to a lower extent, in infected tissues by P. palmivora where its expression is restricted to root cortex cells proximal to pathogen hyphae. Reverse genetics showed that reduction of RAD1 transcript levels as well as a rad1 mutant are impaired in their full colonization by AM fungi as well as by P. palmivora. Thus, the importance of RAD1 extends beyond symbiotic interactions, suggesting a general involvement in M. truncatula microbe-induced root development and interactions with unrelated beneficial and detrimental filamentous microbes.


Subject(s)
Endodeoxyribonucleases/genetics , Gene Expression Regulation, Plant , Medicago truncatula/genetics , Medicago truncatula/microbiology , Mycorrhizae/physiology , Phytophthora/physiology , Plant Proteins/genetics , Disease Susceptibility , Endodeoxyribonucleases/metabolism , Genome-Wide Association Study , Host-Pathogen Interactions , Medicago truncatula/metabolism , Plant Diseases/microbiology , Plant Proteins/metabolism , Symbiosis
9.
Front Plant Sci ; 8: 201, 2017.
Article in English | MEDLINE | ID: mdl-28265280

ABSTRACT

Symbiotic bacteria (rhizobia) are maintained and conditioned to fix atmospheric nitrogen in infected cells of legume root nodules. Rhizobia are confined to the asymmetrical protrusions of plasma membrane (PM): infection threads (IT), cell wall-free unwalled droplets and symbiosomes. These compartments rapidly increase in surface and volume due to the microsymbiont expansion, and remarkably, the membrane resources of the host cells are targeted to interface membrane quite precisely. We hypothesized that the change in the membrane tension around the expanding microsymbionts creates a vector for membrane traffic toward the symbiotic interface. To test this hypothesis, we selected calcium sensors from the group of synaptotagmins: MtSyt1, Medicago truncatula homolog of AtSYT1 from Arabidopsis thaliana known to be involved in membrane repair, and two other homologs expressed in root nodules: MtSyt2 and MtSyt3. Here we show that MtSyt1, MtSyt2, and MtSyt3 are expressed in the expanding cells of the meristem, zone of infection and proximal cell layers of zone of nitrogen fixation (MtSyt1, MtSyt3). All three GFP-tagged proteins delineate the interface membrane of IT and unwalled droplets and create a subcompartments of PM surrounding these structures. The localization of MtSyt1 by EM immunogold labeling has shown the signal on symbiosome membrane and endoplasmic reticulum (ER). To specify the role of synaptotagmins in interface membrane formation, we compared the localization of MtSyt1, MtSyt3 and exocyst subunit EXO70i, involved in the tethering of post-Golgi secretory vesicles and operational in tip growth. The localization of EXO70i in root nodules and arbusculated roots was strictly associated with the tips of IT and the tips of arbuscular fine branches, but the distribution of synaptotagmins on membrane subcompartments was broader and includes lateral parts of IT, the membrane of unwalled droplets as well as the symbiosomes. The double silencing of synaptotagmins caused a delay in rhizobia release and blocks symbiosome maturation confirming the functional role of synaptotagmins. IN CONCLUSION: synaptotagmin-dependent membrane fusion along with tip-targeted exocytosis is operational in the formation of symbiotic interface.

10.
New Phytol ; 210(3): 1011-21, 2016 May.
Article in English | MEDLINE | ID: mdl-26790563

ABSTRACT

In root nodules rhizobia enter host cells via infection threads. The release of bacteria to a host cell is possible from cell wall-free regions of the infection thread. We hypothesized that the VAMP721d and VAMP721e exocytotic pathway, identified before in Medicago truncatula, has a role in the local modification of cell wall during the release of rhizobia. To clarify the role of VAMP721d and VAMP721e we used Glycine max, a plant with a determinate type of nodule. The localization of the main polysaccharide compounds of primary cell walls was analysed in control vs nodules with partially silenced GmVAMP721d. The silencing of GmVAMP721d blocked the release of rhizobia. Instead of rhizobia-containing membrane compartments - symbiosomes - the infected cells contained big clusters of bacteria embedded in a matrix of methyl-esterified and de-methyl-esterified pectin. These clusters were surrounded by a membrane. We found that GmVAMP721d-positive vesicles were not transporting methyl-esterified pectin. We hypothesized that they may deliver the enzymes involved in pectin turnover. Subsequently, we found that GmVAMP721d is partly co-localized with pectate lyase. Therefore, the biological role of VAMP721d may be explained by its action in delivering pectin-modifying enzymes to the site of release.


Subject(s)
Glycine max/metabolism , Glycine max/microbiology , Pectins/metabolism , Plant Proteins/metabolism , Rhizobium/physiology , Root Nodules, Plant/microbiology , Cellulose/metabolism , Esterification , Gene Silencing , Polysaccharide-Lyases/metabolism , Protein Transport , Root Nodules, Plant/metabolism , Root Nodules, Plant/ultrastructure , Symbiosis
11.
Mol Cell Proteomics ; 14(5): 1301-22, 2015 May.
Article in English | MEDLINE | ID: mdl-25724908

ABSTRACT

Legumes form a symbiosis with rhizobia in which the plant provides an energy source to the rhizobia bacteria that it uses to fix atmospheric nitrogen. This nitrogen is provided to the legume plant, allowing it to grow without the addition of nitrogen fertilizer. As part of the symbiosis, the bacteria in the infected cells of a new root organ, the nodule, are surrounded by a plant-derived membrane, the symbiosome membrane, which becomes the interface between the symbionts. Fractions containing the symbiosome membrane (SM) and material from the lumen of the symbiosome (peribacteroid space or PBS) were isolated from soybean root nodules and analyzed using nongel proteomic techniques. Bicarbonate stripping and chloroform-methanol extraction of isolated SM were used to reduce complexity of the samples and enrich for hydrophobic integral membrane proteins. One hundred and ninety-seven proteins were identified as components of the SM, with an additional fifteen proteins identified from peripheral membrane and PBS protein fractions. Proteins involved in a range of cellular processes such as metabolism, protein folding and degradation, membrane trafficking, and solute transport were identified. These included a number of proteins previously localized to the SM, such as aquaglyceroporin nodulin 26, sulfate transporters, remorin, and Rab7 homologs. Among the proteome were a number of putative transporters for compounds such as sulfate, calcium, hydrogen ions, peptide/dicarboxylate, and nitrate, as well as transporters for which the substrate is not easy to predict. Analysis of the promoter activity for six genes encoding putative SM proteins showed nodule specific expression, with five showing expression only in infected cells. Localization of two proteins was confirmed using GFP-fusion experiments. The data have been deposited to the ProteomeXchange with identifier PXD001132. This proteome will provide a rich resource for the study of the legume-rhizobium symbiosis.


Subject(s)
Glycine max/chemistry , Proteome/analysis , Rhizobium/chemistry , Root Nodules, Plant/chemistry , Amino Acid Sequence , Biological Transport , Carrier Proteins/genetics , Carrier Proteins/isolation & purification , Carrier Proteins/metabolism , Cell Membrane/chemistry , Cell Membrane/metabolism , Liquid-Liquid Extraction , Membrane Proteins/genetics , Membrane Proteins/isolation & purification , Membrane Proteins/metabolism , Membrane Transport Proteins/genetics , Membrane Transport Proteins/isolation & purification , Membrane Transport Proteins/metabolism , Metabolic Networks and Pathways/genetics , Molecular Sequence Annotation , Molecular Sequence Data , Phosphoproteins/genetics , Phosphoproteins/isolation & purification , Phosphoproteins/metabolism , Plant Cells/chemistry , Plant Cells/metabolism , Plant Proteins/genetics , Plant Proteins/isolation & purification , Plant Proteins/metabolism , Proteome/genetics , Proteome/metabolism , Rhizobium/genetics , Rhizobium/metabolism , Root Nodules, Plant/genetics , Root Nodules, Plant/metabolism , Glycine max/genetics , Glycine max/metabolism , Symbiosis/physiology , rab GTP-Binding Proteins/genetics , rab GTP-Binding Proteins/isolation & purification , rab GTP-Binding Proteins/metabolism , rab7 GTP-Binding Proteins
12.
Mol Plant Microbe Interact ; 28(5): 605-14, 2015 May.
Article in English | MEDLINE | ID: mdl-25608180

ABSTRACT

The nitrogen-fixing rhizobia in the symbiotic infected cells of root nodules are kept in membrane compartments derived from the host cell plasma membrane, forming what are known as symbiosomes. These are maintained as individual units, with mature symbiosomes having a specific radial position in the host cell cytoplasm. The mechanisms that adapt the host cell architecture to accommodate intracellular bacteria are not clear. The intracellular organization of any cell depends heavily on the actin cytoskeleton. Dynamic rearrangement of the actin cytoskeleton is crucial for cytoplasm organization and intracellular trafficking of vesicles and organelles. A key component of the actin cytoskeleton rearrangement is the ARP2/3 complex, which nucleates new actin filaments and forms branched actin networks. To clarify the role of the ARP2/3 complex in the development of infected cells and symbiosomes, we analyzed the pattern of actin microfilaments and the functional role of ARP3 in Medicago truncatula root nodules. In infected cells, ARP3 protein and actin were spatially associated with maturing symbiosomes. Partial ARP3 silencing causes defects in symbiosome development; in particular, ARP3 silencing disrupts the final differentiation steps in functional maturation into nitrogen-fixing units.


Subject(s)
Actin-Related Protein 2-3 Complex/ultrastructure , Actin-Related Protein 3/ultrastructure , Actins/ultrastructure , Medicago truncatula/ultrastructure , Sinorhizobium meliloti/physiology , Symbiosis , Actin-Related Protein 2-3 Complex/genetics , Actin-Related Protein 2-3 Complex/metabolism , Actin-Related Protein 3/genetics , Actin-Related Protein 3/metabolism , Actins/genetics , Actins/metabolism , Cytoplasm/metabolism , Gene Expression Regulation, Plant , Gene Silencing , Medicago truncatula/genetics , Medicago truncatula/microbiology , Nitrogen Fixation , Phenotype , Plant Proteins/genetics , Plant Proteins/metabolism , Plant Proteins/ultrastructure , Plant Roots/genetics , Plant Roots/microbiology , Plant Roots/ultrastructure , Protein Transport , Root Nodules, Plant/genetics , Root Nodules, Plant/microbiology , Root Nodules, Plant/ultrastructure
13.
Plant Cell ; 26(9): 3809-22, 2014 Sep.
Article in English | MEDLINE | ID: mdl-25217511

ABSTRACT

In legume-rhizobia symbioses, the bacteria in infected cells are enclosed in a plant membrane, forming organelle-like compartments called symbiosomes. Symbiosomes remain as individual units and avoid fusion with lytic vacuoles of host cells. We observed changes in the vacuole volume of infected cells and thus hypothesized that microsymbionts may cause modifications in vacuole formation or function. To examine this, we quantified the volumes and surface areas of plant cells, vacuoles, and symbiosomes in root nodules of Medicago truncatula and analyzed the expression and localization of VPS11 and VPS39, members of the HOPS vacuole-tethering complex. During the maturation of symbiosomes to become N2-fixing organelles, a developmental switch occurs and changes in vacuole features are induced. For example, we found that expression of VPS11 and VPS39 in infected cells is suppressed and host cell vacuoles contract, permitting the expansion of symbiosomes. Trafficking of tonoplast-targeted proteins in infected symbiotic cells is also altered, as shown by retargeting of the aquaporin TIP1g from the tonoplast membrane to the symbiosome membrane. This retargeting appears to be essential for the maturation of symbiosomes. We propose that these alterations in the function of the vacuole are key events in the adaptation of the plant cell to host intracellular symbiotic bacteria.


Subject(s)
Medicago truncatula/cytology , Medicago truncatula/microbiology , Multiprotein Complexes/metabolism , Plant Proteins/metabolism , Symbiosis , Vacuoles/metabolism , Acids/metabolism , Biomarkers/metabolism , Cell Membrane/metabolism , Gene Expression Regulation, Plant , Hydrogen-Ion Concentration , Medicago truncatula/genetics , Nitrogen Fixation , Plant Proteins/genetics , Plants, Genetically Modified , Protein Transport , RNA Interference , Root Nodules, Plant/genetics , Root Nodules, Plant/microbiology , Staining and Labeling
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