A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants

Tyerman, Stephen D.; Whitehead, Lynne; Day, David A.

doi:10.1038/378629a0

Cited by 167 publications

(96 citation statements)

References 27 publications

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“…This, together with the elevated levels of cellular ammonia (owing to the repression of GS) and near-zero levels of ammonia outside the bacteroids, leads to a continuous diffusion of N # -derived ammonia out of the bacteroids (Quispel, 1992). The released ammonia is transported into the host cell via a channel-like NH % + transporter located on the host membrane at the interface between the symbionts (Tyreman et al, 1995). It is likely that the release of ammonia from cyanobiont to the host occurs in a manner analogous to that in legume root nodules.…”

Section: Nutrient Exchangementioning

confidence: 99%

Tansley Review No. 116

2000

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Summary 449 I. INTRODUCTION 450 II. THE PARTNERS 451 1. Cyanobionts and their role 451 2. Hosts and their role 453 3. Location of cyanobionts in their hosts 455 III. INITIATION AND DEVELOPMENT OF SYMBIOSES 458 1. Initiation of symbioses 458 2. Geosiphon pyriforme 458 3. Cyanolichens 459 4. Liverworts and hornworts 460 5. Azolla 460 6. Cycads 461 7. Gunnera 461 IV. THE SYMBIOSES 462 1. Geographical distribution and ecological significance 462 2. Benefits to the partners 462 (a) Benefits to the cyanobionts 462 (b) Benefits to the hosts 463 3. Duration and stability 463 4. Mode of transmission and perpetuation 463 5. Recognition between the partners 464 6. Specificity and diversity 464 7. Symbiosis‐related genes 465 8. Modifications of the cyanobiont 466 (a) Growth and morphology 466 (b) Photosynthesis and carbon metabolism 467 (c) Glutamine synthetase 467 (d) Heterocysts 469 (e) N2fixation 470 9. Nutrient exchange 471 (a) Carbon 471 (b) Nitrogen 472 V. EVOLUTIONARY ASPECTS 472 VI. ARTIFICIAL SYMBIOSES 474 VII. FUTURE OUTLOOK AND PERSPECTIVES 475 1. Cryptic symbioses 476 2. Developmental profile of symbiotic tissues 476 3. Sensing and signalling 476 4. Genetic aspects 476 5. Physiological and biochemical aspects of nutrient exchange 477 6. Microaerobiosis 477 7. Potential applications 477 Acknowledgements 477 References 477 Cyanobacteria are an ancient, morphologically diverse group of prokaryotes with an oxygenic photosynthesis. Many cyanobacteria also possess the ability to fix N2. Although well suited to an independent existence in nature, some cyanobacteria occur in symbiosis with a wide range of hosts (protists, animals and plants). Among plants, such symbioses have independently evolved in phylogenetically diverse genera belonging to the algae, fungi, bryophytes, pteridophytes, gymnosperms and angiosperms. These are N2‐fixing symbioses involving heterocystous cyanobacteria, particularly Nostoc, as cyanobionts (cyanobacterial partners). A given host species associates with only a particular cyanobiont genus but such specificity does not extend to the strain level. The cyanobiont is located under a microaerobic environment in a variety of host organs and tissues (bladder, thalli and cephalodia in fungi; cavities in gametophytes of hornworts and liverworts or fronds of the Azolla sporophyte; coralloid roots in cycads; stem glands in Gunnera). Except for fungi, the hosts form these structures ahead of the cyanobiont infection. The symbiosis lasts for one generation except in Azolla and diatoms, in which it is perpetuated from generation to generation. Within each generation, multiple fresh infections occur as new symbiotic tissues and organs develop. The symbioses are stable over a wide range of environmental conditions, and sensing–signalling between partners ensures their synchronized growth and development. The cyanobiont population is kept constant in relation to the host biomass through controlled initiation and infection, nutrient supply and cell division. In most cases, the partners have remaine...

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Section: Nutrient Exchangementioning

confidence: 99%

Tansley Review No. 116

2000

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“…Dicarboxylates are supplied from the plant to the bacteroids, and a specific transporter present in the PBM has been characterized (see Udvardi and Day, 1997). The transport of the ammonia is probably mediated by a channel (Tyerman et al, 1995), but amino acid transport may also play a role in the delivery of the fixed nitrogen to the plant (see Day et al, 2001). However, only a few genes/proteins have been characterized by molecular genetic studies.…”

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confidence: 99%

Proteome Analysis. Novel Proteins Identified at the Peribacteroid Membrane from Lotus japonicus Root Nodules

2003

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The peribacteroid membrane (PBM) forms the structural and functional interface between the legume plant and the rhizobia. The model legume Lotus japonicus was chosen to study the proteins present at the PBM by proteome analysis. PBM was purified from root nodules by an aqueous polymer two-phase system. Extracted proteins were subjected to a global trypsin digest. The peptides were separated by nanoscale liquid chromatography and analyzed by tandem mass spectrometry. Searching the nonredundant protein database and the green plant expressed sequence tag database using the tandem mass spectrometry data identified approximately 94 proteins, a number far exceeding the number of proteins reported for the PBM hitherto. In particular, a number of membrane proteins like transporters for sugars and sulfate; endomembraneassociated proteins such as GTP-binding proteins and vesicle receptors; and proteins involved in signaling, for example, receptor kinases, calmodulin, 14-3-3 proteins, and pathogen response-related proteins, including a so-called HIR protein, were detected. Several ATPases and aquaporins were present, indicating a more complex situation than previously thought. In addition, the unexpected presence of a number of proteins known to be located in other compartments was observed. Two characteristic protein complexes obtained from native gel electrophoresis of total PBM proteins were also analyzed. Together, the results identified specific proteins at the PBM involved in important physiological processes and localized proteins known from nodule-specific expressed sequence tag databases to the PBM.The model legume Lotus japonicus forms nitrogenfixing root nodules after infection by Mesorhizobium loti. The bacteria enter the plant cell by endocytosis, leading to the formation of a new compartment in the plant cell, the symbiosome. This compartment harbors the bacteroids and is surrounded by a peribacteroid membrane (PBM) formed from the plant plasma membrane (PM) during endocytosis of the bacteria (for review, see Verma and Hong, 1996;Whitehead and Day, 1997). The PBM develops further by receiving material from the endomembrane system (see Robertson et al., 1978;Verma and Hong, 1996) and finally forms the structural and functional interface between the symbionts (Robertson et al., 1978). The PBM plays a central role in the exchange of compounds between the organisms (see Udvardi and Day, 1997). To fulfill this role, the PBM is supplied with the specific components, like transporters and enzymes, necessary for the symbiotic exchange processes (see Verma and Hong, 1996;Whitehead and Day, 1997). Several of these activities have been characterized by biochemical and biophysical studies. For example, the activity of P-type H ϩ -ATPase (PATPase) pumping protons from the cytoplasm to the peribacteroid space has been characterized (see Blumwald et al., 1985, and refs. therein). Dicarboxylates are supplied from the plant to the bacteroids, and a specific transporter present in the PBM has been characterized (see Udvardi an...

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“…The relative contributions of these pathways depends upon the pH of the symbiosome space and cytosolic compartments, the concentration gradient of NH 4 + between the symbiosome and cytosolic compartments, and the resting potential of the SM, which is primarily controlled by an energizing H + -pumping ATPase (discussed in [11]). Under conditions of high H + -ATPase activity, the hyperpolarization of the SM and acidification of the symbiosome space would predominantly favor the efflux of fixed nitrogen in the form of NH 4 + through voltage-activated non-selective cation channels [24]. Movement of NH 3 across the SM to the cytosolic compartment would be favored under conditions of low H + -ATPase activity which would result in a less energized SM and less acidic conditions in the symbiosome space.…”

Section: Discussionmentioning

confidence: 99%

“…The efflux of fixed nitrogen from the symbiosome space to the infected cell cytosol is mediated by SM transport by one of the two potential mechanisms: 1. Directional transport of NH 4 + cations to the cytosol by an inwardly rectified, voltage-activated non-selective cation channel [24]; or 2. Efflux of uncharged NH 3 through the SM with nod26 providing a low energy pathway for this movement.…”

Section: Discussionmentioning

confidence: 99%

Ammonia permeability of the soybean nodulin 26 channel

2010

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a b s t r a c tSoybean nodulin 26 (nod26), a member of the aquaporin superfamily, is the major protein component of the symbiosome membrane that encloses nitrogen-fixing bacteroids in root nodules. Previous work has demonstrated that nod26 facilitates the transport of water and glycerol, although a potential additional role as a channel for fixed ammonia efflux has been hypothesized. In the present study it is shown that recombinant nod26 reconstituted into proteoliposomes facilitates NH 3 transport in an Hg 2+ -sensitive manner with a reduced activation energy, hallmarks of proteinfacilitated transport characteristic of aquaporins. Comparison of the predicted single-channel transport rates of nod26 suggests a 4.9-fold preference for ammonia compared to water.

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A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants

Cited by 167 publications

References 27 publications

Tansley Review No. 116

Tansley Review No. 116

Proteome Analysis. Novel Proteins Identified at the Peribacteroid Membrane from Lotus japonicus Root Nodules

Ammonia permeability of the soybean nodulin 26 channel

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