Physiology of Actinorhizal Nodules

Tjepkema, John D.; Schwintzer, Christa R.; Benson, David R.

doi:10.1146/annurev.pp.37.060186.001233

Cited by 106 publications

(45 citation statements)

References 53 publications

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“…If this is correct, one H^ would be transferred per malate to balance cbarge and pH. The same systems probably occur in the actinorhizal No-fixing symbiosis (Tjepkema, Schwintzer & Benson, 1986). This appears a relatively simple situation when compared with the possibilities discussed for mycorrhizas.…”

Section: Nitrogen-fixing Symbioses In Vascular Plantsmentioning

confidence: 95%

Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport

1990

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Summary In this review we compare the structure and function of the interfaces between symbionts in biotrophic associations. The emphasis is on biotrophic fungal parasites and on mycorrhizas, although necrotrophic parasitic associations and the Rhizobium/legume symbiosis are mentioned briefly. We take as a starting point the observations that in the parasitic associations nutrient transport is polarized towards the parasite, whereas in mutualistic associations it is bidirectional. The structure and function of the interfaces are then compared. An important common feature is that in nearly all cases the heterotrophic symbiont (whether mutualistic or parasitic) is located topologically outside the cytoplasm of the host cells, in an apoplastic compartment. This means that nutrient movements across the interface must involve transport into and out of this apoplastic region through membranes of both organisms. Basic principles of membrane transport in uninfected cells are briefly reviewed to set the scene for a discussion of transport mechanisms which may operate in parasitic and mycorrhizal symbioses. The presence and possible roles of ATPases associated with membranes at the interfaces are discussed. We conclude that cytochemical techniques (used to demonstrate the activity of these enzymes) need to he extended and complemented by biochemical and biophysical studies in order to confirm that the activity is due to transport ATPases. Nevertheless, the distribution of activity appears to he in accord with polarized transport mechanisms in some pathogens and with bidirectional transport in mycorrhizas. The absence of ATPases on many fungal membranes needs re‐examination. We emphasize that transport mechanisms between mycorrhizal symbionts cannot be viewed simply as the exchange of carbon for phosphate. Additional features include provision for transport of carbon and nitrogen as amino acids or amides and for ions such as K+ and H+ involved in the maintenance of charge balance and pH regulation, processes which also occur in parasitic associations. Interplant transport of nutrients via mycorrhizal hyphae is discussed in the context of these complexities. Some suggestions for the directions of future work are made.

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Section: Nitrogen-fixing Symbioses In Vascular Plantsmentioning

confidence: 95%

Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport

1990

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“…However, the anatomy of the nodules formed in these symbioses differs considerably from that of legume nodules, and the main barrier to gas diffusion is thought to be associated with the Frankia endosymbiont itself (18) rather than with the uninfected nodule cortex, as appears to be the case in legumes (20,24). Silvester and Winship (16) have provided evidence that the acetylene-and 02-induced transient responses in several actinomycete symbioses are associated with the Frankia vesicles and are not due to changes in nodule gas permeability.…”

mentioning

confidence: 99%

Effect of Increases in Oxygen Concentration during the Argon-Induced Decline in Nitrogenase Activity in Root Nodules of Soybean

King

Layzell²

1991

Plant Physiol.

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When intact nodulated roots of soybean (Glycine max L. Merr. nodulated with Bradyrhizobium japonicum strain USDA 16) were exposed to an atmosphere lacking N2 gas (Ar:02 80:20), total nitrogenase activity (measured as H2 evolution) and respiration (CO2 evolution) declined with time of exposure. In Ar-inhibited nodules, when the 02 concentration in the rhizosphere was increased in a linear 'ramp' of 2.7% per minute, 93% of the original H2 evolution and 99% of the CO2 evolution could be recovered. The internal nodule 02 concentration (estimated from leghemoglobin oxygenation) declined to 56% of its initial value after 60 minutes of Ar:02 exposure and could be partially recovered by the linear increases in 02 concentration. Nodule gas permeability, as estimated from the lag in ethylene production following exposure of nodules to acetylene, decreased to 26% of its initial value during the Ar-induced decline. Collectively, the results provide direct evidence that the Ar-induced decline results from decreased nodule gas permeability and indicate that the decline in permeability, rather than being immediate, occurs gradually over the period of Ar:02 exposure.The nodules of various legumes undergo a distinct decline in TNA3 and C02 evolution following exposure to 10% acetylene (2, 3, 12-14, 22, 23). A similar decline occurs when N2 in the gas phase is replaced by an inert gas such as Ar (5,13 3 Abbreviations: TNA, total nitrogenase activity as estimated from H2 production in Ar:02 or from acetylene reduction; NR, nodulated root; nod, nodules; Oi, 02 concentration in the cytosol of the infected cells of the nodule; P, nodule permeability to gas diffusion; t, time constant for ethylene production.clines (5, 23), and the ability of 02 at least to partially overcome the acetylene-induced decline (22), suggest that both declines are caused by a decrease in the nodule gas permeability (P), which restricts the entry of 02 for respiration in support of nitrogenase activity (23). However, this suggestion is based on theoretical considerations of the relationship between 02 concentration gradients, 02 uptake rates, and P.To date, neither P nor the infected cell 02 concentration (Os) have been measured in acetylene-or Ar-inhibited nodules, nor has it been demonstrated whether increases in 02 concentration can overcome the Ar-induced decline.In addition, various actinomycete symbioses also exhibit acetylene-induced declines or transient fluctuations of TNA (16,17,19), which are superficially similar to those of legumes. However, the anatomy of the nodules formed in these symbioses differs considerably from that of legume nodules, and the main barrier to gas diffusion is thought to be associated with the Frankia endosymbiont itself (18) rather than with the uninfected nodule cortex, as appears to be the case in legumes (20,24). Silvester and Winship (16) have provided evidence that the acetylene-and 02-induced transient responses in several actinomycete symbioses are associated with the Frankia vesicles and are not due to cha...

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“…In the perennial root nodules of actinorhizal plants, active symbiotic vesicles are apparently formed each growing season in newly infected plant cells (16). Like those in culture, symbiotic vesicles make new septa and increase in size as they mature.…”

mentioning

confidence: 99%

Developmental potential of Frankia vesicles

Schultz

Benson

1989

J Bacteriol

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The ability of nitrogenase-containing Frankia sp. strain CpIl vesicles to regrow vegetative hyphae is demonstrated. Vesicles attached to hyphae in N2-fixing Cpll cultures and sucrose gradient-isolated vesicles exhibited hyphal outgrowths when incubated in certain defined liquid media. Single or multiple hyphal extensions grew out from the vesicles.The onset of nitrogen fixation by Frankia strains in aerobic environments is preceded by the appearance of differentiated cellular structures, the frankial vesicles. Vesicles contain nitrogenase, both in culture (8,11,15) and in the N2-fixing root nodules formed on actinorhizal plants (13,18 screw-cap polycarbonate centrifuge tubes. The pellets were suspended in cold 10 mM potassium phosphate buffer (pH 6.5; buffer A) to a final volume of 6 ml and held on ice. Just prior to homogenization, 20 ml of cold 60% (wt/wt) sucrose in buffer A was added to each tube. The contents were homogenized with a Polytron tissue homogenizer in an ice bath for five cycles of 1-min homogenization followed by a 30-s rest to allow cooling of the suspension. Each suspension was examined microscopically to monitor the release of vesicles from the vegetative hyphae. Following homogenization, an additional 9 ml of cold 60% sucrose was added to each tube to yield a final concentration of 50% sucrose. The homogenates were overlayered with cold 10% (vol/vol) glycerol in buffer A, and the glycerol-sucrose gradients were centrifuged at 35,000 x g for 1 h at 4°C. Vesicles were removed from the glycerol-sucrose interface with Pasteur pipettes and washed by repeated centrifugation in buffer A at 40,000 x g for 15 min at 4°C.Regrowth potential of the isolated vesicles was tested by diluting the vesicles to about 105/ml in growth medium in 15-ml serum vials (Wheaton Scientific, Millville, N.Y.), and incubating them in air at 30°C. Vesicle concentration was kept low to avoid ambiguity in identification of the source of new hyphae. The percentage of vesicles with hyphal outgrowths was determined from direct counts as the ratio of the number of regrown vesicles to the total number of vesicles in several microscopic fields at 400x magnification with the phase-contrast optics of an Olympus BH-2 microscope (Olympus Corp., Woodbury, N.Y.). An Olympus OM-1 camera mounted on the microscope was used to document vesicle regrowth.Vesicles formed hyphal outgrowths when incubated as described above in the following media: succinate (0.5%) with and without NH4Cl (11), propionate (0.3%) or pyruvate (0.3%) with and without NH4Cl (9), QMOD medium (6) without lipid supplement, and R-2A broth (12). The percentages of regrown vesicles after 5 days were as follows: 8% and 10% for succinate medium with and without NH4Cl, respectively; 3% and 2% for propionate medium with and without NH4Cl, respectively; and <1% for the pyruvatecontaining media, the QMOD medium, and the R-2A broth. Regrowth was also observed in these same media solidified with agar (1.5%; Difco Laboratories, Detroit, Mich.) or with 1.0% agar and 6.0% gelatin (bo...

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Physiology of Actinorhizal Nodules

Cited by 106 publications

References 53 publications

Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport

Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport

Effect of Increases in Oxygen Concentration during the Argon-Induced Decline in Nitrogenase Activity in Root Nodules of Soybean

Developmental potential of Frankia vesicles

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