The symbiotic vesicle is a major site for respiration in <i>Frankia</i> from <i>Alnus incana</i> root nodules

Vikman, Per‐Åke

doi:10.1139/m92-127

Cited by 17 publications

(5 citation statements)

References 15 publications

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“…While vesicles formed in the free-living state are always round and non-septate, the shape and cellular location of vesicles formed in planta depends on the host plant genus (Baker and Mullin, 1992), indicating that here, vesicles represent a symbiosis-specific differentiation comparable to bacteroids in legume nodules. In addition to diffusion resistance, the fast respiration rate of Frankia vesicles suggests that metabolic consumption of O 2 also plays a role in O 2 -protection of nitrogenase (Vikman, 1992). In nodules of Datisca, Frankia forms lanceolate vesicles in radial orientation that form a ring around the central vacuole.…”

Section: Regulation Of O 2 Supply To the Microsymbiontmentioning

confidence: 99%

Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads

2005

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In the mutualistic symbioses between legumes and rhizobia, actinorhizal plants and Frankia, Parasponia sp. and rhizobia, and cycads and cyanobacteria, the N 2 -fixing microsymbionts exist in specialized structures (nodules or cyanobacterial zones) within the roots of their host plants. Despite the phylogenetic diversity among both the hosts and the microsymbionts of these symbioses, certain developmental and physiological imperatives must be met for successful mutualisms. In this review, phylogenetic and ecological aspects of the four symbioses are first addressed, and then the symbioses are contrasted and compared in regard to infection and symbio-organ development, supply of carbon to the microsymbionts, regulation of O 2 flux to the microsymbionts, and transfer of fixed-N to the hosts. Although similarities exist in the genetics, development, and functioning of the symbioses, it is evident that there is great diversity in many aspects of these root-based N 2 -fixing symbioses. Each symbiosis can be admired for the elegant means by which the host plant and microsymbiont integrate to form the mutualistic relationships so important to the functioning of the biosphere.

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Section: Regulation Of O 2 Supply To the Microsymbiontmentioning

confidence: 99%

Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads

2005

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“…They contain cytochromes a, b, c, and o (Ching, Monaco & Ching, 1983) and show cyanidesensitive oxygen consumption that is not affected by salicylhydroxamic acid (Vikman & Huss-Danell, 1987fl), an inhibitor of the alternative respiration pathway in plant mitochondria. Although these activities could take place in hyphae as well as in vesicles in vesicle clusters, Vikman (1992) showed that purified vesicles from such clusters have high respiratory capacity.…”

Section: Carbon Metabolism In Nodulesmentioning

confidence: 99%

“…Respiration is one such process. It has not yet been possible to measure respiration rates in vesicles in situ, but when vesicle clusters from Alnus incana nodules were sonicated, the fraction of the homogenate that was enriched in vesicles showed high respiratory capacity (Vikman, 1992). Although respiration consumes Og, it also gives rise to radical formation, as does nitrogenase activity (Gallon, 1992).…”

Section: The Oxygen Problemmentioning

confidence: 99%

Actinorhizal symbioses and their N₂ fixation

1997

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summary More than 200 angiosperms, distributed in 25 genera, develop root nodule symbioses (actinorhizas) with soil bacteria of the actinomycetous genus Frankia. Although most soils studied contain infective Frankia, cultured strains are available only after isolation from root nodules. Frankia infects roots via root hairs in some hosts or via intercellular penetration in others. The nodule originates in the pericycle. The number of nodules in Alnus is determined by the plant in an autoregulated process that, in turn, is modulated by nutrients such as nitrogen and phosphate. Except in the genera Allocausarina and Casuarina, Frankia in nodules develops so‐called vesicles where nitrogenase is localized. Sporulation of Frankia occurs in some symbioses. As a group, actinorhizal plants show a large range of anatomical and biochemical adaptations in order to balance the oxygen tension near nitrogenase. In symbioses with well aerated nodule tissue like Alnus, the vesicles have a multilayered envelope composed mainly of lipids, bacterio‐hopanetetrol and their derivatives. This envelope is assumed to retard the diffusion of oxygen into the nitrogenase‐containing vesicle. In symbioses like Casuarina, the infected plant cells themselves, rather than Frankia, appear to retard oxygen diffusion, and high concentrations of haemoglobin indicate an infected region with a low oxygen tension. At least in Alnus spp., ammonia resulting from N2 fixation is assimilated by glutamine synthetase in the plant. The carbon compound(s) used by Frankia in nodules is not yet known. Nitrogenase activity decreases in response to a number of environmental factors but recovers upon return to normal conditions. This dynamism in nitrogenase activity is often explained by loss and recovery of active nitrogenase and has been traced to loss and recovery of the nitrogenase proteins themselves. Recovery is partly due to growth of Frankia and to development of new vesicles in the Alnus nodules. In the field, varying conditions continuously affect the plants and the measured rate of N2 fixation is a result not only of the conditions prevailing at the moment but also of the conditions experienced over preceding days. N2 fixed by actinorhizal plants is substantial and actinorhizal plants have great potential in soil reclamation and in various types of forestry. Several species are also useful in horticulture.

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“…Respiration both consumes oxygen and provides energy and reducing compounds for nitrogen fixation. It has not been possible to measure actual respiration in vesicles in the nodule, but vesicles prepared from vesicle clusters had high capacity to respire exogenous substrates (Vikman 1992). Radicals are produced in both the respiratory chain and by nitrogenase itself (Gallon 1993).…”

Section: Discussionmentioning

confidence: 99%

Superoxide dismutase, catalase and nitrogenase activities of symbiotic Frankia (Alnus incana) in response to different oxygen tensions

Alskog¹,

Huss‐Danell²

1997

Physiol Plant

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Alskog, G. and Huss-Danell. K. 1997. Superoxide dismutase. catalase and nitrogenase activities of symbiolic Frankia [Alnus incana) in response to different oxygen Presence and activity of the enzymes superoxide dismula.se (SOD) and catalase were studied in Frankia in symbiosis with .\tnus incana (L.) Moench. Analysis on native PAGE gels indicated that symbiotic Frankia contained an FeSOD and calalase. The activity of the enzymes was in Ihe same range as reported for cultured Frankia. Attempts to characterize SOD by western blots with antisera fi'om Escherichia colt and .\zotobacter vinelandii did not give clear-cut results with the antibodies used, .\lnus incana plants were grown with the root system in 5, 10. 21 or407r O; for up to 6 days. Nitrogenase activity, measured as ..\RA (acetylene reducing acli\ ity) dropped within 3 h when roots were exposed to low or high oxygen. .^1 409f O; ARA was almost completely lost while at 5 and 109; O; ARA decreased lo 69 and 74'/f of the initai value, respectively. Nitrogenase activity recovered al a!l oxygen tensions. Recovery rates resembled the continuous increa.se in AR.A in plants continuosly kept al 2I'7r O-. and suggests that new vesicles with envelopes of appropriate thickness were formed. The ARA measurements confirm results from an earlier study where nitrogenase activity was measured as H^ evolution. There was a tendency for increased SOD and catatase activities in Frankia from rool systems exposed to 40'>r O: for 24 h but nol earlier or later than this. When data from all experimenlal times were pooled. SOD activity increased significantly with increased oxygen tension whereas catala.se activity decreased. Although ARA per plant varied wilh oxygen tension, there was no statistically significant correlation between ARA and SOD or between ARA and calalase. It seems that being linked to nitrogenase activity is only one role of SOD and catalase in this symbiotic Frankia.

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The symbiotic vesicle is a major site for respiration in Frankia from Alnus incana root nodules

Cited by 17 publications

References 15 publications

Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads

Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads

Actinorhizal symbioses and their N₂ fixation

Superoxide dismutase, catalase and nitrogenase activities of symbiotic Frankia (Alnus incana) in response to different oxygen tensions

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The symbiotic vesicle is a major site for respiration in Frankia from Alnus incana root nodules

Cited by 17 publications

References 15 publications

Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads

Root-based N2-fixing Symbioses: Legumes, Actinorhizal Plants, Parasponia sp. and Cycads

Actinorhizal symbioses and their N2 fixation

Superoxide dismutase, catalase and nitrogenase activities of symbiotic Frankia (Alnus incana) in response to different oxygen tensions

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Actinorhizal symbioses and their N₂ fixation