The Role of Peribacteroid Membrane in Legume Root Nodules

Robertson, John; Lyttleton, Pamela; Tapper, B.A.

doi:10.1007/978-94-009-6923-0_229

Cited by 16 publications

(8 citation statements)

References 31 publications

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“…During nodule development an extensive synthesis of membrane of about 30-to 50-fold of that in other tissues occurs in infected cells to build the pbm of each symbiosome (Robertson et al, 1984;Bradley et al, 1986). Because most of the B in plants is bound in cell walls (Thellier et al, 1979) and membranes (Torchia and Hirsch, 1982;Parr and Loughman, 1983), it is logical to find high levels of B in nodules (data not shown) and to observe the dramatic alterations produced by B deficiency in this structure.…”

Section: Discussionmentioning

confidence: 99%

Essentiality of Boron for Symbiotic Dinitrogen Fixation in Pea (Pisum sativum) Rhizobium Nodules

et al. 1994

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The effect of boron deficiency on symbiotic nitrogen fixation in pea (Pisum safivum) was examined. l h e absence of boron in the culture medium resulted in a decrease of the number of nodules and an alteration of nodule development leading to an inhibition of nitrogenase activity. Examination of boron-deficient nodules showed dramatic changes in cell walls and in both peribacteroid and infection thread membranes, suggesting a role for boron in the stability of these structures. These results indicate that boron is a requirement for normal nodule development and functionality.

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Section: Discussionmentioning

confidence: 99%

Essentiality of Boron for Symbiotic Dinitrogen Fixation in Pea (Pisum sativum) Rhizobium Nodules

et al. 1994

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“…Infection of the plant root by (Brady)rhizobia leads to the formation of root nodules which provide an environment suitable for symbiotic nitrogen fixation. Bacteroids [the symbiotic form of (Brady) rhizobia] within the infected cells of the nodule cortex are enclosed by the plant-derived PBM2.The PBM is formed initially via endocytosis of the plant cell plasma membrane (2,7,10,17,26), but subsequent proliferation appears to be supported by membrane flow from the biosynthetic endomembrane system (13,19 (27,28). Thus, it is to a large extent the PBM which prevents the symbiosis from degenerating into parasitism.…”

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confidence: 99%

“…The PBM is formed initially via endocytosis of the plant cell plasma membrane (2,7,10,17,26), but subsequent proliferation appears to be supported by membrane flow from the biosynthetic endomembrane system (13,19 obligatory feature of an effective symbiosis. Abberant development of the PBM resulting from incompatibility or a mutation in either partner may lead to a loss of PBM integrity and early nodule senescence (27,28).…”

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Electrogenic ATPase Activity on the Peribacteroid Membrane of Soybean (Glycine max L.) Root Nodules

Udvardi

Day²

1989

Plant Physiol.

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Electrogenic ATPase activity on the peribacteroid membrane from soybean (Glycine max L. cv Bragg) root nodules is demonstrated. Membrane energization was monitored using suspensions of intact peribacteroid membrane-enclosed bacteroids (peribacteroid units; PBUs) and the fluorescent probe for membrane potential (A#), bis-(3-phenyl-5-oxoisoxazol-4yl) pentamethine ox-onol. Generation of a positive A4, across the peribacteroid membrane was dependent upon ATP, inhibited by N,N'-dicyclohexylcarbodiimide and vanadate, but insensitive to N-ethylmaleimide, azide, cyanide, oligomycin, and ouabain. The results suggest the presence of a single, plasma membrane-like, electrogenic ATPase on the peribacteroid membrane. The protonophore, carbonyl-cyanide m-chlorophenyl hydrazone, completely dissipated the established membrane potential. The extent of reduction in the steady state membrane potential upon addition of ions was used to estimate the relative permeability of the peribacteroid membrane to anions. By this criterion, the relative rates of anion transport across the peribacteroid membrane were: N03-> N02-> Cl-> acetate-> malate-. The observation that 10 millimolar N03-completely dissipated the membrane potential was of particular interest in view of the fact that N03-inhibits symbiotic nitrogen fixation. The possible function of the ATPase in symbiotic nitrogen fixation is discussed.Under nitrogen-limited conditions, the growth of legumes can be enhanced by an endosymbiotic association with nitrogen-fixing bacteria from the genera Bradyrhizobium and Rhizobium. Infection of the plant root by (Brady)rhizobia leads to the formation of root nodules which provide an environment suitable for symbiotic nitrogen fixation. Bacteroids [the symbiotic form of (Brady) rhizobia] within the infected cells of the nodule cortex are enclosed by the plant-derived PBM2.The PBM is formed initially via endocytosis of the plant cell plasma membrane (2,7,10,17,26), but subsequent proliferation appears to be supported by membrane flow from the biosynthetic endomembrane system (13,19 (27,28). Thus, it is to a large extent the PBM which prevents the symbiosis from degenerating into parasitism. The PBM, strategically positioned between macro-and microsymbiont, is likely to play a major role in the regulation of nitrogen fixation by controlling exchange of metabolites. The primary exchange which must occur across the PBM is the supply of a reduced-carbon compound(s) by the plant in return for reduced nitrogen (ammonia) from the bacteroid. Other exchanges, such as iron from the plant for haem from the bacteroid also appear essential (14). Additionally, some form of mineral or organic nitrogen must be supplied by the plant to the growing bacterial population prior to the onset of nitrogen fixation. We have recently begun a study of these exchanges using intact peribacteroid units (PBUs: PBM-enclosed bacteroids) isolated from soybean nodules and have described a dicarboxylate carrier on the PBM which catalyses transport of succinate and malate ...

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“…This invagination develops into an infection thread which grows through and between root hair cells until it finally enters meristematic cells. At this point, bacteria that have grown along the infection thread are budded off and surrounded by a membrane (the peribacteroid membrane) of plant origin (14,15,18).Previously, we identified a series of transposon-(Tn5) induced mutants of R. leguminosarum (7) which were affected in their ability to nodulate Pisum sativum (peas). The mutations were all located within a 10-kilobase-pair (kb) region of DNA which had been shown to contain nodulation and host range genes (6,8).…”

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confidence: 99%

Nodulation inhibition by Rhizobium leguminosarum multicopy nodABC genes and analysis of early stages of plant infection

Knight¹,

Rossen²,

Robertson³

et al. 1986

J Bacteriol

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During analysis of early events in the infection and nodulation of Vicia hirsuta roots inoculated with normal and mutant strains of Rhizobium leguminosarum and strains containing cloned nodulation (nod) The morphological steps involved in the nodulation of leguminous plants by Rhizobium spp. have been clearly described. In general, the initial step involves a characteristic curling of the root hair, followed by an invagination of the root hair cell wall. This invagination develops into an infection thread which grows through and between root hair cells until it finally enters meristematic cells. At this point, bacteria that have grown along the infection thread are budded off and surrounded by a membrane (the peribacteroid membrane) of plant origin (14,15,18).Previously, we identified a series of transposon-(Tn5) induced mutants of R. leguminosarum (7) which were affected in their ability to nodulate Pisum sativum (peas). The mutations were all located within a 10-kilobase-pair (kb) region of DNA which had been shown to contain nodulation and host range genes (6,8). Five different classes of mutants were identified on the basis of the phenotypes of the mutant strains and on the locations of the TnS inserts (7). These observations, taken together with DNA sequence data from this part of the nod region (16; C. A. Shearman, L. Rossen, A. W. B. Johnston, and J. A. Downie, submitted for publication), allowed six different nod genes (called nodA, nodB, nodC, nodD, nodE, and nodF) to be identified (Fig. 1) required for root hair curling, and mutations within these genes blocked nodulation; nodD mutant were Nod-but did induce a delayed root hair curling and deformation response; nodE and class V mutations (e.g., nodE68::TnS) caused a delay in nodulation and induced root hair curlingdeformation (7).Only the nodABC genes are essential for root hair curling and deformation because a strain cured of its symbiotic plasmid but containing the subcloned nodABC genes could induce root hair curling and deformation (16) Table 1; media and general growth conditions were those described by Beringer (2). For inoculation of plants, Rhizobium cultures were grown for 2 days on agar slants containing 10 ml of medium, the bacteria were suspended in 4 ml of water, and 0.1 ml was added to the plant roots (this corresponds to about 5 x 107 bacteria). Bacteria were isolated from surface-sterilized nodules as described previously (3).Growth of plants and analysis of nodulation. Peas (variety Wisconsin Perfection) were surface sterilized and grown in 200 ml of sterile agar plant medium as described previously (3). V. hirsuta seeds were treated with concentrated H2SO4 for 20 min, rinsed three times in sterile water, and then left 552

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The Role of Peribacteroid Membrane in Legume Root Nodules

Cited by 16 publications

References 31 publications

Essentiality of Boron for Symbiotic Dinitrogen Fixation in Pea (Pisum sativum) Rhizobium Nodules

Essentiality of Boron for Symbiotic Dinitrogen Fixation in Pea (Pisum sativum) Rhizobium Nodules

Electrogenic ATPase Activity on the Peribacteroid Membrane of Soybean (Glycine max L.) Root Nodules

Nodulation inhibition by Rhizobium leguminosarum multicopy nodABC genes and analysis of early stages of plant infection

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