Structural similarity of the membrane envelopes of rhizobial bacteroids and the host plasma membrane as revealed by freeze-fracturing

Tu, J. C.

doi:10.1128/jb.122.2.691-694.1975

Cited by 16 publications

(5 citation statements)

References 13 publications

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“…Biochemical data (Table IV) suggest that the membrane envelope proteins are synthesized in the host cell cytoplasm. These results, along with earlier observations (5,14,15,35,38,39), confirm that the membrane envelope enclosing the bacteroids originates from plasma membrane of the host and show that most of the known characteristics of the plasma membrane are retained. An extracellular compartment is formed for Rhizobium to develop an "intracellular symbiosis.…”

Section: Origin and Biosynthesis Of The Membrane Envelopesupporting

confidence: 84%

“…These membranes are also sensitive to nonionic detergent (NP-40) both in vitro and in vivo, while bacterial membranes are not. Similarity of these membranes was further borne out by the recent study of Tu (39) showing similar freeze-fracture face particle decoration on these membranes. Analysis of membrane envelope proteins showed a close similarity with the plasma membrane of uninfected cells.…”

Section: Origin and Biosynthesis Of The Membrane Envelopesupporting

confidence: 59%

“…Although the view that it originates from the plasma membrane of the host cell is dominant, the membrane probably undergoes both structural and functional changes due to the symbiotic demands of both host and bacteroid. Apparently, it retains the same configuration, i.e., the surface facing the cell wall of the host cell now faces the bacteroid(s) (38,39); however, it loses the ability to form cell wall material on this surface.…”

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confidence: 99%

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Isolation and characterization of the membrane envelope enclosing the bacteroids in soybean root nodules.

Dp¹,

Kazazian²,

Zogbi³

et al. 1978

The Journal of Cell Biology

107

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The membrane envelope enclosing the bacteroids in soybean root nodules is shown by ultrastructural and biochemical studies to be derived from, and to retain the characteristics of, the host cell plasma membrane. During the early stages of the infection process, which occurs through an invagination, Rhizobium becomes surrounded by the host cell wall and plasma membrane, forming the infection thread. The cell wall of the infection thread is degraded by cellulolytic enzyme(s), leaving behind the enclosed plasma membrane, the membrane envelope. Cellulase activity in young nodules increases two-to threefold as compared to uninfected roots, and this activity is localized in the cell wall matrix of the infection threads.Membrane envelopes were isolated by first preparing bacteroids enclosed in the envelopes on a discontinuous sucrose gradient followed by passage through a hypodermic needle, which released the bacteroids from the membranes. This membrane then sedimented at the interface of 34-45% sucrose (mean density of 1.14 g/cma). Membranes were characterized by phosphotungstic acid (PTA)-chromic acid staining, ATPase activity, and localization, sensitivity to nonionic detergent Nonidet P-40 (NP-40) and sodium dodecyl sulfate (SDS) gel electrophoresis. These analyses revealed a close similarity between plasma membrane and the membrane envelope. Incorporation of radioactive amino acids into the membrane envelope proteins was sensitive to cycloheximide, suggesting that the biosynthesis of these proteins is primarily under host-cell control. No immunoreactive material to leghemoglobin antibodies was found inside or associated with the isolated bacteroids enclosed in the membrane envelope, and its location is confined to the host cell cytoplasmic matrix. KEY WORDS Rhizobium leghemoglobin 9 membrane envelope immunohistochemistryIn symbiotic nitrogen-fixing root nodules of leguminous plants, the bacteroids are enclosed in a membrane envelope which was first observed by Bergersen and Briggs (5). This membrane envelope compartmentalizes the bacteroids from the host cell cytoplasm, and thus may play an important role in segregating eu-and procaryote metab-J. C~LL BIOLOGy 9 The Rockefeller University Press 9

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Section: Origin and Biosynthesis Of The Membrane Envelopesupporting

confidence: 84%

Section: Origin and Biosynthesis Of The Membrane Envelopesupporting

confidence: 59%

mentioning

confidence: 99%

See 1 more Smart Citation

Isolation and characterization of the membrane envelope enclosing the bacteroids in soybean root nodules.

Dp¹,

Kazazian²,

Zogbi³

et al. 1978

The Journal of Cell Biology

107

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show abstract

“…Firstly, several authors have found that the PBM, ITM and plasma membrane all stain with the plasma membrane-specific stain, phosphotungstic acid, whereas other cell membranes do not (Robertson et al 1978b, Roth and Stacy 1989a, Verma et al 1978. Secondly, freeze fracture studies of the PBM and plasma membrane from newly infected nodule cells of soybean, alfalfa and clover have revealed a striking similarity between the particle profiles of the surfaces of the two membranes (Tu 1975). And lastly, antibody studies have shown similarities in the epitopes present on the PBM and plasma membrane throughout PBM development (Perotto et al 1991(Perotto et al , 1995, see further discussion later).…”

Section: Origin Of the Pbmmentioning

confidence: 99%

The peribacteroid membrane

Whitehead¹,

Day²

1997

Physiol Plant

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1997. The peribacteroid membrane. -Physiol. Plant. 100: 30^4.The objective of this review is to summarise current knowledge about the structure and function of the peribacteroid membrane from the root nodules of leguminous plants. The information is presented in terms of development of this symbiotic membrane from its origin, through proliferation and in the mature state. There are clear indications that the peribacteroid membrane has a distinct structure and function at each developmental stage. The mature peribacteroid membrane has been the most intensively studied. The" lipid and protein content of the mature peribacteroid membrane is discussed with particu!ar emphasis on genetic and functional studies of the proteins. The mechanism and control of peribacteroid membrane biogenesis is also discussed. There is evidence for a specific biogenetic pathway for this membrane which requires both symbiotic partners for its correct functioning.

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“…Some authors put forward a route via plasmamembrane, i.e. a membrane recycling (Tu, 1975;Verma et al, 1978;Blumwald et al, 1985), while others propose a more direct membrane flow from ER and Golgi to the peribacteroid membrane (Robertson et al, 1978;Mellor et al, 1984;Mellor and Werner, 1987). We have analysed the fatty acid composition of different nodule-derived membrane systems to contribute further information to this controversy.…”

Section: Introductionmentioning

confidence: 99%

Fatty Acid Composition of the Peribacteroid Membrane and the ER in Nodules of Glycine max Varies after Infection by Different Strains of the Microsymbiont Bradyrhizobiumjaponicum

1989

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The fatty acid composition of ER, Golgi and peribacteroid membrane (PBM) from root nodules formed on Glycine max after infection with different strains of Bradyrhizobium japonicum has been analysed by gas chromatography. In each plant-microsymbiont combination the fatty acid composition (FAC) of the PBM is distinct from ER and Golgi. The similarity between ER and PBM fatty acid composition is significantly stronger than between Golgi and PBM. In addition the fatty acid composition of all membrane systems in nodules is affected by the microsymbiont strain. Acomparison offour strains of Bradyrhizobium japonicum grown in agar surface culture and isolated as the symbiotic bacteroids reveals a decrease in oleic acid during bacteroid differentiation.-

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Structural similarity of the membrane envelopes of rhizobial bacteroids and the host plasma membrane as revealed by freeze-fracturing

Cited by 16 publications

References 13 publications

Isolation and characterization of the membrane envelope enclosing the bacteroids in soybean root nodules.

Isolation and characterization of the membrane envelope enclosing the bacteroids in soybean root nodules.

The peribacteroid membrane

Fatty Acid Composition of the Peribacteroid Membrane and the ER in Nodules of Glycine max Varies after Infection by Different Strains of the Microsymbiont Bradyrhizobiumjaponicum

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