Cytoplasmic bridge formation in the nodule apex of actinorhizal root nodules

1999 ◽  
Vol 77 (9) ◽  
pp. 1351-1357 ◽  
Author(s):  
R Howard Berg
Keyword(s):  
Structural Changes ◽  
Root Nodules ◽  
Parenchyma Cell ◽  
Infection Process ◽  
Infection Thread ◽  
Cytoplasmic Bridge ◽  
Cortical Cells ◽  
Infection Threads ◽  
Related Plant ◽  
Cytoplasmic Bridges

High-pressure frozen - freeze-substituted actinorhizal root nodules of several distantly related plant genera were used to document the sequence of structural changes in cortical cells of the nodule apex that happened prior to their infection. The sequence of mobilization of the plant cell cytoplasm requisite to infection by Frankia was (i) penetration of the parenchyma cell vacuole by cytoplasmic strands, which contained microtubules; (ii) movement of the nucleus and other organelles (Golgi stacks, endoplasmic reticulum, mitochondria), involved later in growth of the infection thread, to the cell center on these strands; (iii) thickening of some of these strands generally located at midpoints of the wall, forming cytoplasmic bridges (preinfection threads); and (iv) infection of the cell by initiation of infection threads (containing Frankia) within the cytoplasmic bridges. The infection thread was caged in microtubules that were oriented along its axis, suggesting the cytoskeleton had a major role in the infection process, perhaps guiding the growth of the infection thread across the cell. The coalignment of cytoplasmic bridges, along several cells, towards the advancing microsymbiont suggested Frankia secretes a diffusible signal eliciting this host response.Key words: actinorhiza, cryofixation, development, infection, microtubules, symbiosis.

Cytological studies of the infection process in nodulating and nonnodulating pea genotypes

1989 ◽  
Vol 67 (8) ◽  
pp. 2435-2443 ◽  
Author(s):  
M. F. Le Gal ◽  
S. L. A. Hobbs
Keyword(s):  
North American ◽  
Rhizobium Leguminosarum ◽  
Root Hairs ◽  
Infection Process ◽  
High Concentration ◽  
Cortical Cells ◽  
Pisum Sativum L ◽  
Infection Threads ◽  
American Strain ◽  
Plant Effect

Pisum sativum L., cv. Afghanistan, does not form nodules with 128C52, a North American strain of Rhizobium leguminosarum. Timing of the abortion of the nodulation process was determined by microscopy in both 'Afghanistan' and nonnodulating 'Trapper,' produced by backcrossing the nonnodulating genes of 'Afghanistan' into 'Trapper,' a North American variety. Three to 5 days after inoculation, we observed deformed roots and localized swellings as well as loosely curled root hairs in these nonnodulating combinations. Rhizobia entered root hairs and epidermal cells, but no infection threads were seen. Cortical cells divided and a nodule meristem was initiated. Some meristematic cells showed abnormal features such as a high concentration of free ribosomes, dilated endoplasmic reticulum often connected to a dilated nuclear envelope, and disrupted mitochondria. Cortical cells around the nodule meristem were devoid of starch grains. Such phenotypes are known to be associated with rhizobial mutants, but in this case a plant effect is responsible.

ELECTRON MICROSCOPY OF THE BACTEROIDS AND ROOT NODULES OF LUPINUS LUTEUS

1965 ◽  
Vol 11 (4) ◽  
pp. 721-725 ◽  
Author(s):  
D. C. Jordan ◽  
I. Grinyer
Keyword(s):  
Plant Cell ◽  
De Novo ◽  
Root Nodules ◽  
Cell Plate ◽  
Lupinus Luteus ◽  
Bacterial Cells ◽  
Intercellular Spaces ◽  
Cortical Cells ◽  
Infection Threads ◽  
Spread Of Infection

No intracellular infection threads were observed in ultrathin sections of young root nodules of lupine, although nodule bacteria could be found in the intercellular spaces between the root cortical cells. Evidence suggests that in certain instances the plant cell walls can be disrupted locally, allowing the bacteria to pass into cytoplasm of the host cell. The spread of infection may be initiated in this manner and extended by division of infected cells. No plant-produced enclosing membranes were present around bacteria in the intercellular spaces but such structures developed after the bacteria had entered the plant cell. Although the origin of these membranes is debatable, in the present work it appeared that they were formed de novo, perhaps in a manner akin to the development of the cell plate during cell division. Most of the bacterial cells possessed a wide subwall space lying between the bacterial cell wall and plasma membrane. Discontinuities present in the latter membrane may account for the ribosome-like material found in the subwall space.

scholarly journals Localization of acid phosphatase activity in the apoplast of root nodules of pea (Pisum sativum)

2011 ◽  
Vol 75 (1) ◽  
pp. 33-38 ◽  
Author(s):  
Marzena Sujkowska ◽  
Wojciech Borucki ◽  
Władysław Golinowski
Keyword(s):  
Enzyme Activity ◽  
Acid Phosphatase ◽  
Pisum Sativum ◽  
Root Nodule ◽  
Root Nodules ◽  
Outer Part ◽  
Inorganic Phosphorus ◽  
Infection Thread ◽  
Symbiotic Bacteria ◽  
Infection Threads

Changes in the activity of acid phosphatase (AcPase) in the apoplast of pea root nodule were investigated. The activity was determined using lead and cerium methods. The results indicated a following sequence of AcPase activity appearance during the development of the infection thread: 1) low AcPase activity appears in the outer part of cells of symbiotic bacteria; 2) bacteria show increased AcPase activity, and the enzyme activity appears in the thread walls; 3) activity exhibits also matrix of the infection thread; 4) bacteria just before their release from the infection threads show high AcPase activity; 5) AcPase activity ceases after bacteria transformation into bacteroids. The increase in bacterial AcPase activity may reflect a higher demand for inorganic phosphorus necessary for propagation of the bacteria within the infection threads and/or involved in bacteria release from the infection threads.

A correlated light and electron microscopic study of symbiotic growth and differentiation in Pisum sativum root nodules

1976 ◽  
Vol 54 (18) ◽  
pp. 2163-2186 ◽  
Author(s):  
William Newcomb
Keyword(s):  
Electron Microscopy ◽  
Pisum Sativum ◽  
Rhizobium Leguminosarum ◽  
Root Nodules ◽  
Light And Electron Microscopy ◽  
Infection Thread ◽  
Electron Microscopic ◽  
Cortical Cells ◽  
Garden Pea ◽  
Host Cytoplasm

Plants of the garden pea Pisum sativum cv. Little Marvel were grown in aeroponic culture to facilitate observations and microscopy and were inoculated with Rhizobium leguminosarum, and nodules were sampled at five weekly intervals for light and electron microscopy. The invasion of the cortical cells by the infection thread, the structure of the infection thread, and the release of bacteria from it into the host cytoplasm and the subsequent symbiotic growth and differentiation of the two organisms are described in detail. The fine structure of the nodule is correlated with light microscopic observations and morphogenesis. A restriction in the use of the term 'vesicle' is proposed because of the current multiple and confusing usage of the term. The loss of the nodule meristem and its morphogenetic significance are discussed.

Early events in the infection of soybean by Rhizobium japonicum. Time course and cytology of the initial infection process

1982 ◽  
Vol 60 (2) ◽  
pp. 152-161 ◽  
Author(s):  
B. Gillian Turgeon ◽  
Wolfgang D. Bauer
Keyword(s):  
Root Hair ◽  
Time Course ◽  
Cortical Cell ◽  
Root Hairs ◽  
Infection Process ◽  
Infection Thread ◽  
Rhizobium Japonicum ◽  
Outer Cortex ◽  
Light Microscope Level ◽  
Infection Threads

The time course of early infection events in Glycine max following inoculation with Rhizobium japonicum is described. Bacteria became attached to epidermal cells and root hairs within minutes of inoculation. Marked root hair curling occurred within 12 h. Infection thread formation was visible at the light microscope level of resolution about 24 h after inoculation. Infections were observed in short, tightly curled root hairs. These root hairs had not yet emerged at the time of inoculation. Infection threads appeared to originate in pockets formed by contact of the cell wall of the curled root hair with itself. Infection threads in the hairs were multiple and (or) branched. By 48 h, the infection thread(s) had progressed to the base of the root hair but had not yet penetrated into the cortex. Increases in cortical cell cytoplasm and in mitotic division occurred in advance of the penetrating infection thread. A nodule meristem developed in the outer cortex next to the infected root hair by 4 days and was accompanied by cell division across the cortex.

scholarly journals Transcriptomic analysis with the progress of symbiosis in ‘crack-entry’ legume Arachis hypogaea highlights its contrast with ‘infection thread’ adapted legumes

2018 ◽  
Author(s):  
Kanchan Karmakar ◽  
Anindya Kundu ◽  
Ahsan Z Rizvi ◽  
Emeric Dubois ◽  
Dany Severac ◽  
...  
Keyword(s):  
Arachis Hypogaea ◽  
Root Nodule ◽  
Infection Thread ◽  
Symbiotic Genes ◽  
Cortical Cells ◽  
Transcriptional Dynamics ◽  
Infection Threads ◽  
Spread Of Infection ◽  
Molecular Framework ◽  
Nodule Symbiosis

ABSTRACTIn root-nodule symbiosis, rhizobial invasion and nodule organogenesis is host controlled. In most legumes, rhizobia enter through infection-threads and nodule primordium in the cortex is induced from a distance. But in dalbergoid legumes like Arachis hypogaea, rhizobia directly invade cortical cells through epidermal cracks to generate the primordia. Herein we report the transcriptional dynamics with the progress of symbiosis in A. hypogaea at 1dpi: invasion; 4dpi: nodule primordia; 8dpi: spread of infection in nodule-like structure; 12dpi: immature nodules containing rod-shaped rhizobia; and 21dpi: mature nodules with spherical symbiosomes. Expression of putative orthologue of symbiotic genes in ‘crack-entry’ legume A. hypogaea was compared with infection thread adapted model legumes. The contrasting features were (i) higher expression of receptors like LYR3, EPR3 as compared to canonical NFRs (ii) late induction of transcription factors like NIN, NSP2 and constitutive high expression of ERF1, EIN2, bHLH476 and (iii) induction of divergent pathogenesis responsive PR-1 genes. Additionally, symbiotic orthologues of SymCRK, FLOT4, ROP6, RR9, NOOT and SEN1 were not detectable and microsynteny analysis indicated the absence of RPG and DNF2 homologues in diploid parental genomes of A. hypogaea. The implications are discussed and a molecular framework that guide ‘crack-entry’ symbiosis in A. hypogaea is proposed.

scholarly journals The Early Nodulin Gene MtN6 Is a Novel Marker for Events Preceding Infection of Medicago truncatula Roots by Sinorhizobium meliloti

1999 ◽  
Vol 12 (6) ◽  
pp. 544-555 ◽  
Author(s):  
R. Mathis ◽  
C. Grosjean ◽  
F. de Billy ◽  
T. Huguet ◽  
P. Gamas
Keyword(s):  
Medicago Truncatula ◽  
Sinorhizobium Meliloti ◽  
Root Nodules ◽  
Cdna Clones ◽  
Specific Marker ◽  
Nod Factors ◽  
Cortical Cells ◽  
Infection Threads ◽  
Early Nodulin ◽  
Cell Layers

MtN6 belongs to a series of cDNA clones representing Medicago truncatula genes transcriptionally activated during nodulation by Sinorhizobium meliloti (P. Gamas, F. de Carvalho Niebel, N. Lescure, and J. V. Cullimore, Mol. Plant-Microbe Interact. 9:233–242, 1996). We show here by in situ hybridization that MtN6 transcripts specifically accumulate first at very localized regions in the outer root cell layers, corresponding to outer cortical cells containing preinfection threads. At later stages, MtN6 expression is observed ahead of growing infection threads, including in the infection zone of mature root nodules. Interestingly, regulation of MtN6 is clearly distinct from that of other early nodulins expressed in the same region of the nodule, in terms of response to bacterial symbiotic mutants and to purified Nod factors. We thus suggest that MtN6 represents the first specific marker of a pathway involved in preparation to infection, which is at least partly controlled by Nod factors. Finally, we discuss the intriguing sequence homology shown by MtN6 to a protein from Emericella (Aspergillus) nidulans, FluG, that plays a key role in controlling the organogenesis of conidiophores (B. N. Lee and T. H. Adams, Genes Dev. 8:641–651, 1994).

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

1978 ◽  
Vol 78 (3) ◽  
pp. 919-936 ◽  
Author(s):  
D P Verma ◽  
V Kazazian ◽  
V Zogbi ◽  
A K Bal
Keyword(s):  
Cell Wall ◽  
Plasma Membrane ◽  
Host Cell ◽  
Root Nodules ◽  
Infection Thread ◽  
Hypodermic Needle ◽  
Soybean Root ◽  
Isolation And Characterization ◽  
Infection Threads ◽  
Membrane Envelope

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/cm3). 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.

Ultrastructure of soybean nodules. I: release of rhizobia from the infection thread

1977 ◽  
Vol 23 (5) ◽  
pp. 573-582 ◽  
Author(s):  
B. Bassett ◽  
R. N. Goodman ◽  
A. Novacky
Keyword(s):  
Root Nodules ◽  
Infection Process ◽  
Infection Thread ◽  
Rhizobium Japonicum ◽  
Wall Material ◽  
Cell Infection ◽  
Host Cytoplasm ◽  
Transmission Electron ◽  
Membrane Envelope ◽  
Membrane Bound

Root nodules on soybeans (var. Clark 63) were examined by transmission electron microscopy 10–12 days after seed inoculation and planting. The cell infection process appeared identical in both effective nodules, induced by Rhizobium japonicum strain 138 (USDA) and in ineffective nodules, induced by strain 8-0 (Iowa). Electron micrographs are presented which suggest that rhizobia are freed from the infection thread by disintegration of the thread wall and compartmentalization of the disintegrated wall material in membrane-bound vesicles derived from the membrane surrounding the thread. As the thread wall is removed in this manner, the bacteria are released into the host cytoplasm by a process which encloses each in an envelope also derived from the thread membrane. Any thread wall material remaining around a bacterium after it has dissociated from the thread is removed from the envelope space by vesiculation of the membrane envelope. Thus, it appears that endocytosis of both the bacteria and the material composing the infection thread wall occurs during release of rhizobia into the host cell.

scholarly journals Transcriptomic Analysis With the Progress of Symbiosis in ‘Crack-Entry’ Legume Arachis hypogaea Highlights Its Contrast With ‘Infection Thread’ Adapted Legumes

2019 ◽  
Vol 32 (3) ◽  
pp. 271-285 ◽  
Author(s):  
Kanchan Karmakar ◽  
Anindya Kundu ◽  
Ahsan Z Rizvi ◽  
Emeric Dubois ◽  
Dany Severac ◽  
...  
Keyword(s):  
Arachis Hypogaea ◽  
Root Nodule ◽  
Infection Thread ◽  
Cortical Cells ◽  
Nod Factor ◽  
Transcriptional Dynamics ◽  
Infection Threads ◽  
Spread Of Infection ◽  
Molecular Framework ◽  
Nodule Symbiosis

In root-nodule symbiosis, rhizobial invasion and nodule organogenesis is host controlled. In most legumes, rhizobia enter through infection threads and nodule primordium in the cortex is induced from a distance. But in dalbergoid legumes like Arachis hypogaea, rhizobia directly invade cortical cells through epidermal cracks to generate the primordia. Herein, we report the transcriptional dynamics with the progress of symbiosis in A. hypogaea at 1 day postinfection (dpi) (invasion), 4 dpi (nodule primordia), 8 dpi (spread of infection in nodule-like structure), 12 dpi (immature nodules containing rod-shaped rhizobia), and 21 dpi (mature nodules with spherical symbiosomes). Expression of putative ortholog of symbiotic genes in ‘crack entry’ legume A. hypogaea was compared with infection thread–adapted model legumes. The contrasting features were i) higher expression of receptors like LYR3 and EPR3 as compared with canonical Nod factor receptors, ii) late induction of transcription factors like NIN and NSP2 and constitutive high expression of ERF1, EIN2, bHLH476, and iii) induction of divergent pathogenesis-responsive PR-1 genes. Additionally, symbiotic orthologs of SymCRK, ROP6, RR9, SEN1, and DNF2 were not detectable and microsynteny analysis indicated the absence of a RPG homolog in diploid parental genomes of A. hypogaea. The implications are discussed and a molecular framework that guides crack-entry symbiosis in A. hypogaea is proposed.

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