The occurrence and ontogeny of transfer cells associated with lateral roots and root nodules in Leguminosae

1979 ◽  
Vol 57 (23) ◽  
pp. 2583-2602 ◽  
Author(s):  
William Newcomb ◽  
R. L. Peterson
Keyword(s):  
Nitrogen Fixation ◽  
Rhizobium Leguminosarum ◽  
Root Nodules ◽  
Lateral Roots ◽  
Transfer Cells ◽  
Xylem Parenchyma ◽  
Cortical Cells ◽  
Nitrogenous Compounds ◽  
Wall Ingrowths ◽  
Xylem Elements

Xylem parenchyma transfer cells are present in the stele of the root tissue adjacent to emergent effective root nodules of garden pea (Pisum sativum), red kidney bean (Phaseolus vulgaris), broad bean (Vicia faba), soybean (Glycine max), and mung bean (Vigna radiata), two types of ineffective pea nodules, and emergent lateral roots of pea. The xylem parenchyma transfer cells contain many polyribosomes and mitochondria near the wall ingrowths which are located adjacent to pits in the xylem elements. Pericycle transfer cells also occur in the three types of pea nodules. In effective pea nodules wall ingrowths begin to form in the pericycle cells 5 days after inoculation with Rhizobium leguminosarum; at this stage rhizobia are only present in the root hair but the cortical cells have enlarged and some have undergone mitosis. The wall ingrowths begin to form in the xylem parenchyma cells 7–8 days after inoculation or the approximate time that rhizobia begin to be released from the infection thread. In both instances the wall ingrowths begin to form before the onset of dinitrogen reduction although previous workers have suggested that a flux of nitrogenous compounds (containing fixed N) induces their formation. The development of wall ingrowths in ineffective pea nodules also occurs independently of nitrogen fixation. Similarly, the wall ingrowths located near soybean nodules also begin to develop before the onset of nitrogen fixation.

PARASITISM IN PHOLISMA (LENNOACEAE): II. ANATOMICAL ASPECTS

1967 ◽  
Vol 45 (7) ◽  
pp. 1155-1162 ◽  
Author(s):  
Job Kuijt
Keyword(s):  
Lateral Roots ◽  
Sieve Tube ◽  
Cambial Activity ◽  
Root Cap ◽  
Xylem Parenchyma ◽  
Vessel Elements ◽  
Xylem Elements ◽  
Host Tissues

The anatomy of roots and haustoria of Pholisma depressum is detailed. Lignified xylem consists of vessel elements only, and is associated with some xylem parenchyma. Sieve tube members exist in both the stem and the root. The pilot root is characterized by a restriction of cambial activity to the primary phloem regions, thus resulting in 3–5 bundle-like structures in older roots. From the protoxylem points between these bundles vascular flanges extend radially outward. The steles of lateral roots are extensions of these vascular flanges. A root cap is recognizable but very thin.The endophyte is a lobed organ with sinuous and irregular vascular strands lacking any phloem-like tissues. Strands, occasionally uniseriate, invade adjacent host tissues, usually in phloem-producing regions of the host cambium. These strands establish xylem-to-xylem contact, but are parallel to host xylem elements. They may subsequently become partially encapsuled by the latter. No radial sinkers exist.The nuclei of the endophyte show a more or less permanent type of heteropycnosis, the significance of which is unknown.A comparison of the parasitism of Lennoaceae and Orobanchaceae yields a number of significant differences in the structure and development of roots and haustoria.

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.

scholarly journals The legume-rhizobia symbiosis can be supported on Mars soil simulants

PLoS ONE ◽  
2021 ◽  
Vol 16 (12) ◽  
pp. e0259957
Author(s):  
Randall Rainwater ◽  
Arijit Mukherjee
Keyword(s):  
Nitrogen Fixation ◽  
Sinorhizobium Meliloti ◽  
Root Nodules ◽  
Lateral Roots ◽  
Model Legume ◽  
Mars Atmosphere ◽  
Future Studies ◽  
Sinorhizobium Medicae ◽  
Total Plant ◽  
Atmospheric Nitrogen Fixation

Legumes (soybeans, peas, lentils, etc.) play important roles in agriculture on Earth because of their food value and their ability to form a mutualistic beneficial association with rhizobia bacteria. In this association, the host plant benefits from atmospheric nitrogen fixation by rhizobia. The presence of nitrogen in the Mars atmosphere offers the possibility to take advantage of this important plant-microbe association. While some studies have shown that Mars soil simulants can support plant growth, none have investigated if these soils can support the legume-rhizobia symbiosis. In this study, we investigated the establishment of the legume-rhizobia symbiosis on different Mars soil simulants (different grades of the Mojave Mars Simulant (MMS)-1: Coarse, Fine, Unsorted, Superfine, and the MMS-2 simulant). We used the model legume, Medicago truncatula, and its symbiotic partners, Sinorhizobium meliloti and Sinorhizobium medicae, in these experiments. Our results show that root nodules could develop on M. truncatula roots when grown on these Mars soil simulants and were comparable to those formed on plants that were grown on sand. We also detected nifH (a reporter gene for nitrogen fixation) expression inside these nodules. Our results indicate that the different Mars soil simulants used in this study can support legume-rhizobia symbiosis. While the average number of lateral roots and nodule numbers were comparable on plants grown on the different soil simulants, total plant mass was higher in plants grown on MMS-2 soil than on MMS-1 soil and its variants. Our results imply that the chemical composition of the simulants is more critical than their grain size for plant mass. Based on these results, we recommend that the MMS-2 Superfine soil simulant is a better fit than the MMS-1 soil and it’s variants for future studies. Our findings can serve as an excellent resource for future studies investigating beneficial plant-microbe associations for sustainable agriculture on Mars.

scholarly journals Introduction of H2-Uptake Hydrogenase Genes Into Rhizobial Strains Improves Symbiotic Nitrogen Fixation in Vicia sativa and Lotus corniculatus Forage Legumes

2021 ◽  
Vol 3 ◽  
Author(s):  
Mariana Sotelo ◽  
Ana Claudia Ureta ◽  
Socorro Muñoz ◽  
Juan Sanjuán ◽  
Jorge Monza ◽  
...  
Keyword(s):  
Nitrogen Fixation ◽  
Rhizobium Leguminosarum ◽  
Symbiotic Nitrogen Fixation ◽  
Nitrogenase Activity ◽  
Root Nodules ◽  
Lotus Corniculatus ◽  
Vicia Sativa ◽  
Uptake Hydrogenase ◽  
Forage Crops ◽  
Mesorhizobium Loti

Biological nitrogen fixation by the Rhizobium-legume symbiosis allows the conversion of atmospheric nitrogen into ammonia within root nodules mediated by the nitrogenase enzyme. Nitrogenase activity results in the evolution of hydrogen as a result of a side reaction intrinsic to the activity of this enzyme. Some rhizobia, and also other nitrogen fixers, induce a NiFe uptake hydrogenase (Hup) to recycle hydrogen produced by nitrogenase, thus improving the efficiency of the nitrogen fixation process. In this work we report the generation and symbiotic behavior of hydrogenase-positive Rhizobium leguminosarum and Mesorhizobium loti strains effective in vetch (Vicia sativa) and birsfoot trefoil (Lotus corniculatus) forage crops, respectively. The ability of hydrogen recycling was transferred to these strains through the incorporation of hup minitransposon TnHB100, thus leading to full recycling of hydrogen in nodules. Inoculation of Vicia and Lotus plants with these engineered strains led to significant increases in the levels of nitrogen incorporated into the host legumes. The level of improvement of symbiotic performance was dependent on the recipient strain and also on the legume host. These results indicate that hydrogen recycling has the potential to improve symbiotic nitrogen fixation in forage plants.

scholarly journals A multi-sensor system provides spatiotemporal oxygen regulation of gene expression in a Rhizobium-legume symbiosis

2020 ◽  
Author(s):  
Paul J. Rutten ◽  
Harrison Steel ◽  
Graham A. Hood ◽  
Lucie McMurtry ◽  
Barney Geddes ◽  
...  
Keyword(s):  
Nitrogen Fixation ◽  
Oxygen Concentration ◽  
Rhizobium Leguminosarum ◽  
Root Nodules ◽  
Regulation Of Gene Expression ◽  
Transcriptional Analysis ◽  
Spatiotemporal Pattern ◽  
Low Oxygen

AbstractRegulation by oxygen (O2) in rhizobia is essential for their symbioses with plants and involves multiple O2 sensing proteins. Three sensors exist in the pea microsymbiont Rhizobium leguminosarum Rlv3841: hFixL, FnrN and NifA. At low O2 concentrations (1%) hFixL signals via FxkR to induce expression of the FixK transcription factor, which activates transcription of downstream genes. These include fixNOQP, encoding the high-affinity cbb3-type terminal oxidase used in symbiosis. In vitro, the Rlv3841 hFixL-FxkR-FixK cascade was active at 1% O2, and confocal microscopy showed the cascade is active in the earliest stages of Rlv3841 differentiation in nodules (zones I-II). In vitro and in vivo work showed that the hFixL-FxkR-FixK cascade also induces transcription of fnrN at 1% O2 and in the earliest stages of Rlv3841 differentiation in nodules. We confirmed past findings suggesting a role for FnrN in fixNOQP expression. However, unlike hFixL-FxkR-FixK, Rlv3841 FnrN was only active in the near-anaerobic zones III-IV of pea nodules. Quantification of fixNOQP expression in nodules showed this was driven primarily by FnrN, with minimal direct hFixL-FxkR-FixK induction. Thus, FnrN is key for full symbiotic expression of fixNOQP. Without FnrN, nitrogen fixation was reduced by 85% in Rlv3841, while eliminating hFixL only reduced fixation by 25%. The hFixL-FxkR-FixK system effectively primes the O2 response by increasing fnrN expression in early differentiation (zones I-II). In Zone III of mature nodules, the near-anaerobic conditions activate FnrN, which induces fixNOQP transcription to the level required to achieve wild-type nitrogen fixation activity. Modelling and transcriptional analysis indicates that the different O2 sensitivities of hFixL and FnrN lead to a nuanced spatiotemporal pattern of gene regulation in different nodule zones in response to changing O2 concentration. Multi-sensor O2 regulation systems are prevalent in rhizobia, suggesting the fine-tuned control they enable is common and maximizes the effectiveness of the symbioses.Author SummaryRhizobia are soil bacteria that form a symbiosis with legume plants. In exchange for shelter from the plant, rhizobia provide nitrogen fertilizer, produced by nitrogen fixation. Fixation is catalysed by the nitrogenase enzyme, which is inactivated by oxygen. To prevent this, plants house rhizobia in root nodules, which create a low oxygen environment. However, rhizobia need oxygen, and must adapt to survive low oxygen in the nodule. Key to this is regulating their genes based on oxygen concentration. We studied one Rhizobium species which uses three different protein sensors of oxygen, each turning on at a different oxygen concentration. As the bacteria get deeper inside the plant nodule and the oxygen concentration drops, each sensor switches on in turn. Our results also show that the first sensor to turn on, hFixL, primes the second sensor, FnrN. This prepares the rhizobia for the core region of the nodule where oxygen concentration is lowest and most nitrogen fixation takes place. If both sensors are removed, the bacteria cannot fix nitrogen. Many rhizobia have several oxygen sensing proteins, so using multiple sensors is likely a common strategy that makes it possible for rhizobia to adapt to low oxygen gradually in stages during symbiosis.

scholarly journals Symbiosis of selected Rhizobium leguminosarum bv. viciae strains with diverse pea genotypes: effects on biological nitrogen fixation

2017 ◽  
Vol 63 (11) ◽  
pp. 909-919 ◽  
Author(s):  
Chao Yang ◽  
Rosalind Bueckert ◽  
Jeff Schoenau ◽  
Axel Diederichsen ◽  
Hossein Zakeri ◽  
...  
Keyword(s):  
Nitrogen Fixation ◽  
Biological Nitrogen Fixation ◽  
Rhizobium Leguminosarum ◽  
Lateral Roots ◽  
Breeding Lines ◽  
Nodule Number ◽  
Pea Mutant ◽  
Greenhouse Assay ◽  
Root Tissues ◽  
Biological Nitrogen

Biological nitrogen fixation (BNF) can be improved by optimizing the interaction between the rhizobial inoculant and pea (Pisum sativum L.), leading to increased productivity and reduced nitrogen (N) fertilizer use. Eight Rhizobium leguminosarum bv. viciae strains were used to inoculate the super-nodulating pea mutant Rondo-nod3 (fix+), the hyper-nodulating pea mutant Frisson P88 Sym29, CDC Meadow commercial control, and the non-nodulating mutant Frisson P56 (nod–) to evaluate BNF in a greenhouse assay. Significant differences in strain × cultivar interactions were detected for shoot and root dry masses, which ranged from 1.8 to 4.7 g and from 0.27 to 0.73 g per plant, respectively; for nodule number on lateral roots, which ranged from 25 to 430 per plant; for amount of fixed N2, which ranged from 15 to 67 mg and from 4 to 15 mg per plant for shoot and root tissues, respectively; and for percentage of N derived from atmosphere (%Ndfa), which ranged from 37% to 61% and from 35% to 65% for shoot and root tissue, respectively. Strain × cultivar interactions in this study could contribute to identification of superior strains and pea breeding lines with genetic superiority in BNF. Nodule production in pea plants was not necessarily correlated with the amount of fixed N2, suggesting nodule activity is more important to BNF than is nodule number.

scholarly journals Auxin: at the root of nodule development?

2008 ◽  
Vol 35 (8) ◽  
pp. 651 ◽  
Author(s):  
Ulrike Mathesius
Keyword(s):  
Lateral Root ◽  
De Novo ◽  
Root Nodules ◽  
Lateral Roots ◽  
Nodule Development ◽  
Nodule Formation ◽  
Cortical Cells ◽  
Lateral Root Development ◽  
Organ Differentiation ◽  
Development And Differentiation

Root nodules are formed as a result of an orchestrated exchange of chemical signals between symbiotic nitrogen fixing bacteria and certain plants. In plants that form nodules in symbiosis with actinorhizal bacteria, nodules are derived from lateral roots. In most legumes, nodules are formed de novo from pericycle and cortical cells that are re-stimulated for division and differentiation by rhizobia. The ability of plants to nodulate has only evolved recently and it has, therefore, been suggested that nodule development is likely to have co-opted existing mechanisms for development and differentiation from lateral root formation. Auxin is an important regulator of cell division and differentiation, and changes in auxin accumulation and transport are essential for lateral root development. There is growing evidence that rhizobia alter the root auxin balance as a prerequisite for nodule formation, and that nodule numbers are regulated by shoot-to-root auxin transport. Whereas auxin requirements appear to be similar for lateral root and nodule primordium activation and organ differentiation, the major difference between the two developmental programs lies in the specification of founder cells. It is suggested that differing ratios of auxin and cytokinin are likely to specify the precursors of the different root organs.

Cytokinin production in relation to the development of pea root nodules

1976 ◽  
Vol 54 (18) ◽  
pp. 2155-2162 ◽  
Author(s):  
Kunihiko Syōno ◽  
William Newcomb ◽  
John G. Torrey
Keyword(s):  
Growth Rate ◽  
Pisum Sativum ◽  
Mitotic Activity ◽  
Rhizobium Leguminosarum ◽  
Root Nodules ◽  
Lateral Roots ◽  
Cytokinin Activity ◽  
Garden Pea ◽  
Meristematic Cells ◽  
Quantitative Changes

Quantitative changes in cytokinins were examined in developing root nodules on the lateral roots of seedlings of the garden pea Pisum sativum cv. Little Marvel infected with Rhizobium leguminosarum strain 128 C53.Cytokinin activity was highest in 2- and 3-week-old nodules, when the growth rate was high, and decreased in older nodules. The cytokinin activities of 3-week-old nodules of various sizes were positively correlated with mitotic indices. In 3- and 4-week-old nodules most of the cytokinins were present in the white meristematic tip and not in the infected nitrogen-fixing or senescent cells. Since high cytokinin levels were associated with nodules having high mitotic rates or with the meristematic cells, it is proposed that cytokinins influence nodule morphogenesis by regulating the mitotic activity of the nodule meristem.

Transfer Cells in the Root Epidermis of Atriplex hastata L. As a Response to Salinity: a Comparative Cytological and X-Ray Microprobe Investigation

1978 ◽  
Vol 5 (6) ◽  
pp. 739 ◽  
Author(s):  
D Kramer ◽  
WP Anderson ◽  
J Preston
Keyword(s):  
Root Apex ◽  
Transfer Cells ◽  
Cytological Investigation ◽  
Xylem Parenchyma ◽  
Salt Treatment ◽  
Selective Uptake ◽  
X Ray ◽  
Root Epidermis ◽  
Wall Ingrowths ◽  
Parenchyma Cells

A cytological investigation has been made of the roots of the halophyte Atriplex hastata L. Transfer cells developed in the epidermis in response to salt treatment. They occurred only in a zone 1-3 mm behind the root apex and possessed a labyrinth only in their outer tangential walls (facing the root environment). When the epidermis was damaged, the adjacent exodermal cells then developed wall ingrowths in saline conditions. Ontogenetically this differentiation is correlated with the formation of the Casparian strip and the disintegration of the vessel contents. The X-ray microanalysis data on deep-frozen hydrated root specimens indicate that the epidermal transfer cells concentrate K+, and exclude Cl-, relative to the medium. It is concluded that the epidermal transfer cells function in selective uptake of K+ which is subsequently transported laterally into the stele and secreted into the vessels by the xylem parenchyma cells.

Occurrence of transfer cells in vascular parenchyma of Hieracium florentinum roots

1976 ◽  
Vol 54 (13) ◽  
pp. 1458-1471 ◽  
Author(s):  
Linda J. Letvenuk ◽  
R. L. Peterson
Keyword(s):  
Lateral Root ◽  
Secondary Xylem ◽  
Lateral Roots ◽  
Transfer Cells ◽  
Main Root ◽  
Sieve Elements ◽  
Parenchyma Cells ◽  
Vascular Parenchyma ◽  
Xylem Elements ◽  
Root Stele

In the roots of Hieracium florentinum plants grown in hydroponic nutrient cultures, vascular parenchyma cells adjacent to both xylem and phloem conducting elements develop wall ingrowths and become transfer cells. Xylem transfer cells occur around the protoxylem elements and secondary xylem elements at the base of the junction of a lateral root with the main root stele and along the xylem elements of the lateral root for some distance into the lateral root. Phloem transfer cells occur adjacent to sieve elements in the phloem regions of the main root stele which have connections with the lateral root phloem and adjacent to sieve elements in the lateral root. Transfer cells were absent in the vascular parenchyma of the main root stele not associated with lateral roots.

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