Host–endophyte interactions in effective and ineffective nodules induced by the endophyte of Myrica gale

1983 ◽  
Vol 61 (11) ◽  
pp. 2898-2909 ◽  
Author(s):  
Kathryn A. VandenBosch ◽  
John G. Torrey
Keyword(s):  
Nitrogenase Activity ◽  
Root Nodules ◽  
Seedling Development ◽  
Nodule Development ◽  
Nodule Formation ◽  
Cortical Tissue ◽  
Intercellular Spaces ◽  
Cortical Cells ◽  
Myrica Gale ◽  
Infected Cells

Suspensions of crushed root nodules of Myrica gale containing the actinomycete Frankia induced nodule formation on roots of seedlings of M. gale and Comptonia peregrina grown in nutrient water culture. Nodules formed on M. gale were normal in structure and exhibited nitrogenase activity (measured as acetylene reduction) and provided the necessary nitrogen for seedling development. These effective nodules showed typical external and internal structure with the endophyte developing both vesicles and sporangia within cortical cells of the host tissue. Small nodules formed on C. peregrina representing the primary nodule stage. They lacked nitrogenase activity and were termed ineffective. Vesicles failed to develop within these ineffective nodules. However, sporangia were formed in infected cells and within intercellular spaces of the nodule cortical tissue. In addition, prominent amyloplasts occurred in infected cells of the ineffective nodules, a feature lacking in effective nodules. Exogenously supplied combined nitrogen increased seedling growth but did not improve nodule development or endophyte morphogenesis in the ineffective nodules.

Determinate development of nodule roots in actinomycete-induced root nodules of Myrica gale

1978 ◽  
Vol 56 (11) ◽  
pp. 1357-1364 ◽  
Author(s):  
John G. Torrey ◽  
Dale Callaham
Keyword(s):  
Root Development ◽  
Root Nodules ◽  
Cortical Cell ◽  
Gas Diffusion ◽  
Nodule Development ◽  
Nodule Formation ◽  
Low Oxygen ◽  
Cortical Cells ◽  
Continuous Growth ◽  
Myrica Gale

Young seedlings of Myrica gale L. grown in water culture were inoculated with a nodule suspension containing the effective actinomycete which induced root nodule formation. Nodule development was followed from initiation to nodule lobe formation and nodule root development using living materials and fixed nodules sectioned for light microscopy. After root hair infection and prenodule formation, three stages were observed: nodule lobe formation, a transition or arrested state, and nodule root development. The primary nodule lobe meristem originates endogenously and its formation involves pericycle, endodermis, and cortical cell derivatives. The lobe develops slowly to about 2 mm in length while the cortical cells are invaded by the actinomycete endophyte. After a period of arrest of variable duration, from a few days to several weeks, the nodule lobe meristem begins altered development, forming the elongate nodule root which undergoes slow but continuous growth to about 3- to 4-cm final length. New nodule lobe primordia are initiated endogenously at the base of existing nodules lobes, ultimately forming a cluster of nodule roots. Each nodule root, which elongates at about 0.1–1.0 mm per day, has a terminal apical meristem with reduced root cap formation and produces a modified root structure possessing an elaborate cortical intercellular space system and a reduced central cylinder. Nodule root growth is distinctive in that it shows strong negative geotropism. The endophyte is restricted to cortical cells of the nodule lobe and is totally absent from tissues of the nodule root. A probable role for nodule roots is to facilitate gas diffusion to the nitrogen-fixing endophyte site in the nodule lobe when nodules occur under conditions of low oxygen tension.

Effective and ineffective root nodules in Myrica faya

1976 ◽  
Vol 194 (1116) ◽  
pp. 285-293 ◽  
Keyword(s):  
Root Nodules ◽  
Light And Electron Microscopy ◽  
Nodule Formation ◽  
Culture Solution ◽  
Myrica Gale ◽  
Main Site ◽  
Myrica Faya ◽  
Modern Methods ◽  
Infected Cells ◽  
Nodule Endophytes

In cross-inoculation trials, inocula containing the nodule endophytes of Myrica gale, M. cerifera, M. cordifolia and M. pilulifera respectively were applied to the roots of young plants of M. faya Ait. growing in nitrogen-free culture solution. All four inocula induced nodule formation, and except where the M. gale inoculum had been used the nodules were of effective type and enabled the plants bearing them to grow nearly as well as other M. faya plants associated with the normal endophyte. The nodules induced by the M. gale endophyte were very numerous, but remained small and fixed no significant amount of nitrogen, and were thus ineffective. Light and electron microscopy showed that in the effective nodules induced by the normal endophyte or by that of M. cordifolia , the endophyte was confined to a layer 1-2 cells deep near the middle of the nodule cortex, and that in respect of the width of the hyphae and their production of club-shaped internally subdivided vesicles, the endophytes resembled closely those in the nodules of the few other species of Myrica that have been studied by modern methods of microscopy. In ineffective nodules the disposition of the infected cells was unchanged, but within the cells only a sparse development of the endophyte was observed, and no vesicles were found. The finding that nodules lacking vesicles showed little or no fixation is consistent with other evidence that the vesicles normally produced by non-legume nodule endophytes are the main site of nitrogen fixation.

Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity, and shoot development in Myrica gale

1982 ◽  
Vol 60 (6) ◽  
pp. 746-757 ◽  
Author(s):  
Christa R. Schwintzer ◽  
Alison M. Berry ◽  
Lynn D. Disney
Keyword(s):  
Root Nodule ◽  
Nitrogenase Activity ◽  
Shoot Development ◽  
Infected Tissue ◽  
Actinorhizal Plants ◽  
Seasonal Patterns ◽  
Cortical Cells ◽  
Myrica Gale ◽  
Nodule Biomass ◽  
Infected Cells

Myrica gale L. populations growing in central Massachusetts were observed throughout the ice-free season. Nitrogenase activity appeared in mid-May shortly after budbreak, was at its maximum between late June and mid-August, and disappeared in late October after all leaves had fallen. Growth of overwintering nodules began in early May and was largely complete by mid-July. Most nodules (88%) lived for 3 years or less and 61% of the nodule biomass present in autumn was produced during the current season.Colonizing hyphae of the Frankia sp. endophyte were seen throughout the year in partially expanded cortical cells near the nodule lobe apex. Vesicles first appeared in mature cortical cells coincident with the onset of nitrogenase activity in mid-May, occupied the bulk of the infected tissue during the summer, and disappeared as nitrogenase activity ceased in late October. Evidence is presented that the vesicles are the site of nitrogenase activity and are newly produced each season in freshly formed nodule lobe tissue. Sporangia frequently formed in mature infected cells in nodules at one site but were rare at another. The processes described here in M. gale are probably typical of winter-deciduous actinorhizal plants.

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.

scholarly journals Silencing of Putative Cytokinin Receptor Histidine Kinase1 Inhibits Both Inception and Differentiation of Root Nodules in Arachis hypogaea

2018 ◽  
Vol 31 (2) ◽  
pp. 187-199 ◽  
Author(s):  
Anindya Kundu ◽  
Maitrayee DasGupta
Keyword(s):  
Arachis Hypogaea ◽  
Root Nodules ◽  
Nodule Development ◽  
Response Regulators ◽  
Cytokinin Signaling ◽  
Cortical Cells ◽  
Cytokinin Receptor ◽  
Undifferentiated State ◽  
Mitotic Cyclin ◽  
Infected Cells

Rhizobia–legume interaction activates the SYM pathway that recruits cytokinin signaling for induction of nodule primordia in the cortex. In Arachis hypogaea, bradyrhizobia invade through natural cracks developed in the lateral root base and are directly endocytosed in the cortical cells to generate the nodule primordia. To unravel the role of cytokinin signaling in A. hypogaea, RNA-interference (RNAi) of cytokinin receptor histidine-kinase1 (AhHK1) was done. AhHK1-RNAi downregulated the expression of type-A response regulators such as AhRR5 and AhRR3 along with several symbiotic genes, indicating that both cytokinin signaling and the SYM pathway were affected. Accordingly, there was a drastic downregulation of nodulation in AhHK1-RNAi roots and the nodules that developed were ineffective. These nodules were densely packed, with infected cells having a higher nucleo-cytoplasmic ratio and distinctively high mitotic index, where the rod-shaped rhizobia failed to differentiate into bacteroids within spherical symbiosomes. In accordance with the proliferating state, expression of a mitotic-cyclin AhCycB2.1 was higher in AhHK1-RNAi nodules, whereas expression of a retinoblastoma-related (AhRBR) nodule that restrains proliferation was lower. Also, higher expression of the meristem maintenance factor WUSCHEL-RELATED HOMEOBOX5 correlated with the undifferentiated state of AhHK1-RNAi nodules. Our results suggest that AhHK1-mediated cytokinin signaling is important for both inception and differentiation during nodule development in A. hypogaea.

Seasonal pattern of energy use, respiration, and nitrogenase activity in root nodules of Myrica gale

1983 ◽  
Vol 61 (11) ◽  
pp. 2937-2942 ◽  
Author(s):  
Christa R. Schwintzer ◽  
John D. Tjepkema
Keyword(s):  
Energy Cost ◽  
Energy Use ◽  
Nitrogenase Activity ◽  
Root Nodules ◽  
Seasonal Pattern ◽  
Uptake Ratio ◽  
Experimental Conditions ◽  
Myrica Gale ◽  
Net Production ◽  
N Requirement

Annual CO2 evolution, H2 evolution, and C2H2 reduction were measured in root nodules from a vigorous Myrica gale stand in a Massachusetts peatland at 3-week intervals in 1980. Nodule activity was approximately the same under the experimental conditions (excised nodules reducing C2H2) as in nature (attached nodules reducing N2) and the CO2 evolution to O2 uptake ratio averaged 1.07. Nitrogenase activity was first detectable in late May, reached its maximum [Formula: see text] in mid-July, and disappeared in late October. The seasonal pattern of CO2 evolution was similar except that it continued at low rates when nitrogenase activity was absent. Hydrogen evolution was barely detectable. The energy cost of nitrogen fixation, expressed as the molar CO2:C2H4 ratio, was relatively low [Formula: see text] throughout the period of substantial nitrogenase activity and had a mean annual value of 4.9. Annual N2 fixation was estimated to be 2.8 g N m−2year−1, contributing about 33% of the annual N requirement measured in 1979. Annual C use by nodules was about 21.0 g C m−2 year−1. If this C were available for additional net production, it would increase it by about 5.5%.

Effect of rhizobia and soil nitrate on the establishment and functioning of the soybean symbiosis in the field

1984 ◽  
Vol 35 (2) ◽  
pp. 149 ◽  
Author(s):  
DF Herridge ◽  
RJ Roughley ◽  
J Brockwell
Keyword(s):  
Soil Depth ◽  
Root Nodules ◽  
Xylem Sap ◽  
Progressive Increase ◽  
Rhizobium Japonicum ◽  
Nodule Development ◽  
Initial Increase ◽  
Nodule Formation ◽  
Mineral N ◽  
Nodule Initiation

The symbiosis of the root-nodules of Bragg soybean [Glycine max (L.) Merrill] and the relative dependence of the plants on symbiotic and soil sources of N were evaluated in an experiment conducted on a vertisol which was high in organic- and mineral-N, free of Rhizobium japonicum, and where poor nodulation was characteristic of inoculated, new sowings. Effective inoculant containing R. japonicum strain CB 1809 was sprayed into the seed bed at three rates of application (10-fold intervals). Increasing rates of inoculant led to greater numbers of rhizobia in the rhizosphere and in the soil, and to improved nodulation. Uninoculated plants did not nodulate. High soil NO-3 (30 �g N/g, top 30 cm) did not prevent prompt, abundant colonization of rhizospheres by the bacteria from the inoculant, but nodule initiation was delayed and nodule development was retarded until 42 days after sowing. There was an acceleration in nodule formation and development between 42 and 62 days which coincided with a depletion of NO-3 from the top 60 cm of the soil profile. Nodulated and unnodulated soybeans took up NO-3 at similar times and rates to a soil depth of 90 cm; only unnodulated plants utilized soil NO-3 below 90 cm. Vacuum-extracted stem (xylem) exudate was sampled from plants throughout growth and analysed for nitrogenous solutes. The proportion of ureide-N relative to total-solutes-N in xylem sap was used as an index of symbiotic N2-fixation. The initial increase in concentrations of ureides coincided with the period of accelerated nodule formation and development between 42 and 62 days. Thereafter, there was a progressive increase in ureide concentrations in nodulated plants, and the levels were related to rate of inoculation, extent of nodulation, and to the decline in concentrations of soil NO-3. Ureide concentrations in unnodulated plants remained low throughout. The quantities of NO-3-N and �-NH2- N in xylem sap were not related to nodulation. The differences between treatments in terms of whole-plant N and grain N were less than predicted from the symbiotic parameters. This indicated that soybeans compensated for symbiotic deficiencies by more efficient exploitation of soil N and/or by more efficient redistribution of vegetative N into grain N, and that nodulation and soil NO-3 were interactive and complementary in meeting the N requirements of the crop.

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 Excess nitrate induces nodule greening and reduces transcript and protein expression levels of soybean leghaemoglobins

2020 ◽  
Vol 126 (1) ◽  
pp. 61-72
Author(s):  
Mengke Du ◽  
Zhi Gao ◽  
Xinxin Li ◽  
Hong Liao
Keyword(s):  
Nitrogenase Activity ◽  
Expression Patterns ◽  
Bioinformatic Analysis ◽  
Nodule Development ◽  
Nodule Formation ◽  
N Availability ◽  
Soybean Plants ◽  
Systematic Identification ◽  
Biological Nitrogen ◽  
Soybean Nodulation

Abstract Background and Aims Efficient biological nitrogen fixation (BNF) requires leghaemoglobin (Lb) to modulate oxygen pressure in nodules. Excess N supply severely inhibits BNF through effects on Lb during nodulation. As yet, a systematic identification and characterization of Lb-encoding genes in soybean has not been reported. Methods The effects of N on BNF were studied in soybean plants inoculated with rhizobia and exposed to excess or low N availability in hydroponic cultures. To identify soybean Lb proteins, BLAST searches were performed on the Phytozome website. Bioinformatic analysis of identified GmLbs was then carried out to investigate gene structure, protein homology and phylogenetic relationships. Finally, quantitative real-time PCR was employed to analyse the expression patterns of soybean Lb genes in various tissues and in response to high N availability. Key Results Excess N significantly accelerated nodule senescence and the production of green Lb in nodules. In total, seven haemoglobin (Hb) genes were identified from the soybean genome, with these Hb genes readily split into two distinct clades containing predominantly symbiosis-associated or non-symbiotic Hb members. Expression analysis revealed that all of the symbiosis-associated Lbs except GmLb5 were specifically expressed in nodules, while the non-symbiotic GmHbs, GmHb1 and GmHb2, were predominantly expressed in leaves and roots, respectively. Among identified GmLbs, GmLb1–4 are the major Lb genes acting in soybean nodulation, and each one is also significantly suppressed by exposure to excess N. Conclusions Taken together, the results show that excess N inhibits BNF by reducing nodule formation, Lb concentration and nitrogenase activity. The characteristics of the entire Hb family were analysed, and we found that GmLb1–4 are closely associated with nodule development and N2 fixation. This works forms the basis for further investigations of the role of Lbs in soybean nodulation.

A D-pinitol transporter, LjPLT11, regulates plant growth and nodule development in Lotus japonicus

2021 ◽  
Author(s):  
Lu Tian ◽  
Leru Liu ◽  
Shaoming Xu ◽  
Rufang Deng ◽  
Pingzhi Wu ◽  
...  
Keyword(s):  
Plant Growth ◽  
Nitrogenase Activity ◽  
Lotus Japonicus ◽  
Nodule Development ◽  
Xenopus Laevis Oocytes ◽  
Oxygen Species ◽  
In Planta ◽  
Osmotic Balance ◽  
Infected Cells ◽  
Functional Analyses

Abstract Polyol transporters (PLTs) have been functionally characterized in yeast and Xenopus laevis oocytes as H +-symporters with broad substrate specificity, but little is known about their physiological roles in planta. To extend this knowledge we investigated roles of LjPLT11 in Lotus japonicus-Mesorhizobium symbiosis. Functional analyses of the LjPLT11 in yeast characterized this protein as an energy-independent transporter of xylitol, two O-methyl inositols, xylose and galactose. We also showed that LjPLT11 is located on peribacteroid membranes (PBMs) and functions as a facilitative transporter of D-pinitol within infected cells of L. japonicus nodules. Knockdown of LjPLT11 (LjPLT11i) in L. japonicus accelerated plant growth under nitrogen-sufficiency, but resulted in abnormal bacteroids with corresponding reductions in nitrogenase activity in nodules and plant growth in the nitrogen-fixing symbiosis. LjPLT11i nodules had higher osmotic pressure in cytosol and fewer in bacteroids than wildtype nodules both three and four weeks after inoculation of M. loti. Levels and distributions of reactive oxygen species were also perturbed in infected cells of four-week-old nodules in LjPLT11i plants. The results indicate that LjPLT11 plays a key role in adjustment of levels of its substrate pinitol, and thus maintenance of osmotic balance in infected cells and PBM stability during nodule development.

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