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

Schwintzer, Christa R.; Berry, Alison M.; Disney, Lynn D.

doi:10.1139/b82-098

Cited by 78 publications

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“…The prefixation zone (zone 2) contains enlarging cortical cells. Some of them are infected and in turn enlarge more than uninfected cells, while being gradually filled with hyphae from the center outward (Lalonde, 1979;Schwintzer et al, 1982;Berry and Sunell, 1990). When they are completely filled with hyphae, provesicles are formed; they represent terminal swellings on hyphae or on short side branches (Fontaine et al, 1984).…”

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“…Both Ag12 and Ara12 show significant homology to prokaryotic serine proteases of the subtilisin family (Barr, 1991; Siezen , 1991). Homology is particularly high around the four residues forming the active site of subtilases (Barr, 1991;Siezen et al, 1991; Figures 4 and 5). Subtilases are produced as preproenzymes, therefore remaining inactive until secreted and processed (Siezen et al, 1991).…”

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A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development.

et al. 1995

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To identify genes specifically expressed during early stages of actinorhizal nodule development, a cDNA library made from poly(A) RNA from root nodules of Alnus glutinosa was screened differentially with nodule and root cDNA, respectively. Seven nodule-enhanced and four nodule-specific cDNA clones were isolated. By using in situ hybridization, two of the nodule-specific cDNAs were shown to be expressed at the highest levels in infected cells before the onset of nitrogen fixation; one of them, ag12 @. glutinosa), was examined in detail. Sequencing showed that ag12 codes for a serine protease of the subtilisin (EC 3.4.21.14) family. Subtilisins previously appeared to be limited to microorganlsms. However, subtilisin-like serine proteases have recently been found in archaebacteria, fungi, and yeasts as well as in mammals; a plant subtilisin has also been sequenced. In yeast and mammals, subtilases are responsible for processing peptide hormones. A homolog of ag12, ara12, was identified in Arabidopsis; it was expressed in all organs, and its expression levels were highest during silique development. Hence, our study shows that subtilases are also involved in both symbiotic and nonsymbiotic processes in plant development. INTRODUCTIONActinorhizal root nodules are induced by actinomycetes of the genus Frankia on severa1 woody dicotyledonous plant species belonging to eight different plant families (Benson and Silvester, 1993). The tissue organization of single lobes of these nodules resembles that of lateral roots in that they contain a central vascular bundle. However, they lack root caps and have both infected and uninfected cortical cells (Berry and Sunell, 1990). The formation of these lobes is initiated in the pericycle. The structure of actinorhizal nodules is dissimilar to nodules induced by Azorhizobium, Bradyrhizobium, or Rhizobium on legume roots (Hirsch, 1992), which are initiated in the root cortex of the plant and contain peripheral vascular bundles, yet similar to that of nodules induced by Bradyrhizobium or Rhizobium on Parasponia, the only non-legume nodulated by Rhizobium (Trinick, 1979).Similar to nodules formed on temperate legumes, actinorhizal nodule lobes have an indeterminate growth pattern due to the presence of an apical meristem that differentiates continuously in a proximal direction (Berry and Sunell, 1990; Hirsch, 1992). A part of the new cortical cells formed by the meristem is subsequently infected by bacterial hyphae. This continuous production and infection of new cells leads to a 1 To whom correspondence should be addressed. zonation of the nodule lobe. Thus, starting from the apical meristem, we can distinguish four zones. The meristematic zone (zone 1) consists of small dividing cells that do not contain bacteria. The prefixation zone (zone 2) contains enlarging cortical cells. Some of them are infected and in turn enlarge more than uninfected cells, while being gradually filled with hyphae from the center outward (Lalonde, 1979;Schwintzer et al., 1982;Berry and Sunell, 1990). When...

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A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development.

et al. 1995

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“…Like those in culture, symbiotic vesicles make new septa and increase in size as they mature. In Myrica gale nodules, vesicle senescence is a gradual process initiated midway through the growing season and completed by the end of the growing season (14). Only vegetative hyphae and, in some nodules, spores overwinter in the root nodules.…”

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Developmental potential of Frankia vesicles

Schultz

Benson

1989

J Bacteriol

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The ability of nitrogenase-containing Frankia sp. strain CpIl vesicles to regrow vegetative hyphae is demonstrated. Vesicles attached to hyphae in N2-fixing Cpll cultures and sucrose gradient-isolated vesicles exhibited hyphal outgrowths when incubated in certain defined liquid media. Single or multiple hyphal extensions grew out from the vesicles.The onset of nitrogen fixation by Frankia strains in aerobic environments is preceded by the appearance of differentiated cellular structures, the frankial vesicles. Vesicles contain nitrogenase, both in culture (8,11,15) and in the N2-fixing root nodules formed on actinorhizal plants (13,18 screw-cap polycarbonate centrifuge tubes. The pellets were suspended in cold 10 mM potassium phosphate buffer (pH 6.5; buffer A) to a final volume of 6 ml and held on ice. Just prior to homogenization, 20 ml of cold 60% (wt/wt) sucrose in buffer A was added to each tube. The contents were homogenized with a Polytron tissue homogenizer in an ice bath for five cycles of 1-min homogenization followed by a 30-s rest to allow cooling of the suspension. Each suspension was examined microscopically to monitor the release of vesicles from the vegetative hyphae. Following homogenization, an additional 9 ml of cold 60% sucrose was added to each tube to yield a final concentration of 50% sucrose. The homogenates were overlayered with cold 10% (vol/vol) glycerol in buffer A, and the glycerol-sucrose gradients were centrifuged at 35,000 x g for 1 h at 4°C. Vesicles were removed from the glycerol-sucrose interface with Pasteur pipettes and washed by repeated centrifugation in buffer A at 40,000 x g for 15 min at 4°C.Regrowth potential of the isolated vesicles was tested by diluting the vesicles to about 105/ml in growth medium in 15-ml serum vials (Wheaton Scientific, Millville, N.Y.), and incubating them in air at 30°C. Vesicle concentration was kept low to avoid ambiguity in identification of the source of new hyphae. The percentage of vesicles with hyphal outgrowths was determined from direct counts as the ratio of the number of regrown vesicles to the total number of vesicles in several microscopic fields at 400x magnification with the phase-contrast optics of an Olympus BH-2 microscope (Olympus Corp., Woodbury, N.Y.). An Olympus OM-1 camera mounted on the microscope was used to document vesicle regrowth.Vesicles formed hyphal outgrowths when incubated as described above in the following media: succinate (0.5%) with and without NH4Cl (11), propionate (0.3%) or pyruvate (0.3%) with and without NH4Cl (9), QMOD medium (6) without lipid supplement, and R-2A broth (12). The percentages of regrown vesicles after 5 days were as follows: 8% and 10% for succinate medium with and without NH4Cl, respectively; 3% and 2% for propionate medium with and without NH4Cl, respectively; and <1% for the pyruvatecontaining media, the QMOD medium, and the R-2A broth. Regrowth was also observed in these same media solidified with agar (1.5%; Difco Laboratories, Detroit, Mich.) or with 1.0% agar and 6.0% gelatin (bo...

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“…Due to the activity of the apical meristem, a developmental gradient of infected cells is formed in the cortex which can be divided into four zones. The meristematic zone (zone 1) consists of small dividing cells that are not infected by Frankia. The infection zone (zone 2) contains enlarging cortical cells some of which are infected by Frankia and are gradually filled with Frankia hyphae from the center outward (Lalonde, 1979 ;Schwintzer et al, 1982 ;Berry and Sunell, 1990). In cells completely filled with hyphae, provesicles are formed as terminal swellings on hyphae (Fontaine et al, 1984).…”

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Gene expression in ineffective actinorhizal nodules ofAlnus glutinosa

Guan¹,

Wolters²,

Dijk³

et al. 1996

Acta Botanica Gallica

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Summary.-Several Frankia strains have been shown to induce ineffective, i.e.non-nitrogen fixing nodules, sometimes in a host-plant dependent manner. Previous studies have demonstrated that the resistance to nodulation of Alnus glutinosa by ineffective Frankia strains is genetically determined. In this study, ineffective nodules induced on susceptible Alnus glutinosa clones by soil suspensions from a local swamp were analysed cytologically. Comparisons with effective nodules showed that ineffective nodules contain higher amounts of polyphenols than effective nodules, indicating a plant defense reaction. Polyphenols were found even in the infected cortical cells. In situ hybridization with a Frankia antisense 168 rRNA probe showed that Frankia is degraded at an early stage of development of infected cells. The mRNAs of two plant genes, ag12 and ag13, which had been found to be expressed in the infected cells of effective nodules, were localized in ineffective nodules. Their expression patterns seemed to be analogous in both types of nodules.Resume.-Plusieurs souches de Frankia induisent des nodules non-effectifs, c'est-a-dire non fixateurs d'azote, parfois sous Ia dependance de Ia plante-h6te. De precedentes etudes ont montre que Ia resistance d'Ainus glutinosa a l'infection par des souches de Frankia non-effectives repond a un determinisme genetique. Au cours de Ia presents etude, des nodules non-effectifs, induits sur des clones susceptibles d'Ainus glutinosa par des suspensions de sols locaux, ont fait l'objet d'une analyse cytologique. Une comparaison avec des nodules effectifs montre que les nodules non-effectifs contiennent plus de polyphenols, ce qui indique qu'une reaction de defense a lieu. Des polyphenols ont egalement ete observes dans les cellules infectees du cortex. Une hybridation in situ avec une sonde antisens pour I'ARNr 168 de Frankia montre que Frankia subit Ires tot une degradation lors du developpement des cellules infectees. La localisation des ARNm d'ag12 et ag13, deux genes de Ia plante qui sont exprimes dans les cellules infectees des nodules effectifs, a ete realises. Une expression analogue semble exister dans les deux types de nodules.

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

Cited by 78 publications

References 25 publications

A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development.

A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development.

Developmental potential of Frankia vesicles

Gene expression in ineffective actinorhizal nodules ofAlnus glutinosa

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