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PubMed2006

Identification of ethylene-mediated protein changes during nodulation in Medicago truncatula using proteome analysis.

Ethylene has been hypothesised to be a regulator of root nodule development in legumes, but its molecular mechanisms of action remain unclear. The skl mutant is an ethylene-insensitive legume mutant showing a hypernodulation phenotype when inoculated with its symbiont Sinorhizobium meliloti. We used the skl mutant to study the ethylene-mediated protein changes during nodule development in Medicago truncatula. We compared the root proteome of the skl mutant to its wild-type in response to the ethylene precursor aminocyclopropane carboxylic acid (ACC) to study ethylene-mediated protein expression in root tissues. We then compared the proteome of skl roots to its wild-type after Sinorhizobium inoculation to identify differentially displayed proteins during nodule development at 1 and 3 days post inoculation (dpi). Six proteins (pprg-2, Kunitz proteinase inhibitor, and ACC oxidase isoforms) were down-regulated in skl roots, while three protein spots were up-regulated (trypsin inhibitor, albumin 2, and CPRD49). ACC induced stress-related proteins in wild-type roots, such as pprg-2, ACC oxidase, proteinase inhibitor, ascorbate peroxidase, and heat-shock proteins. However, the expression of stress-related proteins such as pprg-2, Kunitz proteinase inhibitor, and ACC oxidase, was down-regulated in inoculated skl roots. We hypothesize that during early nodule development, the plant induces ethylene-mediated stress responses to limit nodule numbers. When a mutant defective in ethylene signaling, such as skl, is inoculated with rhizobia, the plant stress response is reduced, resulting in increased nodule numbers.

Amino Acid Sequence↗

PubMed2000

Construction of transgenic pea lines with modified expression of diamine oxidase and modified nodulation responses with exogenous putrescine.

Diamine oxidase (DAO) might influence pea nodule development either by regulating the peroxide-driven cross-linking of glycoproteins in the infection thread matrix or by modifying the metabolism of diamines and polyamines in host cells. Transformed lines of pea (Pisum sativum) with the coding sequence for DAO (PSAO-1) in sense orientation behind a tissue-specific promoter (pENOD12A) showed strong co-suppression of DAO activity in extracts from nodules and epicotyls, whereas the antisense constructs were relatively unaffected. No difference in nodule number was observed between transformed lines and controls, suggesting that DAO does not normally have an essential role in nodule initiation. However, lines showing co-suppression of DAO were less sensitive to the inhibitory effects of exogenous putrescine and less active in the cross-linking of matrix glycoprotein, indicating that putrescine-derived products of DAO activity could retard nodule development. Inoculation of co-suppressed lines with Rhizobium strain B661 (a lipopolysaccharide-defective mutant) resulted in more extreme impairment of nodule development and nitrogen fixation capacity, relative to lines with normal levels of DAO, which suggests that DAO may serve to reduce the endogenous level of inhibitory diamines or polyamines in nodules under physiological stress. We conclude that the most critical role of DAO in pea nodule development is apparently in the regulation of diamine levels in host tissues.

Amine Oxidase (Copper-Containing)↗

PubMed2001

The Bradyrhizobium japonicum hsfA gene exhibits a unique developmental expression pattern in cowpea nodules.

The Bradyrhizobium japonicum host-specific fixation gene hsfA was identified as essential for nitrogen fixation on cowpea, but not required for nitrogen fixation on soybean or siratro. The DNA sequence of the hsfA promoter contains a consensus RpoN, -24/-12 binding site, suggesting the involvement of a regulatory protein that binds to an upstream activating sequence (UAS). To further explore the regulation of this interesting gene, serial deletions of the hsfA promoter were made and fused with the beta-glucuronidase (GUS) gene. The HsfA3 deletion, containing 60 bp 5' of the -24/-12 sequence, showed a similar level of GUS expression to that shown by the longest fusion construct (HsfA1), containing 464 bp of upstream sequence. In contrast, the HsfA4-GUS fusion, containing only 20 bp 5' of the -24/-12 region, showed no GUS activity, delimiting the location of a putative UAS to a 40-bp region. During nodule development, GUS expression first appeared in nodules 12 days postinoculation (dpi) and reached a maximum level of expression in approximately 17-day-old nodules. By 28 dpi, HsfA-GUS expression had returned to a low, basal level. These data were consistent with the detection of hsfA mRNA by in situ hybridization in 17-day-old nodules, but not in 28-day-old nodules. In contrast to the stage-specific expression in cowpea, HsfA-GUS expression increased with nodule development in HsfA3-inoculated soybean. These data indicate that HsfA expression is regulated in cowpea in a unique developmental manner and that the DNA regulatory regions that control this expression are confined to a short, promoter-proximal region.

Bacterial Proteins↗

PubMed2000

Inhibitory effects of 22-oxa-calcitriol and all- trans retinoic acid on the growth of a canine osteosarcoma derived cell-line in vivo and its pulmonary metastasis in vivo.

Pulmonary metastasis is a major cause of death and a major obstacle to the successful treatment of canine osteosarcoma. However, the residual capacity of the neoplasia for differentiation and its susceptibility to undergo apoptosis may be used to suppress its growth and metastatic properties. The highly metastasizing POS (HMPOS) canine osteosarcoma cell line which preferentially metastasize to the lungs was used to test the possible efficacy of 22-oxa-calcitriol (OCT) and all- trans retinoic acid (ATRA) to inhibit growth and pulmonary metastasis of the subcutaneously grown osteosarcoma in nude mice. Treatments in vitro, morphologically elongated and increased alkaline phosphatase activity and staining of cells. Tumour growth in vivo was inhibited significantly and the combination treatment of OCT and ATRA (OCT + ATRA) exerted a synergistic and stronger suppression at concentration of 1.0 microg kg(-1)body weight when given subcutaneously three times a week for 5 weeks. The subcutaneous tumours of the control mice consisted of osteoblast-like cells and isolated chondroblast-like cells, but formed several areas of osteoid and increased amount of collagen tissue in all treated mice. Pinpoint macrometastatic nodules developed only in all control mice. Micrometastatic nodule developed only in two of six mice treated with ATRA. However, nodule size and number, and lung wet weight were all reduced significantly. Metastasis were not seen in the mice treated with OCT or OCT + ATRA. This study demonstrated that inhibition of growth and pulmonary metastasis was induced by subcutaneous treatment with these drugs and suggest that both its differentiating and apoptotic inducing activities may be responsible for the antitumour effects. These drugs may be useful in the clinic as an adjunct for the treatment of canine osteosarcoma.

Alkaline Phosphatase↗

PubMed1968

Calcium and Nodulation in Subterranean Clover (Trifolium subterraneum L.).

From a study of the effects of Ca ions on the nodulation of subterranean clover in flowing culture solutions it is concluded that root infection or nodule initiation has a higher Ca requirement than either nodule development or host plant growth in the presence of fixed nitrogen.Increasing Ca concentration from 246 to 720 mum had no effect on growth of the host plant but increased the number of nodules from 7 to 24 per plant. Decreasing Ca concentration from 246 to 4 mum progressively decreased both plant growth and nodule numbers.It is suggested that nodule infection or initiation required higher solution concentration of Ca than nodule development since transferring plants after 10 days in lower Ca treatments to 720 mum Ca for 7 days did not increase nodule numbers above those on plants treated continuously at low Ca. Similarly transferring plants from 720 mum Ca to lower Ca treatments did not decrease nodule numbers much below those on plants grown continuously at 720 mum Ca even though growth was depressed. Once initiated, nodule development proceeded at concentrations of Ca too low for plant growth.The high Ca requirement for root infection or nodule initiation was not thought to be due to effects on survival or growth of Rhizobium and could not be related to effects of Ca on a number of relevant processes:-tap root length, root hair development, or lateral root initiation.

Journal Article↗

PubMed1979

Development of the nitrogen-fixing and protein-synthesizing apparatus of bacteroids in pea root nodules.

Some aspects of root nodule development of Pisum sativum inoculated with Rhizobium leguminosarum were examined. 1. Nitrogenase activity (measured as acetylene reduction) appears to be preceded by leghemoglobin synthesis (measured immunologically). 2. Syntheses of component I and component II of nitrogenase are not strictly coordinated. Synthesis of component I starts before component II. 3. Plant and bacteroid protein synthesis (measured by [35S]sulfate labeling) in root nodules declines rapidly during nodule development. Corresponding with this decline is a decrease in quantity and quality of rRNA.

Fabaceae↗

PubMed2006

Nuclear DNA endoreduplication and expression of the mitotic inhibitor Ccs52 associated to determinate and lupinoid nodule organogenesis.

Lotus japonicus determinate nodules differ greatly from indeterminate nodules in their organogenesis and morphological characteristics, whereas Lupinus albus lupinoid nodules share features of determinate and indeterminate nodules. The mitotic inhibitor Ccs52A is essential for endoreduplication and ploidy-dependent cell enlargement during symbiotic cell differentiation in Medicago truncatula indeterminate nodules. ccs52A homolog genes were isolated from lupin and lotus nodules; the deduced Ccs52A proteins showed high sequence similarity with other Cdh-1-type activators of the anaphase-promoting complex and were grouped with A-type Ccs52 proteins from different plants. In lupin, ccs52A expression was restricted to the earlier stages of nodule development, whereas ccs52A transcripts accumulated in lotus nodule primordia and, to a lesser extent, in mature nodules. Nodule development in Lupinus albus involved a progressive increase in nuclear and cellular size and ploidy level; similarly, Lotus japonicus nodules contained polyploid nuclei and enlarged cells in the infected zone. Nevertheless, in situ hybridization experiments showed the highest ccs52A expression in the inner cortex cells of the lupin nodule primordium, probably associated to the increased size of these cells in mature nodules. In view of our results, Ccs52A-mediated endoreduplication appears to be a universal mechanism required for nodule cell differentiation during the establishment of nitrogen-fixing symbioses.

Amino Acid Sequence↗

PubMed2002

Effect of exogenous flavonoids on nodulation of pea (Pisum sativum L.).

Selected flavonoids that are known as inducers and a suppressor of nodulation (nod) genes of the symbiotic bacterium Rhizobium leguminosarum bv. viciae were tested for their effect on symbiosis formation with garden pea as the host. A solid substrate was omitted from the hydroponic growing system in order to prevent losses of flavonoids due to adsorption and degradation. The presumed interaction of the tested flavonoids with nod genes has been verified for the genetic background of strain 128C30. A stimulatory effect of a nod gene inducer naringenin on symbiotic nodule number formed per plant 14 d after inoculation was detected at concentrations of 0.1 and 1 micro g ml(-1) nutrient solution. At 10 micro g ml(-1), the highest concentration tested, naringenin was already inhibitory. By contrast, nodulation was negatively affected by a nod gene suppressor, quercetin, at concentrations above 1 micro g ml(-1), as well as by another tested nod gene inducer, hesperetin. The deleterious effect of hesperetin might be due to its toxicity or to the toxicity of its degradation product(s) as indicated by the inhibition of root growth. Both the stimulatory effect of naringenin and the inhibitory effect of quercetin on nodule number were more pronounced at earlier stages of nodule development as revealed with specific staining of initial nodules. The lessening of the flavonoid impact during nodule development was ascribed to the plant autoregulatory mechanisms. Feedback regulation of nodule metabolism might also be responsible for the fact that the naringenin-conditioned increase in nodule number was not accompanied by any increase in nitrogenase activity. By contrast, the inhibitory action of quercetin and hesperetin on nodule number was associated with decreases in total nitrogenase activity. Naringenin also stimulated root hair curling (RHC) as one of the earliest nodulation responses at concentrations of 1 and 10 microg ml(-1), however, the same effect was exerted by the nod gene suppressor, quercetin, suggesting that feedback regulatory mechanisms control RHC in the range of nodulation-inhibiting high flavonoid concentrations. The comparison of the effect of the tested flavonoids in planta with nod gene activity response showed a two orders of magnitude shift to higher concentrations. This shift is explained by the absorption and degradation of flavonoids by both the symbionts during 3 d intervals between hydroponic solution changes. The losses were 99, 96.4, and 90% of the initial concentration of 10 micro g ml(-1) for naringenin, hesperetin, and quercetin, respectively.

Flavanones↗

PubMed1998

Patterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata.

At the base of adventitious root primordia, located on the stem of the tropical legume Sesbania rostrata, nitrogen-fixing nodules are formed upon inoculation with the microsymbiont Azorhizobium caulinodans. This pattern of nodule development presents features of indeterminate and determinate nodules in early and later stages, respectively. A S. rostrata cDNA clone homologous to early nodulin ENOD40 genes was isolated from a cDNA library of developing stem nodules. SrENOD40-1 contained the conserved regions I and II of other ENOD40 genes. By reverse transcriptase PCR, enhanced SrENOD40-1 expression was observed in the adventitious root primordia between 4 and 8 h after inoculation with A. caulinodans. In situ hybridization showed that SrENOD40-1 transcripts, present around the central vascular bundle of the uninfected root primordia, were strongly enhanced upon induction of nodule development. De novo SrENOD40-1 expression was observed in the initiating and growing nodule primordia and around vascular bundles. When cell type specification sets in, the expression became pronounced in cells derived from the meristematic regions. In other parts of the plant, weak SrENOD40-1 expression was associated with vascular bundles and was observed in leaf and stipule primordia.

Amino Acid Sequence↗

PubMed2002

Shoot control of root development and nodulation is mediated by a receptor-like kinase.

In legumes, root nodule organogenesis is activated in response to morphogenic lipochitin oligosaccharides that are synthesized by bacteria, commonly known as rhizobia. Successful symbiotic interaction results in the formation of highly specialized organs called root nodules, which provide a unique environment for symbiotic nitrogen fixation. In wild-type plants the number of nodules is regulated by a signalling mechanism integrating environmental and developmental cues to arrest most rhizobial infections within the susceptible zone of the root. Furthermore, a feedback mechanism controls the temporal and spatial susceptibility to infection of the root system. This mechanism is referred to as autoregulation of nodulation, as earlier nodulation events inhibit nodulation of younger root tissues. Lotus japonicus plants homozygous for a mutation in the hypernodulation aberrant root (har1) locus escape this regulation and form an excessive number of nodules. Here we report the molecular cloning and expression analysis of the HAR1 gene and the pea orthologue, Pisum sativum, SYM29. HAR1 encodes a putative serine/threonine receptor kinase, which is required for shoot-controlled regulation of root growth, nodule number, and for nitrate sensitivity of symbiotic development.

Alleles↗

PubMed2000

Carbon metabolism in developing soybean root nodules: the role of carbonic anhydrase.

A full-length cDNA clone encoding carbonic anhydrase (CA) was isolated from a soybean nodule cDNA library. In situ hybridization and immunolocalization were performed in order to assess the location of CA transcripts and protein in developing soybean nodules. CA transcripts and protein were present at high levels in all cell types of young nodules, whereas in mature nodules they were absent from the central tissue and were concentrated in cortical cells. The results suggested that, in the earlier stages of nodule development, CA might facilitate the recycling of CO2 while at later stages it may facilitate the diffusion of CO2 out of the nodule system. In parallel, sucrose metabolism was investigated by examination of the temporal and spatial transcript accumulation of sucrose synthase (SS) and phosphoenolpyruvate carboxylase (PEPC) genes, with in situ hybridization. In young nodules, high levels of SS gene transcripts were found in the central tissue as well as in the parenchymateous cells and the vascular bundles, while in mature nodules the levels of SS gene transcripts were much lower, with the majority of the transcripts located in the parenchyma and the pericycle cells of the vascular bundles. High levels of expression of PEPC gene transcripts were found in mature nodules, in almost all cell types, while in young nodules lower levels of transcripts were detected, with the majority of them located in parenchymateous cells as well as in the vascular bundles. These data suggest that breakdown of sucrose may take place in different sites during nodule development.

Amino Acid Sequence↗

PubMed1990

Sequential induction of nodulin gene expression in the developing pea nodule.

A set of cDNA clones have been characterized that represent early nodulin mRNAs from pea root nodules. By RNA transfer blot analyses, the different early nodulin mRNAs were found to vary in time course of appearance during the development of the indeterminate pea root nodule. In situ hybridization studies demonstrated that the transcripts were located in different zones, representing subsequent steps in development of the central tissue of the root nodule. ENOD12 transcripts were present in every cell of the invasion zone, whereas ENOD5, ENOD3, and ENOD14 transcripts were restricted to the infected cells in successive but partially overlapping zones of the central tissue. We conclude that the corresponding nodulin genes are expressed at subsequent developmental stages. The amino acid sequence derived from the nucleotide sequences of the cDNAs, in combination with the localization data, showed that ENOD5 is an arabinogalactan-like protein involved in the infection process, whereas ENOD3 and ENOD14 have a cysteine cluster suggesting that these are metal-binding proteins. Furthermore, we showed that there is a clear difference in the way Rhizobium induced the infection-related early nodulin genes ENOD5 and ENOD12. A factor acting over a long distance induced the ENOD12 gene, whereas a factor acting over a short distance activated the ENOD5 gene.

Amino Acid Sequence↗

PubMed1996

Gene structure and differential regulation of the Rhizobium-induced peroxidase gene rip1.

Primary expression of the Rhizobium meliloti-induced peroxidase gene rip1 occurs prior to nodule morphogenesis, specifically at the site of impending rhizobial infection (D. Cook, D. Dreyer, D. Bonnet, M. Howell, E. Nony, K. VandenBosch [1995] Plant Cell 7: 43-55). We examined the distribution and structure of rip1 transcript throughout nodule development. We determined that expression of rip1 in root tips is correlated with the competence of this zone for symbiotic association, whereas after rhizobial infection rip1 transcript is specifically associated with the zone of nodule development, including nascent nodule primordia. rip1 transcripts are characterized by multiple polyadenylation sites distributed within 200 to 400 bp of the translation stop site, and a single major transcription initiation site in close proximity to the rip1 open reading frame. Thus, rip1 expression is likely to be mediated through effects on a single transcription unit. Immediately 5' of the rip1 transcription unit DNA sequence analysis identified a 377-bp DNA element containing extensive repeat structure that is widely distributed in the Medicago truncatula genome.

Base Sequence↗

PubMed2006

Redox regulation of peroxiredoxin and proteinases by ascorbate and thiols during pea root nodule senescence.

Redox factors contributing to nodule senescence were studied in pea. The abundance of the nodule cytosolic peroxiredoxin but not the mitochondrial peroxiredoxin protein was modulated by ascorbate. In contrast to redox-active antioxidants such as ascorbate and cytosolic peroxiredoxin that decreased during nodule development, maximal extractable nodule proteinase activity increased progressively as the nodules aged. Cathepsin-like activities were constant throughout development but serine and cysteine proteinase activities increased during senescence. Senescence-induced cysteine proteinase activity was inhibited by cysteine, dithiotreitol, or E-64. Senescence-dependent decreases in redox-active factors, particularly ascorbate and peroxiredoxin favour decreased redox-mediated inactivation of cysteine proteinases.

Antioxidants↗

PubMed2004

The galactolipid digalactosyldiacylglycerol accumulates in the peribacteroid membrane of nitrogen-fixing nodules of soybean and Lotus.

The peribacteroid membrane (PBM) surrounding nitrogen fixing rhizobia in the nodules of legumes is crucial for the exchange of ammonium and nutrients between the bacteria and the host cell. Digalactosyldiacylglycerol (DGDG), a galactolipid abundant in chloroplasts, was detected in the PBM of soybean (Glycine max) and Lotus japonicus. Analyses of membrane marker proteins and of fatty acid composition confirmed that DGDG represents an authentic PBM lipid of plant origin and is not derived from the bacteria or from plastid contamination. In Arabidopsis, DGDG is known to accumulate in extraplastidic membranes during phosphate deprivation. However, the presence of DGDG in soybean PBM was not restricted to phosphate limiting conditions. Complementary DNA sequences corresponding to the two DGDG synthases, DGD1 and DGD2 from Arabidopsis, were isolated from soybean and Lotus. The two genes were expressed during later stages of nodule development in infected cells and in cortical tissue. Because nodule development depends on the presence of high amounts of phosphate in the growth medium, the accumulation of the non-phosphorus galactolipid DGDG in the PBM might be important to save phosphate for other essential processes, i.e. nucleic acid synthesis in bacteroids and host cells.

Arabidopsis Proteins↗

PubMed1984

Rhizobium phaseoli symbiotic mutants with transposon Tn5 insertions.

Rhizobium phaseoli CFN42 DNA was mutated by random insertion of Tn5 from suicide plasmid pJB4JI to obtain independently arising strains that were defective in symbiosis with Phaseolus vulgaris but grew normally outside the plant. When these mutants were incubated with the plant, one did not initiate visible nodule tissue (Nod-), seven led to slow nodule development (Ndv), and two led to superficially normal early nodule development but lacked symbiotic nitrogenase activity (Sna-). The Nod- mutant lacked the large transmissible indigenous plasmid pCFN42d that has homology to Klebsiella pneumoniae nitrogenase (nif) genes. The other mutants had normal plasmid content. In the two Sna- mutants and one Ndv mutant, Tn5 had inserted into plasmid pCFN42d outside the region of nif homology. The insertions of the other Ndv mutants were apparently in the chromosome. They were not in plasmids detected on agarose gels, and, in contrast to insertions on indigenous plasmids, they were transmitted in crosses to wild-type strain CFN42 at the same frequency as auxotrophic markers and with the same enhancement of transmission by conjugation plasmid R68.45. In these Ndv mutants the Tn5 insertions were the same as or very closely linked to mutations causing the Ndv phenotype. However, in two mutants with Tn5 insertions on plasmid pCFN42d, an additional mutation on the same plasmid, rather than Tn5, was responsible for the Sna- or Ndv phenotype. When plasmid pJB4JI was transferred to two other R. phaseoli strains, analysis of symbiotic mutants was complicated by Tn5-containing deleted forms of pJB4JI that were stably maintained.

Bacterial Proteins↗

PubMed1994

Fine-needle aspiration cytology of suture granulomas of the breast: a potential pitfall in the cytologic diagnosis of recurrent breast cancer.

The fine-needle aspirates of three cases of suture granulomas of the breast area following mastectomy, lumpectomy, or axillary node dissection were reviewed. The original histologic diagnoses were mucinous (colloid) carcinoma, intraductal carcinoma, and low-grade phyllodes tumor. In two patients a new nodule developed in the surgical scar, and in the third a nodule developed in the axilla 2 cm away from the scar. The cellularity of the aspirates ranged from low to moderate, and all three cases contained variable numbers of spindled cells and fragments of cellular stroma. Multinucleated giant cells characteristic of suture granulomas were absent in all cases. Abundant metachromatic amorphous background material was present in one case, which was interpreted as recurrent mucinous carcinoma. The remaining cases were interpreted as suspicious for recurrent neoplasm. Upon excision, all were suture granulomas with fibroblastic proliferation. Suture granulomas can both clinically and cytologically mimic recurrent malignancy. The predominance of spindled cells and dissimilarity to the original tumor appear to be the most helpful features to cytologically distinguish suture granuloma from recurrent carcinoma in the absence of the characteristic multinucleated giant cells.

Adult↗

PubMed1981

Light and electron microscopic studies of nodule structure of alfalfa.

Light and electron microscopy was used to establish the structural organisation of the developing nodule of alfalfa. In these nodules three distinct regions were noted: (1) the base region, site of original infection where the nodule is attached to the root and now composed of degenerating nodule tissue, (2) the central region, or active region composed of nodule cells containing tightly packed bacteroids surrounding a central vacuole, and (3) the meristematic region, a site of new growth, behind which newly formed cells are continually invaded. The ongoing infection process accompanying continued nodule development provided the opportunity to study the release of Rhizobium cells from the infection threads. In the nodules of alfalfa it would appear that the Rhizobium cells are released from infection thread into the nodule tissue in two different ways: (i) release with infection thread membrane and (ii) release in thin-walled vesicular structures. Thus it is concluded that Rhizobium cells are surrounded by the infection thread membrane when they are released from the infection thread into nodule tissue.

Medicago sativa↗