Academic literature on the topic 'Frankia symbiosis'
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Journal articles on the topic "Frankia symbiosis"
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Benson, David R., James M. Brooks, Ying Huang, Derek M. Bickhart, and Juliana E. Mastronunzio. "The Biology of Frankia sp. Strains in the Post-Genome Era." Molecular Plant-Microbe Interactions® 24, no. 11 (November 2011): 1310–16. http://dx.doi.org/10.1094/mpmi-06-11-0150.
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Progress in understanding symbiotic determinants involved in the N2-fixing actinorhizal plant symbioses has been slow but steady. Problems persist with studying the bacterial contributions to the symbiosis using traditional microbiological techniques. However, recent years have seen the emergence of several genomes from Frankia sp. strains and the development of techniques for manipulating plant gene expression. Approaches to understanding the bacterial side of the symbiosis have employed a range of techniques that reveal the proteomes and transcriptomes from both cultured and symbiotic frankiae. The picture beginning to emerge provides some perspective on the heterogeneity of frankial populations in both conditions. In general, frankial populations in root nodules seem to maintain a rather robust metabolism that includes nitrogen fixation and substantial biosynthesis and energy-generating pathways, along with a modified ammonium assimilation program. To date, particular bacterial genes have not been implicated in root nodule formation but some hypotheses are emerging with regard to how the plant and microorganism manage to coexist. In particular, frankiae seem to present a nonpathogenic presence to the plant that may have the effect of minimizing some plant defense responses. Future studies using high-throughput approaches will likely clarify the range of bacterial responses to symbiosis that will need to be understood in light of the more rapidly advancing work on the plant host.
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Popovici, Jean, Gilles Comte, �milie Bagnarol, Nicole Alloisio, Pascale Fournier, Floriant Bellvert, C�dric Bertrand, and Maria P. Fernandez. "Differential Effects of Rare Specific Flavonoids on Compatible and Incompatible Strains in the Myrica gale-Frankia Actinorhizal Symbiosis." Applied and Environmental Microbiology 76, no. 8 (February 26, 2010): 2451–60. http://dx.doi.org/10.1128/aem.02667-09.
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ABSTRACT Plant secondary metabolites, and specifically phenolics, play important roles when plants interact with their environment and can act as weapons or positive signals during biotic interactions. One such interaction, the establishment of mutualistic nitrogen-fixing symbioses, typically involves phenolic-based recognition mechanisms between host plants and bacterial symbionts during the early stages of interaction. While these mechanisms are well studied in the rhizobia-legume symbiosis, little is known about the role of plant phenolics in the symbiosis between actinorhizal plants and Frankia genus strains. In this study, the responsiveness of Frankia strains to plant phenolics was correlated with their symbiotic compatibility. We used Myrica gale, a host species with narrow symbiont specificity, and a set of compatible and noncompatible Frankia strains. M. gale fruit exudate phenolics were extracted, and 8 dominant molecules were purified and identified as flavonoids by high-resolution spectroscopic techniques. Total fruit exudates, along with two purified dihydrochalcone molecules, induced modifications of bacterial growth and nitrogen fixation according to the symbiotic specificity of strains, enhancing compatible strains and inhibiting incompatible ones. Candidate genes involved in these effects were identified by a global transcriptomic approach using ACN14a strain whole-genome microarrays. Fruit exudates induced differential expression of 22 genes involved mostly in oxidative stress response and drug resistance, along with the overexpression of a whiB transcriptional regulator. This work provides evidence for the involvement of plant secondary metabolites in determining symbiotic specificity and expands our understanding of the mechanisms, leading to the establishment of actinorhizal symbioses.
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Popovici, Jean, Vincent Walker, Cédric Bertrand, Floriant Bellvert, Maria P. Fernandez, and Gilles Comte. "Strain specificity in the Myricaceae - Frankia symbiosis is correlated to plant root phenolics." Functional Plant Biology 38, no. 9 (2011): 682. http://dx.doi.org/10.1071/fp11144.
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Plant secondary metabolites play an important role in the interaction between plants and their environment. For example, mutualistic nitrogen-fixing symbioses typically involve phenolic-based recognition between host plants and bacteria. Although these mechanisms are well studied in the rhizobia–legume symbiosis, little is known about the role of plant phenolics in the symbiosis between actinorhizal plants and the actinobacterium Frankia. In this study, the responsiveness of two Myricaceae plant species, Myrica gale L. and Morella cerifera L., to Frankia inoculation was correlated with the plant–bacteria compatibility status. Two Frankia strains were inoculated: ACN14a, compatible with both M. gale and M. cerifera and Ea112, compatible only with M. cerifera. The effect of inoculation on root phenolic metabolism was evaluated by metabolic profiling based on high-performance liquid chromatography (HPLC) and principal component analysis (PCA). Our results revealed that: (i) both Frankia strains induced major modifications in root phenolic content of the two Myricaceae species and (ii) strain-dependant modifications of the phenolic contents were detected. The main plant compounds differentially affected by Frankia inoculation are phenols, flavonoids and hydroxycinnamic acids. This work provides evidence that during the initial phases of symbiotic interactions, Myricaceae plants adapt their secondary metabolism in accordance with the compatibility status of Frankia bacterial strains.
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Berg, R. Howard. "Frankia forms infection threads." Canadian Journal of Botany 77, no. 9 (December 18, 1999): 1327–33. http://dx.doi.org/10.1139/b99-073.
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Frankia forms symbioses with a great variety of plant hosts, and because nodule development is under plant control, this results in an interesting diversity in the structure of developing symbiotic cells. However, it is apparent that, in all these symbioses, the microsymbiont Frankia follows a similar pattern of development within symbiotic cells of the nodule: the cell is invaded by formation of an infection thread containing invasive hyphae sheathed in plant cell wall material, parasitic vegetative hyphae proliferate by branching from this infection thread, and N2-fixing symbiotic vesicles differentiate from tips of these vegetative hyphae. Infection threads are recognized by their ontogeny and morphology, being the cell-invasive structures in the case of the former and straight-growing hyphae in the case of the latter. Formation of infection threads is a feature shared in common with legumes. Unlike in legumes, the infection thread in actinorhizae is not defined by the presence of sheathing plant cell wall material; all forms of the bacterium have this. Rather than using the term "encapsulation," which suggests a bacterial origin, it is proposed the term "interfacial matrix" be used to describe this plant cell wall material separating Frankia from host cytoplasm.Key words: Frankia, infection thread, interfacial matrix, microsymbiont, nodule, symbiosis.
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Mastronunzio, J. E., Y. Huang, and D. R. Benson. "Diminished Exoproteome of Frankia spp. in Culture and Symbiosis." Applied and Environmental Microbiology 75, no. 21 (September 11, 2009): 6721–28. http://dx.doi.org/10.1128/aem.01559-09.
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ABSTRACT Frankia species are the most geographically widespread gram-positive plant symbionts, carrying out N2 fixation in root nodules of trees and woody shrubs called actinorhizal plants. Taking advantage of the sequencing of three Frankia genomes, proteomics techniques were used to investigate the population of extracellular proteins (the exoproteome) from Frankia, some of which potentially mediate host-microbe interactions. Initial two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis analysis of culture supernatants indicated that cytoplasmic proteins appeared in supernatants as cells aged, likely because older hyphae lyse in this slow-growing filamentous actinomycete. Using liquid chromatography coupled to tandem mass spectrometry to identify peptides, 38 proteins were identified in the culture supernatant of Frankia sp. strain CcI3, but only three had predicted export signal peptides. In symbiotic cells, 42 signal peptide-containing proteins were detected from strain CcI3 in Casuarina cunninghamiana and Casuarina glauca root nodules, while 73 and 53 putative secreted proteins containing signal peptides were identified from Frankia strains in field-collected root nodules of Alnus incana and Elaeagnus angustifolia, respectively. Solute-binding proteins were the most commonly identified secreted proteins in symbiosis, particularly those predicted to bind branched-chain amino acids and peptides. These direct proteomics results complement a previous bioinformatics study that predicted few secreted hydrolytic enzymes in the Frankia proteome and provide direct evidence that the symbiosis succeeds partly, if not largely, because of a benign relationship.
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Anne-Emmanuelle, Hay, Boubakri Hasna, Buonomo Antoine, Rey Marjolaine, Meiffren Guillaume, Cotin-Galvan Laetitia, Comte Gilles, and Herrera-Belaroussi Aude. "Control of Endophytic Frankia Sporulation by Alnus Nodule Metabolites." Molecular Plant-Microbe Interactions® 30, no. 3 (March 2017): 205–14. http://dx.doi.org/10.1094/mpmi-11-16-0235-r.
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A unique case of microbial symbiont capable of dormancy within its living host cells has been reported in actinorhizal symbioses. Some Frankia strains, named Sp+, are able to sporulate inside plant cells, contrarily to Sp− strains. The presence of metabolically slowed-down bacterial structures in host cells alters our understanding of symbiosis based on reciprocal benefits between both partners, and its impact on the symbiotic processes remains unknown. The present work reports a metabolomic study of Sp+ and Sp− nodules (from Alnus glutinosa), in order to highlight variabilities associated with in-planta sporulation. A total of 21 amino acids, 44 sugars and organic acids, and 213 secondary metabolites were detected using UV and mass spectrometric–based profiling. Little change was observed in primary metabolites, suggesting that in-planta sporulation would not strongly affect the primary functionalities of the symbiosis. One secondary metabolite (M27) was detected only in Sp+ nodules. It was identified as gentisic acid 5-O-β-d-xylopyranoside, previously reported as involved in plant defenses against microbial pathogens. This metabolite significantly increased Frankia in-vitro sporulation, unlike another metabolite significantly more abundant in Sp− nodules [M168 = (5R)-1,7-bis-(3,4-dihydroxyphenyl)-heptane-5-O-β-d-glucopyranoside]. All these results suggest that the plant could play an important role in the Frankia ability to sporulate in planta and allow us to discuss a possible sanction emitted by the host against less cooperative Sp+ symbionts.
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Markham, John H., and Chris P. Chanway. "Does past contact reduce the degree of mutualism in the Alnus rubra - Frankia symbiosis?" Canadian Journal of Botany 77, no. 3 (August 20, 1999): 434–41. http://dx.doi.org/10.1139/b98-227.
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Although most vascular plants have symbiotic relationships with soil microbes, and there is an extensive theoretical literature on the evolution of mutualism, there has been little experimental examination of the evolution of mutualism between plants and their microbial symbionts. We inoculated red alder (Alnus rubra Bong.) seedlings from three high- and three low-elevation populations with crushed nodule suspensions containing the nitrogen fixing bacterium Frankia from either the parent trees (familiar strains) or the other plant population sampled within the parent watershed (unfamiliar strains). The inoculated seedlings were planted on three high- and three low-elevation sites. Growth was monitored over the second and third year following planting, after which the whole plants were harvested. The proportion of nitrogen derived from fixation was estimated from the ratio of stable nitrogen isotopes in the harvested leaves. On low-elevation sites, which had high soil nitrogen, plants with familiar Frankia strains were half the size and derived less fixed nitrogen from their symbionts compared with plants inoculated with unfamiliar Frankia strains. On high-elevation sites, which had low soil nitrogen, the type of inoculum had little effect on plant performance, although plants with familiar inoculum were consistently larger than plants with unfamiliar inoculum. These results suggest that the degree of mutualism in this symbiosis depends on environmental conditions and may decrease with time.Key words: coevolution, Frankia, Alnus rubra, mutualism, nitrogen fixation, symbiosis.
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Pujic, Petar, Nicole Alloisio, Guylaine Miotello, Jean Armengaud, Danis Abrouk, Pascale Fournier, and Philippe Normand. "The Proteogenome of Symbiotic Frankia alni in Alnus glutinosa Nodules." Microorganisms 10, no. 3 (March 18, 2022): 651. http://dx.doi.org/10.3390/microorganisms10030651.
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Omics are the most promising approaches to investigate microbes for which no genetic tools exist such as the nitrogen-fixing symbiotic Frankia. A proteogenomic analysis of symbiotic Frankia alni was done by comparing those proteins more and less abundant in Alnus glutinosa nodules relative to N2-fixing pure cultures with propionate as the carbon source. There were 250 proteins that were significantly overabundant in nodules at a fold change (FC) ≥ 2 threshold, and 1429 with the same characteristics in in vitro nitrogen-fixing pure culture. Nitrogenase, SuF (Fe–Su biogenesis) and hopanoid lipids synthesis determinants were the most overabundant proteins in symbiosis. Nitrogenase was found to constitute 3% of all Frankia proteins in nodules. Sod (superoxide dismutase) was overabundant, indicating a continued oxidative stress, while Kats (catalase) were not. Several transporters were overabundant including one for dicarboxylates and one for branched amino acids. The present results confirm the centrality of nitrogenase in the actinorhizal symbiosis.
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Ribeiro, Ana, Inês Graça, Katharina Pawlowski, and Patrícia Santos. "Actinorhizal plant defence-related genes in response to symbiotic Frankia." Functional Plant Biology 38, no. 9 (2011): 639. http://dx.doi.org/10.1071/fp11012.
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Actinorhizal plants have become increasingly important as climate changes threaten to remake the global landscape over the next decades. These plants are able to grow in nutrient-poor and disturbed soils, and are important elements in plant communities worldwide. Besides that, most actinorhizal plants are capable of high rates of nitrogen fixation due to their capacity to establish root nodule symbiosis with N2-fixing Frankia strains. Nodulation is a developmental process that requires a sequence of highly coordinated events. One of these mechanisms is the induction of defence-related events, whose precise role in a symbiotic interaction remains to be elucidated. This review summarises what is known about the induction of actinorhizal defence-related genes in response to symbiotic Frankia and their putative function during symbiosis.
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Wilkinson, Helen, Alice Coppock, Bethany L. Richmond, Beatriz Lagunas, and Miriam L. Gifford. "Plant–Environment Response Pathway Regulation Uncovered by Investigating Non-Typical Legume Symbiosis and Nodulation." Plants 12, no. 10 (May 12, 2023): 1964. http://dx.doi.org/10.3390/plants12101964.
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Nitrogen is an essential element needed for plants to survive, and legumes are well known to recruit rhizobia to fix atmospheric nitrogen. In this widely studied symbiosis, legumes develop specific structures on the roots to host specific symbionts. This review explores alternate nodule structures and their functions outside of the more widely studied legume–rhizobial symbiosis, as well as discussing other unusual aspects of nodulation. This includes actinorhizal-Frankia, cycad-cyanobacteria, and the non-legume Parasponia andersonii-rhizobia symbioses. Nodules are also not restricted to the roots, either, with examples found within stems and leaves. Recent research has shown that legume–rhizobia nodulation brings a great many other benefits, some direct and some indirect. Rhizobial symbiosis can lead to modifications in other pathways, including the priming of defence responses, and to modulated or enhanced resistance to biotic and abiotic stress. With so many avenues to explore, this review discusses recent discoveries and highlights future directions in the study of nodulation.
Dissertations / Theses on the topic "Frankia symbiosis"
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Bajwa, Balwinder Singh. "Molecular charecterisation of Frankia and Alder- Frankia symbiosis in Eastern India." Thesis, University of North Bengal, 2004. http://hdl.handle.net/123456789/918.
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Nguyen, Thi Thanh Van. "The actinorhizal symbiosis of the earliest divergent Frankia cluster." Doctoral thesis, Stockholms universitet, Institutionen för ekologi, miljö och botanik, 2017. http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-139969.
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In recent years, the need to reduce reliance on synthetic nitrogen fertilizer has led to extensive research on biological nitrogen fixation, especially on root nodule symbioses. My study focuses on actinorhizal symbioses, the symbiotic interactions between members of nitrogen-fixing soil actinobacteria from the genus Frankia and a diverse group of plants from eight families, collectively called actinorhizal plants. Frankia cluster II has been shown to be sister to all other clusters. Thus, one of my aims was to gain insight into this cluster to get more information about the evolution of actinorhizal symbioses. The first sequenced genome of a member from this cluster Candidatus Frankia datiscae Dg1 originated from Pakistan. This strain contains the canonical nod genes nodABC responsible for the synthesis of lipochitooligosaccharide Nod factors. In this thesis, we obtained three Frankia inocula from North America (USA), one from Europe (France), one from Asia (Japan) and one from Oceania (Papua New Guinea). Thirteen metagenomes were sequenced based on gDNA isolated from root nodules of Datisca glomerata (Datiscaceae), Ceanothus thyrsiflorus (Rhamnaceae), Coriaria myrtifolia and Coriaria arborea (Coriariaceae). This study shows that members of Frankia cluster II come in teams, helping to explain the ability of cluster II to nodulate a wide host range, four families from two orders. The inoculum from Papua New Guinea, the only sequenced strain from the Southern Hemisphere so far, contains a new Frankia species, which was proposed as Candidatus Frankia meridionalis. All cluster II strains in this study contain the canonical nod genes nodABC, with the exception of the strain from Papua New Guinea which contains only nodB’C. All North American metagenomes also contain the sulfotransferase gene nodH. This gene shows host plant-specific expression in that it was expressed in nodules of C. thyrsiflorus but not in D. glomerata. Phylogenetic analysis and transposase frequencies of the new genomes strongly support the hypothesis that the extension of the cluster II host range from Coriaria to Datisca occurred in Eurasia and that cluster II strains came to North America via the Bering Strait. To acquire more information of the influence of the host plant on the behavior of the microsymbionts, the bacterial metabolism in nodules of D. glomerata (Cucurbitales) and C. thyrsiflorus (Rosales) were compared at the level of transcription. The system to protect nitrogenase from oxygen in Ceanothus nodules seems to be more efficient than in Datisca nodules, whereas the bacterial nitrogen metabolism is likely to be similar in both host plants. The amino acid profile of D. glomerata nodules shows that the nitrogenous solutes are dominated by glutamate and arginine, supporting the suggestion that Frankia in D. glomerata nodules exports an assimilated form of nitrogen, most likely arginine. Thus, our data show that cluster II Frankia strains differ from all other Frankia clusters with regard to the presence of the canonical nod genes and their nitrogen metabolism in symbiosis.At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: Manuscript. Paper 3: Manuscript.
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Oakley, Brian B. "The ecology and biogeography of the Ceanothus-Frankia symbiosis in California /." Thesis, Connect to this title online; UW restricted, 2003. http://hdl.handle.net/1773/5589.
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Benabdoun, Faïza Meriem. "Étude moléculaire des étapes précoces de la symbiose actinorhizienne Casuarina-Frankia : analyse fonctionnelle des gènes de la plante hôte contrôlant l’infection." Thesis, Montpellier 2, 2012. http://www.theses.fr/2012MON20103/document.
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Étude moléculaire des étapes précoces de la symbiose actinorhizienne Casuarina-Frankia : analyse fonctionnelle des gènes de la plante hôte contrôlant l'infectionPlus de 80% des plantes peuvent établir une symbiose racinaire avec des champignons de l'ordre des Glomales et former des endomycorhizes à arbuscules (AM). En revanche, seules certaines espèces appartenant à dix familles d'angiospermes réunies dans le Clade des Eurosidées I peuvent établir une symbiose racinaire fixatrice d'azote. Il s'agit d'une part, des plantes de la famille des légumineuses (Fabacées) et de Parasponia associées à Rhizobium et d'autre part, des plantes actinorhiziennes associées à l'actinomycète Frankia. Comme chez les légumineuses, la symbiose actinorhizienne aboutit à la formation de nodosités (ou « nodules »), siège de la fixation d'azote par les bactéries. Cependant, contrairement aux nodules des légumineuses, le nodule actinorhizien présente une structure et un développement s'apparentant aux racines latérales. L'étude des nodosités actinorhiziennes est donc particulièrement intéressante tant pour rechercher les spécificités de cette symbiose, que pour déterminer quelles sont les caractéristiques communes avec les légumineuses. Nous avons étudié le rôle du gène CCaMK dans le processus symbiotique et l'organogenèse nodulaire chez l'arbre actinorhizien Casuarina glauca. CCaMK code pour une protéine kinase dépendante du calcium et de la calmoduline (« calcium and calmodulin dependent protein kinase »). Dans la cascade de signalisation conduisant à la nodulation et à la mycorhization chez les légumineuses, ce gène est positionné en aval des oscillations calciques (« calcium spiking ») qui ont lieu durant les premières étapes de l'interaction symbiotique. CCaMK jouerait un rôle dans la perception et le décodage des oscillations calciques, ainsi que leur transduction aux différents composants contrôlant les endosymbioses racinaires. Nous avons suivi l'expression spatio-temporelle de la fusion transcriptionnelle PromCgCCaMK::GUS au cours de la nodulation et montré que celle-ci était corrélée à la présence de Frankia tout au long du processus symbiotique, soulignant ainsi le rôle clé de CCaMK dans l'infection. Par ailleurs, nous avons cherché à déterminer l'importance du domaine autoinhibiteur de la protéine CCaMK dans l'activation du processus d'organogenèse du nodule. Pour cela, nous avons réalisé et introduit chez C. glauca des constructions géniques de CgCCaMK permettant l'expression de formes tronquées constitutivement actives, car dépourvues du domaine autoinhibiteur/CaM. Nous avons aussi utilisé des formes tronquées du gène MtCCaMK de Medicago truncatula. L'expression de ces formes tronquées de CCaMK a révélé que la levée de l'autoinhibition induit la formation de nodules spontanés indépendamment de l'actinobactérie Frankia. Les résultats obtenus suggèrent que la protéine dérégulée est capable de réactiver la voie de signalisation, ainsi que les gènes situés en aval de CCaMK, qui sont nécessaires à l'organogenèse nodulaire.Mots clés : Casuarina glauca, Frankia, CCaMK, infection, autoinhibition, nodules spontanésMolecular study of the early stages of actinorhizal symbiosis Casuarina-Frankia: functional analysis of the host plant genes controlling the infectionMore than 80% of plant species are able to develop arbuscular mycorrhizal (AM) symbiosis in association with glomeromycete fungi. In contrast, only some species of the Eurosid I clade, confined to four orders and ten Angiosperm families, are able to form nitrogen-fixing root nodule symbioses with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia associated with Rhizobium bacteria and actinorhizal plants associated with the actinomycete Frankia. Similarly to Legumes, the actinorhizal symbiosis results in the formation of nitrogen-fixing root nodules. However, unlike legume nodule, the actinorhizal nodule has a same origin and structure than a lateral root. Thus, the study of actinorhizal nodules is of particular interest not only for investigating its specific properties but also, for determining common characteristics shared with legume nodules.We have studied the role of CgCCaMK gene during the symbiotic process and nodule organogenesis in the actinorhizal tree Casuarina glauca. CCaMK encodes a calcium and calmodulin dependent protein kinase. In the signalisation cascade leading to both nodulation and mycorrhization in legumes, this gene is acting downstream the calcium oscillations (« calcium spiking ») that occur during the early steps of the symbiotic interaction. It has been suggested that these calcium oscillations are decoded and transduced by the CCaMK protein.We have monitored the spatio-temporal expression of a PromCgCCaMK::GUS fusion during actinorhizal nodulation and have shown that reporter gene expression was correlated with the presence of Frankia along the symbiotic process. This data highlights the role of CgCCaMK during Frankia infection. In addition, we have investigated the role of the CCaMK autoinhibitory/CaM domain in actinorhizal nodule organogenesis. To achieve this goal, we have obtained truncated versions of CgCCaMK lacking the autoinhibitory/CaM domain, and then expressed them into C. glauca. We have also used truncated forms of MtCCaMK from Medicago truncatula. The expression of these CCaMK constructs from C. glauca and M. truncatula was found to induce spontaneous nodulation in the absence of Frankia bacteria. These results suggest that deregulation of the calcium and calmodulin dependent protein kinase is able to reactivate the symbiotic signalling pathway and genes acting downstream CCaMK that are needed for nodule organogenesis.Key words: Casuarina glauca, Frankia, CCaMK, infection, autoinhibition, spontaneous nodules
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Abdel-Lateif, Khalid. "Flavonoids and actinorhizal symbiosis : Impact of RNA interference-mediated silencing of chalcone synthase gene on symbiosis between Casuarina glauca and Frankia." Thesis, Montpellier 2, 2012. http://www.theses.fr/2012MON20244/document.
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Les deux systèmes nodulaires symbiotiques les plus importants au niveau agronomique et environnemental sont, d'une part, les symbioses Rhizobium-légumineuses qui concernent environ 14 000 espèces, et d'autre part, les symbioses entre les plantes actinorhiziennes (environ 200 espèces) et l'actinomycète du sol Frankia. La plupart des plantes actinorhiziennes sont capables de fixer des quantités d'azote comparable à celles des Légumineuses ; ce sont généralement des plantes pionnières capables de coloniser des environnements pauvres en éléments minéraux. Elles représentent donc un atout écologique important. Si la symbiose Rhizobium-légumineuse est très étudiée, les mécanismes moléculaires à l'origine de la formation des nodules actinorhiziens restent actuellement peu connus. Ainsi, chez les Légumineuses, les flavonoïdes sont des molécules-clefs du processus de nodulation, alors que chez les plantes actinorhiziennes, l'implication des flavonoïdes dans la nodulation reste imprécise. L'objectif de cette thèse était de comprendre l'implication des flavonoïdes au cours de l'interaction symbiotique entre l'arbre actinorhizien tropical Casuarina glauca et son symbiote Frankia. L'analyse d'une base de données d'unigènes couplée à celle de données d'expression de puces à ADN a permis l'identification de huit genes de C. glauca impliqués dans la voie de biosynthèse des flavonoïdes. L'étude de leur expression dans les racines par PCR quantitative au cours d'une cinétique d'infection de C. glauca par Frankia a montré que les transcrits de la chalcone isomerase et de l'isoflavone reductase s'accumulaient très tôt après l'inoculation, suggérant ainsi une implication des isoflavonoïdes dans la symbiose actinorhizienne. Nous avons alors utilisé une stratégie d'ARN interférent pour réduire l'expression du gène de la chalcone synthase, la première enzyme de la voie de biosynthèse des flavonoïdes. La réduction de l'expression du gène de la chalcone synthase a provoqué une réduction significative du taux de flavonoïdes dans les racines ainsi qu'une très forte diminution du taux de nodulation chez les plantes transformées. Une restauration du taux de nodulation a pu être obtenu en présence de naringenin, une molécule centrale de la voie de biosynthèse des flavonoïdes.Nos résultats apportent donc, pour la première fois, une évidence directe de l'implication forte des flavonoïdes au cours de la nodulation des plantes actinorhiziennesNitrogen-fixing root nodulation, confined to four plant orders, encompasses more than 14,000 Leguminosae species, and approximately 200 actinorhizal species forming symbioses with rhizobia and Frankia bacterial species, respectively. Most actinorhizal plants are capable of high rates of nitrogen fixation comparable to the nitrogen fixing symbiosis between legumes and Rhizobium. As a consequence, these plants are able to grow in poor and disturbed soils and are important elements in plant community worldwide. The basic knowledge of the symbiotic interaction between Frankia and actinorhizal plants is still poorly understood, although it offers striking differences with the Rhizobium-legume symbiosis. In the symbiosis between legumes and Rhizobium, flavonoids are key molecules for nodulation. In actinorhizal plants, the involvement of flavonoids in symbiosis is poorly understood, but because of the similarities of the infection process between some actinorhizal plants and legumes, flavonoids were proposed to act as plant signals for the bacteria Frankia. The objective of this thesis was to investigate the involvement of flavonoids during the actinorhizal nodulation process resulting from the interaction between the tropical tree Casuarina glauca and the actinomycete Frankia.Eight C. glauca genes involved in flavonoid biosynthesis were identified from a unigene database and their expression patterns were monitored by quantitative real-time PCR during the nodulation time course. Our results showed that chalcone isomerase and isoflavone reductase transcripts accumulated preferentially early after inoculation with Frankia, suggesting thus for the first time that isoflavonoids are implicated in actinorhizal nodulation. To go deeper in the understanding of the role of these molecules in actinorhizal symbiosis, we used RNA interference strategy to silence chalcone synthase, the enzyme that catalyzes the first committed step of the flavonoid pathway. Knockdown of chalcone synthase expression led to a strong reduction of specific flavonoids levels and resulted in a severely impaired nodulation. Nodule formation could be rescued by supplementation of plants with naringenin, which is an upstream intermediate in flavonoid biosynthesis. Our results provide, for the first time, direct evidence of a strong implication of flavonoids during actinorhizal nodulation
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Schwob, Guillaume. "Rôle écologique de la sporulation in-planta dans les symbioses actinorhiziennes : cas de la symbiose Alnus - Frankia." Thesis, Lyon, 2018. http://www.theses.fr/2018LYSE1037/document.
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Les patrons de distribution chez les micro-organismes reposeraient sur leurs capacités à disperser dans le temps et dans l'espace, en lien avec des facteurs abiotiques comme les propriétés du sol, le climat, et des interactions biotiques, notamment avec l'hôte dans le cas des symbiontes, mais aussi sur les traits d'histoire de vie propres aux micro-organismes, telle que la capacité à sporuler. Frankia sp. est une actinobactérie sporulante et fixatrice d'azote à la biogéographie complexe, car vivant à la fois de façon saprophytique dans le sol, en symbiose racinaire (nodosité) avec les plantes actinorhiziennes dont les aulnes (Alnus, Betulaceae). Deux types de souches de Frankia génétiquement différentes ont été décrites dont la distinction phénotypique majeure réside dans la capacité à maintenir (Sp+) ou non (Sp-) leur sporulation in planta. Cette sporulation endophytique est à notre connaissance unique dans un contexte symbiotique et son implication dans la biogéographie de Frankia, reste peu connue. Ces travaux de thèse intègrent à la fois des approches descriptives et expérimentales, sur le terrain et au laboratoire, afin d'accroître la compréhension du rôle écologique de la sporulation in planta de Frankia. Dans un premier temps, nous avons étendu la description de la phylobiogéographie des souches de Frankia Sp+ afin de tester la validité du patron de distribution centré sur les milieux froids des zones de haute altitude et de haute latitude de l'hémisphère nord. Un intérêt tout particulier a été porté sur les aires géographiques où une plus forte diversité de Frankia était attendue, dans la zone d'origine de l'aulne et ses refuges glaciaires. Dans un second temps, nous avons étudié l'influence du partenaire végétal dans la distribution observée des Frankia Sp+ et l'implication du trait Sp+ dans la capacité d'association à l'hôte. Des croisements expérimentaux ont été réalisés au laboratoire afin de découpler les effets de l'espèce-hôte et du climat, et tester les implications du trait Sp+ en termes d'infectivité, compétitivité et spectre d'hôte. Enfin, nous avons étudié les conséquences écosystémiques de l'expansion subalpine du complexe symbiotique Alnus/Frankia, au niveau de la diversité microbienne et du fonctionnement du cycle de l'azote, en fonction du phénotype de sporulation des souches associées. Des analyses pédologiques, en association avec des mesures de nitrification, dénitrification et fixation d'azote, ainsi que des analyses de diversité microbienne (globale et fonctionnelle), ont été réalisées dans différentes aulnaies Sp+, Sp- ou mixte, à différents stades de colonisation de l'aulne. Les résultats obtenus démontrent une prédominance des souches Sp+ associées aux espèces d'aulne des milieux froids sur les 3 continents de la zone Holarctique, avec une diversité nouvelle dans l'aire d'origine et les zones refuges de l'aulne. Les croisements effectués révèlent une infectivité et compétitivité plus forte des Sp+ par rapport aux Sp-. De plus, contrairement aux Sp- à spectre d'hôte très large, les Sp+ présentent un spectre limité entraînant des incompatibilités d'association suggérant une dépendance forte à une espèce-hôte donnée. Les modifications des communautés microbiennes du sol en réponse à l'expansion du complexe symbiotique Alnus/Frankia ont été démontrées, en lien avec la stimulation du cycle de l'azote dans les milieux sub-/alpins. Les premiers résultats sur l'efficience comparée de la fixation d'azote in natura des souches Sp- par rapport aux Sp+ suggèrent que 100% de l'azote de l'aulne est obtenu par le biais de la fixation. Aucun patron n'est mis en évidence entre souches Sp+ et Sp-, suggérant un effet plus complexe de la saisonnalité, de l'âge de l'arbre et de celui de la nodosité. Les résultats obtenus nous permettent de mieux appréhender les facteurs guidant la biogéographie de Frankia et de discuter de l'évolution de ces patrons de distribution en réponse au réchauffement climatiqueMicrobial biogeography would be based on the ability of microorganisms to disperse across time and space, as a function of abiotic factors such as soil properties, climate, and of biotic interactions, in particular with the host in the case of symbionts, but also on life history traits such as the ability to sporulate. Frankia sp. is a spore-forming and nitrogen-fixing actinobacterium that has a complex biogeography given its abilities for both saprophytic life and root symbiotic interaction with actinorhizal plants such as alders (Alnus, Betulaceae). Two distinct groups of Frankia lineages have been described according to a major phenotypic divergence, based on the presence (Sp+) or the absence (Sp-) of spores in planta.. To the best of our knowledge, this endophytic sporulation is an original trait in a symbiotic context and very little is known about its incidence in Frankia biogeography. This work integrates descriptive and experimental approaches on both field and laboratory areas, in order to improve the understanding of the ecological role of Frankia in planta sporulation. First, we have extended the description of the phylobiogeography of Sp+ Frankia strains to validate the previously proposed distribution pattern focused on cold environements at high altitude or high latitude. A phylogeny has been computed using a large number of nodular strains coming from the 3 continents of the Northern Hemisphere and 10 different Alnus species. Special attention was paid to geographic areas where a higher diversity was expected, in Asia, and in its glacial refuges. Second, we studied the influence of the host-plant on the distribution of Fankia Sp+ and the incidence of Sp+ in the symbiotic interaction. Experimental crosses have been performed to disentangle host and climate effects and to test the incidence of the Sp+ trait in terms of infectivity, competitiveness and host-range. Finally, we studied the ecological consequences of the Alnus/Frankia symbiotic complex, on the microbial diversity and on the nitrogen cycle functionning, with respect to the sporulation of Frankia and to the Alnus expansion on sub-/alpine grasslands. Soils analyses were performed in association with measures of nitrification and denitrification, as well as global and functional microbial diversity analyses, in Sp+, Sp- or mixed alder stands and at different colonization stages. In each part of this work, alder ectomycorhizae were analyzed to compare the distribution pattern between the two symbionts and to highlight potential interactions with the Sp+ trait of Frankia. Our results show the dominance of Sp+ strains in nodules of alder species from cold environments over the 3 continents of the Holarctic zone, with original diversity patterns in alder area of origin and in glacial refuges. Even if these strains are genetically homogenous, host-specific clusters were observed in the phylogeny. Crosses revealed that Sp+ strains were more infective and competitive than Sp- strains. Moreover, unlike Sp- strains that harbor a wide host-range, Sp+ strains have a narrower specificity leading to association’s incompatibilities and suggesting strong host dependence. For the first time, modifications of microbial communities were revealed in response to the Alnus-Frankia symbiotic complex colonization and were linked to a stimulation of the nitrogen cycle in the sub-/alpine grasslands. The first comparative results of nitrogen fixation between Sp+ and Sp- strains in natura suggest a maximal efficiency of fixation, representing almost 100% of the alder nitrogen. However, unlike previous reports in literature, no pattern was observed between Sp+ and Sp- strains, suggesting a complex effect of seasonality, alder age as well as that of nodules. Altogether, the previous results contribute to a better understanding of the Frankia biogeography drivers and allow us to discuss the expected evolution of distribution pattern in response to the global warming
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Bhattacharya, Sanghati. "Characterization and diversity of selected actinorhizal haemoglobin genes and proteins with reference to Alnus-Frankia symbiosis." Thesis, University of North Bengal, 2017. http://ir.nbu.ac.in/hdl.handle.net/123456789/2629.
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Wilcox, Dale Adrian. "Diversity of Frankia associated with Morella species of the Cape floristic region of Southern Africa." Thesis, University of the Western Cape, 2016. http://hdl.handle.net/11394/5346.
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Philosophiae Doctor - PhDFrankia is one of two partners in the globally distributed N2-fixing actinorhizal symbiosis between this filamentous soil-dwelling actinomycete and almost 300 species of host plants from eight diverse angiosperm families. The actinorhizal symbiosis is a major contributor to nitrogen reservoirs in terrestrial ecosystems, and allows actinorhizal plants to perform the role of pioneers in newly formed and nitrogen-poor soils. Frankia are differentiated into four main host-infection groups (1: Alnus/Comptonia/Myrica-infective, 2: Rosaceae/Datisca/Coriaria-infective, 3: Elaeagnaceae/Gymnostoma-infective and 4: Casuarina-infective), and there is a large degree of phylogenetic clustering within these HIGs. Of these host lineages, species from the genus Morella, from the family Myricaceae, are notable as they have the ability to establish effective partnerships with Frankia from more than one host-infection group. Africa houses 16 of the world’s 33 currently accepted Morella species, and Morella is the continents only genus containing endemic actinorhizal species. Despite this, the diversity of Frankia in symbiosis with African Morella has never been explored. To address this lack of knowledge I investigated Frankia in root nodules of six Morella species from the Cape flora of Southern Africa, as well as in rhizosphere soils from selected hosts. Partial nif H gene fragments recovered from 202 root nodules yielded 26 unique sequences, which phylogenetic analysis assigned to Frankia Cluster I (the Alnus host infection group) and Frankia Cluster III (the Elaeagnus host infection group)1. Nineteen nif H sequences were assigned to three sub-clusters within Frankia Cluster III (CC-3, CC-4 and CC-5), and the remaining seven sequences to two sub-clusters within Cluster I (CC-1 and CC-2), one of which (CC-1) is novel to the current study. Identical sequences were recovered from nodules collected at geographically distant locations, suggesting a cosmopolitan distribution within the region for some subgroups from both clusters, but more localized distribution (or tighter host-specificity) for others. Soil pH correlated with strain presence in nodules, with Cluster I sequences being associated with hosts growing in acidic soils exclusively. Furthermore, three Morella species from the Cape flora of southern Africa are promiscuous in their natural habitats, with host infection group influenced by habitat edaphic conditions. In order to explore the correlation between soil characteristics and Frankia presence in nodules, nif H soil libraries were created from selected host rhizospheres. While Cluster III sequences from these libraries corresponded closely to sequences found in nodules from the same sites, the dominant Cape Cluster I group (CC-1) was absent from all six libraries, even when present in nodules recovered from the same soils. Whether this was due to low abundance of -but strong selection for- these strains by hosts under particular conditions, or due to the absence in soil of hyphal forms of these strains could not be determined. Cluster III strains are known to be better able to persist saprophytically than their relatives from other host-infection groups. A second group of Cluster I strains, detected at only one sampling site, was present in that site's corresponding soil library. An Alnus-infective subgroup, cluster AI, which has been detected in soils collected on five continents, was also detected in the of the Cape soil libraries but never in nodules, raising questions as to this group’s ability to persist in soil in the absence of known suitable hosts. Ten Frankia strains representing all three of the numerically dominant subgroups (CC-1, CC-3 and CC-4, found in 186 of 202 root nodules) were isolated from four Morella species. These isolates represent six of the most abundant unique nodular nif H sequences found in the field survey, and display morphological and cultural characteristics typical of Frankia. Phylogenetic analysis confirmed their identity as Frankia, and multilocus analysis revealed that the isolates belong to three genospecies. Two of these genospecies fall into existing groups within the Elaeagnus-infective Cluster III, while the remaining genospecies is a novel addition to the otherwise well-described Alnus-infective Cluster I. Whole genome sequencing of a representative from each of the Cape genospecies allowed for basic annotation and genome descriptions, which agreed in each case with what has been previously found for strains from the Elaeagnus and Alnus host-infection groups, respectively. Similarly, the organization of nitrogenase gene clusters in each of the sequenced strains mirrors that found in other strains from their respective host-infection groups, indicating that this gene cluster is highly conserved in different Frankia lineages. For the first time the diversity of Frankia nodulating endemic African Morella, and present in root-associated soils of these species, has been explored. This is also the first study to report isolation and description of Frankia strains from actinorhizal plants endemic to Africa.
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Pozzi, Adrien C. "Rôles adaptatifs et contraintes de la sporulation chez les microorganismes associés aux plantes : cas de la sporulation in planta dans la symbiose actinorhizienne Frankia (Frankiaceae)–Alnus (Betulaceae)." Thesis, Lyon 1, 2014. http://www.theses.fr/2014LYO10359/document.
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Frankia est une actinobactérie capable d'établir une symbiose racinaire avec les plantes actinorhiziennes dont le genre Alnus. Seulement certaines souches de Frankia sont capables de sporuler in planta, ce qui est illustré par la présence (Sp+) ou l'absence (Sp–) de sporanges dans les cellules végétales de la nodosité. C’est à notre connaissance un cas unique de sporulation endophyte. Cependant la description et l’interprétation écologique de ce trait d’histoire de vie (THV) original étaient incomplètes. Notre contribution à l’étude de la sporulation in planta des Frankia infectives de l’aulne intègre des approches théorique, descriptive et expérimentale, pour préciser (i) l’influence relative de la souche bactérienne, de l’espèce de la plante-hôte et des conditions pédoclimatiques sur ce THV, (ii) le rôle de la variabilité environnementale sur la distribution, la diversité et la sélection du trait, ainsi que (iii) les coûts et bénéfices associés pour les deux partenaires. Nous avons démontré pour la première fois que la sporulation in planta est un THV (i) spécifique de certaines lignées de Frankia, (ii) majeur pour en comprendre l'histoire évolutive et (iii) significativement corrélé à des caractéristiques génétiques des souches. Nous avons également confirmé que l’occurrence du trait varie selon l’environnement. Nous avons enfin établi un modèle de l'évolution du trait abordant sa valeur adaptative. L’ensemble des réflexions menées et des résultats obtenus nous permet de discuter de la sporulation in planta dans le cadre d’un continuum de stratégies symbiotiques, et plus généralement de discuter de l’écologie évolutive des symbioses entre microorganismes et plantesFrankia sp. is a telluric actinobacteria able to establish a root symbiosis with actinorhizal plant such as Alnus sp. Only some Frankia strains are able to sporulate in-planta, as spores can be present in (Sp+) or absent from (Sp–) the vegetal cells of the root nodule. It is to our knowledge a unique case of endophytic sporulation. However, the description and the ecological interpretation of this original life-history trait (LHT) were scarce. Our contribution to the study of the in-planta sporulation of Alnus-infective Frankia sp. combines theoretical, descriptive and experimental approaches to precise (i) the relative effect of the bacterial strain, the host-plant species and the pedoclimatic conditions on this LHT, (ii) the effect of the of the environmental variability on the distribution, diversity and selection of the trait, and (iii) the associated costs and benefits for the two symbiotic partners. We demonstrated for the first time that the in-planta sporulation is a LHT (i) specific to some Frankia lineages, (ii) major to understand their evolutionary history and (iii) significantly correlated to particular genetic features. We also shown that the occurrence of the trait varies according to the environment We also proposed a model of the evolution of the trait taking its fitness into account. We bring all the previous considerations and results to discuss the inplanta sporulation trait within a continuum of symbiotic strategies and more generally to discuss the evolutionary ecology of plant-microbe symbioses
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Queiroux, Clothilde. "Signalisation moléculaire dans la symbiose Frankia-aulne." Thesis, Lyon 1, 2009. http://www.theses.fr/2009LYO10228.
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L'azote est essentiel au développement de toutes les cellules vivantes. Il est un des facteurs limitant de la croissance végétale. La seule source d'azote abondante est l'atmosphère contenant 80 % de diazote mais cette forme n'est assimilable que par certains procaryotes. Ces microorganismes sont capables de fixer l'azote atmosphérique sous leur forme libre ou en symbiose avec des plantes. Ainsi, ils fournissent à leur plante partenaire des substrats azotés, sous forme d'ammoniaque, tandis qu'en retour celle-ci fournit à la bactérie des substrats carbonés issus de sa photosynthèse. Il s'agit d'une association à bénéfices réciproques. Il existe deux grands types de symbiose fixatrice d'azote : la symbiose rhizobienne, impliquant diverses Protéobactéries et la symbiose actinorhizienne impliquant une Actinobactérie, Frankia. Les bactéries pénètrent les cellules des plantes pour former un nouvel organe, la nodosité dans laquelle va avoir lieu la fixation d'azote. Les bases moléculaires à l'origine de la symbiose rhizobienne sont très bien caractérisées tandis que celles de la symbiose actinorhizienne restent en grande partie inconnue, de par l'absence d'outils génétiques. Toutefois, les premières étapes de mise en place de la symbiose présentent des similarités. Les deux bactéries sont capables d'induire la déformation du poil racinaire en sécrétant un facteur déformant, le facteur Nod pour la plupart des symbioses rhizobiennes et un facteur encore non caractérisé dans le cas de la symbiose actinorhizienne. La problématique de mes travaux de thèse est de savoir si le dialogue moléculaire s'établissant entre la plante et la bactérie est basé sur des composants universels. Ce travail a utilisé deux approches. Une approche ciblée visait à mettre en évidence la fonction. Une approche non-ciblée par le biais des puces transcriptomiques chez Frankia a permis de comparer l'expression génétique entre des conditions de vie libre et des conditions de vie symbiotique. Enfin, une dernière approche a concerné les composés aromatiques chez Frankia. Il s'agissait d'établir si Frankia était capable de cataboliser différents composés aromatiques. En effet, beaucoup d'entre eux sont impliqués dans les interactions plante-bactérie, notamment dans les réactions de défense de la planteNitrogen is essential for cells development. It's one of the limiting factors of plant growth. The only abundant source of this component is the atmosphere which contains 80 % of dinitrogen, but this form can only be assimilated by some prokaryotes. These microorganisms are able to fix atmospheric nitrogen under freeliving condition or in symbiosis with some plants. Thus, they provide nitrogen substrates to the plant in the form of ammonium, and in return the plant provides carbon substrates from photosynthesis. It is an association with reciprocal profits for both partners. There are two major nitrogen-fixing symbioses: rhizobial symbiosis, which involves various Proteobacteria and actinorhizal symbiosis, which involves the Actinobacterium, Frankia. Bacteria enter plant root cells and develop a new organ, the nodule where nitrogen fixation takes place. Molecular bases are well characterized for rhizobial symbiosis, whereas little is known about the actinorhizal symbiosis. This fact is in part due to absence of genetic tools for Frankia. However, early steps of the interaction show some similarities. These two bacteria are able to induce root hair deformation by secreting a deforming factor, Nod factor in most rhizobial symbioses and a noncharacterized factor in the actinorhizal symbiosis. The aim of this thesis was to determine if molecular dialogue between plant and bacteria is based on universal components. This work used two approaches. One was targeted on nodC-like gene from Frankia alni ACN14a. We tried to characterize their function. Another used trancriptomic microarrays in Frankia. This technique allowed us to compare transcripts from 2 conditions: free-living cells and symbiosis. A last approach focused on aromatic compounds in Frankia. We wanted to determine if Frankia was able to use different aromatic compounds to grow. Indeed, a lot of aromatic compounds are involved in plant-bacteria interaction such as plant defense
Books on the topic "Frankia symbiosis"
1
Normand, P., J. O. Dawson, and K. Pawlowski, eds. Frankia Symbiosis. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7.
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1957-, Normand P., Dawson J. O, and Pawlowski K, eds. Frankia symbiosis: Proceedings of the 12th Meeting on Frankia and Actinorhizal Plants, Carry-le-Rouet, France, June 2001. Dordrecht: Kluwer Academic Publishers, 2003.
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Dawson, J. O., P. Normand, and K. Pawlowski. Frankia Symbiosis. Springer, 2010.
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Dawson, J. O., P. Normand, and K. Pawlowski. Frankia Symbiosis. Springer London, Limited, 2013.
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(Editor), P. Normand, K. Pawlowski (Editor), and J. O. Dawson (Editor), eds. Frankia Symbiosis (Developments in Plant and Soil Sciences). Springer, 2003.
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Jeong, Soon-Chun. Evolution and ecology of the Ceanothus-Frankia symbiosis. 1997.
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Frankia Symbioses. Springer, 2011.
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Baker, D., A. D. Akkermans, K. Huss-Danell, and J. D. Tjepkema. Frankia Symbioses. Springer, 2012.
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Baker, D., A. D. Akkermans, K. Huss-Danell, J. D. Tjepkema, and Akke Jitske Van der Zijpp. Frankia Symbioses. Springer, 2011.
Find full textBook chapters on the topic "Frankia symbiosis"
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Zimpfer, J. F., C. M. Kaelke, C. A. Smyth, D. Hahn, and J. O. Dawson. "Frankia inoculation, soil biota, and host tissue amendment influence Casuarina nodulation capacity of a tropical soil." In Frankia Symbiosis, 1–10. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_1.
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Myers, Anna K., and Louis S. Tisa. "Effect of electroporation conditions on cell viability of Frankia EuI1c." In Frankia Symbiosis, 83–88. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_10.
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Kwon, Hyuk Jun, Chang Jae Oh, Ho Bang Kim, and Chung Sun An. "Molecular cloning and characterization of adr and ivd genes from Frankia EuIK1 strain." In Frankia Symbiosis, 89–96. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_11.
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Cournoyer, B., and D. Blaha. "Cloning, characterisation and phylogenetic analysis of the sigA σ 70 factor gene sequence from the actinomycete Frankia." In Frankia Symbiosis, 97–106. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_12.
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John, Theodore R., James Wiggington, Joyce V. Bock, Ryan Klemt, and Jerry D. Johnson. "An insertion sequence unique to Frankia strain ArI5." In Frankia Symbiosis, 107–13. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_13.
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Igual, José M., Angel Valverde, Raúl Rivas, Pedro F. Mateos, C. Rodríguez-Barrueco, Eustoquio Martínez-Molina, Emilio Cervantes, and Encarna Velázquez. "Genomic fingerprinting of Frankia strains by PCR-based techniques. Assessment of a primer based on the sequence of 16S rRNA gene of Escherichia coli." In Frankia Symbiosis, 115–23. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_14.
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Lavire, C., and B. Cournoyer. "Progress on the genetics of the N2-fixing actinorhizal symbiont Frankia." In Frankia Symbiosis, 125–37. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_15.
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Valverde, Claudio, and Luis Gabriel Wall. "Ammonium assimilation in root nodules of actinorhizal Discaria trinervis. Regulation of enzyme activities and protein levels by the availability of macronutrients (N, P and C)." In Frankia Symbiosis, 139–53. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_16.
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Valverde, Claudio, and Luis Gabriel Wall. "The regulation of nodulation, nitrogen fixation and ammonium assimilation under a carbohydrate shortage stress in the Discaria trinervis-Frankia symbiosis." In Frankia Symbiosis, 155–65. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_17.
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Kaelke, C. M., and J. O. Dawson. "Seasonal flooding regimes influence survival, nitrogen fixation, and the partitioning of nitrogen and biomass in Alnus incana ssp. rugosa." In Frankia Symbiosis, 167–77. Dordrecht: Springer Netherlands, 2003. http://dx.doi.org/10.1007/978-94-017-1601-7_18.
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