Genetic complementation of rhizobial nod mutants with Frankia DNA: artifact or reality?

Cérémonie, Hélène; Cournoyer, Benoît; Maillet, Fabienne; Normand, Philippe; Fernández, María P.

doi:10.1007/s004380050877

Cited by 31 publications

(15 citation statements)

References 31 publications

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“…Part of this signaling cascade is also involved in transduction of the symbiotic signal in AM symbioses (5). This gave rise to the hypothesis that the evolutionarily recent legume-rhizobia symbiosis reuses some of the molecular mechanisms of the more ancient AM symbiosis (16 indicate only that the Frankia symbiotic signal is likely chemically different from NFs (10)(11)(12). Here, we report the isolation and characterization of CgSymRK, a SymRK/DMI2 homolog from the actinorhizal tree C. glauca.…”

Section: Discussionmentioning

confidence: 97%

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SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria

Gherbi

Markmann

Svistoonoff

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

255

178

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Root endosymbioses vitally contribute to plant nutrition and fitness worldwide. Nitrogen-fixing root nodulation, confined to four plant orders, encompasses two distinct types of associations, the interaction of legumes (Fabales) with rhizobia bacteria and actinorhizal symbioses, where the bacterial symbionts are actinomycetes of the genus Frankia. Although several genetic components of the host-symbiont interaction have been identified in legumes, the genetic basis of actinorhiza formation is unknown. Here, we show that the receptor-like kinase gene SymRK, which is required for nodulation in legumes, is also necessary for actinorhiza formation in the tree Casuarina glauca. This indicates that both types of nodulation symbiosis share genetic components. Like several other legume genes involved in the interaction with rhizobia, SymRK is also required for the interaction with arbuscular mycorrhiza (AM) fungi. We show that SymRK is involved in AM formation in C. glauca as well and can restore both nodulation and AM symbioses in a Lotus japonicus symrk mutant. Taken together, our results demonstrate that SymRK functions as a vital component of the genetic basis for both plant-fungal and plant-bacterial endosymbioses and is conserved between legumes and actinorhiza-forming Fagales.actinorhizal symbioses ͉ Casuarina glauca ͉ mycorrhizae ͉ signaling R oot endosymbioses are associations between plants and soil microorganisms involving intracellular accommodation of microbes within host cells. The most widespread of these associations is arbuscular mycorrhiza (AM), which is formed by the majority of land plants with fungi belonging to the phylum Glomeromycota (1). In contrast, nitrogen-fixing nodulation symbioses of plant roots and bacteria are restricted to four orders of eurosid dicots (2). Actinorhiza, formed by members of the Fagales, Rosales, and Cucurbitales with Gram-positive Frankia bacteria, differs from the interaction of legumes with Gramnegative rhizobia in several morphological and cytological aspects (3). Although these differences suggest independent regulatory mechanisms, the close relatedness of nodulating lineages indicates a common evolutionary basis of root nodulation symbioses (2). In the legume-rhizobia interaction, among the key factors mediating recognition between the plant and the bacteria are Nod factors (NFs). NFs are bacterial lipochitooligosaccharides with an N-acetylglucosamine backbone (4). The perception of NFs induces a series of responses in host roots, including ion flux changes and membrane depolarization, rhythmic calcium oscillations in and around the nucleus (calcium spiking), cytoskeletal modifications and root hair curling, and activation of cortical cell divisions (5). Extensive mutant screenings performed in legumes led to the identification of several loci involved in this signaling cascade, and recently most of the corresponding genes were identified by map-based approaches (6). In Lotus japonicus, two genes, NFR1 and NFR5 encoding receptor-like serine/threonine kinases with L...

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Section: Discussionmentioning

confidence: 97%

“…Analyses of the genome of three Frankia strains (10), the biochemical characterization of a Frankia root hair-deforming factor whose chemical structure is unknown (11), and the failure of Frankia DNA to complement rhizobial nod gene mutants (12) (Fig. 1A).…”

mentioning

confidence: 99%

SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria

Gherbi

Markmann

Svistoonoff

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

255

178

View full text Add to dashboard Cite

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“…c Pseudolongitudinal section of a nodular lobe from A. verticillata; the nitrogen-fixing zone contains large cells filled with Frankia (f), and the infection zone (iz) is located in the apex of the nodular lobe. Bars: A= 10 μm; B=5 mm; C=200 μm genes homologous to the nod genes of rhizobia in Frankia had failed (Cérémonie et al 1998) until preliminary analysis of the Frankia genome revealed disperse putative nod-like genes. However, these do not appear to be organized in clusters as in rhizobia, and the key nodA gene is absent.…”

Section: Frankiamentioning

confidence: 99%

Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants

2008

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Nitrogen is generally considered one of the major limiting nutrients in plant growth. The biological process responsible for reduction of molecular nitrogen into ammonia is referred to as nitrogen fixation. A wide diversity of nitrogen-fixing bacterial species belonging to most phyla of the Bacteria domain have the capacity to colonize the rhizosphere and to interact with plants. Leguminous and actinorhizal plants can obtain their nitrogen by association with rhizobia or Frankia via differentiation on their respective host plants of a specialized organ, the root nodule. Other symbiotic associations involve heterocystous cyanobacteria, while increasing numbers of nitrogen-fixing species have been identified as colonizing the root surface and, in some cases, the root interior of a variety of cereal crops and pasture grasses. Basic and advanced aspects of these associations are covered in this review.

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“…Furthermore, in actinorhizal symbioses where chitinases were also expressed in mature nodules, no equivalents of rhizobial Nod factors have been identified. While the presence of a root hair-deforming factor could be shown (van Ghelue et al 1997), this factor was structurally different from rhizobial Nod factors (Cérémonie et al 1998;, and apparently not degraded by chitinases (Cérémonie et al 1999). Furthermore, no homologues of the common nod genes nodA and nodC were found in the three sequenced Frankia genomes (Normand et al 2007), making it extremely unlikely that Frankia strains can produce molecules resembling rhizobial Nod factors.…”

Section: Chitinases In Root Nodulesmentioning

confidence: 99%