Characterisation of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants

Morandi, Dominique; Prado, Emilce; Sagan, Muriel; Duc, Gérard

doi:10.1007/s00572-004-0331-4

Cited by 49 publications

(59 citation statements)

References 25 publications

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“…At the root surface, hyphae developed abundant appressoria, but these colonization attempts rarely succeeded, pointing to a role of CgSymRK during hyphal penetration. Similar results were shown for L. japonicus symrk (14) and M. truncatula dmi2 mutants (20,21). This work report a role of SymRK in AM symbiosis formation in a nonlegume plant.…”

Section: Discussionsupporting

confidence: 83%

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.

258

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: Discussionsupporting

confidence: 83%

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.

258

178

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“…Bacteria fail to differentiate or senesce prematurely in several mutants of the host plants M. truncatula and pea (Pisum sativum), but none of the genes carrying these mutations has yet been cloned [62][63][64]93,94 . In the pea sym13 mutant, symbiosome membranes are not closely associated with the bacteroid and the bacteroids senesce early 95 .…”

Section: Box 3 Host Invasion Parallels Between Rhizobia and Animal Pamentioning

confidence: 99%

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).The recent completion of the Sinorhizobium meliloti genome sequence, and the progress towards the completion of the Medicago truncatula genome sequence, have led to a surge in the molecular characterization of the determinants that are involved in the development of the symbiosis between rhizobial bacteria and leguminous plants. Aromatic compounds from legumes called flavonoids first signal the rhizobial bacteria to produce lipochitooligosaccharide compounds called Nod factors 1 . Nod factors that are secreted by the bacteria activate multiple responses in the host plant that prepare the plant to receive the invading bacteria. Nod factors and symbiotic exopolysaccharides induce the plant to form infection threads, which are thin tubules filled with bacteria that penetrate into the plant cortical tissue and deliver the bacteria to their target cells. Plant cells in the inner cortex internalize the invading bacteria in host-membrane-bound compartments that mature into structures known Correspondence to G.C.W. gwalker@mit.edu. Competing interests statementThe authors declare no competing financial interests. DATABASES Invasion of plant rootsAlthough plant roots are exposed to various micro-organisms in the soil, their cell walls form a strong protective barrier against most harmful species. The early steps in the invasion of barrel medic (M. truncatula) and alfalfa (Medicago sativa) roots by S. meliloti are characterized by the reciprocal exchange of signals that allow the bacteria to use the plant root hair cells as a means of entry. Initial signal exchangeFlavonoid compounds (2-phenyl-1,4-benzopyrone derivatives) produced by leguminous plants are the first signals to be exchanged by host-rhizobial symbiont pairs 1 (FIG. 1). Flavonoids bind bacterial NodD proteins, which are members of the LysR family of transcriptional regulators, and activate these proteins to induce the transcription of rhizobial genes 1,2 . For example, the M. sativa-derived flavonoid luteolin stimulates binding of an active form of NodD1 to an S. meliloti 'nod-box' p...

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“…Genetic dissection has revealed a number of loci important for nodule formation, infection thread growth, and bacterial release (Benaben et al, 1995;Schauser et al, 1998;Szczyglowski et al, 1998;Kawaguchi et al, 2002;Kuppusamy et al, 2004;Veereshlingam et al, 2004;Bright et al, 2005;Morandi et al 2005;Starker et al, 2006;Arrighi et al, 2008;Teillet et al, 2008). However, to date, there are very few loci that have been cloned to reveal the underlying mechanisms inherent to these processes.…”

Section: Introductionmentioning

confidence: 99%

EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation inMedicago truncatula

et al. 2008

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Mechanisms regulating legume root nodule development are still poorly understood, and very few regulatory genes have been cloned and characterized. Here, we describe EFD (for ethylene response factor required for nodule differentiation), a gene that is upregulated during nodulation in Medicago truncatula. The EFD transcription factor belongs to the ethylene response factor (ERF) group V, which contains ERN1, 2, and 3, three ERFs involved in Nod factor signaling. The role of EFD in the regulation of nodulation was examined through the characterization of a null deletion mutant (efd-1), RNA interference, and overexpression studies. These studies revealed that EFD is a negative regulator of root nodulation and infection by Rhizobium and that EFD is required for the formation of functional nitrogen-fixing nodules. EFD appears to be involved in the plant and bacteroid differentiation processes taking place beneath the nodule meristem. We also showed that EFD activated Mt RR4, a cytokinin primary response gene that encodes a type-A response regulator. We propose that EFD induction of Mt RR4 leads to the inhibition of cytokinin signaling, with two consequences: the suppression of new nodule initiation and the activation of differentiation as cells leave the nodule meristem. Our work thus reveals a key regulator linking early and late stages of nodulation and suggests that the regulation of the cytokinin pathway is important both for nodule initiation and development.

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Characterisation of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants

Cited by 49 publications

References 25 publications

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

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

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

EFD Is an ERF Transcription Factor Involved in the Control of Nodule Number and Differentiation inMedicago truncatula

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