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Papers by Françoise Billy

Research paper thumbnail of Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa

Development (Cambridge, England), 1998

Reorganization of the plant cytoskeleton is thought to play an important role during nodule ontog... more Reorganization of the plant cytoskeleton is thought to play an important role during nodule ontogeny. In situ immunolocalisation of tubulin reveals that important cytoskeletal changes, implying a transient disorganization followed by a newly patterned reorganization, occur in indeterminate and determinate nodules. In alfalfa nodules, cytoskeletal changes closely parallel the symbiotic differentiation features related to cell infection, bacterial release, endopolyploidization, cell enlargement, cell spatial organization and organelle ultrastructure and positioning. Moreover, the fact that microtubule disorganization can be correlated with Nod factor internalization in central infected cells suggests that Nod factors are possibly involved in the control of cytoskeletal changes which direct the differentiation of bacteria-containing cells.

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Research paper thumbnail of Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules

Journal of bacteriology, 1990

Bacteroid differentiation was examined in developing and mature alfalfa nodules elicited by wild-... more Bacteroid differentiation was examined in developing and mature alfalfa nodules elicited by wild-type or Fix- mutant strains of Rhizobium meliloti. Ultrastructural studies of wild-type nodules distinguished five steps in bacteroid differentiation (types 1 to 5), each being restricted to a well-defined histological region of the nodule. Correlative studies between nodule development, bacteroid differentiation, and acetylene reduction showed that nitrogenase activity was always associated with the differentiation of the distal zone III of the nodule. In this region, the invaded cells were filled with heterogeneous type 4 bacteroids, the cytoplasm of which displayed an alternation of areas enriched with ribosomes or with DNA fibrils. Cytological studies of complementary halves of transversally sectioned mature nodules confirmed that type 4 bacteroids were always observed in the half of the nodule expressing nitrogenase activity, while the presence of type 5 bacteroids could never be co...

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Research paper thumbnail of Cellular expression and regulation of the Medicago truncatula cytosolic glutamine synthetase genes in root nodules

Plant Molecular Biology, 2000

In this paper we have studied the localisation of expression of the two functional cytosolic glut... more In this paper we have studied the localisation of expression of the two functional cytosolic glutamine synthetase (GS) genes, MtGSa and MtGSb, in root nodules of the model legume Medicago truncatula. We have used a combination of different techniques, including immunocytochemistry, in situ hybridisation and promoter beta-glucuronidase (GUS) fusions in transgenic plants, to provide the means of correlating gene expression with protein localisation. These studies revealed that transcriptional regulation (mRNA synthesis) plays an important part in controlling GS protein levels in nodules of M. truncatula. The major locations of cytosolic GS mRNA and protein are the central tissue, the parenchyma and the pericycle of the vascular bundles. These findings indicate that in nodules, GS might be involved in other physiological processes in addition to the primary assimilation of ammonia released by the bacterial nitrogenase. The two genes show different but overlapping patterns of expression with MtGSa being the major gene expressed in the infected cells of the nodule. Promoter fragments of 2.6 kb and 3.1 kb of MtGSa and MtGSb, respectively, have been sequenced and primer extension revealed that the MtGSb promoter is expressed in nodules from an additional start site that is not used in roots. Generally these fragments in the homologous transgenic system were sufficient to drive GUS expression in almost all the tissues and cell types where GS proteins and transcripts are located except that the MtGSa promoter fragment did not express GUS highly in the nodule infected cells. These results indicate that the cis-acting regulatory elements responsible for infected-cell expression are missing from the MtGSa promoter fragment.

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Research paper thumbnail of Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa

The Plant Journal, 1994

Extracellular lipo-oligosaccharides of Rhizobium, known as Nod factors, play a key role in the mo... more Extracellular lipo-oligosaccharides of Rhizobium, known as Nod factors, play a key role in the molecular signal exchange which leads to the specific nitrogen-fixing symbiotic association between the soil microbe and its host legume. The biological activity of Nod factors and their perception by the host plant during the earliest stages of the Rhizobium/legume interaction have been studied using transgenic alfalfa carrying a fusion between the promoter of the early nodulin gene MtENOD12 and the beta-glucuronidase (GUS) reporter gene. Histochemical staining has shown that GUS accumulates specifically in the differentiating root epidermis, prior to and during root hair emergence, within 2-3 h following the addition of purified Rhizobium meliloti Nod factors. This precocious transcriptional activation of the MtENOD12 gene, reminiscent of that observed after inoculation with intact Rhizobium, implies that the Nod factor signal can be perceived at a developmental stage preceding root hair formation. GUS activity can be detected following treatment with a wide range of R. meliloti Nod factor concentrations down to 10(-13) M, and furthermore, this rapid response to the bacterial elicitor appears to be non-systemic. Significantly, MtENOD12-GUS expression is not observed after inoculation with a R. meliloti nodH mutant which synthesizes exclusively non-sulphated Nod factors. Indeed purified Nod factors which lack the sulphate substituent are approximately 1000-fold less active than their sulphated counterparts. Thus, the triggering of ENOD12 transcription in the alfalfa root epidermis is a rapid molecular response which is subject to the same host-specificity determinant (Nod factor sulphation) that governs the interaction between alfalfa and its bacterial symbiont.

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Research paper thumbnail of Leghaemoglobin gene transcription is triggered in a single cell layer in the indeterminate nitrogen-fixing root nodule of alfalfa

The Plant Journal, 1991

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Research paper thumbnail of Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction

The Plant Journal, 1993

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Research paper thumbnail of Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway

THE PLANT CELL ONLINE, 2000

Rhizobium nodulation (Nod) factors are lipo-chitooligosaccharides that act as symbiotic signals, ... more Rhizobium nodulation (Nod) factors are lipo-chitooligosaccharides that act as symbiotic signals, eliciting several key developmental responses in the roots of legume hosts. Using nodulation-defective mutants of Medicago truncatula, we have started to dissect the ...

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Research paper thumbnail of Rhizobium meliloti Elicits Transient Expression of the Early Nodulin Gene ENOD12 in the Differentiating Root Epidermis of Transgenic Alfalfa

THE PLANT CELL ONLINE, 1992

Page 1. The Plant Cell, Vol. 4, 1199-1211, October 1992 O 1992 American Society of Plant Physiolo... more Page 1. The Plant Cell, Vol. 4, 1199-1211, October 1992 O 1992 American Society of Plant Physiologists Rhizobium meliloti Elicits Transient Expression of the Early Nodulin Gene ENOD12 in the Differentiating Root Epidermis of Transgenic Alfalfa ...

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Research paper thumbnail of TheRhizobium-legume symbiosis Two methods to discriminate between nodules and other root-derived structures

Protoplasma, 1989

... G. Truchet*, S. Camut, F. de Billy, R. Odorico, and J. Vasse ... commercial solution containi... more ... G. Truchet*, S. Camut, F. de Billy, R. Odorico, and J. Vasse ... commercial solution containing 12.5% of active chlo-rine and diluted with distilled water (V/V). Whole plants, collected at different times following inocuiation, were immersed in this so-lution for 15 rain under vacuum ...

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Research paper thumbnail of The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection

Proceedings of the National Academy of Sciences, 2008

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Research paper thumbnail of Transcription Reprogramming during Root Nodule Development in Medicago truncatula

PLoS ONE, 2011

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Research paper thumbnail of The MtMMPL1 Early Nodulin Is a Novel Member of the Matrix Metalloendoproteinase Family with a Role in Medicago truncatula Infection by Sinorhizobium meliloti

PLANT PHYSIOLOGY, 2007

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Research paper thumbnail of Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa

Nature, 1991

RHIZOBIUM meliloti is a symbiotic bacterium that elicits the morphogenesis of nitrogen-fixing nod... more RHIZOBIUM meliloti is a symbiotic bacterium that elicits the morphogenesis of nitrogen-fixing nodules, specific organs on the roots of alfalfa (Medicago sativa) 1 . In R. meliloti a series of nodulation (nod) genes have been identified which are involved in root-hair curling and infection and ...

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Research paper thumbnail of Genetic and Cytogenetic Mapping of DMI1, DMI2 , and DMI3 Genes of Medicago truncatula Involved in Nod Factor Transduction, Nodulation, and Mycorrhization

Molecular Plant-Microbe Interactions, 2002

The DMI1, DMI2, and DMI3 genes of Medicago truncatula, which are required for both nodulation and... more The DMI1, DMI2, and DMI3 genes of Medicago truncatula, which are required for both nodulation and mycorrhization, control early steps of Nod factor signal transduction. Here, we have used diverse approaches to pave the way for the map-based cloning of these genes. Molecular amplification fragment length polymorphism markers linked to the three genes were identified by bulked segregant analysis. Integration of these markers into the general genetic map of M. truncatula revealed that DMI1, DMI2, and DMI3 are located on linkage groups 2, 5, and 8, respectively. Cytogenetic studies using fluorescent in situ hybridization (FISH) on mitotic and pachytene chromosomes confirmed the location of DMI1, DMI2, and DMI3 on chromosomes 2, 5, and 8. FISH-pachytene studies revealed that the three genes are in euchromatic regions of the genome, with a ratio of genetic to cytogenetic distances between 0.8 and 1.6 cM per microm in the DMI1, DMI2, and DMI3 regions. Through grafting experiments, we showed that the genetic control of the dmi1, dmi2, and dmi3 nodulation phenotypes is determined at the root level. This means that mutants can be transformed by Agrobacterium rhizogenes to accelerate the complementation step of map-based cloning projects for DMI1, DMI2, and DMI3.

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Research paper thumbnail of The Early Nodulin Gene MtN6 Is a Novel Marker for Events Preceding Infection of Medicago truncatula Roots by Sinorhizobium meliloti

Molecular Plant-Microbe Interactions, 1999

MtN6 belongs to a series of cDNA clones representing Medicago truncatula genes transcriptionally ... more MtN6 belongs to a series of cDNA clones representing Medicago truncatula genes transcriptionally activated during nodulation by Sinorhizobium meliloti (P. Gamas, F. de Carvalho Niebel, N. Lescure, and J. V. Cullimore, Mol. Plant-Microbe Interact. 9:233-242, 1996). We show here by in situ hybridization that MtN6 transcripts specifically accumulate first at very localized regions in the outer root cell layers, corresponding to outer cortical cells containing preinfection threads. At later stages, MtN6 expression is observed ahead of growing infection threads, including in the infection zone of mature root nodules. Interestingly, regulation of MtN6 is clearly distinct from that of other early nodulins expressed in the same region of the nodule, in terms of response to bacterial symbiotic mutants and to purified Nod factors. We thus suggest that MtN6 represents the first specific marker of a pathway involved in preparation to infection, which is at least partly controlled by Nod factors. Finally, we discuss the intriguing sequence homology shown by MtN6 to a protein from Emericella (Aspergillus) nidulans, FluG, that plays a key role in controlling the organogenesis of conidiophores (B. N. Lee and T. H. Adams, Genes Dev. 8:641-651, 1994).

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Research paper thumbnail of Symbiosis-Specific Expression of Two Medicago truncatula Nodulin Genes, MtN1 and MtN13 , Encoding Products Homologous to Plant Defense Proteins

Molecular Plant-Microbe Interactions, 1998

Two Medicago truncatula nodulin genes putatively encoding proteins structurally related to two cl... more Two Medicago truncatula nodulin genes putatively encoding proteins structurally related to two classes of proteins commonly associated with plant defense reactions have been characterized. MtN1 is homologous to two small, cysteine-rich, pathogen-inducible proteins from pea (pI39 and pI230), whereas MtN13 is closely related to the PR10 family of pathogenesis-related proteins. We show that neither MtN1 nor MtN13 is induced in leaves in response to pathogenic bacteria, and that both are exclusively expressed during nodulation. In situ hybridization experiments as well as Northern (RNA) studies of interactions between M. truncatula and either wild-type Rhizobium meliloti or mutants deficient in infection establish that MtN1 is associated with the infection process, while MtN13 represents the first specific marker described for the nodule outer cortex. Possible roles for MtN1 and MtN13 are discussed. We also present the identification of another member of the PR10 family, designated as MtPR10-1, whose regulation is strikingly different from that observed for MtN13, being constitutively expressed in roots and pathogen-inducible in leaves.

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Research paper thumbnail of Medicago truncatula ENOD11 : A Novel RPRP-Encoding Early Nodulin Gene Expressed During Mycorrhization in Arbuscule-Containing Cells

Molecular Plant-Microbe Interactions, 2001

Leguminous plants establish endosymbiotic associations with both rhizobia (nitrogen fixation) and... more Leguminous plants establish endosymbiotic associations with both rhizobia (nitrogen fixation) and arbuscular mycorrhizal fungi (phosphate uptake). These associations involve controlled entry of the soil microsymbiont into the root and the coordinated differentiation of the respective partners to generate the appropriate exchange interfaces. As part of a study to evaluate analogies at the molecular level between these two plant-microbe interactions, we focused on genes from Medicago truncatula encoding putative cell wall repetitive proline-rich proteins (RPRPs) expressed during the early stages of root nodulation. Here we report that a novel RPRP-encoding gene, MtENOD11, is transcribed during preinfection and infection stages of nodulation in root and nodule tissues. By means of reverse transcription-polymerase chain reaction and a promoter-reporter gene strategy, we demonstrate that this gene is also expressed during root colonization by endomycorrhizal fungi in inner cortical cells containing recently formed arbuscules. In contrast, no activation of MtENOD11 is observed during root colonization by a nonsymbiotic, biotrophic Rhizoctonia fungal species. Analysis of transgenic Medicago spp. plants expressing pMtENOD11-gusA also revealed that this gene is transcribed in a variety of nonsymbiotic specialized cell types in the root, shoot, and developing seed, either sharing high secretion/metabolite exchange activity or subject to regulated modifications in cell shape. The potential role of early nodulins with atypical RPRP structures such as ENOD11 and ENOD12 in symbiotic and nonsymbiotic cellular contexts is discussed.

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Research paper thumbnail of api , A Novel Medicago truncatula Symbiotic Mutant Impaired in Nodule Primordium Invasion

Molecular Plant-Microbe Interactions, 2008

Genetic approaches have proved to be extremely useful in dissecting the complex nitrogen-fixing R... more Genetic approaches have proved to be extremely useful in dissecting the complex nitrogen-fixing Rhizobium-legume endosymbiotic association. Here we describe a novel Medicago truncatula mutant called api, whose primary phenotype is the blockage of rhizobial infection just prior to nodule primordium invasion, leading to the formation of large infection pockets within the cortex of noninvaded root outgrowths. The mutant api originally was identified as a double symbiotic mutant associated with a new allele (nip-3) of the NIP/LATD gene, following the screening of an ethylmethane sulphonate-mutagenized population. Detailed characterization of the segregating single api mutant showed that rhizobial infection is also defective at the earlier stage of infection thread (IT) initiation in root hairs, as well as later during IT growth in the small percentage of nodules which overcome the primordium invasion block. Neither modulating ethylene biosynthesis (with L-alpha-(2-aminoethoxyvinylglycine or 1-aminocyclopropane-1-carboxylic acid) nor reducing ethylene sensitivity in a skl genetic background alters the basic api phenotype, suggesting that API function is not closely linked to ethylene metabolism or signaling. Genetic mapping places the API gene on the upper arm of the M. truncatula linkage group 4, and epistasis analyses show that API functions downstream of BIT1/ERN1 and LIN and upstream of NIP/LATD and the DNF genes.

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Research paper thumbnail of Saprophytic Intracellular Rhizobia in Alfalfa Nodules

Molecular Plant-Microbe Interactions, 2000

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Research paper thumbnail of Alfalfa nodulation in the absence of Rhizobium

MGG Molecular & General Genetics, 1989

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Research paper thumbnail of Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa

Development (Cambridge, England), 1998

Reorganization of the plant cytoskeleton is thought to play an important role during nodule ontog... more Reorganization of the plant cytoskeleton is thought to play an important role during nodule ontogeny. In situ immunolocalisation of tubulin reveals that important cytoskeletal changes, implying a transient disorganization followed by a newly patterned reorganization, occur in indeterminate and determinate nodules. In alfalfa nodules, cytoskeletal changes closely parallel the symbiotic differentiation features related to cell infection, bacterial release, endopolyploidization, cell enlargement, cell spatial organization and organelle ultrastructure and positioning. Moreover, the fact that microtubule disorganization can be correlated with Nod factor internalization in central infected cells suggests that Nod factors are possibly involved in the control of cytoskeletal changes which direct the differentiation of bacteria-containing cells.

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Research paper thumbnail of Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules

Journal of bacteriology, 1990

Bacteroid differentiation was examined in developing and mature alfalfa nodules elicited by wild-... more Bacteroid differentiation was examined in developing and mature alfalfa nodules elicited by wild-type or Fix- mutant strains of Rhizobium meliloti. Ultrastructural studies of wild-type nodules distinguished five steps in bacteroid differentiation (types 1 to 5), each being restricted to a well-defined histological region of the nodule. Correlative studies between nodule development, bacteroid differentiation, and acetylene reduction showed that nitrogenase activity was always associated with the differentiation of the distal zone III of the nodule. In this region, the invaded cells were filled with heterogeneous type 4 bacteroids, the cytoplasm of which displayed an alternation of areas enriched with ribosomes or with DNA fibrils. Cytological studies of complementary halves of transversally sectioned mature nodules confirmed that type 4 bacteroids were always observed in the half of the nodule expressing nitrogenase activity, while the presence of type 5 bacteroids could never be co...

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Research paper thumbnail of Cellular expression and regulation of the Medicago truncatula cytosolic glutamine synthetase genes in root nodules

Plant Molecular Biology, 2000

In this paper we have studied the localisation of expression of the two functional cytosolic glut... more In this paper we have studied the localisation of expression of the two functional cytosolic glutamine synthetase (GS) genes, MtGSa and MtGSb, in root nodules of the model legume Medicago truncatula. We have used a combination of different techniques, including immunocytochemistry, in situ hybridisation and promoter beta-glucuronidase (GUS) fusions in transgenic plants, to provide the means of correlating gene expression with protein localisation. These studies revealed that transcriptional regulation (mRNA synthesis) plays an important part in controlling GS protein levels in nodules of M. truncatula. The major locations of cytosolic GS mRNA and protein are the central tissue, the parenchyma and the pericycle of the vascular bundles. These findings indicate that in nodules, GS might be involved in other physiological processes in addition to the primary assimilation of ammonia released by the bacterial nitrogenase. The two genes show different but overlapping patterns of expression with MtGSa being the major gene expressed in the infected cells of the nodule. Promoter fragments of 2.6 kb and 3.1 kb of MtGSa and MtGSb, respectively, have been sequenced and primer extension revealed that the MtGSb promoter is expressed in nodules from an additional start site that is not used in roots. Generally these fragments in the homologous transgenic system were sufficient to drive GUS expression in almost all the tissues and cell types where GS proteins and transcripts are located except that the MtGSa promoter fragment did not express GUS highly in the nodule infected cells. These results indicate that the cis-acting regulatory elements responsible for infected-cell expression are missing from the MtGSa promoter fragment.

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Research paper thumbnail of Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa

The Plant Journal, 1994

Extracellular lipo-oligosaccharides of Rhizobium, known as Nod factors, play a key role in the mo... more Extracellular lipo-oligosaccharides of Rhizobium, known as Nod factors, play a key role in the molecular signal exchange which leads to the specific nitrogen-fixing symbiotic association between the soil microbe and its host legume. The biological activity of Nod factors and their perception by the host plant during the earliest stages of the Rhizobium/legume interaction have been studied using transgenic alfalfa carrying a fusion between the promoter of the early nodulin gene MtENOD12 and the beta-glucuronidase (GUS) reporter gene. Histochemical staining has shown that GUS accumulates specifically in the differentiating root epidermis, prior to and during root hair emergence, within 2-3 h following the addition of purified Rhizobium meliloti Nod factors. This precocious transcriptional activation of the MtENOD12 gene, reminiscent of that observed after inoculation with intact Rhizobium, implies that the Nod factor signal can be perceived at a developmental stage preceding root hair formation. GUS activity can be detected following treatment with a wide range of R. meliloti Nod factor concentrations down to 10(-13) M, and furthermore, this rapid response to the bacterial elicitor appears to be non-systemic. Significantly, MtENOD12-GUS expression is not observed after inoculation with a R. meliloti nodH mutant which synthesizes exclusively non-sulphated Nod factors. Indeed purified Nod factors which lack the sulphate substituent are approximately 1000-fold less active than their sulphated counterparts. Thus, the triggering of ENOD12 transcription in the alfalfa root epidermis is a rapid molecular response which is subject to the same host-specificity determinant (Nod factor sulphation) that governs the interaction between alfalfa and its bacterial symbiont.

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Research paper thumbnail of Leghaemoglobin gene transcription is triggered in a single cell layer in the indeterminate nitrogen-fixing root nodule of alfalfa

The Plant Journal, 1991

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Research paper thumbnail of Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction

The Plant Journal, 1993

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Research paper thumbnail of Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway

THE PLANT CELL ONLINE, 2000

Rhizobium nodulation (Nod) factors are lipo-chitooligosaccharides that act as symbiotic signals, ... more Rhizobium nodulation (Nod) factors are lipo-chitooligosaccharides that act as symbiotic signals, eliciting several key developmental responses in the roots of legume hosts. Using nodulation-defective mutants of Medicago truncatula, we have started to dissect the ...

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Research paper thumbnail of Rhizobium meliloti Elicits Transient Expression of the Early Nodulin Gene ENOD12 in the Differentiating Root Epidermis of Transgenic Alfalfa

THE PLANT CELL ONLINE, 1992

Page 1. The Plant Cell, Vol. 4, 1199-1211, October 1992 O 1992 American Society of Plant Physiolo... more Page 1. The Plant Cell, Vol. 4, 1199-1211, October 1992 O 1992 American Society of Plant Physiologists Rhizobium meliloti Elicits Transient Expression of the Early Nodulin Gene ENOD12 in the Differentiating Root Epidermis of Transgenic Alfalfa ...

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Research paper thumbnail of TheRhizobium-legume symbiosis Two methods to discriminate between nodules and other root-derived structures

Protoplasma, 1989

... G. Truchet*, S. Camut, F. de Billy, R. Odorico, and J. Vasse ... commercial solution containi... more ... G. Truchet*, S. Camut, F. de Billy, R. Odorico, and J. Vasse ... commercial solution containing 12.5% of active chlo-rine and diluted with distilled water (V/V). Whole plants, collected at different times following inocuiation, were immersed in this so-lution for 15 rain under vacuum ...

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Research paper thumbnail of The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection

Proceedings of the National Academy of Sciences, 2008

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Research paper thumbnail of Transcription Reprogramming during Root Nodule Development in Medicago truncatula

PLoS ONE, 2011

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Research paper thumbnail of The MtMMPL1 Early Nodulin Is a Novel Member of the Matrix Metalloendoproteinase Family with a Role in Medicago truncatula Infection by Sinorhizobium meliloti

PLANT PHYSIOLOGY, 2007

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Research paper thumbnail of Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa

Nature, 1991

RHIZOBIUM meliloti is a symbiotic bacterium that elicits the morphogenesis of nitrogen-fixing nod... more RHIZOBIUM meliloti is a symbiotic bacterium that elicits the morphogenesis of nitrogen-fixing nodules, specific organs on the roots of alfalfa (Medicago sativa) 1 . In R. meliloti a series of nodulation (nod) genes have been identified which are involved in root-hair curling and infection and ...

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Research paper thumbnail of Genetic and Cytogenetic Mapping of DMI1, DMI2 , and DMI3 Genes of Medicago truncatula Involved in Nod Factor Transduction, Nodulation, and Mycorrhization

Molecular Plant-Microbe Interactions, 2002

The DMI1, DMI2, and DMI3 genes of Medicago truncatula, which are required for both nodulation and... more The DMI1, DMI2, and DMI3 genes of Medicago truncatula, which are required for both nodulation and mycorrhization, control early steps of Nod factor signal transduction. Here, we have used diverse approaches to pave the way for the map-based cloning of these genes. Molecular amplification fragment length polymorphism markers linked to the three genes were identified by bulked segregant analysis. Integration of these markers into the general genetic map of M. truncatula revealed that DMI1, DMI2, and DMI3 are located on linkage groups 2, 5, and 8, respectively. Cytogenetic studies using fluorescent in situ hybridization (FISH) on mitotic and pachytene chromosomes confirmed the location of DMI1, DMI2, and DMI3 on chromosomes 2, 5, and 8. FISH-pachytene studies revealed that the three genes are in euchromatic regions of the genome, with a ratio of genetic to cytogenetic distances between 0.8 and 1.6 cM per microm in the DMI1, DMI2, and DMI3 regions. Through grafting experiments, we showed that the genetic control of the dmi1, dmi2, and dmi3 nodulation phenotypes is determined at the root level. This means that mutants can be transformed by Agrobacterium rhizogenes to accelerate the complementation step of map-based cloning projects for DMI1, DMI2, and DMI3.

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Research paper thumbnail of The Early Nodulin Gene MtN6 Is a Novel Marker for Events Preceding Infection of Medicago truncatula Roots by Sinorhizobium meliloti

Molecular Plant-Microbe Interactions, 1999

MtN6 belongs to a series of cDNA clones representing Medicago truncatula genes transcriptionally ... more MtN6 belongs to a series of cDNA clones representing Medicago truncatula genes transcriptionally activated during nodulation by Sinorhizobium meliloti (P. Gamas, F. de Carvalho Niebel, N. Lescure, and J. V. Cullimore, Mol. Plant-Microbe Interact. 9:233-242, 1996). We show here by in situ hybridization that MtN6 transcripts specifically accumulate first at very localized regions in the outer root cell layers, corresponding to outer cortical cells containing preinfection threads. At later stages, MtN6 expression is observed ahead of growing infection threads, including in the infection zone of mature root nodules. Interestingly, regulation of MtN6 is clearly distinct from that of other early nodulins expressed in the same region of the nodule, in terms of response to bacterial symbiotic mutants and to purified Nod factors. We thus suggest that MtN6 represents the first specific marker of a pathway involved in preparation to infection, which is at least partly controlled by Nod factors. Finally, we discuss the intriguing sequence homology shown by MtN6 to a protein from Emericella (Aspergillus) nidulans, FluG, that plays a key role in controlling the organogenesis of conidiophores (B. N. Lee and T. H. Adams, Genes Dev. 8:641-651, 1994).

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Research paper thumbnail of Symbiosis-Specific Expression of Two Medicago truncatula Nodulin Genes, MtN1 and MtN13 , Encoding Products Homologous to Plant Defense Proteins

Molecular Plant-Microbe Interactions, 1998

Two Medicago truncatula nodulin genes putatively encoding proteins structurally related to two cl... more Two Medicago truncatula nodulin genes putatively encoding proteins structurally related to two classes of proteins commonly associated with plant defense reactions have been characterized. MtN1 is homologous to two small, cysteine-rich, pathogen-inducible proteins from pea (pI39 and pI230), whereas MtN13 is closely related to the PR10 family of pathogenesis-related proteins. We show that neither MtN1 nor MtN13 is induced in leaves in response to pathogenic bacteria, and that both are exclusively expressed during nodulation. In situ hybridization experiments as well as Northern (RNA) studies of interactions between M. truncatula and either wild-type Rhizobium meliloti or mutants deficient in infection establish that MtN1 is associated with the infection process, while MtN13 represents the first specific marker described for the nodule outer cortex. Possible roles for MtN1 and MtN13 are discussed. We also present the identification of another member of the PR10 family, designated as MtPR10-1, whose regulation is strikingly different from that observed for MtN13, being constitutively expressed in roots and pathogen-inducible in leaves.

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Research paper thumbnail of Medicago truncatula ENOD11 : A Novel RPRP-Encoding Early Nodulin Gene Expressed During Mycorrhization in Arbuscule-Containing Cells

Molecular Plant-Microbe Interactions, 2001

Leguminous plants establish endosymbiotic associations with both rhizobia (nitrogen fixation) and... more Leguminous plants establish endosymbiotic associations with both rhizobia (nitrogen fixation) and arbuscular mycorrhizal fungi (phosphate uptake). These associations involve controlled entry of the soil microsymbiont into the root and the coordinated differentiation of the respective partners to generate the appropriate exchange interfaces. As part of a study to evaluate analogies at the molecular level between these two plant-microbe interactions, we focused on genes from Medicago truncatula encoding putative cell wall repetitive proline-rich proteins (RPRPs) expressed during the early stages of root nodulation. Here we report that a novel RPRP-encoding gene, MtENOD11, is transcribed during preinfection and infection stages of nodulation in root and nodule tissues. By means of reverse transcription-polymerase chain reaction and a promoter-reporter gene strategy, we demonstrate that this gene is also expressed during root colonization by endomycorrhizal fungi in inner cortical cells containing recently formed arbuscules. In contrast, no activation of MtENOD11 is observed during root colonization by a nonsymbiotic, biotrophic Rhizoctonia fungal species. Analysis of transgenic Medicago spp. plants expressing pMtENOD11-gusA also revealed that this gene is transcribed in a variety of nonsymbiotic specialized cell types in the root, shoot, and developing seed, either sharing high secretion/metabolite exchange activity or subject to regulated modifications in cell shape. The potential role of early nodulins with atypical RPRP structures such as ENOD11 and ENOD12 in symbiotic and nonsymbiotic cellular contexts is discussed.

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Research paper thumbnail of api , A Novel Medicago truncatula Symbiotic Mutant Impaired in Nodule Primordium Invasion

Molecular Plant-Microbe Interactions, 2008

Genetic approaches have proved to be extremely useful in dissecting the complex nitrogen-fixing R... more Genetic approaches have proved to be extremely useful in dissecting the complex nitrogen-fixing Rhizobium-legume endosymbiotic association. Here we describe a novel Medicago truncatula mutant called api, whose primary phenotype is the blockage of rhizobial infection just prior to nodule primordium invasion, leading to the formation of large infection pockets within the cortex of noninvaded root outgrowths. The mutant api originally was identified as a double symbiotic mutant associated with a new allele (nip-3) of the NIP/LATD gene, following the screening of an ethylmethane sulphonate-mutagenized population. Detailed characterization of the segregating single api mutant showed that rhizobial infection is also defective at the earlier stage of infection thread (IT) initiation in root hairs, as well as later during IT growth in the small percentage of nodules which overcome the primordium invasion block. Neither modulating ethylene biosynthesis (with L-alpha-(2-aminoethoxyvinylglycine or 1-aminocyclopropane-1-carboxylic acid) nor reducing ethylene sensitivity in a skl genetic background alters the basic api phenotype, suggesting that API function is not closely linked to ethylene metabolism or signaling. Genetic mapping places the API gene on the upper arm of the M. truncatula linkage group 4, and epistasis analyses show that API functions downstream of BIT1/ERN1 and LIN and upstream of NIP/LATD and the DNF genes.

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