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1.
J Exp Bot ; 2024 Jun 28.
Artículo en Inglés | MEDLINE | ID: mdl-38941269

RESUMEN

Plants use a combination of sophisticated local and systemic pathways to optimize growth depending on heterogeneous nutrient availability in the soil. Legume plants can acquire mineral nitrogen (N) either through their roots or via a symbiotic interaction with N-fixing rhizobia bacteria housed in so-called root nodules. To identify shoot-to-root systemic signals acting in Medicago truncatula plants at N-deficit or N-satiety, plants were grown in a split-root experimental design, in which either high or low N was provided to a half of the root system, allowing the analysis of systemic pathways independently of any local N response. Among the plant hormone families analyzed, the cytokinin trans-Zeatin accumulated in plants at N-satiety. Cytokinin application by petiole feeding led to an inhibition of both root growth and nodulation. In addition, an exhaustive analysis of miRNAs revealed that miR2111 accumulates systemically under N-deficit in both shoots and non-treated distant roots, whereas a miRNA related to inorganic Phosphate (Pi)-acquisition, the miR399, does so in plants grown at N-satiety. These two accumulation patterns are dependent on CRA2 (Compact Root Architecture 2), a receptor required for CEP (C-terminally Encoded Peptide) signaling. Constitutive ectopic expression of the miR399 reduced nodule numbers and root biomass depending on Pi availability, suggesting that the miR399-dependent Pi-acquisition regulatory module controlled by N-availability affects the development of the whole legume plant root system.

2.
New Phytol ; 241(1): 24-27, 2024 Jan.
Artículo en Inglés | MEDLINE | ID: mdl-37924218

RESUMEN

C-terminally encoded peptides (CEP) signaling peptides are drivers of systemic pathways regulating nitrogen (N) acquisition in different plants, from Arabidopsis to legumes, depending on mineral N availability (e.g. nitrate) and on the whole plant N demand. Recent studies in the Medicago truncatula model legume revealed how root-produced CEP peptides control the root competence for endosymbiosis with N fixing rhizobia soil bacteria through the activity of the Compact Root Architecture 2 (CRA2) CEP receptor in shoots. Among CEP genes, MtCEP7 was shown to be tightly linked to nodulation, and the dynamic temporal regulation of its expression reflects the plant ability to maintain a different symbiotic root competence window depending on the symbiotic efficiency of the rhizobium strain, as well as to reinitiate a new window of root competence for nodulation.


Asunto(s)
Medicago truncatula , Rhizobium , Nódulos de las Raíces de las Plantas/microbiología , Nodulación de la Raíz de la Planta/genética , Simbiosis/fisiología , Raíces de Plantas/metabolismo , Señales de Clasificación de Proteína , Rhizobium/fisiología , Medicago truncatula/microbiología , Péptidos/metabolismo , Fijación del Nitrógeno , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo
3.
Sante Publique ; 35(2): 159-170, 2023 08 10.
Artículo en Francés | MEDLINE | ID: mdl-37558621

RESUMEN

Introduction: The uptake rate of colorectal cancer screening remains insufficient in France and decreases as the level of deprivation increases. Participants' health literacy appears to be an important determinant of screening uptake. Aim of the study: The aim of this study, nested in our multicenter-randomized controlled trial, was to present the development and acceptability of interventional material (training and a pictorial brochure) for general practitioners and healthcare users in disadvantaged geographical areas using a participatory involvement approach. Methods: The development of the brochure and the training was carried out in three stages, two for the development, usability, and acceptability testing and a third for its evaluation with the target audience. We used a qualitative approach based on focus groups and cognitive interviews. The qualitative analysis was based on Morville's "Honeycomb" conceptual model and the COREQ checklist. Results: The development and test of the acceptability of the material enabled us to adjust the content of the training by proposing examples that were more rooted in professional reality, and to produce a brochure that was easy to read, understand, acceptable and adapted to the intervention's targeted audience. Conclusions: This experience illustrates in a concrete way the feasibility of public participation and its value in the context of interventional research, and more generally in the creation of interventional material.


Introduction: Le taux de participation au dépistage du cancer colorectal reste insuffisant en France et diminue à mesure que le niveau de précarité augmente. La littératie en santé est un déterminant important du recours au dépistage. But de l'étude: Cette étude, nichée dans notre essai randomisé multicentrique, a pour but de présenter la procédure d'élaboration (procédé itératif de test d'utilisabilité et d'acceptabilité) et de vérification de l'acceptabilité de l'intervention (formation et brochure imagée) ciblant les médecins généralistes et usagers du soin dans des zones géographiques défavorisées, selon une approche participative. Méthodes: Le développement de la brochure et de la formation a été réalisé en trois étapes : deux pour l'élaboration et tests itératifs d'utilisabilité et acceptabilité et une troisième pour vérifier l'acceptabilité auprès des publics cibles. Nous avons utilisé une approche qualitative par focus group et entretiens individuels cognitifs dont l'analyse repose sur le « nid d'abeille ¼ de Morville et la grille COREQ. Résultats: Le développement itératif et la vérification de l'acceptabilité du matériel nous ont permis, d'une part, de réaliser des ajustements quant au contenu de la formation, en proposant des exemples plus ancrés dans la réalité professionnelle et, d'autre part, de produire une brochure imagée facile à lire et à comprendre, acceptable et adaptée au public ciblé par l'intervention. Conclusions: Cette expérience illustre, de manière concrète, la faisabilité de cette modalité de participation des publics concernés et son intérêt dans le cadre de la recherche interventionnelle et, plus généralement, dans le matériel interventionnel.


Asunto(s)
Médicos Generales , Salud Pública , Humanos , Participación de la Comunidad , Grupos Focales , Francia
4.
Plant Physiol ; 191(3): 2012-2026, 2023 03 17.
Artículo en Inglés | MEDLINE | ID: mdl-36653329

RESUMEN

Legumes acquire soil nutrients through nitrogen-fixing root nodules and lateral roots. To balance the costs and benefits of nodulation, legumes negatively control root nodule number by autoregulatory and hormonal pathways. How legumes simultaneously coordinate root nodule and lateral root development to procure nutrients remains poorly understood. In Medicago (Medicago truncatula), a subset of mature C-TERMINALLY ENCODED PEPTIDE (CEP) hormones can systemically promote nodule number, but all CEP hormones tested to date negatively regulate lateral root number. Here we showed that Medicago CEP7 produces a mature peptide, SymCEP7, that promotes nodulation from the shoot without compromising lateral root number. Rhizobial inoculation induced CEP7 in the susceptible root nodulation zone in a Nod factor-dependent manner, and, in contrast to other CEP genes, its transcription level was elevated in the ethylene signaling mutant sickle. Using mass spectrometry, fluorescence microscopy and expression analysis, we demonstrated that SymCEP7 activity requires the COMPACT ROOT ARCHITECTURE 2 receptor and activates the shoot-to-root systemic effector, miR2111. Shoot-applied SymCEP7 rapidly promoted nodule number in the pM to nM range at concentrations up to five orders of magnitude lower than effects mediated by root-applied SymCEP7. Shoot-applied SymCEP7 also promoted nodule number in White Clover (Trifolium repens) and Lotus (Lotus japonicus), which suggests that this biological function may be evolutionarily conserved. We propose that SymCEP7 acts in the Medicago shoot to counter balance the autoregulation pathways induced rapidly by rhizobia to enable nodulation without compromising lateral root growth, thus promoting the acquisition of nutrients other than nitrogen to support their growth.


Asunto(s)
Lotus , Medicago truncatula , Rhizobium , Trifolium , Nodulación de la Raíz de la Planta/genética , Raíces de Plantas/metabolismo , Medicago truncatula/metabolismo , Rhizobium/fisiología , Lotus/genética , Péptidos/metabolismo , Trifolium/metabolismo , Hormonas/metabolismo , Nitrógeno/metabolismo , Nódulos de las Raíces de las Plantas/metabolismo , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo , Simbiosis , Regulación de la Expresión Génica de las Plantas
6.
Mol Plant ; 15(12): 1868-1888, 2022 12 05.
Artículo en Inglés | MEDLINE | ID: mdl-36321199

RESUMEN

Medicago truncatula is a model legume species that has been studied for decades to understand the symbiotic relationship between legumes and soil bacteria collectively named rhizobia. This symbiosis called nodulation is initiated in roots with the infection of root hair cells by the bacteria, as well as the initiation of nodule primordia from root cortical, endodermal, and pericycle cells, leading to the development of a new root organ, the nodule, where bacteria fix and assimilate the atmospheric dinitrogen for the benefit of the plant. Here, we report the isolation and use of the nuclei from mock and rhizobia-inoculated roots for the single nuclei RNA-seq (sNucRNA-seq) profiling to gain a deeper understanding of early responses to rhizobial infection in Medicago roots. A gene expression map of the Medicago root was generated, comprising 25 clusters, which were annotated as specific cell types using 119 Medicago marker genes and orthologs to Arabidopsis cell-type marker genes. A focus on root hair, cortex, endodermis, and pericycle cell types, showing the strongest differential regulation in response to a short-term (48 h) rhizobium inoculation, revealed not only known genes and functional pathways, validating the sNucRNA-seq approach, but also numerous novel genes and pathways, allowing a comprehensive analysis of early root symbiotic responses at a cell type-specific level.


Asunto(s)
Medicago truncatula , Medicago truncatula/genética
7.
Trends Plant Sci ; 26(4): 392-406, 2021 04.
Artículo en Inglés | MEDLINE | ID: mdl-33358560

RESUMEN

Plant nutrient acquisition is tightly regulated by resource availability and metabolic needs, implying the existence of communication between roots and shoots to ensure their integration at the whole-plant level. Here, we focus on systemic signaling pathways controlling nitrogen (N) nutrition, achieved both by the root import of mineral N and, in legume plants, through atmospheric N fixation by symbiotic bacteria inside dedicated root nodules. We explore features conserved between systemic pathways repressing or enhancing symbiotic N fixation and the regulation of mineral N acquisition by roots, as well as their integration with other environmental factors, such as phosphate, light, and CO2 availability.


Asunto(s)
Fabaceae , Nodulación de la Raíz de la Planta , Nitrógeno , Fijación del Nitrógeno , Raíces de Plantas , Nódulos de las Raíces de las Plantas , Simbiosis
8.
Nat Commun ; 11(1): 3167, 2020 06 23.
Artículo en Inglés | MEDLINE | ID: mdl-32576831

RESUMEN

Legumes tightly regulate nodule number to balance the cost of supporting symbiotic rhizobia with the benefits of nitrogen fixation. C-terminally Encoded Peptides (CEPs) and CLAVATA3-like (CLE) peptides positively and negatively regulate nodulation, respectively, through independent systemic pathways, but how these regulations are coordinated remains unknown. Here, we show that rhizobia, Nod Factors, and cytokinins induce a symbiosis-specific CEP gene, MtCEP7, which positively regulates rhizobial infection. Via grafting and split root studies, we reveal that MtCEP7 increases nodule number systemically through the MtCRA2 receptor. MtCEP7 and MtCLE13 expression in rhizobia-inoculated roots rely on the MtCRE1 cytokinin receptor and on the MtNIN transcription factor. MtNIN binds and transactivates MtCEP7 and MtCLE13, and a NIN Binding Site (NBS) identified within the proximal MtCEP7 promoter is required for its symbiotic activation. Overall, these results demonstrate that a cytokinin-MtCRE1-MtNIN regulatory module coordinates the expression of two antagonistic, symbiosis-related, peptide hormones from different families to fine-tune nodule number.


Asunto(s)
Péptidos/química , Nodulación de la Raíz de la Planta/fisiología , Rhizobium/metabolismo , Factores de Transcripción/metabolismo , Citocininas/metabolismo , Epidermis , Regulación de la Expresión Génica de las Plantas , Lotus/metabolismo , Medicago truncatula , Péptidos/genética , Proteínas de Plantas , Nodulación de la Raíz de la Planta/genética , Raíces de Plantas/metabolismo , Regiones Promotoras Genéticas , Proteínas Quinasas , Señales de Clasificación de Proteína/genética , Nódulos de las Raíces de las Plantas , Sinorhizobium meliloti/metabolismo , Simbiosis
9.
Plant Physiol ; 183(3): 1319-1330, 2020 07.
Artículo en Inglés | MEDLINE | ID: mdl-32376762

RESUMEN

Nitrogen-fixing root nodulation in legumes challenged with nitrogen-limiting conditions requires infection of the root hairs by soil symbiotic bacteria, collectively referred to as rhizobia, and the initiation of cell divisions in the root cortex. Cytokinin hormones are critical for early nodulation to coordinate root nodule organogenesis and the progression of bacterial infections. Cytokinin signaling involves regulation of the expression of cytokinin primary response genes by type-B response regulator (RRB) transcription factors. RNA interference or mutation of MtRRB3, the RRB-encoding gene most strongly expressed in Medicago truncatula roots and nodules, significantly decreased the number of nodules formed, indicating a function of this RRB in nodulation initiation. Fewer infection events were also observed in rrb3 mutant roots associated with a reduced Nod factor induction of the Early Nodulin 11 (MtENOD11) infection marker, and of the cytokinin-regulated Nodulation Signaling Pathway 2 (Mt NSP2) gene. Rhizobial infections correlate with an expansion of the nuclear area, suggesting the activation of endoreduplication cycles linked to the cytokinin-regulated Cell Cycle Switch 52A (Mt CCS52A) gene. Although no significant difference in nucleus size and endoreduplication were detected in rhizobia-infected rrb3 mutant roots, expression of the MtCCS52A endoreduplication marker was reduced. As the MtRRB3 expression pattern overlaps with those of MtNSP2 and MtCCS52A in roots and nodule primordia, chromatin immunoprecipitation-quantitative PCR and protoplast trans-activation assays were used to show that MtRRB3 can interact with and trans-activate MtNSP2 and MtCCS52A promoters. Overall, we highlight that the MtRRB3 cytokinin signaling transcription factor coordinates the expression of key early nodulation genes.


Asunto(s)
Citocininas/metabolismo , Nodulación de la Raíz de la Planta , Transducción de Señal , Factores de Transcripción/metabolismo , Tamaño del Núcleo Celular , Endorreduplicación , Regulación de la Expresión Génica de las Plantas , Genes de Plantas , Medicago truncatula/genética , Medicago truncatula/microbiología , Fenotipo , Proteínas de Plantas/química , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo , Nodulación de la Raíz de la Planta/genética , Regiones Promotoras Genéticas , Unión Proteica , Dominios Proteicos , Sinorhizobium meliloti/fisiología , Activación Transcripcional/genética
10.
Curr Biol ; 30(7): 1339-1345.e3, 2020 04 06.
Artículo en Inglés | MEDLINE | ID: mdl-32109394

RESUMEN

Nitrogen-deprived legume plants form new root organs, the nodules, following a symbiosis with nitrogen-fixing rhizobial bacteria [1]. Because this interaction is beneficial for the plant but has a high energetic cost, nodulation is tightly controlled by host plants through systemic pathways (acting at long distance) to promote or limit rhizobial infections and nodulation depending on earlier infections and on nitrogen availability [2]. In the Medicago truncatula model legume, CLE12 (Clavata3/Embryo surrounding region 12) and CLE13 signaling peptides produced in nodulated roots act in shoots through the SUNN (Super Numeric Nodule) receptor to negatively regulate nodulation and therefore autoregulate nodule number [3-5]. Conversely, CEP (C-terminally Encoded Peptide) signaling peptides produced in nitrogen-starved roots act in shoots through the CRA2 (Compact Root Architecture 2) receptor to promote nodulation already in the absence of rhizobia [6-9]. We show in this study that a downstream shoot-to-root signaling effector of these systemic pathways is the shoot-produced miR2111 microRNA [10] that negatively regulates TML1 (Too Much Love 1) and TML2 [11] transcripts accumulation in roots, ultimately promoting nodulation. Low nitrogen conditions and CEP1 signaling peptides induce in the absence of rhizobia the production of miR2111 depending on CRA2 activity in shoots, thus favoring root competence for nodulation. Together with the SUNN pathway negatively regulating the same miR2111 systemic effector when roots are nodulated, this allows a dynamic fine-tuning of the nodulation capacity of legume roots by nitrogen availability and rhizobial cues.


Asunto(s)
Medicago truncatula/fisiología , MicroARNs/genética , Proteínas de Plantas/genética , Nodulación de la Raíz de la Planta/genética , ARN de Planta/genética , Medicago truncatula/genética , MicroARNs/metabolismo , Proteínas de Plantas/metabolismo , ARN de Planta/metabolismo , Nódulos de las Raíces de las Plantas/genética , Nódulos de las Raíces de las Plantas/fisiología
11.
Sci Rep ; 9(1): 2335, 2019 02 20.
Artículo en Inglés | MEDLINE | ID: mdl-30787350

RESUMEN

The root system displays a remarkable plasticity that enables plants to adapt to changing environmental conditions. This plasticity is tightly linked to the activity of root apical meristems (RAMs) and to the formation of lateral roots, both controlled by related hormonal crosstalks. In Arabidopsis thaliana, gibberellins (GAs) were shown to positively control RAM growth and the formation of lateral roots. However, we showed in Medicago truncatula that GAs negatively regulate root growth and RAM size as well as the number of lateral roots depending at least on the MtDELLA1 protein. By using confocal microscopy and molecular analyses, we showed that GAs primarily regulate RAM size by affecting cortical cell expansion and additionally negatively regulate a subset of cytokinin-induced root expansin encoding genes. Moreover, GAs reduce the number of cortical cell layers, resulting in the formation of both shorter and thinner roots. These results suggest contrasting effects of GA regulations on the root system architecture depending on plant species.


Asunto(s)
Giberelinas/farmacología , Medicago truncatula/crecimiento & desarrollo , Raíces de Plantas/crecimiento & desarrollo , Medicago truncatula/citología , Medicago truncatula/efectos de los fármacos , Meristema/anatomía & histología , Meristema/citología , Meristema/efectos de los fármacos , Proteínas de Plantas/metabolismo , Raíces de Plantas/efectos de los fármacos
12.
J Exp Bot ; 70(4): 1407-1417, 2019 02 20.
Artículo en Inglés | MEDLINE | ID: mdl-30753553

RESUMEN

The number of legume root nodules resulting from a symbiosis with rhizobia is tightly controlled by the plant. Certain members of the CLAVATA3/Embryo Surrounding Region (CLE) peptide family, specifically MtCLE12 and MtCLE13 in Medicago truncatula, act in the systemic autoregulation of nodulation (AON) pathway that negatively regulates the number of nodules. Little is known about the molecular pathways that operate downstream of the AON-related CLE peptides. Here, by means of a transcriptome analysis, we show that roots ectopically expressing MtCLE13 deregulate only a limited number of genes, including three down-regulated genes encoding lysin motif receptor-like kinases (LysM-RLKs), among which are the nodulation factor (NF) receptor NF Perception gene (NFP) and two up-regulated genes, MtTML1 and MtTML2, encoding Too Much Love (TML)-related Kelch-repeat containing F-box proteins. The observed deregulation was specific for the ectopic expression of nodulation-related MtCLE genes and depended on the Super Numeric Nodules (SUNN) AON RLK. Moreover, overexpression and silencing of these two MtTML genes demonstrated that they play a role in the negative regulation of nodule numbers. Hence, the identified MtTML genes are the functional counterpart of the Lotus japonicus TML gene shown to be central in the AON pathway. Additionally, we propose that the down-regulation of a subset of LysM-RLK-encoding genes, among which is NFP, might contribute to the restriction of further nodulation once the first nodules have been formed.


Asunto(s)
Regulación hacia Abajo , Medicago truncatula/fisiología , Proteínas de Plantas/genética , Nodulación de la Raíz de la Planta/genética , Regulación de la Expresión Génica de las Plantas , Homeostasis/genética , Medicago truncatula/genética , Proteínas de Plantas/metabolismo , Nódulos de las Raíces de las Plantas/metabolismo
13.
Plant Physiol ; 180(1): 559-570, 2019 05.
Artículo en Inglés | MEDLINE | ID: mdl-30782966

RESUMEN

Plant systemic signaling pathways allow the integration and coordination of shoot and root organ metabolism and development at the whole-plant level depending on nutrient availability. In legumes, two systemic pathways have been reported in the Medicago truncatula model to regulate root nitrogen-fixing symbiotic nodulation. Both pathways involve leucine-rich repeat receptor-like kinases acting in shoots and proposed to perceive signaling peptides produced in roots depending on soil nutrient availability. In this study, we characterized in the M. truncatula Jemalong A17 genotype a mutant allelic series affecting the Compact Root Architecture2 (CRA2) receptor. These analyses revealed that this pathway acts systemically from shoots to positively regulate nodulation and is required for the activity of carboxyl-terminally encoded peptides (CEPs). In addition, we generated a double mutant to test genetic interactions of the CRA2 systemic pathway with the CLAVATA3/EMBRYO SURROUNDING REGION peptide (CLE)/Super Numeric Nodule (SUNN) receptor systemic pathway negatively regulating nodule number from shoots, which revealed an intermediate nodule number phenotype close to the wild type. Finally, we showed that the nitrate inhibition of nodule numbers was observed in cra2 mutants but not in sunn and cra2 sunn mutants. Overall, these results suggest that CEP/CRA2 and CLE/SUNN systemic pathways act independently from shoots to regulate nodule numbers.


Asunto(s)
Medicago truncatula/fisiología , Proteínas de Plantas/metabolismo , Nodulación de la Raíz de la Planta/fisiología , Redes y Vías Metabólicas , Mutación , Proteínas de Plantas/genética , Raíces de Plantas/fisiología , Simbiosis
14.
Sci Rep ; 8(1): 2046, 2018 02 01.
Artículo en Inglés | MEDLINE | ID: mdl-29391543

RESUMEN

Peptides are signaling molecules regulating various aspects of plant development, including the balance between cell division and differentiation in different meristems. Among those, CLAVATA3/Embryo Surrounding Region-related (CLE-ESR) peptide activity depends on leucine-rich-repeat receptor-like-kinases (LRR-RLK) belonging to the subclass XI. In legume plants, such as the Medicago truncatula model, specific CLE peptides were shown to regulate root symbiotic nodulation depending on the LRR-RLK SUNN (Super Numeric Nodules). Amongst the ten M. truncatula LRR-RLK most closely related to SUNN, only one showed a nodule-induced expression, and was so-called MtNRLK1 (Nodule-induced Receptor-Like Kinase 1). MtNRLK1 expression is associated to root and nodule vasculature as well as to the proximal meristem and rhizobial infection zone in the nodule apex. Except for the root vasculature, the MtNRLK1 symbiotic expression pattern is different than the one of MtSUNN. Functional analyses either based on RNA interference, insertional mutagenesis, and overexpression of MtNRLK1 however failed to identify a significant nodulation phenotype, either regarding the number, size, organization or nitrogen fixation capacity of the symbiotic organs formed.


Asunto(s)
Medicago/genética , Proteínas de Plantas/metabolismo , Nodulación de la Raíz de la Planta/genética , Proteínas Serina-Treonina Quinasas/metabolismo , Receptores de Péptidos/metabolismo , Regulación de la Expresión Génica de las Plantas , Medicago/crecimiento & desarrollo , Proteínas de Plantas/química , Proteínas de Plantas/genética , Dominios Proteicos , Proteínas Serina-Treonina Quinasas/química , Proteínas Serina-Treonina Quinasas/genética , Receptores de Péptidos/química , Receptores de Péptidos/genética , Regulación hacia Arriba
15.
Mol Cells ; 40(1): 17-23, 2017 Jan.
Artículo en Inglés | MEDLINE | ID: mdl-28152300

RESUMEN

Mitogen-activated protein kinase (MAPK) signaling cascades play critical roles in various cellular events in plants, including stress responses, innate immunity, hormone signaling, and cell specificity. MAPK-mediated stress signaling is also known to negatively regulate nitrogen-fixing symbiotic interactions, but the molecular mechanism of the MAPK signaling cascades underlying the symbiotic nodule development remains largely unknown. We show that the MtMKK5-MtMPK3/6 signaling module negatively regulates the early symbiotic nodule formation, probably upstream of ERN1 (ERF Required for Nodulation 1) and NSP1 (Nod factor Signaling Pathway 1) in Medicago truncatula. The overexpression of MtMKK5 stimulated stress and defense signaling pathways but also reduced nodule formation in M. truncatula roots. Conversely, a MAPK specific inhibitor, U0126, enhanced nodule formation and the expression of an early nodulation marker gene, MtNIN. We found that MtMKK5 directly activates MtMPK3/6 by phosphorylating the TEY motif within the activation loop and that the MtMPK3/6 proteins physically interact with the early nodulation-related transcription factors ERN1 and NSP1. These data suggest that the stress signaling-mediated MtMKK5/MtMPK3/6 module suppresses symbiotic nodule development via the action of early nodulation transcription factors.


Asunto(s)
Medicago truncatula/enzimología , Medicago truncatula/crecimiento & desarrollo , Proteínas Quinasas Activadas por Mitógenos/metabolismo , Sistema de Señalización de MAP Quinasas , Fijación del Nitrógeno , Nodulación de la Raíz de la Planta/fisiología , Nódulos de las Raíces de las Plantas/enzimología , Nódulos de las Raíces de las Plantas/crecimiento & desarrollo , Simbiosis
16.
New Phytol ; 213(2): 822-837, 2017 Jan.
Artículo en Inglés | MEDLINE | ID: mdl-27582377

RESUMEN

We investigated the role of KNOX genes in legume root nodule organogenesis. Class 1 KNOX homeodomain transcription factors (TFs) are involved in plant shoot development and leaf shape diversity. Class 2 KNOX genes are less characterized, even though an antagonistic function relative to class 1 KNOXs was recently proposed. In silico expression data and further experimental validation identified in the Medicago truncatula model legume three class 2 KNOX genes, belonging to the KNAT3/4/5-like subclass (Mt KNAT3/4/5-like), as expressed during nodulation from early stages. RNA interference (RNAi)-mediated silencing and overexpression studies were used to unravel a function for KNOX TFs in nodule development. Mt KNAT3/4/5-like genes encoded four highly homologous proteins showing overlapping expression patterns during nodule organogenesis, suggesting functional redundancy. Simultaneous reduction of Mt KNAT3/4/5-like genes indeed led to an increased formation of fused nodule organs, and decreased the expression of the MtEFD (Ethylene response Factor required for nodule Differentiation) TF and its direct target MtRR4, a cytokinin response gene. Class 2 KNOX TFs therefore regulate legume nodule development, potentially through the MtEFD/MtRR4 cytokinin-related regulatory module, and may control nodule organ boundaries and shape like class 2 KNOX function in leaf development.


Asunto(s)
Medicago truncatula/crecimiento & desarrollo , Medicago truncatula/metabolismo , Proteínas de Plantas/metabolismo , Nódulos de las Raíces de las Plantas/crecimiento & desarrollo , Nódulos de las Raíces de las Plantas/metabolismo , Simbiosis , Factores de Transcripción/metabolismo , Biomasa , Regulación de la Expresión Génica de las Plantas , Silenciador del Gen , Genes de Plantas , Medicago truncatula/genética , Modelos Biológicos , Organogénesis/genética , Fenotipo , Nodulación de la Raíz de la Planta/genética , Brotes de la Planta/crecimiento & desarrollo , Simbiosis/genética
17.
Plant Physiol ; 171(4): 2536-48, 2016 08.
Artículo en Inglés | MEDLINE | ID: mdl-27342310

RESUMEN

C-TERMINALLY ENCODED PEPTIDEs (CEPs) control root system architecture in a non-cell-autonomous manner. In Medicago truncatula, MtCEP1 affects root development by increasing nodule formation and inhibiting lateral root emergence by unknown pathways. Here, we show that the MtCEP1 peptide-dependent increase in nodulation requires the symbiotic signaling pathway and ETHYLENE INSENSITIVE2 (EIN2)/SICKLE (SKL), but acts independently of SUPER NUMERIC NODULES. MtCEP1-dependent inhibition of lateral root development acts through an EIN2-independent mechanism. MtCEP1 increases nodulation by promoting rhizobial infections, the developmental competency of roots for nodulation, the formation of fused nodules, and an increase in frequency of nodule development that initiates at proto-phloem poles. These phenotypes are similar to those of the ein2/skl mutant and support that MtCEP1 modulates EIN2-dependent symbiotic responses. Accordingly, MtCEP1 counteracts the reduction in nodulation induced by increasing ethylene precursor concentrations, and an ethylene synthesis inhibitor treatment antagonizes MtCEP1 root phenotypes. MtCEP1 also inhibits the development of EIN2-dependent pseudonodule formation. Finally, mutants affecting the COMPACT ROOT ARCHITECTURE2 (CRA2) receptor, which is closely related to the Arabidopsis CEP Receptor1, are unresponsive to MtCEP1 effects on lateral root and nodule formation, suggesting that CRA2 is a CEP peptide receptor mediating both organogenesis programs. In addition, an ethylene inhibitor treatment counteracts the cra2 nodulation phenotype. These results indicate that MtCEP1 and its likely receptor, CRA2, mediate nodulation and lateral root development through different pathways.


Asunto(s)
Etilenos/metabolismo , Medicago truncatula/crecimiento & desarrollo , Reguladores del Crecimiento de las Plantas/metabolismo , Proteínas de Plantas/metabolismo , Nodulación de la Raíz de la Planta , Receptores de Péptidos/metabolismo , Rhizobium/fisiología , Medicago truncatula/citología , Medicago truncatula/genética , Medicago truncatula/metabolismo , Fenotipo , Proteínas de Plantas/genética , Raíces de Plantas/citología , Raíces de Plantas/genética , Raíces de Plantas/crecimiento & desarrollo , Raíces de Plantas/metabolismo
18.
Plant Cell ; 27(8): 2210-26, 2015 Aug.
Artículo en Inglés | MEDLINE | ID: mdl-26253705

RESUMEN

Initiation of symbiotic nodules in legumes requires cytokinin signaling, but its mechanism of action is largely unknown. Here, we tested whether the failure to initiate nodules in the Medicago truncatula cytokinin perception mutant cre1 (cytokinin response1) is due to its altered ability to regulate auxin transport, auxin accumulation, and induction of flavonoids. We found that in the cre1 mutant, symbiotic rhizobia cannot locally alter acro- and basipetal auxin transport during nodule initiation and that these mutants show reduced auxin (indole-3-acetic acid) accumulation and auxin responses compared with the wild type. Quantification of flavonoids, which can act as endogenous auxin transport inhibitors, showed a deficiency in the induction of free naringenin, isoliquiritigenin, quercetin, and hesperetin in cre1 roots compared with wild-type roots 24 h after inoculation with rhizobia. Coinoculation of roots with rhizobia and the flavonoids naringenin, isoliquiritigenin, and kaempferol, or with the synthetic auxin transport inhibitor 2,3,5,-triiodobenzoic acid, rescued nodulation efficiency in cre1 mutants and allowed auxin transport control in response to rhizobia. Our results suggest that CRE1-dependent cytokinin signaling leads to nodule initiation through the regulation of flavonoid accumulation required for local alteration of polar auxin transport and subsequent auxin accumulation in cortical cells during the early stages of nodulation.


Asunto(s)
Flavonoides/metabolismo , Ácidos Indolacéticos/metabolismo , Medicago truncatula/genética , Mutación , Proteínas de Plantas/genética , Nodulación de la Raíz de la Planta/genética , Transporte Biológico/efectos de los fármacos , Chalconas/metabolismo , Chalconas/farmacología , Citocininas/metabolismo , Flavanonas/metabolismo , Flavanonas/farmacología , Flavonoides/farmacología , Interacciones Huésped-Patógeno/efectos de los fármacos , Quempferoles/metabolismo , Quempferoles/farmacología , Medicago truncatula/metabolismo , Medicago truncatula/microbiología , Microscopía Fluorescente , Reguladores del Crecimiento de las Plantas/metabolismo , Reguladores del Crecimiento de las Plantas/farmacología , Proteínas de Plantas/metabolismo , Nodulación de la Raíz de la Planta/efectos de los fármacos , Raíces de Plantas/efectos de los fármacos , Raíces de Plantas/genética , Raíces de Plantas/metabolismo , Raíces de Plantas/microbiología , Plantas Modificadas Genéticamente , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Sinorhizobium meliloti/fisiología , Simbiosis/efectos de los fármacos , Ácidos Triyodobenzoicos/farmacología
19.
PLoS One ; 10(1): e0116819, 2015.
Artículo en Inglés | MEDLINE | ID: mdl-25562779

RESUMEN

Cytokinins are phytohormones that regulate many developmental and environmental responses. The Medicago truncatula cytokinin receptor MtCRE1 (Cytokinin Response 1) is required for the nitrogen-fixing symbiosis with rhizobia. As several cytokinin signaling genes are modulated in roots depending on different biotic and abiotic conditions, we assessed potential involvement of this pathway in various root environmental responses. Phenotyping of cre1 mutant roots infected by the Gigaspora margarita arbuscular mycorrhizal (AM) symbiotic fungus, the Aphanomyces euteiches root oomycete, or subjected to an abiotic stress (salt), were carried out. Detailed histological analysis and quantification of cre1 mycorrhized roots did not reveal any detrimental phenotype, suggesting that MtCRE1 does not belong to the ancestral common symbiotic pathway shared by rhizobial and AM symbioses. cre1 mutants formed an increased number of emerged lateral roots compared to wild-type plants, a phenotype which was also observed under non-stressed conditions. In response to A. euteiches, cre1 mutants showed reduced disease symptoms and an increased plant survival rate, correlated to an enhanced formation of lateral roots, a feature previously linked to Aphanomyces resistance. Overall, we showed that the cytokinin CRE1 pathway is not only required for symbiotic nodule organogenesis but also affects both root development and resistance to abiotic and biotic environmental stresses.


Asunto(s)
Citocininas/metabolismo , Medicago truncatula/metabolismo , Proteínas de Plantas/metabolismo , Aphanomyces/patogenicidad , Citocininas/genética , Glomeromycota/patogenicidad , Medicago truncatula/crecimiento & desarrollo , Mutación , Nitrógeno/metabolismo , Fenotipo , Proteínas de Plantas/genética , Raíces de Plantas/efectos de los fármacos , Raíces de Plantas/crecimiento & desarrollo , Raíces de Plantas/metabolismo , Transducción de Señal/efectos de los fármacos , Cloruro de Sodio/farmacología , Simbiosis , Transcriptoma/efectos de los fármacos
20.
PLoS Genet ; 10(12): e1004891, 2014 Dec.
Artículo en Inglés | MEDLINE | ID: mdl-25521478

RESUMEN

In plants, root system architecture is determined by the activity of root apical meristems, which control the root growth rate, and by the formation of lateral roots. In legumes, an additional root lateral organ can develop: the symbiotic nitrogen-fixing nodule. We identified in Medicago truncatula ten allelic mutants showing a compact root architecture phenotype (cra2) independent of any major shoot phenotype, and that consisted of shorter roots, an increased number of lateral roots, and a reduced number of nodules. The CRA2 gene encodes a Leucine-Rich Repeat Receptor-Like Kinase (LRR-RLK) that primarily negatively regulates lateral root formation and positively regulates symbiotic nodulation. Grafting experiments revealed that CRA2 acts through different pathways to regulate these lateral organs originating from the roots, locally controlling the lateral root development and nodule formation systemically from the shoots. The CRA2 LRR-RLK therefore integrates short- and long-distance regulations to control root system architecture under non-symbiotic and symbiotic conditions.


Asunto(s)
Medicago truncatula/genética , Proteínas de Plantas/fisiología , Proteínas Tirosina Quinasas Receptoras/fisiología , Nódulos de las Raíces de las Plantas/genética , Medicago truncatula/crecimiento & desarrollo , Medicago truncatula/microbiología , Meristema/genética , Meristema/crecimiento & desarrollo , Meristema/microbiología , Filogenia , Rhizobium/fisiología , Nódulos de las Raíces de las Plantas/crecimiento & desarrollo , Nódulos de las Raíces de las Plantas/microbiología , Simbiosis
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