MicroRNA166 controls root and nodule development in <i>Medicago truncatula</i>

Boualem, Adnane; Laporte, Philippe; Jovanovic, Mariana; Laffont, Carole; Plet, Julie; Combier, Jean-Philippe; Niebel, Andréas; Crespi, Martín; Frugier, Florian

doi:10.1111/j.1365-313x.2008.03448.x

Cited by 286 publications

(254 citation statements)

References 59 publications

(85 reference statements)

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“…The bZIP transcription factor (TF) seems to be the target of gma-MIR-Cand017; this TF negatively regulates nodulation (Nishimura et al, 2002) and is present in plant-defense responses (Dröge-Laser et al, 1997). Other transcription factors have been shown to be regulated by miRNAs during nodulation, such as MtHAP2, which is controlled by miR169; HD-ZIPIII, regulated by miR166; and NAC1, regulated by miR164; all were identified during nodulation in M. truncatula (Combier et al, 2006;Boualem et al, 2008;D'haeseleer et al, 2011). In the soybean, Subramanian et al (2008) also showed that the TFs are targets of miRNAs during nodulation, as confirmed recently by Joshi et al (2010).…”

Section: Discussionmentioning

confidence: 99%

Prediction of potential novel microRNAs in soybean when in symbiosis

Barros-Carvalho¹,

Paschoal²,

Marcelino-Guimarães³

et al. 2014

Genet. Mol. Res.

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ABSTRACT. MicroRNAs (miRNAs) are small molecules, noncoding proteins that are involved in many biological processes, especially in plants; among these processes is nodulation in the legume. Biological nitrogen fixation is a key process, with critical importance to the soybean crop. This study aimed to identify the potential of novel miRNAs to act during the root nodulation process. We utilized a set of transcripts that were differentially expressed in soybean roots 10 days after inoculation with Bradyrhizobium japonicum, which were obtained in a previous study, and performed a set of computational analyses that led us to select new miRNAs potentially involved in nodulation. Among these analyses, the set of transcripts were submitted to an in silico annotation of noncoding RNAs, including a search of similarity against miRNA public databases, ab initio tools for miRNA identification, structural search against miRNA families, prediction of the secondary structure of miRNA precursors, and prediction of the sequences of mature miRNAs. Subsequently, we applied filter procedures based on miRNA selections described in the literature (e.g., free energy value). In the next step, a manual curation inspection of the annotation was performed and the top candidates were selected and used for prediction of potential target genes, which were later checked manually in the database of the soybean genome. This prediction led us to the identification of 9 potential new miRNAs; among these, 4 were conserved in other plants. Moreover, we predicted their target genes might play important roles in the regulation of nodulation.

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Section: Discussionmentioning

confidence: 99%

Prediction of potential novel microRNAs in soybean when in symbiosis

Barros-Carvalho¹,

Paschoal²,

Marcelino-Guimarães³

et al. 2014

Genet. Mol. Res.

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“…Produced in the endodermis, this miRNA acts non-cell autonomously and diffuses towards the stele, which produces a gradient of its target mRNAs, which encode class III HD-ZIP transcription factors [45]. In M. truncatula, Boualem et al [18] showed that mtr-miR166 and its class III HD-ZIP targets are co-expressed in vascular bundles and in the apical regions of roots and nodules (table 1). The over-expression of a miR166 polycistronic precursor led to reductions in nodule and lateral root numbers in addition to the ectopic development of vascular bundles in transgenic roots.…”

Section: Conserved Micrornas Regulate Transcription Factors That Arementioning

confidence: 99%

“…In recent years, small riboregulators, such as the microRNAs (miRNAs) miR166 and miR169, have been added to the complex signalling pathways that control nodulation, mainly as repressors of key transcription factors [18,19]. In plants, several pathways are known to generate endogenous small non-coding RNAs [20,21], which share common biochemical reactions.…”

Section: Introductionmentioning

confidence: 99%

Complexity of miRNA-dependent regulation in root symbiosis

Bazin

Bustos-Sanmamed

Hartmann

et al. 2012

Phil. Trans. R. Soc. B

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The development of root systems may be strongly affected by the symbiotic interactions that plants establish with soil organisms. Legumes are able to develop symbiotic relationships with both rhizobial bacteria and arbuscular mycorrhizal fungi leading to the formation of nitrogen-fixing nodules and mycorrhizal arbuscules, respectively. Both of these symbiotic interactions involve complex cellular reprogramming and profound morphological and physiological changes in specific root cells. In addition, the repression of pathogenic defence responses seems to be required for successful symbiotic interactions. Apart from typical regulatory genes, such as transcription factors, microRNAs (miRNAs) are emerging as riboregulators that control gene networks in eukaryotic cells through interactions with specific target mRNAs. In recent years, the availability of deep-sequencing technologies and the development of in silico approaches have allowed for the identification of large sets of miRNAs and their targets in legumes. A number of conserved and legume-specific miRNAs were found to be associated with symbiotic interactions as shown by their expression patterns or actions on symbiosis-related targets. In this review, we combine data from recent literature and genomic and deep-sequencing data on miRNAs controlling nodule development or restricting defence reactions to address the diversity and specificity of miRNA-dependent regulation in legume root symbiosis. Phylogenetic analysis of miRNA isoforms and their potential targets suggests a role for miRNAs in the repression of plant defence during symbiosis and revealed the evolution of miRNA-dependent regulation in legumes to allow for the modification of root cell specification, such as the formation of mycorrhized roots and nitrogen-fixing nodules.

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“…For Mt RR4, in situ hybridizations were performed following the procedure described by Valoczi et al (2006) and Boualem et al (2008). The following primers were used for generating the Mt RR4-specific probe (251 nucleotides long): 59-AATGTGGGAAGCCAAGACAC-39 and 59-CGGTGCCGGTCATTTAAG-39.…”

Section: In Situ Hybridizationsmentioning

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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MicroRNA166 controls root and nodule development in Medicago truncatula

Cited by 286 publications

References 59 publications

Prediction of potential novel microRNAs in soybean when in symbiosis

Prediction of potential novel microRNAs in soybean when in symbiosis

Complexity of miRNA-dependent regulation in root symbiosis

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

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