Structural motifs in the RNA encoded by the early nodulation gene enod40 of soybean

Girard, Geneviève; Roussis, Andreas; Gultyaev, Alexander P.; Pleij, C.W.A.; Spaink, Herman P.

doi:10.1093/nar/gkg721

Cited by 39 publications

(66 citation statements)

References 45 publications

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“…Secondary RNA structures seem to be required for the elicitation of the cell-specific growth response in M. sativa roots (Sousa et al, 2001). The secondary structure of the G. max enod40 RNA has been determined recently, which has allowed the identification of five conserved domains in the enod40 RNAs of numerous leguminous species (Girard et al, 2003). In particular, several motifs, such as U-containing stem-loops and bulges, have been found to be conserved.…”

Section: Introductionmentioning

confidence: 99%

Enod40, a Short Open Reading Frame–Containing mRNA, Induces Cytoplasmic Localization of a Nuclear RNA Binding Protein in Medicago truncatula

2004

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In eukaryotes, diverse mRNAs containing only short open reading frames (sORF-mRNAs) are induced at specific stages of development. Their mechanisms of action may involve the RNA itself and/or sORF-encoded oligopeptides. Enod40 genes code for highly structured plant sORF-mRNAs involved in root nodule organogenesis. A novel RNA binding protein interacting with the enod40 RNA, MtRBP1 (for Medicago truncatula RNA Binding Protein 1), was identified using a yeast three-hybrid screening. Immunolocalization studies and use of a MtRBP1-DsRed2 fluorescent protein fusion showed that MtRBP1 localized to nuclear speckles in plant cells but was exported into the cytoplasm during nodule development in enod40-expressing cells. Direct involvement of the enod40 RNA in MtRBP1 relocalization into cytoplasmic granules was shown using a transient expression assay. Using a (green fluorescent protein)/MS2 bacteriophage system to tag the enod40 RNA, we detected in vivo colocalization of the enod40 RNA and MtRBP1 in these granules. This in vivo approach to monitor RNA-protein interactions allowed us to demonstrate that cytoplasmic relocalization of nuclear proteins is an RNA-mediated cellular function of a sORF-mRNA.

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Section: Introductionmentioning

confidence: 99%

Enod40, a Short Open Reading Frame–Containing mRNA, Induces Cytoplasmic Localization of a Nuclear RNA Binding Protein in Medicago truncatula

2004

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“…A region of RNA secondary structure separates the two enod40 ORFs. This RNA segment is essential for enod40 activity and has a noncoding role in root nodule formation (Girard et al, 2003;Campalans et al, 2004). It was also shown that, in alfalfa, enod40 RNA is essential for a growth response in the root cortex (Sousa et al, 2001).…”

Section: Plant Cncrnasmentioning

confidence: 98%

“…By using a combination of RNA structure prediction, comparison and structure probing, various regions of soybean enod40 RNA were identified to be key for root nodule formation. Of these, five domains are conserved amongst leguminous plants and are presumed to be required for the non-coding activity of enod40 RNA (Girard et al, 2003). Indeed, the deletion of an inter-ORF RNA region with predicted structure resulted in reduced activity of alfalfa enod40 without affecting the production of ENOD40 peptides (Sousa et al, 2001).…”

Section: Plant Cncrnasmentioning

confidence: 99%

“…Specific regions or elements of RNA also appear to play crucial roles in determining coding versus non-coding functions. For example, the non-coding activity of sqt and osk resides in elements within the 3′UTR of these RNAs (Jenny et al, 2006;Lim et al, 2012), whereas an RNA element located between the two ORFs of enod40 harbors its non-coding activity (Girard et al, 2003). In each of these RNAs, the coding and non-coding roles can be clearly ascribed to distinct RNA segments.…”

Section: Coding Rolementioning

confidence: 99%

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CncRNAs: RNAs with both coding and non-coding roles in development

Sampath

Ephrussi

2016

Development

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RNAs are known to regulate diverse biological processes, either as protein-encoding molecules or as non-coding RNAs. However, a third class that comprises RNAs endowed with both protein coding and non-coding functions has recently emerged. Such bi-functional 'coding and non-coding RNAs' (cncRNAs) have been shown to play important roles in distinct developmental processes in plants and animals. Here, we discuss key examples of cncRNAs and review their roles, regulation and mechanisms of action during development.

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“…Recently, we reported direct binding of SuSy to peptide A (12 aa residues) and peptide B (24 aa residues) encoded by the early nodulin gene ENOD40 [8]. In addition to the two small peptides, the secondary structure of ENOD40 mRNA has been shown to be a key element in the signaling process underlying nodule organogenesis [9,10]. The plant gene ENOD40 is one of the earliest nodulin genes specifically induced by nodulation factor-secreting rhizobia and appears to play an important role in root nodule organogenesis.…”

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confidence: 99%

Modification of soybean sucrose synthase by S-thiolation with ENOD40 peptide A

Röhrig

John

Schmidt

2004

Biochemical and Biophysical Research Communications

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The gene ENOD40 is expressed at an early stage of root nodule organogenesis and has been postulated to play a central regulatory role in the Rhizobium-legume interaction. In vitro translation of soybean ENOD40 mRNA showed that the gene encodes two peptides of 12 and 24 aa residues (peptides A and B) that bind to sucrose synthase. Here we show that the small Cys-containing peptide A binds to sucrose synthase by disulfide bond formation, which may represent a novel form of posttranslational modification of this important metabolic enzyme. Assays using nanomolar concentrations of peptide A revealed that the monomeric reduced form of this peptide binds to purified sucrose synthase. Using a cysteinyl capture strategy combined with MALDI-TOF MS analysis we identified the Cys residue C264 of soybean sucrose synthase as the binding site of peptide A. Modification of sucrose synthase with ENOD40 peptide A activates sucrose cleavage activity whereas the synthesis activity of the enzyme is unaffected. The results are discussed in relation to the role of sucrose synthase in the control of sucrose utilization in nitrogen-fixing nodules. Ó 2004 Elsevier Inc. All rights reserved. The symbiotic interaction between leguminous plants and rhizobia results in the development of the nodule, a new organ on plant roots. In these nodules the bacteria are hosted intracellularly as bacteroids and find the ideal environment to fix atmospheric nitrogen. Nitrogen fixation is an energy-demanding process which is dependent on the supply of photosynthate. Sucrose, as the major end product of photosynthesis, is synthesized in leaves and is transported in the phloem to various sink tissues such as nodules. This disaccharide is cleaved by the homotetrameric enzyme sucrose synthase (SuSy) catalyzing the reversible, UDP-dependent cleavage of sucrose into UDP-glucose and fructose. This reaction is considered to function in vivo in the sucrose breakdown direction providing substrates for rapidly growing tissues and sink organs. SuSy is one of the most abundant proteins in mature legume nodules [1,2], and breakdown of sucrose is a key step in nitrogen fixation and a necessary prerequisite for normal nodule development and function [3].Due to the important role of SuSy in the control of sucrose utilization in sink tissues, the expression of SuSy genes is highly regulated on the transcriptional and translational levels [4]. Moreover, SuSy is posttranslationally modified by reversible protein phosphorylation [5,6], and the soluble form of SuSy can bind to the actin cytoskeleton in plants [7]. Recently, we reported direct binding of SuSy to peptide A (12 aa residues) and peptide B (24 aa residues) encoded by the early nodulin gene ENOD40 [8]. In addition to the two small peptides, the secondary structure of ENOD40 mRNA has been shown to be a key element in the signaling process underlying nodule organogenesis [9,10].

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Structural motifs in the RNA encoded by the early nodulation gene enod40 of soybean

Cited by 39 publications

References 45 publications

Enod40, a Short Open Reading Frame–Containing mRNA, Induces Cytoplasmic Localization of a Nuclear RNA Binding Protein in Medicago truncatula

Enod40, a Short Open Reading Frame–Containing mRNA, Induces Cytoplasmic Localization of a Nuclear RNA Binding Protein in Medicago truncatula

CncRNAs: RNAs with both coding and non-coding roles in development

Modification of soybean sucrose synthase by S-thiolation with ENOD40 peptide A

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