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![(Previous two pages and above) Phylogenetically predicted domains for enod40 mRNA of several leguminous plant species abbreviated as follows: Gm1 (Glycine max enod 40-1), Pv (Phaseolus vulgaris), Vr (Vigna radiata), Sr (Sesbania rostrata), Lj1 (Lotus japonicus enod40-1), Lj2 (L.japonicus enod40-2), Mt (Medicago truncatula), MsI [Medicago sativa (cultivar Iroquois) enod40], Ms2 (M.sativa enod40), Tr (Trifolium repens), Ps (Pisum sativum), Vs (Vicia sativa) and Ll (Lupinus luteus). (A) Domain 1; (B) domain 3; (C) domain 5; (D) domain 2; (E) domain 4; (F) domain 6.](profile/Andreas-Roussis/publication/6221829/figure/fig5/AS:668903617343490@1536490458317/Previous-two-pages-and-above-Phylogenetically-predicted-domains-for-enod40-mRNA-of.png)
(Previous two pages and above) Phylogenetically predicted domains for enod40 mRNA of several leguminous plant species abbreviated as follows: Gm1 (Glycine max enod 40-1), Pv (Phaseolus vulgaris), Vr (Vigna radiata), Sr (Sesbania rostrata), Lj1 (Lotus japonicus enod40-1), Lj2 (L.japonicus enod40-2), Mt (Medicago truncatula), MsI [Medicago sativa (cultivar Iroquois) enod40], Ms2 (M.sativa enod40), Tr (Trifolium repens), Ps (Pisum sativum), Vs (Vicia sativa) and Ll (Lupinus luteus). (A) Domain 1; (B) domain 3; (C) domain 5; (D) domain 2; (E) domain 4; (F) domain 6.
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The plant gene enod40 is highly conserved among legumes and also present in various non‐legume species. It is presumed to play a central regulatory
role in the Rhizobium–legume interaction, being expressed well before the initiation of cortical cell divisions resulting in nodule formation.
Two small peptides encoded by enod40 mRNA as well as its se...
Contexts in source publication
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... an iterative process identi®ed six conserved domains, one of them being folded only in part of the enod40 RNAs containing an insertion of ~75±130 nucleotides, absent in G.max and some other sequences (Fig. 1E). The ®rst stem± loop structure (Fig. 1A), located 7±13 nucleotides downstream of sORF1, is a hairpin of variable length, containing several internal loops. In all sequences, the 5¢ half of the hairpin is purine-rich, whereas the 3¢ part is pyrimidine-rich, resulting in possiblè¯ipping' of pairs. This structure, conserved in non-legume ...
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... an iterative process identi®ed six conserved domains, one of them being folded only in part of the enod40 RNAs containing an insertion of ~75±130 nucleotides, absent in G.max and some other sequences (Fig. 1E). The ®rst stem± loop structure (Fig. 1A), located 7±13 nucleotides downstream of sORF1, is a hairpin of variable length, containing several internal loops. In all sequences, the 5¢ half of the hairpin is purine-rich, whereas the 3¢ part is pyrimidine-rich, resulting in possiblè¯ipping' of pairs. This structure, conserved in non-legume enod40 RNAs, has also been predicted by ...
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... the distance of 4±13 nucleotides downstream of hairpin 1, a much extended conserved stem±loop structure 2 was predicted (Fig. 1D). This domain, spanning 123±135 nucle- otides (in G.max, positions 148±272), has a very peculiar feature: despite some structural variation in the interior loops, all structures contain multiple loops containing exclusively U residues. Such loops are represented by both bulges and symmetric or asymmetric interior loops. The top part of ...
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... 3¢-proximal part of this region II is folded into a small hairpin 3 (Fig. 1B). It seems that the stem±loop structure 2 and hairpin 3 could also be traced as the peaks in thèmountain plots' produced for a set of enod40 sequences by the program RNAalifold for folding the aligned RNAs ...
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... enod40 sequences downstream of the conserved region II are very variable in both sequence and length. In M.truncatula, M.sativa and T.repens sequences, an extended stem±loop structure can be predicted just downstream of the hairpin 3 (Fig. 1E). With a remarkable similarity to domain 2, this stem±loop structure (domain 4) is also characterised by a conserved pattern of multiple U-containing loops and bulges, while the top hairpin has a less conserved structure, with possible alternative foldings. Figure 1E shows the most conserved hairpin at the top, which corresponds to ...
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... a remarkable similarity to domain 2, this stem±loop structure (domain 4) is also characterised by a conserved pattern of multiple U-containing loops and bulges, while the top hairpin has a less conserved structure, with possible alternative foldings. Figure 1E shows the most conserved hairpin at the top, which corresponds to either the lowest free energy con®guration or the second (suboptimal) folding of this domain, as predicted by the mfold package. Indirect support for the existence of such a stem±loop structure in these species could be derived from the fact that in some other enod40 RNAs, including that of G.max, almost the whole structure is deleted, suggesting that such a large deletion (~5±130 nucleotides) could leave the remaining structure unperturbed. ...
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... downstream, two conserved stem±loop structures can be predicted in all legume enod40 sequences (structures 5 and 6, Fig. 1C and F, respectively). Despite some structural variation in the interiors of these hairpins due to substitutions and deletions, the terminal stems seem to be much ...
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... and/ or deletions cluster around internal loops and bulges, preserving an overall topology of alternating stems and loops, therefore also being indirect support for the proposed structural elements. In the small hairpin 3, formed by one of the most conserved enod40 sequence regions, the substitutions and deletions occur mostly in the hairpin loop (Fig. 1B). One of the base pairs is also variable, being either U´G, U±A or C± G, which can be the result of single mutations preserving the pairing. Structural probing of the Gmenod40 RNA The proposed secondary structure of Gmenod40 RNA pro- vided by the STAR program and by sequence comparison represents a rough indication of the folding of the ...
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... presented probing data, together with computer-assisted predictions and structural comparisons, indicate the presence of several structured regions in the soybean enod40 RNA. Five domains of the G.max enod40 RNA secondary structure are also conserved in other known leguminous enod40 sequences (Fig. 1). The conservation of the domains points to their possible role in enod40 RNA functioning. This is also consistent with the data on Medicago enod40 RNA, which show that deletion of the structure located in the non- translated region, corresponding to domain 1 (Fig. 1A), impairs biological activity (26). Domain 1, represented by a ...
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... structure are also conserved in other known leguminous enod40 sequences (Fig. 1). The conservation of the domains points to their possible role in enod40 RNA functioning. This is also consistent with the data on Medicago enod40 RNA, which show that deletion of the structure located in the non- translated region, corresponding to domain 1 (Fig. 1A), impairs biological activity (26). Domain 1, represented by a stem±loop structure, is strongly conserved in all leguminous plants (Fig. 1A) and also in non- legumes (Fig. 5A), and is particularly well supported by probing. This structure is very stable, and its presence has already been suggested on the basis of a comparison of folding ...
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... role in enod40 RNA functioning. This is also consistent with the data on Medicago enod40 RNA, which show that deletion of the structure located in the non- translated region, corresponding to domain 1 (Fig. 1A), impairs biological activity (26). Domain 1, represented by a stem±loop structure, is strongly conserved in all leguminous plants (Fig. 1A) and also in non- legumes (Fig. 5A), and is particularly well supported by probing. This structure is very stable, and its presence has already been suggested on the basis of a comparison of folding free energies in the comparable region of related enod40 RNAs with statistically expected values (26), and detected by a program searching ...
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... of the top of the hairpin can be better understood from the probing results. Remarkably, the interior (which is the part of domain 2 best supported by probing) exhibits an intriguing conserved feature, namely multiple internal loops and bulges consisting of U residues (Fig. 3B). Interestingly, only the locations of these loops are conserved (Fig. 1D), whereas their dimensions and symmetry vary due to deletions and/or insertions on both sides of the loops. Thus, the UU/U loop of the G.max structure (positions 166±167/254) has the same 2 Q 1 symmetry at S.rostrata, P.sativum and V.sativa homologous positions, but 2 Q 2 topology is found at equivalent position in P.vulgaris structure, ...
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... both sides of the loops. Thus, the UU/U loop of the G.max structure (positions 166±167/254) has the same 2 Q 1 symmetry at S.rostrata, P.sativum and V.sativa homologous positions, but 2 Q 2 topology is found at equivalent position in P.vulgaris structure, 1 Q 1 in V.radiata, 3 Q 2 in L.japonicus and 4 Q 3 in all three available Medicago sequences (Fig. 1D). Two U-containing loops, separated by a single G±C pair can be suggested in the homologous position of L.luteus enod40-1 RNA structure, one of them being a UUU-bulge, while another is a symmetric UU/UU 2 Q 2 loop (Fig. 1D). The same diversity is observed for other loops, still consisting of uridines ...
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... in P.vulgaris structure, 1 Q 1 in V.radiata, 3 Q 2 in L.japonicus and 4 Q 3 in all three available Medicago sequences (Fig. 1D). Two U-containing loops, separated by a single G±C pair can be suggested in the homologous position of L.luteus enod40-1 RNA structure, one of them being a UUU-bulge, while another is a symmetric UU/UU 2 Q 2 loop (Fig. 1D). The same diversity is observed for other loops, still consisting of uridines ...
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... is observed in the structure folded in the region representing a rather large insertion in some legume sequences (domain 4), such as Medicago, T.repens, P.sativum and V.sativa. Again, a global topology of an extended stem±loop structure with duplexes separated by U-containing loops is preserved, while the dimensions of these loops are variable (Fig. 1E). Intriguingly, these sequences represent the species with indeterminate nodules. Indeterminate nodules are different in many ways from determinate nodules that are formed by species such as G.max, P.vulgaris, V.radiata and L.japonicus. The difference is most obviously noted in their morphology and ontological development: determinate ...
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... to the diversity of the U-containing loops in domains 2 and 4 in enod40 RNAs (Fig. 1D and E), it is dif®cult to derive a straightforward de®nition of a speci®c motif on the basis of available data. It is known that asymmetry and adjacent (non- canonical) base pairs are very important factors affecting both geometry and thermodynamics of internal loops (40,41). In addition to diversity of symmetric properties, described above, ...
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... conserved structure in enod40 RNA is the small hairpin 3, located at the 3¢-proximal part of the conserved region II (Fig. 1B). Interestingly, this hairpin is also strongly conserved in non-legume sequences. Domains 5 and 6 seem to be conserved in all legume enod40 RNAs, but we failed to recognise their equivalents in non-legume ...
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... Experimental data on enod40 RNA structure have been obtained for the molecules from only two species, Glycine max ( 21 ) and Lupinus luteus ( 16 ) . Despite the relatively low sequence similarity, even within legumes, RNA structure 2 NAR Genomics and Bioinformatics , 2023, Vol. 5, No. 4 probing of these enod40 RNA molecules has demonstrated the formation of homologous structured stem-loop domains, also supported by comparisons with enod40 sequences from other legumes ( 16 ,21 ) . ...
... Despite the relatively low sequence similarity, even within legumes, RNA structure 2 NAR Genomics and Bioinformatics , 2023, Vol. 5, No. 4 probing of these enod40 RNA molecules has demonstrated the formation of homologous structured stem-loop domains, also supported by comparisons with enod40 sequences from other legumes ( 16 ,21 ) . RNA structure predictions have identified six stem-loop domains, named domains 1-6 in the 5 -3 direction, conserved in enod40 RNAs from all legumes or at least in some of them ( 21 ) . Domains 1-3 are conserved in diverse leguminous species, whereas domain 4 insertion has been observed only in a cluster of plants known to produce indeterminate nodules. ...
... Homologous extended stem-loop structures of domain 4 have previously been identified in a group of closely related leguminous plants known to produce indeterminate nodules, such as Medicago truncatula, Trifolium repens, Pisum sativum and Vicia sativa ( 21 ). The structures are folded by sequences inserted in the enod40 RNAs of this group in the regions between the more conserved domains 3 and 5. ...
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... lncrnadb.org), we identified only seven functionally annotated lncRNAs in Arabidopsis (IPS1, At4, COOLAIR, COLDAIR, npc536, npc48 and TERRA; Franco-Zorrilla et al., 2007;Shin et al., 2006;Swiezewski et al., 2009); two in Glycine max (IPS1, alias: TPSI/Mt4 family; At4, alias: TPSI family; Mart ın et al., 2000); three in Medicago truncatula (IPS1, At4 and ENOD40) (Girard et al., 2003); two in Oryza sativa (IPS1 and ENOD40); one in Vitis vinifera (IPS1) and none functionally characterized in Phaseolus vulgaris. Of those functionally characterized, the chickpea lncRNAs showed strong homology with only three lncRNAs: COOLAIR, IPS1 and At4. ...
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... The 10-to 13-mer oligopeptide encoded by ORF1 is conserved among all species (Compaan et al. 2001;Varkonyi-Gasic and White 2002), except for Casuarina glauca (Santi et al. 2003) (Supplementary Fig. S2A and B). ORF2 possibly does not encode for peptides but may contribute to the folding of the RNA into a highly structured form (Compaan et al. 2001;Girard et al. 2003;Sousa et al. 2001). The region encompassing ORF1 and ORF2 (inter-ORF) shows a high degree of conservation, and this region of ENOD40 RNA sequences tends to form particularly stable secondary structures, indicating these regions to be functionally essential for ENOD40 (Wan et al. 2007). ...
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... The 10-to 13-mer oligopeptide encoded by ORF1 is conserved among all species (Compaan et al. 2001;Varkonyi-Gasic and White 2002), except for Casuarina glauca (Santi et al. 2003) (Supplementary Fig. S2A and B). ORF2 possibly does not encode for peptides but may contribute to the folding of the RNA into a highly structured form (Compaan et al. 2001;Girard et al. 2003;Sousa et al. 2001). The region encompassing ORF1 and ORF2 (inter-ORF) shows a high degree of conservation, and this region of ENOD40 RNA sequences tends to form particularly stable secondary structures, indicating these regions to be functionally essential for ENOD40 (Wan et al. 2007). ...
... Structure of three domains was found to be more structured in comparison to other two domains. Motifs such as U-rich internal loops and bulges were observed in all the analyzed transcripts, indicating regulatory relevance of ENOD40 transcripts (Girard et al., 2003). In Arachis hypogea, a total of 6407 putative lncRNAs have been identified . ...
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... Comparing ENOD40 structure in different leguminous species, Girard et al. showed that five domains in ENOD40 were highly conserved, and that uridine residues were numerous in most of these conserved terminals and loops [76]. However, ENOD40 is not restricted to symbiotic plant development [73], and new studies have shown that it can function as a guide, directing the relocation of NSR (nuclear speckle RNA-binding proteins). ...
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dimethyl sulfate-sequencing (DMS-seq), selective 21-hydroxyl acylation analyzed by primer
extension-sequencing (SHAPE-seq), parallel analysis of RNA structure (PARS), and fragmentation
sequencing (FragSeq). The aim of this review is to provide a better understanding of lncRNA
biological functions by studying them at the structural level.
... Comparing ENOD40 structure in different leguminous species, Girard et al. showed that five domains in ENOD40 were highly conserved, and that uridine residues were numerous in most of these conserved terminals and loops [76]. However, ENOD40 is not restricted to symbiotic plant development [73], and new studies have shown that it can function as a guide, directing the relocation of NSR (nuclear speckle RNA-binding proteins). ...
Although thousands of long non-coding RNAs (lncRNAs) have been discovered in eukaryotes, very few molecular mechanisms have been characterized due to an insufficient understanding of lncRNA structure. Therefore, investigations of lncRNA structure and subsequent elucidation of the regulatory mechanisms are urgently needed. However, since lncRNA are high molecular weight molecules, which makes their crystallization difficult, obtaining information about their structure is extremely challenging, and the structures of only several lncRNAs have been determined so far. Here, we review the structure-function relationships of the widely studied lncRNAs found in the animal and plant kingdoms, focusing on the principles and applications of both in vitro and in vivo technologies for the study of RNA structures, including dimethyl sulfate-sequencing (DMS-seq), selective 2'-hydroxyl acylation analyzed by primer extension-sequencing (SHAPE-seq), parallel analysis of RNA structure (PARS), and fragmentation sequencing (FragSeq). The aim of this review is to provide a better understanding of lncRNA biological functions by studying them at the structural level.
... 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). ...
... 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). ...
... 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. ...
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... Among the peptide types discussed in this review, ENOD40 is the only non-secreted peptide. It is encoded by a small open reading frame (sORF) that produces a conserved and highly structured RNA (Compaan et al., 2001;Sousa et al., 2001;Girard et al., 2003), which contains a very short conserved peptide-encoding domain of 10-13 aa (Compaan et al., 2001;Varkonyi-Gasic and White, 2002). The conserved peptide domain of ENOD40 is encoded by a translatable sORF at the 5′ end termed box I (Sousa et al., 2001), which is also conserved in other legumes (Girard et al., 2003). ...
... It is encoded by a small open reading frame (sORF) that produces a conserved and highly structured RNA (Compaan et al., 2001;Sousa et al., 2001;Girard et al., 2003), which contains a very short conserved peptide-encoding domain of 10-13 aa (Compaan et al., 2001;Varkonyi-Gasic and White, 2002). The conserved peptide domain of ENOD40 is encoded by a translatable sORF at the 5′ end termed box I (Sousa et al., 2001), which is also conserved in other legumes (Girard et al., 2003). The other conserved nucleotide region, box II, is located at the 3′ end. ...
... The other conserved nucleotide region, box II, is located at the 3′ end. Although box II is postulated to encode a peptide in soybean (Röhrig et al., 2002), translational analysis of box II suggests that it may not encode a peptide but instead could act as a structural RNA (Compaan et al., 2001;Sousa et al., 2001;Girard et al., 2003). Thus, ENOD40 is postulated to have a dual role as a peptide-encoding gene and a structural RNA. ...
Many legumes have the capacity to enter into a symbiotic association with soil bacteria generically called rhizobia that results in the formation of new lateral organs on roots called nodules within which the rhizobia fix atmospheric nitrogen (N). Up to 200 million tonnes of N per annum is fixed by this association. Therefore, this symbiosis plays an integral role in the N cycle and is exploited in agriculture to support the sustainable fixation of N for cropping and animal production in developing and developed nations. Root nodulation is an expendable developmental process and competency for nodulation is coupled to low-N conditions. Both nodule initiation and development is suppressed under high-N conditions. Although root nodule formation enables sufficient N to be fixed for legumes to grow under N-deficient conditions, the carbon cost is high and nodule number is tightly regulated by local and systemic mechanisms. How legumes co-ordinate nodule formation with the other main organs of nutrient acquisition, lateral roots, is not fully understood. Independent mechanisms appear to regulate lateral roots and nodules under low- and high-N regimes. Recently, several signalling peptides have been implicated in the local and systemic regulation of nodule and lateral root formation. Other peptide classes control the symbiotic interaction of rhizobia with the host. This review focuses on the roles played by signalling peptides during the early stages of root nodule formation, in the control of nodule number, and in the establishment of symbiosis. Here, we highlight the latest findings and the gaps in our understanding of these processes.
... As an example in Table 3, the homologous lncRNAs IPS1/ At4/Mt4 behave similarly in response to phosphate starvation in several plant species such as A. thaliana (Shin et al., 2006), M. truncatula (Burleigh and Harrison, 1999), and Brassica rapa (Franco-Zorrilla et al., 2007). Another example is enod40, which has a regulatory role in nodule initiation and is conserved among leguminous plants (Glycine max (Girard et al., 2003), Medicago sativa (Crespi et al., 1994), and M. truncatula (Charon et al., 1999)) and non-legumes species (Nicotiana tabacum (Rymarquis et al., 2008), O. sativa (Kouchi et al., 1999), and Z. mays (Compaan et al., 2003)). The exploration of conserved plant lncRNAs by using a comparative genomics approach will facilitate an understanding of the evolutionary relationship of a specific lncRNA family in different plant species. ...
