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Identification of Conserved Secondary Structures and Expansion Segments in Enod40 Rnas Reveals New Enod40 Homologues in Plants Alexander P

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Identification of Conserved Secondary Structures and Expansion Segments in Enod40 Rnas Reveals New Enod40 Homologues in Plants Alexander P 3144–3152 Nucleic Acids Research, 2007, Vol. 35, No. 9 Published online 22 April 2007 doi:10.1093/nar/gkm173 Identification of conserved secondary structures and expansion segments in enod40 RNAs reveals new enod40 homologues in plants Alexander P. Gultyaev1 and Andreas Roussis2,* 1Leiden Institute of Biology, Leiden University, Kaiserstraat 63, 2311 GP Leiden, The Netherlands and 2Agricultural University of Athens, Department of Agricultural Biology and Biotechnology, Iera Odos 75, 118 55 Votanikos, Athens, Greece Received December 12, 2006; Revised February 5, 2007; Accepted March 6, 2007 Downloaded from ABSTRACT INTRODUCTION enod40 is a plant gene that participates in the While a majority of land plants are able to enter an regulation of symbiotic interaction between legumi- endosymbiotic programme with mycorrhizal fungi (1–3), nous plants and bacteria or fungi. Furthermore, it root nodule symbiosis is almost strictly confined to has been suggested to play a general role in non- legumes and a few non-legumes that interact with rhizobia http://nar.oxfordjournals.org/ symbiotic plant development. Although enod40 and other nitrogen-fixing bacteria (4,5). In both cases, specific signalling pathways activate, establish and main- seems to have multiple functions, being present in tain the symbiotic plant–microbe programme (6–9). The many land plants, the molecular mechanisms of its soyabean enod40 gene was initially identified as one of the activity are unclear; they may be determined plant genes that are expressed during the early stages of though, by short peptides and/or RNA structures the formation of nitrogen-fixing root nodules in the encoded in the enod40 genes. We utilized con- symbiotic association of legumes with soil rhizobial served RNA structures in enod40 sequences to bacteria (10,11). It is also activated in roots colonized at Selcuk Univesitesi on February 1, 2015 search nucleotide sequence databases and identi- by fungi forming phosphate-acquiring arbuscular mycor- fied a number of new enod40 homologues in plant rhizae (12).The enod40 gene is present in all legumes species that belong to known, but also, to yet studied so far, and is also found in many non-legume unknown enod40-containing plant families. RNA plants [reviewed in (13)]. secondary structure predictions and comparative In both legumes and non-legumes, various experiments sequence analysis of enod40 RNAs allowed us have demonstrated enod40 expression to be important in to determine the most conserved structural fea- nodule organogenesis and development [e.g. (14–25)]. tures, present in all known enod40 genes. The data accumulated so far on the biological effects of Remarkably, the topology and evolution of one of enod40 suggest that this gene may have multiple functions that are not restricted to the regulation of symbiosis. the conserved structural domains are similar to However, the molecular mechanisms of its activity are those of the expansion segments found in structural unclear. The enod40 genes lack long open reading frames RNAs such as rRNAs, RNase P and SRP RNAs. (ORFs), but encode for short conserved peptides which Surprisingly, the enod40 RNA structural elements were shown to be functional (26,27). The soyabean are much more stronger conserved than the Enod40 peptides bind to sucrose synthase, suggesting a encoded peptides. This finding suggests that role in the regulation of sucrose utilization in nodules (27). some general functions of enod40 gene could be The analysis of enod40 sequences and RNA secondary determined by the encoded RNA structure, structures from various plants also depicts a role for whereas short peptides may be responsible enod40 as a regulatory RNA (14,26,28–30). This role is for more diverse functions found only in certain supported by experiments in alfalfa roots which showed plant families. that deletion of RNA structural elements in a mutated *To whom correspondence should be addressed. Tel: þ30-210-9402952; Fax: þ30-210-9402952; Email: [email protected] Present address: Andreas Roussis, Technological Educational Institute of Athens, Department of Conservation of Antiquities and Works of Art, Agiou Spyridonos 122 10, Egaleo, Athens, Greece ß 2007 The Author(s) This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/ by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Nucleic Acids Research, 2007, Vol. 35, No. 9 3145 enod40 gene, while retaining proper translation, decreased enod40 homologues. In particular, we discovered putative enod40 activity with respect to stimulation of cortical enod40 genes in another five plant families: Myrtales, cell division (26). Furthermore, an alfalfa enod40 RNA- Malvales, Brassicales, Apiales and Gentianales. binding protein MtRBP1 was isolated and found to co- Despite the relatively low global sequence similarity in localize with enod40 RNA in cytoplasmic granules during some cases, the suggested enod40 assignments are strongly nodulation (31). MtRBP1 and its homologues possess an supported by the presence of similar secondary structures. RNA recognition motif (RRM), but the binding sites in The deduced global enod40 structure is shown schemati- enod40 RNA have not yet been identified (31). cally in Figure 1. The most conserved structure is domain A comparative analysis of possible enod40 RNA 3 [nomenclature of (29)], represented by a relatively small, structures (29) suggests that the presence of some though stable, hairpin found in all (putative) enod40 structural domains correlates with the plant’s ability to RNAs. Figure 2 shows these hairpins in non-legume form nitrogen-fixing root nodules. While part of the sequences [legume analogues are described in (29)], with enod40 structure seems to be well conserved in several the nucleotide positions given in Table 1. The hairpins plant families, certain domains are typical for legumes, the consist of 5–9 bp, sometimes interrupted by a mismatch. only group able to develop root nodule symbioses with All hairpins are located in the 30-proximal part of rhizobia. Furthermore, a structured domain conserved region II, where many base covariations are observed in enod40 RNA of leguminous plants forming indetermi- and sequence diversity is increased as compared to the Downloaded from nate nodules is completely eliminated in plants forming 50-end of the region. The hairpins are located at similar determinate nodules. In general, the non-legume enod40 positions downstream of the conserved region II core (13) RNAs seem to be less structured as compared to those of and are easily found by eye inspection of the alignment in legumes (29). this region, even without using an RNA folding program. The presence of strongly conserved RNA structural The only sequence motif, present in almost all hairpins, http://nar.oxfordjournals.org/ elements may be used to increase the efficiency of database is a 3-bp unit [CUC/GAG] in the middle of the stem. mining for un-annotated enod40 homologues. The nucleo- With some deviations, the motif is found in all hairpins. tide sequence similarity in distantly related species is rather A similar pattern is observed in homologous legume low, and only two high sequence similarity regions (named structures (29). region I and region II) have been revealed [e.g. (13,17,32)]. Domain 2 is more variable compared to domain 3. 0 While the most conserved short ORF I is encoded by While the 3 -ends of the predicted domain 2 are all located region I, the highest conservation at the nucleotide level is at similar positions just upstream of the region II, the size observed in the short region II, where no conserved of this structure varies in a broad range of 40–140 nt peptides can be proposed (13). On the other hand, the core (Table 1). Nevertheless, the shape of the domain is at Selcuk Univesitesi on February 1, 2015 of region II is flanked by previously identified (29) strongly conserved in all putative enod40 sequences: it is conserved RNA secondary structure elements. In this an extended stem-loop structure, sometimes (in larger work, we have used this feature to search for unidentified domains) with branching in the interior (Figure 3). Similar enod40 orthologs in nucleotide sequence databases, in structures can also be folded in legume enod40 RNAs, particular, in the GenBank database of expressed sequence typically with a size of 120–135 nt, which are sometimes tags (ESTs). This allowed us to extend considerably the extended in paralogous genes (29). Bearing in mind a very number of known enod40-possessing non-legume families high diversity of enod40 sequences in this region, such a and species. Furthermore, the analysis of possible RNA conserved shape is remarkable. Interestingly, the majority secondary structures reveals structural elements that are of structures contain rather similar paired sequences conserved in enod40 RNAs across the plant kingdom. A GUUUG and CAAAC, or their minor variations comparison of the predicted structures suggests that the (examples are shown in Figure 3), preserving the pairing evolution of one of the conserved domains resembles that at the very ends, while interior sequences from different of expansion segments that are found in some structural families are not similar and difficult to align. RNAs. Within plant families, conservation of terminal sequences and structures is extended further inside domain 2,
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