Comprehensive survey and evolutionary analysis of genome-wide miRNA genes from ten diploid Oryza species
© The Author(s). 2017
Received: 28 July 2016
Accepted: 25 August 2017
Published: 11 September 2017
MicroRNAs (miRNAs) are non-coding RNAs that play versatile roles in post-transcriptional gene regulation. Although much is known about their biogenesis, and gene regulation very little is known about their evolutionary relation among the closely related species.
All the orthologous miRNA genes of Oryza sativa (japonica) from 10 different Oryza species were identified, and the evolutionary changes among these genes were analysed. Significant differences in the expansion of miRNA gene families were observed across the Oryza species. Analysis of the nucleotide substitution rates indicated that the mature sequences show the least substitution rates among the different regions of miRNA genes, and also show a very much less substitution rates as compared to that of all protein-coding genes across the Oryza species. Evolution of miRNA genes was also found to be contributed by transposons. A non-neutral selection was observed at 80 different miRNA loci across Oryza species which were estimated to have lost ~87% of the sequence diversity during the domestication. The phylogenetic analysis revealed that O. longistaminata diverged first among the AA-genomes, whereas O. brachyantha and O. punctata appeared as the eminent out-groups. The miR1861 family organised into nine distinct compact clusters in the studied Oryza species except O. brachyantha. Further, the expression analysis showed that 11 salt-responsive miRNAs were differentially regulated between O. coarctata and O. glaberrima.
Our study provides the evolutionary dynamics in the miRNA genes of 10 different Oryza species which will support more investigations about the structural and functional organization of miRNA genes of Oryza species.
MicroRNAs (miRNAs) are a class of non-protein-coding small RNAs playing versatile roles in post-transcriptional gene regulation. These regulatory genetic elements are formed from long self-complementary precursor sequences which in turn originate from still much longer primary miRNA sequences . In contrast to the only seed sequence of mature miRNA for target recognition in animals, the plants employ entire mature miRNA sequence with near-perfect base pairing . There are two main categories of the genes encoding the miRNA precursors . In the first category, several highly expressed and greatly conserved miRNA gene families across plant lineages occur. miRNAs formed from such loci participate in various processes such as plant development and stress response. On the contrary, the second category contains less conserved miRNA genes that are expressed at lower levels. The roles of miRNAs belonging to this category are substantially unclear in plants . Despite their small size, miRNAs have versatile functions. Through numerous experimental and genetic analyses, miRNAs have been shown to be involved in essential processes such as, plant growth and development, reproduction, and stress responses [4–9].
Some of the miRNA gene families in both plants and animals are highly conserved through millions of years [10, 11]. Nevertheless, specific and very recently evolved miRNA genes also occur in individual species [12, 13]. Gene duplication and subsequent sub- and neo-functionalization have been found leading to the expansion and specialization of highly conserved miRNA gene families [14, 15], whereas neutral evolution may act on the young and recently evolved miRNA genes . Due to their evolutionary conservation, the miRNA genes with significant similarity can be found in different orthologous species . This assumption is usually regarded as a basis for the identification of miRNA genes from the orthologous species. Several hypotheses regarding the origin of new miRNA genes exist such as, origin from the duplication of protein coding and miRNA genes [17–19], origin from terminal inverted repeats of transposable elements , and origin from random intronic or intergenic hairpin structures . The plant miRNAs from the same family as well as their corresponding coding loci have been found not to be as diverse as the animal miRNAs, indicating that plant miRNA gene families have recently originated , and hence further assisting in the homology search of the miRNA genes in different plant species. However, the number of miRNA genes in plants has changed in a lineage-specific manner subsequent to the divergence of eudicots and monocots . In addition, some members of plant miRNA precursors from the same family have also been found to be diverged in a lineage specific manner [23–25].
The comprehension about how genetic diversity influences the phenotypic differences among the species has been a major challenge in the evolutionary biology. The genus Oryza, due to its wealth of species, well-described phylogeny, plentiful genetic resources available and diversification across a wide-ranging ecology within a restricted evolutionary time period (~15 million years [MY]), has emerged as an exceptionally ideal model system for studying the short-term evolutionary dynamism shaping the plant kingdom [26–28]. The genus Oryza encompasses approximately 24 species that are classified into 10 distinctive genome types and distributed across a wide ecological range [26, 28]. It is widely established that wild species of Oryza have an immense genetic potential and agronomically important traits for the crop improvement. However, owing to the sterility barriers, majority of the Oryza species still remain underutilized for the rice improvement . Genetic resources coupled with the enormous functional experimental resources of the AA-genomes of Oryza have certainly been attracting the attention of rice breeders. The interest of breeders in AA-genomes is also due to the fact that two species of this group are cultivated ones. Getting to the bottom of phylogenetic relationships among the different genomes and essentially the AA-genomes of Oryza will considerably pave the way for future efforts to explore and mine the beneficial alleles, which would eventually prove beneficial from the perspective of efficient rice germplasm conservation and utilization. Although the phylogenetic relationships among these genomes have been undertaken [30, 31], yet the realization of code and context of their genome evolution has not been achieved altogether. Through comparative genomic studies, it has been revealed that evolutionary dynamism among the different diploid genomes of Oryza is brought about by significant variations in the size of many protein-coding gene families which are in turn influenced by the directional selection . Although few reports about the evolution of miRNA genes in rice exist [32–34], however, the evolution and selection among the Oryza genomes on the basis of non-protein-coding miRNA genes is still not well-characterized. Though a very recent report by Baldrich et al.  has identified and shown the conservation of some polycistronic miRNAs across the AA-genomes of Oryza, even their study has not identified all the orthologous miRNA genes of rice from the AA-, BB-, and FF-genomes of Oryza. The homology search is a reliable methodology for the identification of miRNA genes from the homologous species as well as genus, and has been exploited in the identification homologous miRNA gene sequences from different plant species. Therefore, in this study, we performed a comparative genome-based homology search to identify and analyze all the orthologous miRNA genes of rice in the 10 different Oryza species for uncovering the changes that might have occurred in them during the course of evolution. The 10 species were selected for this study on the basis of their sequenced genomes as well as due to immensely high importance of eight AA-genomes in studying the short evolutionary events for which the BB- and FF-genomes were selected as eminent out-group species. The changes in the number and sequence in different miRNA genes among the Oryza species will provide clues about the divergence and convergence of such genes. Further, the estimates of evolutionary divergence among the Oryza genomes from the genome-wide miRNA sequence variations would prove as a worthwhile effort beneficial to rice scientific community. This is the first report of its kind on the genome-wide investigation of all the orthologous miRNA genes of rice (Oryza sativa subsp. japonica) in the diploid Oryza group.
Results and discussion
Number and distribution of miRNA genes in the 10 Oryza genomes
No. of different miRNA gene families derived from transposons, miRNA genes and paralogues in the 10 Oryza species
No. of TE-derived miRNA gene families
Total no. of gene families
Total no. of genes
Total number of hits
Av. no. of genes/gene family
Av. no. of paralogous duplicates/gene
O. sativa (indica)
Analysis of genomic organisation of miRNA genes provided good information regarding their genomic locations and the rearrangements that might have occurred during the evolution. In all the Oryza species, miRNA genes were found broadly distributed throughout the corresponding genomes. For most of the miRNA genes in a particular species, the orthologues could be found in the other Oryza genomes (O. brachyantha and O. punctata being the strong exceptions in this case). However, the order of these orthologous genes on the corresponding chromosomes of Oryza genomes was either not found to be conserved or they were found on the different chromosomes of the Oryza species, indicating that the extensive rearrangements in miRNA genes might be due to several chromosomal inversions and translocations within or between the different chromosomes of Oryza. The highest number of homologous genes was found between O. nivara and O. sativa (indica) which is justified from the fact that they are evolutionarily separated by just 0.75 MY . Analysis of the genomic organisation of miRNA genes revealed that, on average across Oryza, the maximum number (122) of miRNA genes are located in the intergenic regions (Additional file 3), whereas the minimum number (45) of them were found to be located at the boundaries of introns and exons (intron-exon). The similar results about the frequency of intergenic and intragenic miRNAs have also been found by certain mapping studies for other plant species [22, 41, 42]. It was also found that the number of different intergenic or intragenic miRNA genes was not uniform across Oryza species which further substantiates the idea that significant rearrangements in the genomes of Oryza have taken place during the course of evolution which might have caused the movement of miRNA genes from intergenic to intragenic locations and vice-versa.
TE-derived miRNA genes in Oryza
Transposable elements are known to cause a plethora of changes in the gene expression and function of plants, which has significantly led to the understanding that TEs have played a fundamental part in the adaptive evolution of plant genomes . The illustration of the relationships between transposable elements and miRNAs has been suggested to ease the elucidation of miRNA functionality . To examine if any miRNA genes of Oryza species are derived from TEs, we employed the RepeatMasker (open-4.0.5) to screen the precursor sequences for the repetitive elements. We found that miRNA genes representing an average number of ~46 different miRNA gene families (averaging ~29% of total gene families across Oryza) from the studied Oryza species were found to possess the sequence similarity to the TEs (Table 1 and Additional file 1), implying that TEs might have given birth to these miRNA gene families. This result is corroborated by the findings of Zhang et al. , who also found a similar percentage (~29%) of TEs in the genomes of five Oryza species.. However, the result is in disagreement with the findings of Nozawa et al. , who found just 8% of miRNA gene families of different plant species to be derived from TEs. Among the different TE families found in the miRNA genes of Oryza, virtually none was found to be species-specific, indicating the importance of these transposons in the origin of miRNA gene families as well as in the evolution of Oryza genomes. Among the Oryza genomes, the maximum number of TE-derived miRNA gene families were found in O. nivara and O. rufipogon, whereas the minimum number of such gene families was found in the BB- and FF- genomes, indicating that expansion in the transposon number in miRNA genes from FF- and BB- to AA- genomes might have played a considerable contributory role in the evolution of Oryza. Although we found different TEs belonging to the families such as copia-, gypsy-like LTR retroelements, MITEs, MULEs, Harbinger etc. (Additional file 1) in the miRNA genes of Oryza species, the majority of the identified TEs were found to share similarity with nonautonomous DNA transposons known as MITEs. For instance, miR437, miR443, miR812, miR814, miR816, miR818, miR1862 and miR5788 families showed similarity to and hence might be derived from a MITE namely STOWAWAY which has been reported to be highly abundant in the rice genome . Therefore, our results are consistent with the genomic enrichment of MITEs in rice . Since the MITEs have been reported to play important roles in species diversity in rice , their relatively high abundance in the miRNA genes may also contribute to the species diversity in Oryza. Besides, many gypsy-like and copia-like LTR retrotransposons were also detected in the miRNA genes of Oryza with the gypsy-like elements being more abundant than copia-like elements. The higher abundance of gypsy-like elements than copia-like ones is also reported in rice genome . For example, miR531 and miR5833 families were likely derived from the copia-like TEs, whereas miR2827, miR2907, miR5072, miR5074, miR5075 and miR5802 families appeared to have derived from the gypsy-like elements across the 10 studied Oryza genomes. Further, many miRNA gene families of Oryza were also found to be likely derived from TEs belonging to a MULE (Mutator-like elements) family known as MuDR. For example, we found that miR439, miR2122, miR2877, miR5149, miR5153 and miR5827 gene families originated from MuDR TEs virtually across the Oryza. This family of transposons has also been reported to be one of the abundant TE families in rice genome . In addition, some more putative non-autonomous DNA transposons were also detected in the miRNA genes of the studied Oryza genomes (Additional file 1). Overall, these results indicate that the different families of transposable elements have distinct amplification patterns in the miRNA genes of Oryza species which might have contributed to some extent to the evolution of Oryza genomes.
Evolutionary rates of miRNA genes in Oryza
To investigate the sequence conservation in the different regions (left, middle and right regions) of mature and star sequences of the selected conserved and non-conserved miRNA genes, the corresponding mature and star sequencesfrom the 10 Oryza species were aligned seperately. It was found that the left region (at 5′-end) of both conserved and non-conserved mature miRNAs showed the highest conservation than the middle and right (at 3′-end) regions (Fig. 1c and Additional file 9). This might be due to the presence of the seed-like sequence (2nd to 7th nt) in this region of mature miRNAs. This result implies that this conserved seed-like region is particularly under a strong selection pressure across the Oryza species, indicating the importance of this region in target recognition than the middle and right regions, which is substantiated by some earlier studies [54, 55]. In the conserved miRNA genes, the right region of the mature miRNAs was found to be the least conserved, whereas the middle region of the mature miRNAs in non-conserved miRNA genes was found to be the least conserved. In case of star sequences of conserved miRNA genes, the proportion of conserved sites in different regions was found to be reverse as that of their corresponding mature sequences, whereas in non-conserved miRNA genes, the star regions had the similar proportion of conserved sites in the left and middle regions but slightly higher in the right region. Consequently, the proportion of unpaired sites in conserved miRNA-miRNA* duplexes might be higher in the right region, whereas in non-conserved miRNAs the higher number of unpaired sites might prevail at the middle of miRNA-miRNA* duplexes. To a certain degree these findings are in agreement with the results obtained for different plant species , however, some discrepancy may be due to the analysis of different miRNA genes and the different plant species representing various taxonomical positions.
Further, to know if there was a relation between the base content of miRNA genes and their conservation, we calculated the base composition (AT- and GC-content) of mature, star and precursor regions of the selected conserved as well as non-conserved miRNA genes of Oryza. It was found that AT-content was lesser than GC-content in mature and star regions of both conserved as well as non-conserved miRNA genes (Additional files 10 and 11). However, as also reported for rice miRNA genes , AT-content in the conserved Oryza pre-miRNAs was lesser than GC-content as compared to the non-conserved miRNAs which possessed relatively higher AT-content than GC-content, indicating that diverged forces might link base content and conservation in miRNAs.
Selection and patterns of sequence variation
Phylogenetic analysis of conserved and non-conserved miRNAs from the Oryza species
Genomic organization and conservation of miR1861 family in Oryza
Expression analysis of salt-responsive miRNAs
In the present study, we identified the orthologous miRNA genes of rice from the ten different Oryza species and performed a comprehensive evolutionary analysis in terms of rate of sequence variations and selection pressures on these orthologous genes. The species-specific gain and loss of miRNA genes and their duplicated paralogues signified the importance of gene duplication in the birth of new genes which might have led to phenotypic divergence and hence in the evolution of the Oryza genomes. The extensive rearrangements in the genomic order, differential amplification patterns of transposable elements, variations in the precursor sequences than the variations in purifyingly selected mature and star sequences as well as differential frequency of transition substitutions in precursors of miRNA genes may act as crucial contributory factors in the divergence and evolution of Oryza. Hence, diverged forces might link genomic rearrangements, sequence variants and base content with the conservation in miRNA genes of Oryza. The non-neutral selection at numerous miRNA loci suggested a recent selective sweep and/or purifying selection in the Oryza genomes. The loss of average sequence diversity in domestic rice during the course of domestication at different miRNA loci strongly alludes that the wild species of rice are potential genetic resources that are significantly untapped from the perspective of crop improvement. These sequence variants might eventually lead to the difference in the expression patterns under specific developmental and stress conditions which is evidenced by our expression study in O. glaberrima and O. coarctata. It hence attests that nature has focussed significantly on the miRNAs as the one of the main elements for the differential accumulation of variations in populations under selection pressures.
Sequence identification from different Oryza species
In order to identify the homologous sequences of rice (O. sativa subsp. japonica) in the 10 different Oryza species, we first downloaded all the miRNA precursor sequences of rice from the miRBase (Release 21.0, June 2014). These sequences were used as queries for performing the BLASTn search  against each of the 10 Oryza species (E-value 10−4) in gramene . Criteria described by some previous studies [38, 73–75] were used for assigning a BLAST output hit as a potential precursor. These are i) BLAST hit should not be more than 20 nt lesser than the query and should have an E-value of ≤10−4, ii) the mismatches in the mature sequence of desired sized hit with the mature sequence of rice should be ≤2, iii) the sequence should adopt an appropriate hairpin structure when analysed by RNA Fold , iv) the minimum free energy of the predicted hairpin structure should be ≤ −15 kcal/mol, v) the maximum bulge size in the hairpin should not be more than 12, vi) the maximum number of mismatches allowed between miRNA and miRNA* is 6.
The sequences of all miRNA precursors from the 10 Oryza species and their other details are shown in Additional file 1.
Plant materials and PCR reactions for sequencing of miR1861 clusters
miR1861 gene family is one of the miRNA gene families that might be organized into distinct compact clusters, and can be transcribed as single units. The idea of existence of this gene family into clusters was appreciated due to most of its members occurring as tandem and polycistronic miRNAs [35, 64]. Therefore, we attempted to isolate the clusters of this family from the four Oryza species (O. sativa sp. indica, O. glaberrima, O. nivara and O. rufipogon) with the O. brachyantha as the negative control as none of the genes from this family was found in O. brachyantha by our in-silico results (Additional file 1). Genomic DNA was extracted from the leaf samples of these Oryza species as described in our earlier study , and was used as a template for amplification of miR1861 clusters from each genotype using cluster-specific primers (Additional file 19) in C1000 Touch™ thermal cycler (Bio-Rad Laboratories, Hercules, CA, USA). The parameters for the PCR reaction were: 5 min at 95 °C, 45 cycles of 15 s at 95 °C, 30 s at varying annealing temperatures and 30 s at 72 °C. The amplification products were cloned in pGEMT-easy vector, transformed into DH5α and sequenced. For each cluster, primers were designed from the flanking regions of individual pre-miRNA members (e.g. in 2-membered cluster-II, the primers were designed from upstream of ‘b’ and downstream of ‘c’ so that both members ‘b’ and ‘c’ including the genomic region between them was amplified). Precursor sequences of individual members of osa-miR1861 clusters were determined from the miRBase, and then each cluster sequence was used as a query to extract miR1861 clusters from the other Oryza species.
Multiple sequence alignment and phylogenetic analysis
In order to analyse the sequence convergence or divergence in nine sequenced miR1861 clusters from the five Oryza species, each cluster from all these species was aligned using Clustal X 1.83 with default parameters. The phylogenetic tree was constructed using Clustal Omega , whereas dendrograms from a conserved and a non-conserved miRNA were constructed using MEGA 6  with the Neighbor-joining method .
Stress treatments and quantitative PCR-based expression analysis of miRNA sequence variants
In order to find out the relation between the sequence variations of some miRNA loci and their corresponding probable expression variations, we selected 11 known salt responsive miRNAs based on the published literature [80, 81] for studying their expression in two wild species of rice namely O. coarctata and O. glaberrima under salinity stress. While O. coarctata is a halophytic wild relative of rice that grows normally under highly saline conditions , O. glaberrima is a well-adapted and cultivable species of Oryza in West Africa that has acquired traits for increased biotic and abiotic stress tolerance . The young plants (at tillering stage) of O. coarctata and O. glaberrima were given a salt stress by keeping them submerged in 450 mM and 200 mM NaCl solutions respectively, for 24 h. Plants treated with distilled water for 24 h were considered as control. After 24 h, the leaf tissues were harvested from both salt stressed and control plants in three biological replicates and frozen until further use. The isolation of miRNA, cDNA synthesis and qPCR analysis for all the salt-responsive miRNAs was performed as per our previous study . The details of primers are given in Additional file 19.
Evaluation of substitution rates of miRNA genes from Oryza species
In order to estimate the substitution rates in the miRNA genes of 10 Oryza species, the sequences of mature, star (miRNA-complementary region) and precursor regions of 32 conserved and 22 non-conserved miRNA genes representing 19 families each were taken [64, 83, 84]. They were aligned separately using clustalW in MEGA 6. For miRNA members having more than one hit or paralogue in a species, all the hits were taken for the analysis. Initially, the average numbers of nucleotide substitutions per site N for each region were calculated  among the particular miRNA genes from the 10 Oryza species. The N was then used to estimate the substitution rate (R) for a particular region of miRNA gene using the formula R = N/2 T, where T is the divergence time of Oryza which is 15 MY . In order to see whether the rate of nucleotide substitutions in the precursor sequences of conserved and non-conserved miRNA genes was biased more towards transitions or transversions, the transition/transversion ratios  were calculated for each precursor from the all Oryza species. To know the probability of substitution from one base to another base, patterns of all transition and transversion substitutions were estimated . Further, the conservation in the different regions (left, middle and right regions) of mature and corresponding star sequences of the above miRNA genes was analyzed.
To compare with the studied miRNA genes, the substitution rates at synonymous (dS) and non-synonymous (dN) sites in all the orthologous protein coding genes of 10 Oryza species were determined using GrameneMart . The average dN/dS ratios were calculated across the 10 Oryza species which were then used for computing the substitution rate in the same manner as done for miRNA genes.
Tests of neutrality
The neutrality of miRNA sequence polymorphisms among Oryza was assessed by means of neutrality tests such as, Tajima’s D  and Fu and Li’s F  performed on 80 different miRNA loci using the software DnaSP v5.10 . Based on the segregating sites in the pre-miRNA sequences of Oryza, the values for the two neutrality tests were calculated.
The authors thank Dr. K.V. Bhat, Head, Division of Genomic Resources, NBPGR, New Delhi for his support and advice to carry out this work. Mr. Showkat Ahmad Ganie is grateful to the Department of Biotechnology, Government of India for the award of Senior Research Fellow.
The project was funded through in-house grant.
Availability of data and materials
SAG, ABD, ABG performed the data mining, data analysis. SAG participated in the drafting of the manuscript. TKM conceived the study, coordinated the research and wrote the manuscript. All authors read and approved the final manuscript.
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