MicroRNAs (miRNAs) are endogenous, single-stranded, small (~21-23nt), non-coding, regulatory RNA molecules that manipulate messenger RNA (mRNA) degradation and translation repression by binding complementary sites in the protein-encoding, or 3’-untranslated regions, of target mRNAs [1–3]. Contemporary research has revealed numerous miRNAs in diverse plant species, such as Arabidopsis thaliana (mouse-ear cress), Oryza sativa (Asian rice), Chlamydomonas reinhardtii (flagellated green algae), and Populus euphratica (subtropical poplar tree) [4–7]. An abundance of recent evidence suggests that plant miRNAs are critical to several essential biological processes in plant physiology, such as floral organ identity, leaf morphogenesis, cellular signaling, and stress responses [8–11]. Because of the diverse and important functions of miRNAs in plants, the dysfunction, mutation, and dysregulation of specific miRNAs has the potential to negatively influence plant growth and productivity.

Initially discovered as regulators of developmental timing in Caenorbabditis elegans (transparent nematode), miRNAs have already been demonstrated to play important regulatory roles, particularly in the complex network of gene regulatory pathways. During abiotic stress to plants, such as drought, salinity, wounding, and high temperature, miRNAs act at the posttranscriptional level in gene regulatory networks associated with stress adaptation and tolerance. Under adverse stress conditions, gene expression can be elaborately regulated to facilitate the action of these tolerance mechanisms [12–14], providing further evidence of the importance of miRNAs in regulation of plant responses to abiotic stress conditions.

In the past decade, the regulatory mechanisms of miRNAs involved in plant stress responses have garnered increasing attention. For example, miRNAs have been identified to regulate plant response to drought [15, 16], salinity [17, 18], low temperature [19, 20], and nutrient deficiency [21–23]. More recently, a set of conserved and non-conserved miRNAs from Medicago truncatula (barrel clover) [24], Oryza sativa (Asian rice) [25], Brassica napus (rapeseed) [26], and Arabidopsis thaliana (mouse-ear cress) [27] that act to regulate plant response to heavy metal exposure, have been idenfified. These findings indicated that certain stress conditions stimulate specific plant species to produce miRNAs involved in species-specific regulatory processes that vary highly between different species, potentially accounting for differences in plant tolerances to specific stress conditions. Additionally, these results indicate that miRNAs could represent a discriminative evolutionary footprint associated with abiotic stress regulation, relationships that can only be determined by comprehensive organization of miRNA regulation data from many plant species.

To date, more than one thousand miRNAs have been discovered in diverse plant species [28]. Many of these miRNAs have confirmed involvement in regulatory networks associated with plant stress response. Despite notable recent progress in identifying miRNA regulation during stress conditions, detailed data of miRNA molecular regulation in different plant abiotic stresses, such as miRNA expression pattern and target genes of miRNAs, remains widely distributed in published literature. In the current stage, a cohesive database system is sorely needed for data deposit and further application. Therefore, development of the literature-curated database system “PASmiR” (miRNA molecular regulation in Plant Abiotic Stress) for the storage of regulatory relationships between miRNAs and plant abiotic stresses will be a valuable resource for contemporary researchers. While these immediate, tangible benefits are apparent, the PASmiR database may also serve as a valuable ongoing program for the study of miRNA regulatory mechanisms associated with plant responses to abiotic stress as additional information becomes available in this field.

Contemporary exploration of miRNA molecular regulation associated with plant abiotic stresses has demonstrated that miRNAs act as important regulators in plant physiological adaption mechanisms during response to unfavor-able stresses. Unfortunately, data information on specific miRNAs involved in regulation of plant responses to abiotic stress is widely dispersed throughout current scientific literature. To provide a comprehensive repository for collection, standardization, and searching of these miRNA-abiotic stress regulatory relationships, the literature-curated and web-accessible PASmiR database was established.

Notably, the number of miRNAs involved in particular abiotic stress responses is highly dependent on the experimental approaches proposed in the original investigations. For example, more miRNAs will be observed using a microarray platform than other low-throughput technologies [37, 38]. In different plant species, miRNAs may be defined as functionally conserved if their homologs behave as regulators of specific abiotic stress responses in more than one other plant species. For example, the miRNA homologs peu-miR164 and mtr-miR164 are functionally conserved in plant responses to drought stress in both Populus euphratica (Euphrates Poplar) [6] and Medicago truncatula (Barrel Clover) [39]. Of 682 total plant miRNAs, 242 (35.5%) represent functional conserved miRNAs, and 16 (6.6%) of which are functionally conserved in more than 3 abiotic stresses response in different plant species (see Additional file 1). Investigation of these conserved miRNAs using a structured database approach, such as that provided by PASmiR, will facilitate improvements in the understanding of stress-focused miRNA functional evolutionarily relationship in plant species. This data has potential applications for experimental biology aiming to improve plant crop performance and breeding characteristics.

Current efforts have demonstrated that miRNAs play critical roles in regulating plant responses to abiotic stresses in a complicated network manner [40–43]. Thus, it is possible that analysis of the miRNA-stress regulation data archived in PASmiR may be able to yield novel information about the network regulatory mechanisms of miRNAs involved in stress response. In the staple food crop Oryza sativa (Asian rice), a bipartite network can be used to describe the 162 regulatory relationships between 113 miRNAs and 13 abiotic stresses known in this species (Figure 4). Within the network, drought, arsenite treatment, cadmium (Cd), low temperature, aluminum (Al) excess, and high salt demonstrate the highest connectivity by involving 35, 25, 25, 22, 19, and 13 regulatory miRNAs in the stress response, respectively.

Several miRNAs, such as osa-miR156, osa-miR393, and osa-miR528, have been demonstrated to play regulatory roles in more than two types of abiotic stress responses. Among these miRNAs, a small portion (solid purple circles) exhibit opposite expression patterns in different abiotic stresses response. The miRNA osa-miR156, for example, has a high-expression tendency when subjected to radiation exposure, but exhibits the opposite tendency when exposed to either low temperature or drought, indicating that, as a regulator of stress, osa-miR156 exhibits unique behaviors under variant stress conditions. Cumulatively, these findings indicate the complex network regulatory relationships between miRNAs and abiotic stresses. By using PASmiR, researchers will have access to a comprehensive knowledge base for assembling bipartite networks for plant species documented, allowing the completion of novel derivations for detailed stress-driven miRNA molecular regulatory mechanisms.

The PASmiR database project, reported herein, provides the initial groundwork for an ongoing program for cataloging and utilizing miRNA-abiotic stress regulatory information in plants. Notably, the current version is not as comprehensive as we envision future versions to be. Ongoing collection and curation of new publications related to miRNA-stress response regulation is essential to this program’s success. New versions of the databases are currently scheduled to be released on a monthly basis, incorporating all new submissions to the database over the preceding month. While this work is currently time and resource intensive, the pending employment of a natural language processing (NLP) technique to allow more rapid abstract prescreening will facilitate the addition of many new entries to the database in the near future. This strategy is expected to increase comprehensiveness and accessibility of the database, promoting broader interest from researchers worldwide.

We constructed the first comprehensive database for miRNA molecular regulation in plant abiotic stress responses. The web-based program was created by manually reviewing widely scattered scientific literature. This database, however, also provides a convenient submission interface for contribution of novel miRNA-stress regulatory relationship by independent researchers. PASmiR provides comprehensive, keyword-searchable miRNA-abiotic regulatory relationships focused on a specific plant species, abiotic stress, and miRNA family. Thus, PASmiR will aid in rapid and complete exploration of the complex network of miRNA regulatory mechanisms involved in plant abiotic stress responses, serving as a valuable resource for future investigators in experimental biology concerned with commercial crop breeding and characteristics.

Project name: PASmiR: A literature-curated database for miRNA molecular regulation in plant response to abiotic stress

Project home pages: http://hi.ustc.edu.cn:8080/PASmiR

http://pcsb.ahau.edu.cn:8080/PASmiR

Operating system(s): Platform independent

Programming languages: JSP, MySQL, HTML and JavaScript

License: Not required.

Any restrictions to use by non-academics: None