Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor
- Botao Zhao†1,
- Liangfa Ge†2,
- Ruqiang Liang1,
- Wei Li1,
- Kangcheng Ruan1,
- Hongxuan Lin2 and
- Youxin Jin1Email author
© Zhao et al; licensee BioMed Central Ltd. 2009
Received: 13 January 2009
Accepted: 08 April 2009
Published: 08 April 2009
MicroRNAs (miRNAs) are endogenously expressed small RNAs with a length of about 21 nt. MiRNAs silence their target genes at the post-transcriptional level. In plants, miRNAs play various developmental and physiological roles by cleavaging mRNAs predominantly. Drought and high salinity are the most severe environmental abiotic stresses and cause crop losses all over the world.
In this study, we identified miR-169g and miR-169n (o) as high salinity-responsive miRNAs in rice. MiR-169n and miR169o were in a miRNA cluster with a distance of 3707 base pairs (bp). The high degree of conservation and close phylogenic distance of pre-miR-169n and pre-miR-169o indicated that they were derived from a very recent tandem duplication evolutionary event. The existence of a cis-acting abscisic acid responsive element (ABRE) in the upstream region of miR-169n (o) suggested that miR-169n (o) may be regulated by ABA. In our previous study, we found that miR-169g was induced by the osmotic stress caused by drought via a dehydration-responsive element (DRE). Thus, our data showed that there were both overlapping and distinct responses of the miR-169 family to drought and salt stresses. We also showed that these miR-169 members selectively cleaved one of the NF-YA genes, Os03g29760, which is a CCAAT-box binding transcription factor and participates in transcriptional regulation of large number genes. Finally, we found one or more ath-miR-169 member that was also induced by high salinity.
We identified members of the miR-169 family as salt-induced miRNAs and analyzed their evolution, gene organization, expression, transcriptional regulation motif and target gene. Our data also indicated that the salt-induction of some miR-169 members was a general property in plants.
MicroRNAs (miRNAs) are a newly identified class of small single-stranded non-coding RNAs that range in length from roughly 18 to 24 nucleotides (nt). Most miRNA genes are thought to exist as independent transcriptional units and are transcribed by RNA polymerase II into long primary transcripts, termed pri-microRNAs [1–4]. Mature miRNA formation is a multi-step process involving many complicated enzymes [5–12]. MiRNAs regulate their target genes via two main mechanisms: target mRNA cleavage and translational repression. In plants, most miRNAs have perfect or near perfect complementarity to their mRNA targets and cleave them [1, 13–16]. MiRNAs are involved in plant development, signal transduction, protein degradation, response to environmental stress and pathogen invasion, and they also regulate their own biogenesis [14, 16–19]. In the past few years, more and more miRNAs have been identified. However, their functions remain mostly unknown.
Abiotic stresses such as drought, soil salinity, extreme temperatures, chemical toxicity and oxidative stress are serious threats to agriculture and result in environmental deterioration. For plants, drought and high salinity are the main abiotic stresses and are becoming widespread through the world. Many genes and biochemical molecules are involved in the responses to abiotic stress in plants. However there is only a very limited view on miRNAs involved in abiotic stress [20–24]. Rice is a major worldwide crop for food supply, but its yield is frequently affected by abiotic stress. We had analyzed a miRNA profile under drought stress in rice (Oryza sativa) and identified two drought-induced miRNAs: miR-169g and miR-393 . MiR-169g was the only member of the miR-169 family induced by drought. Sequence analysis revealed two proximate DREs (Dehydration-Responsive Element) in the upstream region of the MIR-169g promoter, suggesting that miR-169g could be regulated directly by the transcriptional factors CBF/DREBs, in response to abiotic stress in plants. These results suggested that miR-169g might play a role under drought stress in rice.
The CCAAT box is one of the most common elements in eukaryotic promoters. It is present in 30% of all eukaryotic genes and is located 80 to 100 base pairs (bp) upstream of the transcription start site (TSS) [25, 26]. The NF-Y complex (also known as CBF or HAP) was isolated as a CCAAT-binding protein complex and is an evolutionarily conserved transcription factor that occurs in a wide range of organisms from yeast to humans. It includes three subunits: NF-YA (CBF-B or HAP2), NF-YB (CBF-A or HAP3), and NF-YC (CBF-C or HAP5), all of which are required for DNA binding [25, 26]. In Arabidopsis, there are 10 genes encoding for the NF-YA subunit, 10 genes for the NF-YB subunit and 9 genes for the NF-YC subunit [27, 28]. Further, 10 NF-YA genes, 11 NF-YB genes and 7 NF-YC genes have been identified in rice . All of these plant NF-Y genes contain an evolutionarily conserved domain, which is responsible for DNA binding and protein-protein interactions, and various non-conserved regions in both length and amino acid sequence [25, 26].
In this study, we found that not only miR-169g but also miR-169n and miR-169o were induced by high salinity. MiR-169n and miR-169o were located in a miRNA gene cluster and derived from a recent tandem duplication event. There were DRE and ABRE cis-acting elements in the upstream region of miR-169g and miR-169n-o, respectively. We also showed that NF-YA transcription factor, Os03g29760, is a target gene of these salt-inducible miR-169 members and were cleaved rapidly after high salinity treatment. Finally, we found that one or more ath-miR-169 member was also induced by high salinity. This indicated that some members of miR-169 family might be a general property in plants.
Response of the miR-169 family to high salinity in rice
MIR-169n and MIR-169o genes were involved in gene duplication evolution
The cis-acting element analysis of the salt-induced microRNAs
The promoters of drought- and salt-inducible genes contain two major classes of cis-acting elements, ABRE and DRE, both of which are involved in stress-inducible gene expression [33, 34]. ABRE and DRE are the major cis-acting elements that function in ABA-dependent and ABA-independent gene expression respectively [33, 35].
a Cis-acting element analysis of MIR-169g and MIR-169n-o
Comparison of the cis-elements of drought- and salt- induced miRNAs
Target genes of the salt-induced miR-169 genes
The response of the miR-169 family to high salinity in Arabidopsis
Drought and salinity are becoming particularly widespread in many regions and are the primary cause of crop loss worldwide. Many genes that are induced by these stresses have been identified [39, 40]. However, little is known about the relation between the miRNA and these stresses [20–22, 24, 41]. Our studies have shown that some miR-169 members were induced by these stresses in rice and Arabidopsis. Interestingly, it seemed that only a minority of members of the large miR-169 family responded to these stresses. Furthermore, these inducible microRNAs displayed specificity to different stresses.
Plant microRNA families are usually much larger than those of animals. MiR-169 is one of the largest families of miRNAs in plants. To date, the rice miR-169 family contains 17 members in the MicroRNA Registry 10.0 [42, 43]. These members have very similar or the same mature sequences and almost the same predicted target genes. However, their expression profiles were very different (Figure 1A). Noticeably, miR-169g and miR-169n (o) exhibited identical responses to high salinity, but different responses to drought. From our studies, we speculated that miR-169 could be a miRNA family that responds to various stress conditions. In our study, the stress condition was more moderate than those of some other groups [21, 44, 45]. For this reason, we thus could not exclude that other members of miR-169 could be induced by more intense salt stress condition.
At least five signal transduction pathways exist in drought and high salinity stress responses: three are ABA dependent and two are ABA independent [33, 34]. In the ABA-dependent pathways, ABRE functions as a major ABA-responsive element. DRE is a major responsive element in the ABA-independent pathway. In this study, high salinity induced both miR-169g and miR-169n (o) which contain DRE and ABRE respectively. In our previous study , only drought had induced miR-169g, which contains DREs. PEG treatment only mimics osmotic stress, while salt treatment also brings ionic toxicity except for osmotic stress to plants. From this point, we concluded that miR-169g could have been induced by osmotic stress, while miR-169n and miR-169o were induced by ionic stress. The difference of the cis-acting regulative elements on MIR-169g and MIR-169n (o) could be part of the molecular base of their diverse responses to stresses.
In addition, we searched the target genes of the miR169 family in silica, and genes of NF-YA family were predicted as its target genes. Our subsequent data validated that two of the predicted target genes were down-regulated as the members of the miR-169 were induced by high salinity. NF-YA is one of the subunits of NF-Y complex, which was isolated as a CCAAT-box binding complex and is an evolutionarily conserved transcription factor [25, 26]. The CCAAT box is one of the most common elements in eukaryotic promoters and is present in 30% of all eukaryotic genes. A study in Triticum aestivum revealed that nine subunits of the NF-Y complex were responsive to drought . TaNF-YA1 mRNA levels showed a significant reduction in drought-affected leaves to around one-third of that seen in leaves of the non-stressed control. A similar level of down-regulation in the drought-stressed leaves was seen for four TaNF-YB genes (TaNF-YB3, 6, 7 and 8) and three TaNF-YC genes (TaNF-YC5, 11 and 12). Only TaNF-YB2 was up-regulated under drought condition . That so many NF-Y subunits were down-regulated by drought indicated the expression of many genes controlled by NF-Y complexes were turned off as a result and also that NF-Y complexes should play quite important and comprehensive roles in plant adaptation to drought.
The mRNA levels of Os03g29760 and Os07g41720 declined immediately after high salinity treatment, according to the induction of miR-169 in rice. However, rapid compensation was observed at 24 hours after treatment despite the fact that the miRNAs were still being induced. Our data partially explained the mRNAs reduction of some NF-Y subunits as observed by Stephenson et al . The transient inhibition suggested some mechanisms help the NY-YA gene to escape from cleavage by miR-169 after long-time treatment of high salinity. Given that the NF-Y complex potentially regulates so many genes, we speculated that the roles of miR-169g, miR-169n and miR-169o under salt-stress in rice could be involved in comprehensive physiological processes. Therefore, we thought that these miRNAs are one of the crucial molecules at an upstream node in transcriptional regulatory networks of salt stress signal transduction. In recent years, although both large numbers of up-regulated and down-regulated genes were identified [44, 45, 47–49], most intention has been focused on genes that were induced in plant under abiotic stresses such as drought and high salinity. The down-regulation of many genes should be also very important for plants to tolerate the environmental stresses, while little is known about that how and why these genes are down-regulated. Our data suggested that the salt-inducible members of the miR-169 family could be pivotal molecules in inhibiting these down-regulated genes under Abiotic stresses.
In this study, we identified that miR-169g and miR-169n(o) were induced by high salinity. We analyzed the gene organization and conservation of the miR-169n and miR-169o. The high level of conservation suggested that these two miRNAs derived from a tandem duplication event. The promoter searching revealed that there were ABRE elements in the sequence upstream of the miR-169n-o cluster and suggested that miR-169n, o may be regulated by ABA-dependent pathway. We further identified Os03g29760 (NF-YA-8 or OsHAP2E) as a target gene of miR-169 by 5'-RACE. In Arabidopsis, at least one member of the ath-miR-169 family was induced significantly by high salinity.
Plant treatments and RNA isolation
The seeds (Oryza sativa, var. japonica) were stimulated to break dormancy, germinated and then transferred to Yoshida's culture solution under a 13-hour light (26°C)/11-hour dark (22°C) photoperiod. After 12 days in culture, the seedlings were used for experiments. For salt treatment, the seedlings were transferred into fresh culture solution containing 150 mM NaCl. Seedlings were harvested at 0, 0.5, 2, 6, 24 and 48 hours after treatment.
Arabidopsis seeds were sterilized and sown on an MS plate containing 0.4% phytage gel and stratified at 4°C for three days, then transferred to 22°C under continuous light for germination and growth. Seven days after germination, the seedings were transferred to a 96-well plate without bottom and grew on MS liquid medium. After 14 days, the MS medium was replaced by MS containing 150 mM NaCl for stress treatment. Seedings were harvested at 0, 24 and 48 hours after treatment.
Samples were then ground to a fine powder and the total RNAs were extracted using the Trizol reagent (Invitrogen).
RNA gel blot analysis
For mature miRNA analysis, total RNA (10 μg) was loaded per lane and resolved on a denaturing 12% polyacrylamide gel. The gel was separated into two parts. One part containing 5S rRNA was stained by ethidium bromide, and the other containing miRNAs was transferred to a Hybond N+ nylon membrane (Amersham). The membranes were cross-linked with UV at 125 mJ/cm2. DNA probes complementary to miRNA sequences were end-labeled with [γ-32P] ATP (3000 Ci/mmol) (Amersham) by T4 polynucleotide kinase (MBI). Unincorporated [γ-32P] ATP was removed using a sephadex G-25 column. Prehybridization and hybridization were carried out using PerfectHyb Hybridization Solution (TOYOBO) at 37°C. Blots were washed in 2 × SSC/0.1% SDS according to the user manual. The membrane was measured with a PhosphorImager and scanned with GE Storm 860 (Amersham) or FUJIFILM FLA-9000. All probes used were described as previous and listed in Additional File 2. The probe (os-miR-169a, b, c, e) were also used to detect ath-miR-169.
RT-PCR and quantitative real-time PCR assay
2 μg total RNA and 0.5 μg random hexamers were heated to 70°C for five minutes and then cooled on ice. The remaining reagents (5 × reaction buffer, dNTPs, RNase inhibitor and M-MLV reverse transcriptase (Promega)) were then added and incubated at 37°C for one hour. The RT product was used as a template for PCR using Ex-Taq Hotstart (Takara). The primers used were listed in Additional File 2. To quantify the predicted target genes, these primers were also used for a quantitative real-time PCR assay with SYBR GREEN PCR Master Mix (Applied Biosystems).
The total RNA from samples at 0.5, 2 and 6 hours were pooled and used for a 5'-RACE assay. Briefly, total RNA was ligated to a synthesized RNA adaptor (T4 RNA ligase, Fermentas) and then transcribed by gene-specific primers (Superscript II, Invitrogen). The adaptor primer (i.e. the DNA version of the RNA adaptor) and gene-specific primers were used to amplify the ligation product (Ex-Taq Hotstart, Takara). The amplicons were cloned to pMD19-T Vector (Takara). Clones with the expected insertions were sequenced. The sequences of adaptor and primers were listed in Additional File 2.
Sequence alignment, RNA folding and phylogenic analysis of Osa-miR-169 family
The surrounding sequences of miR-169n and miR-169o were extracted and aligned by ClustalX using the default parameter. The conserved sequences (sequences in blue parentheses in Figure 2B) were folded by RNAstructure software. The distances of stem-loops of the Osa-miR-169 family stem-loops were calculated with ClustalX and the phylogenic tree was visualized by njplotWin95.
This work was supported by the National Natural Science Foundation of China (No. 30430210), National Key Basic Research and Development Program (2005CB724602, 2002CB713802 and 2003CB114303), Programs from the Chinese Academy of Sciences (KSCX-2-SW-228, KSCX2-YW-R-096 and KSCX1-YW-R-64), and the Science and Technology Committee of Shanghai Municipality (05DJ4008 and 04DZ14006).
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