Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens
© Lee et al.; licensee Springer. 2014
Received: 25 August 2014
Accepted: 6 November 2014
Published: 19 November 2014
Rice is a facultative short-day plant that flowers under long days (LD) after a lengthy vegetative phase. Although several inhibitors that delay flowering have been identified, the process by which rice eventually flowers under non-permissive LD conditions is not well understood.
Overexpression of miR172 reduced flowering time significantly, suggesting its role as an inducer. Levels of miR172 increased as plants aged, further supporting our findings. Transcripts of SNB and OsIDS1, two members of the AP2 family that have the miR172 target site, were reduced in older plants as the level of miR172 rose. Overexpression of those AP2 genes delayed flowering; overexpression of miR172-resistant forms of SNB or OsIDS1 further delayed this process. This demonstrated that the AP2 genes function downstream of miR172. Two florigen genes -- Hd3a and RFT1 -- and their immediate upstream regulator Ehd1 were suppressed in the AP2 overexpression plants. This suggested that the AP2 genes are upstream repressors of Ehd1. In phytochrome mutants, miR172d levels were increased whereas those of SNB and OsIDS1 were decreased. Thus, it appears that phytochromes inhibit miR172d, an AP2 suppresser.
We revealed that miR172d developmentally induced flowering via repressing OsIDS1 and SNB, which suppressed Ehd1. We also showed that phytochromes negatively regulated miR172.
KeywordsAP2 family Floral transition miR172 Phytochromes Rice
Rice flowers earlier under short day (SD) conditions than under long days (LD). The photoperiodic flowering pathway of rice is controlled by OsGIGANTEA (OsGI) (Yano et al. ; Hayama et al. , ; Kojima et al. ; Doi et al. ). This gene regulates flowering time by promoting Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS (CO) (Yano et al. ; Hayama et al. , ). Hd1 enhances Early heading date 1 (Ehd1) expression under SD but inhibits its expression under LD (Wei et al. ; Ishikawa et al. ). Ehd1 is an immediate upstream positive regulator of Heading date 3a (Hd3a) and Rice Flowering Locus T 1 (RFT1), which encode florigens that promote flowering (Doi et al. ; Tamaki et al. ; Komiya et al. , ).
Because Ehd1 is modulated by several regulators, it acts as a mediator of various floral signals. For example, Early heading date 2 (Ehd2)/OsINDETERMINATE 1 (OsId1)/Rice INDETERMINATE 1 (RID1) is a constitutive activator of Ehd1 (Matsubara et al. ; Park et al. ; Wu et al. ). Loss-of-function mutants in the gene do not flower under either SD or LD. OsMADS51 also acts as a positive regulator of Ehd1, specifically under SD (Kim et al. ). One major repressor of Ehd1 is Grain yield and heading date 7 (Ghd7), which functions preferentially under LD (Xue et al. ). Most early-flowering rice cultivars show a disruption in Ghd7 expression (Xue et al. ). A chromatin remodeling factor, OsTrithorax 1 (OsTrx1), suppresses Ghd7 by binding to Early heading date 3 (Ehd3) (Matsubara et al. ; Choi et al. ). In addition, OsLFL1 inhibits Ehd1 when over-expressed (Peng et al. , ). However, expression of the former is suppressed by another chromatin remodeling factor, OsVIN3-like 2 (OsVIL2), when binding to the PRC2 complex (Yang et al. ). OsMADS50 induces Ehd1 by blocking OsLFL1 and Ghd7 (Lee et al. ; Ryu et al. ; Choi et al. ). A third gene, OsCOL4, constitutively inhibits flowering time by suppressing Ehd1 (Lee et al. ). Overexpression of the former delays flowering whereas knockout mutations cause early flowering. Finally, DTH8 and Hd16 preferentially suppress flowering time under LD by inhibiting Ehd1 (Xue et al. ; Wei et al. ; Hori et al. ).
Micro RNAs inhibit expression of target genes by cleaving mRNA or translational suppression (Jones-Rhoades et al. ; Voinnet ). miR172 and miR156 are involved in phase transition (Aukerman and Sakai ; Lauter et al. ; Wu and Poethig ; Poethig ). miR156 plays roles in early vegetative stages, while miR172 functions later stages of develop (Aukerman and Sakai ; Lauter et al. ; Wu and Poethig ; Chuck et al. ; Poethig ). In Arabidopsis, miR156 targets 10 members (SPL2, SPL3, SPL4, SPL5, SPL6, SPL9, SPL10, SPL11, SPL13, and SPL15) of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) family. SPL9 prompts miR172 expression and the other SPL genes redundantly function in regulating miR172. The role of miR172 in controlling flowering time has been reported for Arabidopsis, maize, barley, and soybean (Aukerman and Sakai ; Chen ; Lauter et al. ; Jung et al. ; Mathieu et al. ; Nair et al. ; Yoshikawa et al. ). In Arabidopsis and maize, its temporal expression increases gradually as plants age (Aukerman and Sakai ; Lauter et al. ). In rice, miR172 is most highly expressed during later vegetative stages and in developing panicles (Zhu et al. ; Lee and An ).
AP2 family genes are involved in various processes, including floral organ identity, shattering, and flowering time (Aukerman and Sakai ; Chen ; Lauter et al. ; Lee et al. ; Jung et al. ; Chuck et al. ; Mathieu et al. ; Zhu et al. ; Lee and An ; Zhou et al. ; Yoshikawa et al. ). Six Arabidopsis genes in this family -- APETALA 2 (AP2), TARGET OF EAT 1(TOE1), TOE2, TOE3, SCHLAFMUTZE (SMZ), and SCHNARCHZAPFEN (SNZ) -- delay flowering in an age-dependent manner (Park et al. ; Aukerman and Sakai ; Schmid et al. ; Chen ; Jung et al. ; Mathieu et al. ), and are suppressed by miR172 (Schmid et al. ; Kasschau et al. ; Chen ; Schwab et al. ; Ju ng et al. ; Mathieu et al. ). In maize, enhancement of GLOSSY15 (GL15), an AP2 member, delays phase transition from the vegetative to the reproductive stage (Lauter et al. , Zhu and Helliwell ). Its temporal expression gradually decreases as plants mature, and this gene is also down-regulated by miR172 (Lauter et al. ). In rice, five AP2-like genes (SNB, OsIDS1, SHAT1, Os05g03040, and Os06g43220) contain the miR172 target sites (Sunkar et al. ; Zhu et al. ). While SNB and OsIDS1 control floral organ identity and spikelet development, SHAT1 is involved in seed shattering (Sunkar et al. ; Lee et al. ; Zhu et al. ; Lee and An ; Zhou et al. ).
Although an antagonistic role for miR172 and AP2 genes in floral transition has been described in Arabidopsis and maize, their functions in rice have not been reported. Here, we demonstrated in rice that miR172 induces flowering time by suppressing two AP2 family members - SNB and OsIDS1 - that are negative regulators of Ehd1.
Temporal expression patterns of miR172s and AP2 genes are antagonistic
The miR172 s target several AP2 genes, with temporal expression of the latter type being slowly diminished in Arabidopsis and maize (Aukerman and Sakai ; Lauter et al. ; Jung et al. ; Mathieu et al. ; Zhu and Helliwell ). In all, six AP2 genes have miR172 target sites (Zhu and Helliwell ). Other miRNAs and their targeted genes also show antagonistic expression patterns (Jeong and Green ; Jung et al. ). We examined the temporal expression of two rice AP2 genes in leaf blades: SNB and OsIDS1. As expected, their transcript levels were high at younger developmental stages but rapidly declined to a low level at 35 days after germination (DAG) (Figure 1D and E). Ehd1 mRNA expression began to increase at 57 DAG (Figure 1F). Under SD, transcript levels of the AP2 genes dropped rapidly at 18 DAG, immediately before the level of Ehd1 began to rise (Additional file 1: Figure S1). This suggested that the AP2 genes are likely targets of miR172a and miR172d.
Overexpression of SNB and OsIDScauses late flowering
SNB and OsIDS1 repress the floral transition by inhibiting Ehd1
miR172d induces flowering time by suppressing AP2 genes
The late-flowering phenotype of rSNB OX plants is rescued by overexpression of Ehd1
miR172a and miR172d are negatively regulated by phytochromes in rice
We have demonstrated that miR172d induces flowering by suppressing SNB and OsIDS1. Overexpression of the AP2 genes delays flowering more significantly under SD, the permissive condition. This phenotype is similar to that of Arabidopsis SMZ- OX plants (Mathieu et al. ). Overexpression of SMZ causes a significant delay in flowers under LD, the permissive condition for that species, but not under SD (Mathieu et al. ). These reports provide evidence that AP2 genes preferentially block the floral transition under inductive conditions.
Although flowering is inhibited under LD, rice plants do flower eventually under normally suppressive conditions, albeit after a certain period of vegetative growth. We showed here that miR172d levels were increased in the leaves as a plant aged and that flowering was induced when that gene was over-expressed. This indicated that the microRNA plays a role in the developmental control of flowering time in rice, as also observed from Arabidopsis (Jung et al. ).
SNB and OsIDS1 are flowering repressors that are highly expressed in young leaves. However, their expression gradually declined to minimal levels at 35 DAG when miR172 transcripts started to increase. Expression of the florigens and Ehd1 began at 60 DAG while that of the AP2 genes remained low. This indicated that the latter are major suppressors of the downstream floral signals.
Ghd7 also functions to repress Ehd1, but its transcription peaks at 2 to 3 weeks before declining to a low level. This occurs much earlier than when the florigen genes are expressed (Matsubara et al. ; Kim et al. ). OsCOL4 is another regulator that suppresses Ehd1 and the florigen genes. In particular, OsCOL4 expression is maintained at a high level in the early vegetative stages but decreases when Ehd1 expression begins (Lee et al. ). This temporal expression pattern is similar to SNB and OsIDS1 except that OsCOL4 is reduced later than the AP2 genes. Therefore, these results suggest that the AP2 genes as well as Ghd7 and OsCOL4 coordinately suppress flowering time.
Except in oscol4 and hd1 plants, AP2 expression is not significantly altered in most flowering mutants, thereby implying that those genes are controlled by OsCOL4 and Hd1, but not by other flowering time regulators. We have previously reported that OsCOL4 is a constitutive repressor of Ehd1 (Lee et al. ). Because this is also true of AP2 genes, it is likely that OsCOL4 suppresses Ehd1 by inducing AP2 expression. Hd1 also suppresses flowering time via repressing Hd3a and RFT1 under LD conditions (Yano et al. ; Hayama et al. ). These indicate that the AP2 genes and OsCOL4 co-operatively suppress flowering time.
We observed that miR172d expression is negatively affected by phytochrome activity. Considering that AP2 genes are controlled by miR172, we might conclude that phytochromes support vegetative growth by maintaining AP2 expression. Both Ghd7 and OsCOL4 are positively modulated by OsPhyB (Lee et al. ; Osugi et al. ). Therefore, it is apparent that phytochromes influence these flowering regulators collectively.
In plants, the miR172/AP2 module is inversely correlated with the miR156/SPL module (Aukerman and Sakai ; ; Wu and Poethig ; Chuck et al. ; Poethig ). In rice, miR156 genes are predominantly expressed in the young shoots, etiolated shoots, and seedling leaves (Xie et al. ) and its target OsSPL genes are expressed high in young panicles (Xie et al. ). Overexpression of miR156 OX causes various phenotypes such as increase of tiller numbers, late flowering, dwarfism, and decrease of spikelet numbers (Xie et al. ). In maize, overexpression of the maize miR156 prevents flowering and increases starch content (Chuck et al. ; ). This late-flowering phenotype is similar to that of SNB OX or OsIDS1 OX plants. Overexpression of the maize miR156 also causes increase of biomass and tiller number in maize and also in Arabidopsis, Brachypodium and switchgrass (Chuck et al. ). These phenotypes are similar to those of OsmiR156 OX (Xie et al. ; Chuck et al. ).
We demonstrated that over-expressions of OsIDS1 and SNB inhibited flowering time in rice by suppressing expression of Ehd1. In addition, expressions of the AP2 genes were repressed by miR172 and the later was increased in the osphyB and osphyA osphyB mutants. Based on these findings, we concluded that miR172 induced flowering by suppressing the AP2 genes and the microRNA gene was inhibited by phytochromes. The facultative LD-flowering phenotype of rice can be explained in part by the miR172-AP2 pathway.
Plant material and growth conditions
We have previously developed T-DNA-tagging lines in Oryza sativa japonica cv. Dongjin (Jeon et al. ). The flanking sequences were determined via inverse PCR (An et al. ; Ryu et al. ). T-DNA insertional mutants osphyA-2, osphyB-2, osmads50-1, osmads51-1, hd1-1, oscol4-2, osvil2-1, and ostrx1-1 were reported earlier (Lee et al. ; Jeong et al. ; Kim et al. ; Ryu et al. ; Lee et al. ; Yang et al. ; Choi et al. ). RNAi-suppressed plants of Ehd1 RNAi and OsId1 RNAi have been described previously (Kim et al. ; Park et al. ). A near isogenic line (NIL) that carries the ghd7 allele was presented by Kim et al. (). Seeds were germinated on a half-strength Murashige and Skoog medium containing 3% sucrose. They were incubated for one week at 28°C under constitutive light as previously reported (Yi and An ). Seedlings were transplanted into soil and cultured in growth chambers under either SD (12 h light at 28°C, humidity 70%; 12 h dark at 25°C, humidity 50%) or LD (14.5 h light at 28°C, humidity 70%; 9.5 h dark at 25°C, humidity 50%) as previously reported (Yi and An ).
Construction of osphyA osphyB double mutants
The osphyA osphyB double mutants were obtained by crossing osphyA-2 and osphyB-2 single mutants. This osphyA-2 mutant is a null allele generated by a T-DNA insertion in the fourth exon of OsphyA. The osphyB-2 mutant is also a null allele produced by inserting T-DNA in the third intron of OsphyB (Jeong et al. ). Afterward, F2 segregants were genotyped by PCR (35 cycles of 95°C for 15 s, 55°C for 30 s, and 72°C for 60 s), using a combination of gene-specific primers and the T-DNA primer 5′-TTGGGGTTTCTACAGGACGTAAC-3′. Those gene-specific primers were 5′-CAGGGAAAAGGGATTAGAGT-3′ and 5′-AGTGGACTCGGGTTAACTTT-3′ for osphyA-2, and 5′-AGTTAAGACGGAGCGACATA-3′ and 5′-GTAAGCGATCAGTTTGTGGT-3′ for osphyB-2. For further analyses, we selected F2 progeny that had homozygous mutant alleles for both genes.
Vector construction and transformation
The full-length cDNA clones of SNB and OsIDS1 were isolated by PCR, using primers SNB-FL-F and SNB-FL-R for SNB, and OsIDS1-FL-F and OsIDS1-FL-R for OsIDS1 (Additional file 2: Table S1). After the amplified fragments were digested with Xba I and Xho I, they were inserted into the pGA3780 binary vector between the rice actin promoter (Pact) and the nopaline synthase terminator (nos T) (Lee et al. ; Kim et al. ). For constructing a miR172-resistant form of SNB (rSNB), we introduced synonymous mutations into the miR172 binding site through site-directed mutagenesis, using primer sets rSNB-N-F/rSNB-N-R and rSNB-C-F/rSNB-C-R (Additional file 2: Table S1). Each amplified fragment was digested with Xba I/ACC III or ACC III/Xho I. Afterward, the digested fragments were inserted into the pGA3780 binary vector between the rice Pact and nos T. Similarly, a miR172-resistant form of OsIDS1 (rOsIDS1) was produced using the primer sets of rOsIDS1-N-F/rOsIDS1-N-R and rOsIDS1-C-F/rOsIDS1-C-R (Additional file 2: Table S1). To obtain double-overexpression plants of rSNB and Ehd1, we amplified their full-length cDNA clones with primer sets rSNB-FL-F/rSNB-FL-R and Ehd1-FL-F/Ehd1-FL-R (Additional file 2: Table S1). The rSNB fragment was digested with Bsi WI and Bsr GI, and the Ehd1 fragment was digested with Mlu I and Hpa I. Afterward, these digested fragments were inserted into the pGA3777 binary vector, a double expression cassette (Kim et al. ). We have previously described plants over-expressing miR172d (Lee and An ). The binary constructs were transformed into Agrobacterium tumefaciens LBA4404 (An et al. ) and transgenic plants were generated via Agrobacterium-mediated co-cultivation (Jeon et al. ).
RNA extraction and quantitative real-time RT-PCR
Total RNA was isolated with RNAiso Plus (Takara, Shiga, Japan) and first-strand cDNA was synthesized using Moloney murine leukemia virus (M-MLV) reverse transcriptase (Promega, Madison, WI, USA) as previously reported (Ryu et al. ; Lee et al. ; Yang et al. ). Synthesized cDNAs were used as a template for quantitative real-time RT-PCR (qRT-PCR) with SYBR® Premix Ex Taq™ II (Takara, Shiga, Japan) and the Rotor-Gene 6000 (Corbett Research, Sydney, Australia). Osubi1 served to normalize the quantity of cDNA. All experiments were conducted at least three times, with three or more samples at each point. Primer sequences for qRT-PCR are shown in Additional file 2: Table S1. Changes in expression were calculated via the ΔΔCt method. To ensure primer specificity, we performed the experiments when the melting curve showed a single peak. PCR products were sequenced to verify the specificity of the reaction.
Expression analysis of microRNA
For miRNA gel blot analysis, total RNA samples were extracted from plant materials using RNAiso Plus (Takara), with a few modifications as reported previously (Jung et al. ). After isopropanol precipitation, the Eppendorf tube containing the RNA pellets was briefly centrifuged without rinsing with ethanol to improve both the yield and solubility of miRNA in total RNA preparations. RNA gel blot analyses were performed with 5 μg of total RNA. Locked nucleic acid (LNA) 5′-ATgCAgCAtCAtCAaGAtTCT-3′ (upper- and lower-case letters indicate DNA and LNA, respectively) was used as an antisense oligonucleotide probe for miR172 (Varallyay et al. ). The miR172 LNA probe was either labeled with P32 or 3′-end-labeled with DIG-ddUTP (Roche, Mannheim, Germany). Levels of the primary miR172 (pri-miR172) transcripts were measured by qRT-PCR using the primer pairs described in Additional file 2: Table S1.
YSL and DYL designed the project, produced plant materials, monitored expression profiling, observed flowering time, analyzed data and wrote the manuscript. LHC produced Ehd1 OX plants and observed flowering time of those. GA provided an overall direction for this project and helped with the organization and editing of the manuscript. All authors read and approved the final manuscript.
We thank Sunghee Hong and Kyungsook An for generating the transgenic lines and managing the transgenic seeds, and Priscilla Licht for critical proofreading of the manuscript. We also thank the members of the Crop Biotech Center at Kyung Hee University for their participation in discussions. This work was supported in part by grants from the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center, No. PJ008128), Rural Development Administration, Republic of Korea; the Basic Research Promotion Fund, Republic of Korea (NRF-2007-0093862); and Kyung Hee University (20130214) to G.A.
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