- Research article
- Open Access
Comparative Transcriptomes Profiling of Photoperiod-sensitive Male Sterile Rice Nongken 58S During the Male Sterility Transition between Short-day and Long-day
© Wang et al; licensee BioMed Central Ltd. 2011
Received: 27 March 2011
Accepted: 25 September 2011
Published: 25 September 2011
Photoperiod-sensitive genic male sterile (PGMS) rice, Nongken 58S, was discovered in 1973. It has been widely used for the production of hybrid rice, and great achievements have been made in improving rice yields. However, the mechanism of the male sterility transition in PGMS rice remains to be determined.
To investigate the transcriptome during the male sterility transition in PGMS rice, the transcriptome of Nongken 58S under short-day (SD) and long-day (LD) at the glume primordium differentiation and pistil/stamen primordium forming stages was compared. Seventy-three and 128 differentially expressed genes (DEGs) were identified at the glume primordium differentiation and pistil/stamen primordium forming stages, respectively. Five and 22 genes were markedly up-regulated (≥ 5-fold), and two and five genes were considerably down-regulated (≥ 5-fold) under SD during the male sterility transition. Gene ontology annotation and pathway analysis revealed that four biological processes and the circadian rhythms and the flowering pathways coordinately regulated the male sterility transition. Further quantitative PCR analysis demonstrated that the circadian rhythms of OsPRR1, OsPRR37, OsGI, Hd1, OsLHY and OsDof in leaves were obviously different between Nongken 58S and Nongken 58 under LD conditions. Moreover, both OsPRR37 and Hd1 in the inflorescence displayed differences between Nongken 58S and Nongken 58 under both LD and SD conditions.
The results presented here indicate that the transcriptome in Nongken 58S was significantly suppressed under LD conditions. Among these DEGs, the circadian rhythm and the flowering pathway were involved in the male sterility transition. Furthermore, these pathways were coordinately involved in the male sterility transition in PGMS rice.
Photoperiod-sensitive genic male sterile (PGMS) rice, Nongken 58S, was discovered as a spontaneous mutant in the japonica rice cultivar Nongken 58 (Oryza sativa ssp. japonica) grown in Hubei Province, China in 1973 . It has since been used for production of hybrid rice, and during the past two decades, great achievements have been made in improving rice yields in China using two-line hybrid rice. Several important features of Nongken 58S have been characterised. Its fertility is highly regulated by day length at specific inflorescence developmental stages. Complete male sterility can be induced when the day length is greater than 14 h from the glume primordium differentiation stage to the pollen mother cell forming stage. However, male fertility returns gradually when the day length is shorter than 14 h . This is called the second photoperiod phenomenon , referring to the short day photoperiod that rice requires for the transition from vegetative growth to reproductive growth . This agronomic trait is genetically controlled by a recessive locus within the nuclear genome. However, the genetic loci vary depending on the genetic background of the recipient parents. That is, when crossed with a less photoperiod-sensitive cultivar, the genes for the trait appear as two or three loci [3–7]. The photoperiod sensitivity can also be affected by temperature when the pms gene is crossed into a temperature-sensitive cultivar. Previous studies have indicated that phytochromes and cryptochromes are involved in the male sterility transition . Because male sterility is highly and coordinately regulated by day length and temperature, this leads to difficulty in the accurate identification of the male sterile phenotype in the segregation populations between japonica and indica under natural conditions. Although it would be of great value to breeders, this makes mapping the pms gene challenging [3–5, 8, 9]. It is important to understand the molecular mechanism of the male sterility transition and to explore whether the light or circadian rhythm signal transduction pathway is involved in this process. It may also be useful to understand how light or the circadian rhythm regulates microsporocyte development. This information could assist breeders in selecting recipient parents for molecular breeding programs.
Circadian rhythms, in general, take the form of sinusoidal waves that can be described using mathematical terms such as period, phase and amplitude [10–12]. The expression of several genes has been found to be associated with the circadian rhythm in Arabidopsis. These include TIMING OF CAB EXPRESSION1 (TOC1) , LATE ELONGATED HYPOCOTYL (LHY) , CIRCADIAN AND CLOCK ASSOCIATED1 (CCA1)  and GIGANTEA (GI). TOC1, LHY, CCA1 and unknown factor Y [16, 17] comprise interlocked transcriptional feedback loops. These feedback loops play important roles in the plant central clock. These loops integrate environmental factors, such as light and temperature, into the central clock through the input signaling pathway and import the rhythm signal into downstream signaling pathways through output signaling pathways.
Two main pathways controlling flowering time are found in rice. One is the EARLY HEADING DATE1 (Ehd1)/HEADING DATE3a (Hd3a)/RICE FLOWERING LOCUS T1 (RFT1)-dependent pathway [18–22]. In this pathway, the upstream gene Ehd2/RID1/OsId1, under short-day (SD) conditions, activates Ehd1. Ehd1 then activates Hd3a/RFT1 to promote rice flowering. By contrast, Ehd1 is suppressed under long-day (LD) conditions. Hd3a/RFT1 is also suppressed, leading to the inhibition of rice flowering . The other pathway is the HEADING DATE1 (Hd1)-Hd3a/RFT1-dependent pathway [18, 23]. In this pathway, Hd1 is activated by OsGI under LD or SD conditions. Hd1 then activates Hd3a/RFT1 expression and promotes flowering under SD conditions. However, Hd1 suppresses Hd3a/RFT1 expression and inhibits flowering under LD conditions [18, 24, 25]. Previous research has indicated that circadian rhythms and day length are not only involved in the promotion of reproductive organs from the vegetative stage in higher plants [11, 26, 27], but are also involved in various physiological processes, including photosynthesis [28, 29], starch metabolism [30–32], phytohormone response [32–35], hypocotyl elongation [36, 37], and plant-pathogen interaction . However, the involvement of these two signaling pathways in the male sterility transition has not been reported.
This paper reports the comparison of the transcriptomes of Nongken 58S under SD and LD conditions during the male sterility transition. The repressive expression profile under LD conditions identified 183 differentially expressed genes (DEGs). Gene ontology (GO) and pathway analysis of the DEGs revealed that the circadian rhythm and the flowering pathways were involved in the male sterility transition. In further analysis, qPCR results indicated that the circadian rhythms of OsPRR1, OsPRR37, OsGI, Hd1, OsLHY and OsDof in Nongken 58S were significantly different from those in Nongken 58. This suggests that the circadian rhythm and the flowering pathways were coordinately involved in regulation of the male sterility transition.
The varieties Nongken 58 and the mutant Nongken 58S (Oryza sativa L. ssp. japonica) were used for this study. All plants were grown under natural conditions at Wuhan University Campus. SD (10-h light/14-h dark) treatment was conducted when the seedlings had greater than five leaves. Differentiation from vegetative growth to reproductive growth was promoted after 10-12 days of SD treatment. When the inflorescences had developed to the secondary branch differentiation stage, the rice plants were divided into two groups for LD (15-h light/9-h dark) and SD treatment, respectively.
RNA isolation and cDNA synthesis
For total RNA isolation, the second fully expanded leaf was harvested at two developmental stages: glume primordium differentiation and pistil/stamen primordium formation. For diurnal expression profile analysis, the leaves were harvested at 4 h intervals over 1 day, frozen immediately in liquid nitrogen, and stored at -80°C until use . The samples are annotated in Additional file 1, Table S1.
A TRIzol Reagent Kit (Invitrogen, Carslbad, USA) was used for total RNA isolation following the manufacturer's instructions. Total RNA was treated with RNase-free DNase I (New England Biolabs, Hitchin, UK) to remove DNA contamination before cDNA synthesis. Two micrograms of total RNA and Oligo (dT) were used as template and primers for first strand cDNA synthesis by M-MLV reverse transcriptase (Promega, Madison, USA).
Microarray analysis procedure and comparison strategy
Two micrograms of total RNA were used for double-stranded cDNA synthesis, and biotin-tagged cRNA was prepared using a MessageAmp™ II cRNA Amplification Kit according to the manufacturer's instructions. The resulting bio-tagged cRNA was fragmented into strands of 35-200 bases according to Affymetrix protocols. The fragmented cRNA was hybridised to an Affymetrix GeneChip Rice Genome Array containing 48,564 and 1,260 transcripts representing the japonica and indica cultivars, respectively. The microarray and data analysis were contracted to CapitalBio Corporation (Beijing, China). The hybridisation was performed at 45°C with rotation for 16 h (GeneChip Hybridization Oven 640, Affymetrix). The GeneChip arrays were washed and then stained (streptavidin-phycoerythrin) on an Affymetrix Fluidics Station 450. Scanning was conducted using a GeneChip Scanner 3000. All chip data represented biological triplicates.
The scanned images were examined by visual inspection and then processed to generate raw data using the default setting of GeneChip Operating Software (GCOS 1.4). dChip software was used to perform invariant-set normalization to normalize the arrays according to dChip users' manual. 5% of Perfect-Match (PM) probe signals were used as background removal. Annotation of the samples is shown in Additional file 1, Table S1. The samples were compared as follows: G-SSD2 vs. G-SLD2 and P-SSD2 vs. P-SLD2. The criteria for determining up- and down-regulated genes were fold changes (FCs) of ≥ 2 and ≤ 0.5, respectively. The complete microarray data have been deposited in NCBI's Gene Expression Omnibus and are accessible through GEO series accession number GSE29820.
Cluster, gene ontology annotation and pathway analysis
All microarray data were analysed using Significant Analysis of Microarray (SAM) 3.02 software. Genes with FC ≥ 2 or FC ≤ 0.5 were chosen for the t-test, and genes with P values < 0.05 were chosen for further analysis. Cluster analysis was performed using Cluster 3.0 software. GO annotation was performed using the GeneOntology Enrichment Analysis Software Toolkit (http://omicslab.genetics.ac.cn/GOEAST/php/affymetrix.php) [40, 41]. GOs with P values < 0.01 were selected. Pathway analysis was accomplished using the MAS 3.0 system (http://www.capitalbio.com/index.asp) (CapitalBio Corporation, Beijing, China) and by searching the Kyoto Encyclopedia of Genes and Genomes, BioCarta and GenMAPP databases. Pathways with P values < 0.01 were selected.
Quantitative PCR analysis
For quantitative PCR, the cycling conditions were 95°C for 10 min, followed by 40 cycles of 95°C for 10 s and 60°C for 30 s, and then a melting curve from 60°C to 95°C in 0.3°C increments. Negative controls without the template DNA were used to ensure that primer dimers were not interfering with amplification. qPCR data was captured and analysed using StepOne software (ver. 2.0). The relative gene expression levels in each cDNA sample were obtained by normalisation to ACTIN1 using the formula 2-(CT gene - CT actin1). The primers used in this study are listed in Additional file 2, Table S2. All qPCR data is the result of biological triplicates.
Dynamic transcriptome profiling of photoperiod treatment during the male sterility transition
Defining DEGs for GO annotation and pathway analysis
GO biological process of DEGs1
G-SSD2 vs. G-SLD2
GO:0048510 regulation of timing of transition from vegetative to reproductive phase
GO:0048572 short-day photoperiodism
GO:0010229 inflorescence development
GO:0006950 response to stress
GO:0009628 response to abiotic stimulus
GO:0006352 transcription initiation
GO:0006265 DNA topological change
P-SSD2 vs. P-SLD2
GO:0048510 regulation of transition from vegetative to reproductive phase
GO:0048572 short-day photoperiodism
GO:0010229 inflorescence development
Signal transduction pathway analysis of DEGs1
G-SSD2 vs. G-SLD2
Inositol phosphate metabolism
Starch and sucrose metabolism
P-SSD2 vs. P-SLD2
Cyanoamino acid metabolism
Alanine and aspartate metabolism
Circadian rhythm involvement in the male sterility transition
As mentioned previously, several clock genes [OsPRR1 (LOC_Os02g40510), OsPRR37 (LOC_Os07g49460), OsGI (LOC_Os01g08700), OsLHY (LOC_Os08g06110) and MYB transcription factor (LOC_Os06g51260)] were identified (Additional file 4, Table S4, Additional file 5, Table S5). Among these genes, OsPRR37 and OsGI were up-regulated 3.0-fold and 8.3-fold, respectively; OsLHY and the MYB transcription factor were down-regulated 2.4-fold and 2.6-fold, respectively. No difference in OsPRR1 expression was detected in the G-SSD2 vs. G-SLD2 data (Additional file 4, Table S4); in the P-SSD2 vs. P-SLD2 data, OsPRR1 was up-regulated 2.0-fold and the MYB transcription factor was down-regulated 4.4-fold. No differences in OsPRR37, OsGI and OsLHY were detected at this inflorescence developmental stage. The fold changes indicate that these clock genes were activated or repressed under LD conditions in Nongken 58S, implying that they may participate in the male sterility transition.
OsLHY, a dawn-phased gene, is repressed during the day and activated at night. Its expression level differed significantly between Nongken 58S and Nongken 58 at 22:00 h, 02:00 h, 06:00 h at the glume primordium differentiation stage, and 06:00 h at the pistil/stamen primordium forming stage (Figure 3E). However, no difference was detected under SD conditions (Additional file 6, Figure S1E). The results also indicated circadian rhythm differences between Nongken 58S and Nongken 58. OsDof (LOC_Os01g15900), a Dof-type zinc finger (Additional file 4, Table S4), showed a similar diurnal pattern to OsLHY. The major differences between Nongken 58S and Nongken 58 occurred at 22:00 h and 02:00 h at the glume primordium differentiation stage, and at 22:00 h, 02:00 h, and 06:00 h at the pistil/stamen primordium forming stage (Figure 3F).
Taken together, these differences only occurred under LD conditions at the photoperiod-sensitive developmental stage. Based on the genetic background of Nongken 58S and Nongken 58, these genes were all related to the male sterility transition and the rice circadian rhythm was involved in this process.
Flowering gene Hd1 is involved in the male sterility transition under LD conditions
Ehd1, Hd3a, RFT1 and OsMADS1 were all significantly suppressed under LD conditions in Nongken 58S (Additional file 4, Table S4; Additional file 5, Table S5). Ehd1, Hd3a, RFT1 are crucial genes for rice flowering [18–21, 23], and OsMADS1 plays key roles in specifying floral organ and meristem identity in rice [46–48]. Ehd2 and Hd1 are also important components of the flowering pathway. To determine whether these genes were involved in the male sterility transition, the diurnal expression profiles of these genes were analysed. Hd1 was the only gene exhibiting different daily expression profiles between Nongken 58S and Nongken 58 under LD conditions (Figure 3D and Additional file 7, Figure S2). The main differences occurred at the pistil/stamen primordium forming stage. The transcription levels at 22:00 h and 06:00 h in Nongken 58S were significantly different from those in Nongken 58, indicating that the peak phase of Hd1 was at 06:00 h in Nongken 58 and it was shifted forward to 22:00 h in Nongken 58S. The phase is a mathematical term of plant circadian rhythms . The phase-shift indicated that the circadian rhythm of Hd1 in Nongken 58S was notably different from that in Nongken 58, while the flowering time of Nongken 58 is similar to that of Nongken 58S under LD conditions. This suggests that Hd1 plays a role in the male sterility transition in PGMS.
OsPRR37 and Hd1 were differentially expressed in the inflorescences of Nongken 58S and Nongken 58
Circadian rhythm and light signals have been reported to be involved in several physiological processes, including flowering, various stress responses and metabolism [26, 30, 31, 38]. However, this is the first report suggesting a role for circadian rhythm and flowering signals in the regulation network of male sterility. In general, these genes promote the transition from vegetative growth to reproductive growth under SD conditions in SD plants and under LD conditions in LD plants . Although the male sterility transition in PGMS rice is known to be regulated by LD conditions, the mechanism of regulation remains unknown. Global gene expression profiling under LD conditions revealed a suppressive trend and categorised into the circadian rhythm and flowering pathways. Both pathways regulate the process in a coordinated manner. Further studies revealed that the diurnal expression profiles of OsPRR1, OsPRR37, OsGI, OsLHY, OsDof and Hd1 under LD conditions were reprogrammed.
In this study, OsPRR1, OsPRR37 and OsGI exhibited similar expression patterns in the leaf under LD conditions, suggesting that these three genes may function together. OsLHY and OsDof also exhibit similar differentially expressed patterns, suggesting that they may function coordinately. In Arabidopsis, TOC1/PRR1, LHY and GI, key component factors in the central clock, comprise interlocked transcriptional feedback loops to regulate plant circadian rhythms . In PGMS rice, OsPRR1, OsLHY and OsGI were not only involved in the circadian rhythm, but were also involved in the male sterility transition in coordination with OsPRR37 and OsDof. The LD signals maybe integrated and transmitted to the downstream genes through rice central clock in leaves. The day length signal may have been transmitted to the inflorescence via Hd1 and OsPRR37, ultimately leading to pollen abortion.
In the rice flowering pathway, OsGI is upstream of Hd1 and is positively correlated with Hd1 expression. Hd1 is activated by OsGI under LD or SD conditions. Hd1 activates Hd3a/RFT1 expression under SD conditions to promote flowering. However, Hd1 suppresses Hd3a/RFT1 expression under LD conditions to inhibit flowering . In PGMS rice, Hd1 expression may also have a positive correlation with OsGI under LD conditions in Nongken 58S, as its expression was activated after OsGI expression (Figure 3 C, D). This implies that Hd1 may function downstream of OsGI in the male sterility transition in PGMS rice. In this case, Hd3a/RFT1 may not be the downstream regulator of Hd1 since there were no rhythm differences between Nongken 58S and Nongken 58. Hd1 was activated by OsGI under LD conditions and suppressed the unknown factors. This may influence downstream gene expression and finally affect male fertility.
In leaves, the diurnal expression patterns of OsPRR1, OsPRR37, OsGI, OsLHY, OsDof and Hd1 showed significant differences between Nongken 58S and Nongken 58. In the inflorescence, only OsPRR37 and Hd1 exhibited different expression patterns between Nongken 58S and Nongken 58 under both LD and SD. Therefore, it is speculated that the clock genes in leaves may function as sensors for day length. These genes may receive day length signals and integrate and transmit the signals into the inflorescence through a series of unknown pathways. Both OsPRR37 and Hd1 may be the effectors in the inflorescence, and they are likely involved in regulation of male sterility directly.
Previous studies have indicated that phytochromes and cryptochromes are involved in the male sterility transition. However, there were no diurnal expression differences in OsPhyA, OsPhyB, OsCry1a, OsCry1b, OsCry2 and OsCry3 under LD conditions between Nongken 58S and Nongken 58 (data not shown). Using an ELISA assay, Wang, et al. found that phyA content in Nongken 58S leaves was higher than in Nongken 58 under the identical day length treatment . The differences in phytochromes and cryptochromes may be at the protein level and needs further investigation.
In conclusion, the transcriptome of Nongken 58S was significantly suppressed and the repression effects were markedly intensified when inflorescence development proceeded. Rice circadian rhythm genes OsPRR1, OsPRR37, OsGI, OsLHY and OsDof and the flowering gene Hd1 were coordinately involved in signal transduction in leaves. Furthermore, Hd1 and OsPRR37 may be signal sensors in inflorescences to directly affect the male sterility transition.
Acknowledgements and Funding
This work was supported by the National Basic Research Program of China (973) 2011CB100102. We are grateful to Dr. Hexin Guan for technical assistance.
- Shi MS: The discovery and study of the photosensitive recessive male-sterile rice. Scientia Agricultura Sinica. 1985, 2: 44-48.Google Scholar
- Yuan SC, Zhang ZG, Xu CZ: Studies on the critical stage of fertility change induced by light and its phase development in HPGMR. Acta Agronomica Sinica. 1988, 14: 7-13.Google Scholar
- Li XH, Wang FL, Lu Q, Xu CG: Fine Mapping of PSGMS Gene pms3 in Rice. Acta Agronomica Sinica. 2002, 28: 310-314.Google Scholar
- Mei MH, Chen L, Zhang Z, Li Z, Xu C, Zhang Q: pms3 is the locus causing the original photoperiod-sensitive male sterility mutation of 'Nongken 58S'. Science China Life Sciences. 1999, 42: 316-322. 10.1007/BF03183609.View ArticleGoogle Scholar
- Wang FP, Mei MH, Xu CG, Zhang QF: pms1 is not the Locus Relevant to Fertility Difference between the Photoperiod-sensitive Male Sterile Rice Nongken 58S and Normal Rice "Nongken 58". Acta Botanica Sinica. 1997, 39: 922-925.Google Scholar
- Zhang Q, Shen BZ, Dai XK, Mei MH, Saghai Maroof MA, Li ZB: Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proceedings of National Academic of Science. 1994, 91: 8675-8679. 10.1073/pnas.91.18.8675.View ArticleGoogle Scholar
- Zhang XG, Zhu YG: A Genetic Study on Sterility of Hubei Photoperiod Sensitive Genic Male-Sterile Rice. Journal of Huazhong Agricultural University. 1990, 9: 481-483.Google Scholar
- Liu N, Shan Y, Wang FP, Xu CG, Peng KM, Li XH, Zhang QF: Identification of an 85-kb DNA fragment containing pms1, a locus for photoperiod-sensitive genic male sterility in rice. Molecular Genetics and Genomics. 2001, 266: 271-275. 10.1007/s004380100553.View ArticlePubMedGoogle Scholar
- Lu Q, Li XH, Guo D, Xu CG, Zhang Q: Localization of pms3, a gene for photoperiod-sensitive genic male sterility, to a 28.4-kb DNA fragment. Molecular Genetics and Genomics. 2005, 273: 507-511. 10.1007/s00438-005-1155-4.View ArticlePubMedGoogle Scholar
- Dunlap JC, Loros JJ, DeCoursey P: Chronobiology: Biological Timekeeping. 2004Google Scholar
- McClung CR: Plant circadian rhythms. Plant Cell. 2006, 18: 792-803. 10.1105/tpc.106.040980.View ArticlePubMedPubMed CentralGoogle Scholar
- Harmer SL: The circadian system in higher plants. Annual Review of Plant Biology. 2009, 60: 357-377. 10.1146/annurev.arplant.043008.092054.View ArticlePubMedGoogle Scholar
- Somers DE, Webb AA, Pearson M, Kay SA: The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development. 1998, 125: 485-494.PubMedGoogle Scholar
- Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carre IA, Coupland G: The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell. 1998, 93: 1219-1229. 10.1016/S0092-8674(00)81465-8.View ArticlePubMedGoogle Scholar
- Wang ZY, Tobin EM: Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell. 1998, 93: 1207-1217. 10.1016/S0092-8674(00)81464-6.View ArticlePubMedGoogle Scholar
- Locke JC, Southern MM, Kozma-Bognar L, Hibberd V, Brown PE, Turner MS, Millar AJ: Extension of a genetic network model by iterative experimentation and mathematical analysis. Molecular Systems Biology. 2005, 1: 2005 0013-View ArticlePubMedPubMed CentralGoogle Scholar
- Locke JC, Kozma-Bognar L, Gould PD, Feher B, Kevei E, Nagy F, Turner MS, Hall A, Millar AJ: Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Molecular Systems Biology. 2006, 2: 59-View ArticlePubMedPubMed CentralGoogle Scholar
- Komiya R, Yokoi S, Shimamoto K: A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development. 2009, 136: 3443-3450. 10.1242/dev.040170.View ArticlePubMedGoogle Scholar
- Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K: Hd3a and RFT1 are essential for flowering in rice. Development. 2008, 135: 767-774. 10.1242/dev.008631.View ArticlePubMedGoogle Scholar
- Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K: Hd3a protein is a mobile flowering signal in rice. Science. 2007, 316: 1033-1036. 10.1126/science.1141753.View ArticlePubMedGoogle Scholar
- Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A: Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes & Development. 2004, 18: 926-936. 10.1101/gad.1189604.View ArticleGoogle Scholar
- Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M: Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant & Cell Physiology. 2002, 43: 1096-1105. 10.1093/pcp/pcf156.View ArticleGoogle Scholar
- Izawa T: Daylength measurements by rice plants in photoperiodic short-day flowering. International Review of Cytology. 2007, 256: 191-222.View ArticlePubMedGoogle Scholar
- Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K: Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature. 2003, 422: 719-722. 10.1038/nature01549.View ArticlePubMedGoogle Scholar
- Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T: Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell. 2000, 12: 2473-2484.View ArticlePubMedPubMed CentralGoogle Scholar
- Turck F, Fornara F, Coupland G: Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annual Review of Plant Biology. 2008, 59: 573-594. 10.1146/annurev.arplant.59.032607.092755.View ArticlePubMedGoogle Scholar
- Kobayashi Y, Weigel D: Move on up, it's time for change-mobile signals controlling photoperiod-dependent flowering. Genes & Development. 2007, 21: 2371-2384. 10.1101/gad.1589007.View ArticleGoogle Scholar
- Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA: Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science. 2005, 309: 630-633. 10.1126/science.1115581.View ArticlePubMedGoogle Scholar
- Yakir E, Hilman D, Harir Y, Green RM: Regulation of output from the plant circadian clock. FEBS Journal. 2007, 274: 335-345. 10.1111/j.1742-4658.2006.05616.x.View ArticlePubMedGoogle Scholar
- McClung CR, Gutierrez RA: Network news: prime time for systems biology of the plant circadian clock. Current Opinion in Genetics & Development. 2010, 20: 588-598. 10.1016/j.gde.2010.08.010.View ArticleGoogle Scholar
- de Montaigu A, Toth R, Coupland G: Plant development goes like clockwork. Trends in Genetics. 2010, 26: 296-306. 10.1016/j.tig.2010.04.003.View ArticlePubMedGoogle Scholar
- Doherty CJ, Kay SA: Circadian control of global gene expression patterns. Annual Review of Genetics. 2010, 44: 419-444. 10.1146/annurev-genet-102209-163432.View ArticlePubMedPubMed CentralGoogle Scholar
- Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL: Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biology. 2008, 9: R130-10.1186/gb-2008-9-8-r130.View ArticlePubMedPubMed CentralGoogle Scholar
- Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, Chory J: A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biology. 2008, 6: e225-10.1371/journal.pbio.0060225.View ArticlePubMedPubMed CentralGoogle Scholar
- Mizuno T, Yamashino T: Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant & Cell Physiology. 2008, 49: 481-487. 10.1093/pcp/pcn008.View ArticleGoogle Scholar
- Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN: Rhythmic growth explained by coincidence between internal and external cues. Nature. 2007, 448: 358-361. 10.1038/nature05946.View ArticlePubMedGoogle Scholar
- Niwa Y, Yamashino T, Mizuno T: The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant & Cell Physiology. 2009, 50: 838-854. 10.1093/pcp/pcp028.View ArticleGoogle Scholar
- Roden LC, Ingle RA: Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell. 2009, 21: 2546-2552. 10.1105/tpc.109.069922.View ArticlePubMedPubMed CentralGoogle Scholar
- Yang DC, Zhu YG: Primary study on total leaf RNA in PGMR at different photoperiod treatments and developmental stages. Acta Genetica Sinica. 1990, 17: 308-312.Google Scholar
- Hulsegge I, Kommadath A, Smits MA: Globaltest and GOEAST: two different approaches for Gene Ontology analysis. BMC Proceeding. 2009, 3 (Suppl 4): S10-10.1186/1753-6561-3-s4-s10.View ArticleGoogle Scholar
- Zheng Q, Wang XJ: GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Research. 2008, 36: W358-363. 10.1093/nar/gkn276.View ArticlePubMedPubMed CentralGoogle Scholar
- Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q: Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics. 2008, 40: 761-767. 10.1038/ng.143.View ArticlePubMedGoogle Scholar
- Shi Y, Zhao S, Yao J: Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice. Journal of Integrative Plant Biology. 2009, 51: 774-781. 10.1111/j.1744-7909.2009.00849.x.View ArticlePubMedGoogle Scholar
- Xue GX, Zhao JZ: A Preliminary Study on the Critical-Daylength Evoking the Photoperiodic Sensitive Male Sterility of Rice and Their Responses to Other Environmental Factors. Acta Agronomica Sinica. 1990, 16: 112-122.Google Scholar
- Hedegaard J, Arce C, Bicciato S, Bonnet A, Buitenhuis B, Collado-Romero M, Conley LN, Sancristobal M, Ferrari F, Garrido JJ, et al: Methods for interpreting lists of affected genes obtained in a DNA microarray experiment. BMC Proceeding. 2009, 3 (Suppl 4): S5-View ArticleGoogle Scholar
- Chen ZX, Wu JG, Ding WN, Chen HM, Wu P, Shi CH: Morphogenesis and molecular basis on naked seed rice, a novel homeotic mutation of OsMADS1 regulating transcript level of AP3 homologue in rice. Planta. 2006, 223: 882-890. 10.1007/s00425-005-0141-8.View ArticlePubMedGoogle Scholar
- Agrawal GK, Abe K, Yamazaki M, Miyao A, Hirochika H: Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Mol Biol. 2005, 59: 125-135. 10.1007/s11103-005-2161-y.View ArticlePubMedGoogle Scholar
- Prasad K, Parameswaran S, Vijayraghavan U: OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J. 2005, 43: 915-928. 10.1111/j.1365-313X.2005.02504.x.View ArticlePubMedGoogle Scholar
- Wang W, Tong Z, Kuang TY, Tang PS: Immunoassay of Phytochrome A Content in Photoperiod-sensitive Genic Male-sterile Rice. Developmental and Reproductive Biology. 1996, 5: 51-59.Google Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.