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. 2026 Jun 16;26:1456. doi: 10.1186/s12870-026-08918-8

Comparative transcriptome analysis reveals key genes and regulatory networks regulating flowering in rice varieties with different photoperiod sensitivity

Pengpeng Fang 1, Xinpeng Li 3, Jia Zeng 1, Yi Zhou 3, Qiang He 1,2,3, Fu Shu 2,3, Huafeng Deng 1,2,3,✉, Pingyong Sun 1,2,3,✉, Wuhan Zhang 2,3,✉
PMCID: PMC13508421  PMID: 42304223

Abstract

Background

Rice is a short-day plant whose flowering is critically regulated by photoperiod. Through long-term domestication and selective breeding, rice cultivation has adapted to photoperiod variations across different latitudes, resulting in varieties with broad photoperiod sensitivity (PS). PS is essential for rice to adapt to different geographical regions and a wide range of cultivation environments.

Results

This study compared the panicle differentiation phenotypes of four rice materials with different photoperiod sensitivities under long-day (LD) and short-day (SD) conditions. Results showed that highly photoperiod-sensitive varieties exhibit a stronger response to photoperiod shifts, leading to accelerated young panicle differentiation and earlier heading under SD conditions. For example, the highly photoperiod-sensitive material H26 headed 56 days earlier under SD than under LD conditions. Correspondingly, under SD conditions, the expression of key flowering genes Hd3a and RFT1 was significantly upregulated in H20, H17, and H26. Transcriptome analysis of leaves treated on day 10 revealed that SD conditions significantly upregulated the expression of key flowering genes such as RFT1, Hd3a, and Se5, while downregulating flowering repressor genes such as Ghd7 and Ghd8, thereby promoting photoperiod-induced early heading. Functional enrichment analysis indicated that these DEGs were primarily associated with starch and sucrose metabolism, plant hormone signal transduction, and circadian rhythm-plant pathway. Furthermore, we identified 125 upregulated and 56 downregulated genes that were uniquely co-expressed across all three photoperiod-sensitive materials. Additionally, five uniquely expressed DEGs related to flowering were identified in the highly photoperiod-sensitive material H26.

Conclusions

Our study identified DEGs specifically associated with photoperiod-sensitive materials. These genes represent promising candidates for further investigation into the molecular mechanisms underlying photoperiod responsiveness in rice. Our research helps clarify how rice responds to changes in photoperiod, elucidates the expression pattern of photoperiod-induced genes, and provides valuable insights for breeding rice varieties that are better adapted to changing climatic conditions.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12870-026-08918-8.

Keywords: Photoperiod sensitivity, Young panicle differentiation, Heading date, RNA-seq, Hd3a and RFT1, Rice

Introduction

Rice (Oryza sativa L.) is an important crop worldwide whose regional adaptation and grain yield are largely determined by heading date (flowering). Heading date in rice is affected by various factors such as photoperiod and temperature, but photoperiod acts as the most critical regulator [1]. The young panicles differentiation period serves as an important symbol of rice’s shift from nutrient growth to reproductive growth and directly affects rice flowering. Many plant species sense daylength to determine when to transition from vegetative growth to reproductive development. Plants are classified as long-day (LD), short-day (SD) and day-neutral species according to how they sense photoperiod to induce flowering [2]. Rice is a so-called short-day plant, flowering is promoted under SD conditions and inhibited by LD conditions. After a long period of natural and artificial selection during rice breeding, rice cultivation has expanded to a wider area and adapted to local photoperiodic variations, which requires rice varieties with varying degrees of photoperiod sensitive (PS) to enable them to flower under different daylengths [3–5].

In essence, the heading date of rice determines its yield and regional adaptability. After a long period of extensive research, a number of key regulatory factors controlling the rice tasseling period have been isolated. They can be organized into a complex molecular network including at least three major categories, such as photoperiod, circadian clock pathway, and hormones pathway, respectively. However, as a key factor influencing heading date, PS is regulated by the coordinated action of multiple core effector genes, such as Ghd8/DTH8, Ghd7, Hd1, and DTH7/Ghd7.1 [6–10]. Through their interactions in response to changing daylength, these genes largely define the adaptability and production potential of rice varieties. The underlying genetic architecture of photoperiod regulation in rice is becoming well understood. For example, the Ghd8 delays flowering in rice by regulating Ehd1, RFT1, and Hd3a under LD conditions [11, 12]. The Ghd7 has been proven to have major effects on an array of traits in rice, including number of flowering time, plant height and grains per panicle [13]. Expression of Ghd7 gene was enhanced under LD conditions, which delayed tasselling, increased plant height and number of grains per panicle. A homolog of Arabidopsis thaliana CONSTANS (CO), Heading date 1 (Hd1), play an important regulator of photoperiod sensitive heading. Hd1 promotes flowering and expression of the rice Flowering locus T homolog Heading date 3a (Hd3a) under SD conditions [14, 15]. Ghd7.1/DTH7 encodes a pseudo-response regulator protein, a pleiotropic gene controlling heading date, plant height and the number of spikelets per panicle, and its expression is regulated by photoperiod [16, 17]. Under LD conditions, DTH7 suppresses the expression of the rice florigen gene Hd3a and RFT1 positive regulator Ehd1, thereby delaying flowering [18]. Under LD conditions, the formation of a transcriptional complex containing both Hd1 and Ghd7 proteins could repress Ehd1 expression [19].

Similarly, the remaining flowering-related genes play important roles in the induction of photoperiodic sensation in rice. Under LD conditions, Hd16 down-regulates the transcript levels of Ehd1 and its downstream genes (such as Hd3a and RFT1) by phosphorylating Ghd7, thereby enhancing its function and ultimately delaying flowering [20]. Under both LD and SD conditions, Hd16 can enhance Hd3a expression [19]. OsELF3 is homologous to Arabidopsis ELF3, and OsELF3 acts as a flowering activator that interacts with biological clock genes to promote flowering in rice under LD [21]. DTH2 is a minor-effect quantitative trait locus (QTL) that promotes rice heading under LD, with its expression regulated by circadian rhythms. It mainly promotes heading by inducing the expression of the florigenin genes Hd3a and RFT1 [22, 23]. The photoperiod-sensitive gene Photoperiod Sensitivity 5 (SE5), promotes early flowering in rice with SD conditions. It inhibits heading by affecting both Hd1 and Ehd1 flowering pathways [24, 25]. Phosphorylation modification of OsFD1 facilitates the entry of the florigenin-activating complex into the nucleus and promotes the transition from nutrient to reproductive growth in rice [26]. MADS transcription factors play an important role in plant growth and development, not only involved in the process of plant floral organ formation, but also involved in the regulation of plant flowering time, flowering time and seed size and many other processes related to plant growth and development [27–30]. The knockout and overexpression of the MADS50 gene showed that OsMADS50 is located upstream of OsMADS14, OsMADS15, and Hd3a, thereby regulating multiple flower-forming genes, and playing a crucial role in rice flowering [31]. OsMADS51 functions as a flowering-promoting factor, especially in the SD conditions, where it is located upstream of Ehd1, OsMADS14, and Hd3a [32]. Furthermore, previous studies have demonstrated that bZIP transcription factors and WRKY transcription factors also play crucial roles in regulating rice flowering. Such as, OsbZIP23 delays flowering by repressing the expression of OsMADS14 in rice [33]. Following suppression of Dlf1/WRKY11 expression, plants exhibited a flowering phenotype earlier than wild-type plants under LD conditions [34].

RNA sequencing technology (RNA-Seq) is a powerful tool for genome-wide transcriptomic analysis. Recently, RNA-Seq has been widely used to study gene expression related to fertility, stress responses, and flowering [35–37]. To fully understand the genetic and molecular mechanisms of rice PS and its potential practical applications, it is necessary to comprehensively investigate the genetic interactions among major heading date genes (such as, Ghd7, Ghd8), key flowering genes (Hd3a, RFT1) and other heading date related genes in response to PS. In this study, one non-photoperiod-sensitive rice material and three photoperiod-sensitive materials with different sensitivity levels were grown under artificial long-day (LD, 14 h) and short-day (SD, 12 h) conditions. Through phenotypic analysis and RNA-seq, we aimed to identify key genes involved in photoperiod-induced flowering in rice, reveal the expression patterns of flowering-related genes, and clarify specific regulatory pathways. Our findings provide new insights and potential candidate genes for future research on the molecular regulatory mechanisms controlling rice heading.

Materials and methods

Plant materials and growth conditions

One photoperiod-insensitive material, Yuehesimiao (YH), and three materials with different levels of photoperiod sensitivity: HF200 (H20), HF217 (H17), and HF226 (H26) were used in this study. This study utilized three photoperiod-sensitive rice lines (H20, H17, and H26) sourced from the Rice 3K Database. Photoperiod sensitivity was evaluated by growing plants under different day-length conditions (long-day and short-day) and recording heading dates. Their IRIS accession numbers and resequencing data for four heading-date genes (Hd1, Ghd7, DTH7, and Ghd8) are listed in Table S1.

All materials completed their main vegetative growth 50 days after sowing. They were then transferred to either artificial long-day conditions (LD, 14 h of light and 10 h of darkness, 30,000 lx) and artificial short-day conditions (SD, 12 h of light and 12 h of darkness, 30,000 lx) for treatment. Leaf samples were collected on days 5, 10, and 15 the start of treatment. After 15 days of treatment, the plants were moved to natural conditions and grown for an additional two weeks. To ensure accurate sampling, young panicles were collected and examined to determine their differentiation stage. The standard stages of rice panicle development were determined following the method described by Du et al. [38]. All plant materials were grown at an experimental site located at the Hunan Hybrid Rice Research Center in Changsha, China (28º17′35′′ N, 113º15′55′′ E).

RNA isolation and tanscriptome sequencing

Based on observations from previous studies, under both LD and SD conditions, most photoperiod-sensitive materials begin to exhibit early signs of young panicle differentiation (Stage 2) around day 10, making day 10 a critical turning point for most materials as they enter the reproductive transition. Samples collected on day 10 of treatment were chosen for sequencing. A total of 24 samples were used (four materials × two treatments × three biological replicates). Total RNA was extracted using TRIzol® reagent (Life Technologies, USA) following to the manufacturer’s protocol. Each sample had three biological replicates. RNA quality was checked by gel electrophoresis and a NanoPhotometer® spectrophotometer (IMPLEN, USA) to confirm purity and concentration. RNA integrity was assessed using an Agilent 2100 Bioanalyzer (Agilent, USA). High-quality RNA libraries were sequenced on the Illumina NovaSeq X Plus platform by Novogene Bioinformatics Institute (Beijing, China). The raw data were filtered to remove adapters and low-quality read. This produced clean reads, which were then mapped to the reference genome (http://plants.ensembl.org/Oryza_sativa/Info/Index) from Ensembl using BWA, followed by transcript assembly.

Identification and analysis of differentially expressed genes

Gene expression was quantified based on HTSeq-derived read counts and normalized as FPKM (fragments per kilobase per million mapped reads). Differential expression analysis was performed using DESeq, identifying genes with |log₂(Fold Change)| ≥ 1 and an adjusted P-value (padj) < 0.05 as differentially expressed genes (DEGs). DEGs were analyzed using the Goseq R package to identify significantly enriched Gene Ontology (GO) terms, and KOBAS software was used to detect their enrichment in Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. The RNA-seq data generated in this study are available in the National Genomics Data Center of China under accession number CRA036028.

RNA-seq validation by quantitative real-time PCR

To validate RNA-seq DEG data, 14 genes was selected for quantitative real-time PCR (qRT-PCR). Total RNA was reverse transcribed using the PrimeScript™ RT reagent Kit with gDNA Eraser (Perfect Real Time) for qRT-PCR kit (Takara Biomedical Technology, Beijing, China). Relative expression levels were calculated using the 2−ΔΔCt method, with the rice Ubiquitin5 gene as an internal reference. All experiments were performed with three biological replicates. The primer sequences are listed in Table S2.

Results

Short-day treatment accelerates photoperiod induction and promotes heading

To examine how photoperiod induction differentially affects rice varieties with varying photoperiod sensitivity, we analyzed panicle differentiation in four rice materials under LD and SD conditions using an immature panicle stripping method. The results showed that the photoperiod-insensitive material YH initiated young panicle differentiation and reached at least stage 4 under both LD and SD conditions (Fig. 1A). In contrast, under LD conditions, none of the three photoperiod-sensitive materials (H20, H17, and H26) had begun young panicle differentiation. After 15 days of SD treatment, however, all three sensitive materials showed varying degrees of early panicle differentiation, indicating the initiation of photoperiod induction. Under SD conditions, H20 only reached the initial differentiation stage, while H17 progressed to stage 4 (Fig. 1B - C). Notably, H26 exhibited the most advanced differentiation, approaching the heading stage, reflecting its high sensitivity to photoperiod changes (Fig. 1D). We further compared the heading dates of the four materials under early LD and SD conditions. Photoperiod-insensitive materials showed little response to photoperiod induction, whereas photoperiod-sensitive materials responded to SD treatment to varying degrees. Timely SD treatment significantly accelerated heading in photoperiod-sensitive materials. H26 exhibited the strongest response, with its heading date occurred approximately 56 days earlier under SD than under LD conditions (Fig. 1E). In summary, the results indicate that among the three photoperiod-sensitive materials, H26 showed the strongest photoperiod sensitivity, followed by H17, while H20 exhibited relatively weaker photoperiod sensitivity. Once rice completes its fundamental vegetative growth, appropriate short-day conditions can accelerate photoperiod-induced in photoperiod-sensitive materials, thereby promoting earlier heading.

Fig. 1.

Fig. 1

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Differences in heading date and panicle differentiation under LD and SD conditions. A-D The changes in young panicle differentiation after 15 days of treatment, with YH (A), H20 (B), H17 (C), H26 (D). Bar = 1cm. E Heading date of YH, H20, H17 and H26 under LD and SD conditions. Values are mean ± SD (n = 5). P-value was calculated by Student's t - test. ****P < 0.0001

Hd3a and RFT1 were markedly up-regulated under SD conditions

To elucidate the expression dynamics of key flowering regulators in response to photoperiod, we examined transcript levels of Hd3a and RFT1 in both photoperiod-sensitive and photoperiod-insensitive materials under LD and SD conditions at 5, 10, and 15 days after treatment (Fig. 2). The expression profiles of Hd3a and RFT1 varied markedly with photoperiod and over time. In photoperiod-insensitive materials, the expression patterns of Hd3a and RFT1 exhibited a consistent trend under both LD and SD conditions: remaining relatively stable during the early stage and increasing significantly at later stages. In contrast, photoperiod-sensitive materials maintained low expression levels under LD conditions, but exhibited a sustained upregulation under SD conditions. Notably, expression levels of both genes were significantly upregulated from 10th day onward across all materials and photoperiod treatments, indicating that this time point marks a critical transition in photoperiod-mediated induction. Therefore, we speculate whether other differentially expressed genes are involved in the photoperiod-induced process on the 10th day, thereby influencing photoperiod induction and flowering in rice.

Fig. 2.

Fig. 2

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Expression levels of Hd3a and RFT1 under LD and SD conditions

Comparison of differentially expressed genes

To examine the transcriptional changes associated with photoperiod sensitivity, we performed differential gene expression analysis on four rice materials after 10 days of treatment under LD and SD conditions using DESeq2 (Fig. 3A). Compared with their respective LD conditions, the numbers of differentially expressed genes (DEGs) under SD were 3,815 in YH (1,636 up-regulated and 2,179 down-regulated), 4,113 in H20 (2,207 up-regulated, 1,906 down-regulated), 4,124 in H17 (2,039 up-regulated, 2,085 down-regulated), and 4,460 in H26 (2,779 up-regulated, 1,681 down-regulated) (Tables S3 - S10). And to identify potential regulators of photoperiod-induced specific to photoperiod-sensitive materials, we compared gene expression patterns across the three sensitive materials under the same treatment duration. Compared with the other three materials, 400, 779, 576, and 1,568 genes were uniquely up-regulated in YH, H20, H17, and H26, respectively, while 975, 905, 895, and 829 genes were specifically down-regulated (Fig. 3B - C). Notably, we identified 125 up-regulated and 56 down-regulated DEGs that were co-expressed across all three photoperiod-sensitive materials but not in YH. We therefore propose that these commonly DEGs, unique to photoperiod-sensitive materials, may function in regulating rice panicle differentiation and thus influence the heading date.

Fig. 3.

Fig. 3

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Statistics of differentially expressed genes (DEGs) under SD vs. LD conditions. A Statistics on the number of DEGs. B-C Venn diagram of up-regulated and down-regulated DEGs

Expression change of the heading date genes

We analyzed the expression levels of 40 major heading date related genes. The results revealed significant differences in the expression changes of these genes between photoperiod-sensitive and photoperiod-insensitive materials after 10 days of SD treatment compared to LD conditions (Fig. 4, Table S11). Under SD vs. LD, the expression of OsCCT22, OsCCT38, DTH2, OsSPL2, Ghd2, and EFL4-1 was down-regulated in all materials, regardless of photoperiod sensitivity, while OsCCT11, SE5, OsLHY, and Ghd7.1 were up-regulated. Compared to the photoperiod-insensitive material YH, the photoperiod-sensitive materials consistently showed upregulation of Hd3a, RFT1, OsMADS14, and FTL9 under SD. In contrast, OsCCT01, OsFD1, Ghd7, and OsMADS50 were down-regulated in photoperiod-sensitive materials. The most photoperiod-sensitive material, H26, exhibited the most pronounced expression changes after 10 days of photoperiod treatment. Under SD, genes such as DTH2 (Log₂FC = -3.26), OsCCT22 (Log₂FC = -3.75), and Ghd7 (Log₂FC = -1.57) were significantly down-regulated, whereas RFT1 (Log₂FC = 7.24), Hd3a (Log₂FC = 11.18), FTL9 (Log₂FC = 8.56) and OsMADS14 (Log₂FC = 6.84) were markedly up-regulated.

Fig. 4.

Fig. 4

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Expression changes of 40 heading date associated genes under LD and SD conditions

KEGG pathway analysis of DEGs

To further explore the functional implications of the transcriptomic changes, we performed KEGG enrichment analysis on the DEGs from the day 10 comparison, focusing on the top 20 enriched pathways (Fig. 5). The analysis revealed distinct pathway activation patterns across materials. In the photoperiod-insensitive material YH (YH_10SD vs. YH_10LD), the most significantly enriched pathways included phenylpropanoid biosynthesis (22 genes up-regulated, 16 genes down-regulated), plant hormone signal transduction (30 up, 32 down), starch and sucrose metabolism (15 up, 16 down), and diterpenoid biosynthesis (3 up, 7 down) (Table S12). For the photoperiod-sensitive materials, the major enriched pathways varied. In H20, they were phenylpropanoid biosynthesis (31 up, 5 down), starch and sucrose metabolism (13 up, 15 down), plant hormone signal transduction (39 up, 20 down), and zeatin biosynthesis (6 up) (Table S13). In H17, primary pathways included photosynthesis (20 up, 4 down), phenylpropanoid biosynthesis (26 up, 8 down), and starch and sucrose metabolism (21 up, 15 down) (Table S14). In H26, key pathways were phenylpropanoid biosynthesis (34 up, 3 down), starch and sucrose metabolism (24 up, 12 down), diterpenoid biosynthesis (10 up, 3 down), and circadian rhythm - plant (7 up, 4 down) (Table S15). KEGG analysis indicated that DEGs were significantly enriched in pathways such as plant hormone signal transduction and diterpenoid biosynthesis following SD treatment. This suggests that these pathways may play an indirect role in mediating photoperiod induction, thereby promoting earlier heading under SD conditions.

Fig. 5.

Fig. 5

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Kyoto encyclopedia of genes and genomes (KEGG) enrichment of DEGs

DEGs specifically expressed in photoperiod-sensitive materials

We analyzed DEGs unique to the three photoperiod-sensitive materials to identify those potentially involved in photoperiod-induced processes. A total of 125 up-regulated and 56 down-regulated genes were specifically expressed across all three photoperiod-sensitive materials (Fig. 6A - B, Table S16). Under SD conditions, the flowering genes RFT1, MADS14, and FTL9 were all significantly upregulated. Additionally, several genes associated with IAA and GA signaling were markedly up-regulated, including the auxin-responsive gene OsSAUR19, the GA-stimulated transcript related gene OsGASR1 and GA biosynthesis gene OsGA20ox7 (Fig. 6C). The bHLH transcription factor gene OsbHLH127 was also significantly up-regulated. Previous studies have implicated bZIP transcription factors in regulating rice flowering. In this study, only the photoperiod‑sensitive materials showed significant down‑regulation of OsbZIP29 and OsbZIP64 under SD treatment, suggesting that these genes may participate in photoperiod‑induced flowering through a negative regulatory mechanism. OsMADS26, a member of the AGL12 group, may also be involved in the regulation of rice flowering.

Fig. 6.

Fig. 6

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Analysis of DEGs specifically expressed in photoperiod-sensitive materials. A 125 up-regulated DEGs. B 56 down-regulated DEGs. C 8 DEGs with elevated expression levels potentially associated with photoperiod sensitivity

To further elucidate the role of unique DEGs in photoperiod inducted flowering among highly photoperiod-sensitive materials, we conducted an analysis of the most sensitive material, H26, and identified 1,568 up-regulated and 829 down-regulated DEGs (Tables S17 - S18). Further analysis revealed 5 flowering associated DEGs (Fig. 7A). Specifically, in H26_10SD vs. H26_10LD, the transcription factor OsWRKY11 (Os01g0626400, Log₂FC = 1.59) and OsbZIP18 (Os02g0203000, Log₂FC = 1.80) were significantly up-regulated. Meanwhile, three genes were significantly down-regulated, including the bZIP transcription factor OsbZIP12 (Os01g0867300, Log₂FC = -1.79), the B-box zinc finger gene OsBBX26 (Os08g0536300, Log₂FC = -1.32), and APETALA-2-like transcription factor gene OsAP2-39 (Os04g0610400, Log₂FC = -2.99). At the same time, we performed qRT-PCR validation for the five candidate genes in the highly photoperiod-sensitive material H26 under LD and SD conditions at three time points (days 5, 10, and 15) (Fig. 7B - F). These three time points cover the key developmental stages from the initiation of young panicle differentiation to the pre-heading stage. The results showed that the expression patterns of the five genes under SD and LD conditions were highly consistent with the RNA-seq data (day 10). Based on these results, we speculate that these five genes are likely involved in photoperiod-induced flowering regulation in highly photoperiod-sensitive materials.

Fig. 7.

Fig. 7

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Expression of five flowering-related DEGs in the highly photoperiod-sensitive material H26. A Expression changes of five genes on day 10 from RNA-seq. B-F Relative expression level of OsbZIP18 (B), OsWRKY11 (C), OsbZIP12 (D), OsBBX26 (E), and OsAP2-39 (F) under LD and SD conditions on days 5, 10, and 15 of treatment. The OsUBQ5 was used as an internal reference. Data are presented as mean ± SD from three biological replicates. P-values were calculated by Student’s t - test. Not significant (ns), *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001

qRT-PCR validation of flowering-related genes

To validate the DEGs identified from RNA-seq analysis, we selected nine flowering-related DEGs for qRT-PCR verification. Under both LD and SD conditions, most flowering-related genes showed distinct expression patterns between photoperiod-sensitive and photoperiod-insensitive materials (Fig. 8). Compared with the photoperiod-insensitive material, the flowering genes Hd3a and RFT1, as well as the flowering promoter OsMADS14, and flowering locus T-like gene FTL9 were significantly up-regulated in all three photoperiod-sensitive materials under SD. In contrast, the flowering repressor genes Ghd7, CONSTANS-like protein DTH2, and OsCCT22 were consistently down-regulated under SD vs. LD, regardless of photoperiod sensitivity. Expression of the FT-like gene FTL10 varied across the different sensitive materials, while FTL4 showed no expression change in the weakly sensitivity material H20 under either photoperiod. Overall, the qRT-PCR results confirmed expression trends consistent with the RNA-Seq data for the selected flowering associated genes.

Fig. 8.

Fig. 8

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Expression patterns of selected DEGs were analysed by qRT-PCR. The OsUBQ5 was used as an internal reference. Data are presented as mean ± SD from three biological replicates. P-values were calculated by Student’s t - test. Not significant (ns), *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001

Discussion

Flowering time is a crucial agronomic trait that determines seasonal and regional adaptation as well as crop productivity [39, 40]. If local varieties flower too early, light resources are underutilised and the vegetative growth period is shortened, leading to reduced yields. Conversely, yields are also severely affected if the variety flowering too late, resulting in an excessively long growth period, delayed maturation, or failure to harvest before temperatures drop. Photoperiod-sensitive genes regulate heading date, which corresponds to the maturity of the variety [41]. Although some genes controlling heading date have been identified, rice possesses numerous photoperiod-sensitive genes with extremely complex regulatory mechanism. Their molecular genetic pathways need to be further investigated. In recent years, RNA-seq has been widely applied to study the transcriptome of many plants species under various environment conditions, including rice [42, 43], maize [44], and wheat [45] among others. Compared to photoperiod-insensitive materials, photoperiod-sensitive materials exhibit a greater number of DEGs. This may be because photoperiod-sensitive materials respond more strongly to photoperiod cycles, leading to more intricate changes in gene expression. In most rice cultivars, LD conditions promote vegetative growth, while flowering is induced in response to a transition from LD to SD conditions [46, 47].

Therefore, we employed RNA-seq to analyze the expression profiles of photoperiod-insensitive and photoperiod-sensitive materials under LD and SD conditions. We further examined the expression changes of known heading date genes and the expression patterns of flowering-related DEGs. Results revealed that under SD conditions, genes such as DTH2, Ghd7, and OsCCT22 were significantly down-regulated, while genes including Hd3a, RFT1, MADS14, and FTL9 were significantly up-regulated. DTH2 expression is regulated by circadian rhythms, promoting the expression of the auxin genes Hd3a and RFT1 to accelerate rice heading [48]. OsCCT22 suppresses heading under LD conditions and promotes heading under SD conditions [49]. The SD treatment confirmed that Ghd7 was sensitive to photoperiod and that long days delayed heading but did not alter the basic vegetative phase and reproductive growth phase [18]. We found that Ghd7 was down-regulated after SD treatment of both photosensitive and non-photosensitive materials, indicating that suggesting that its expression is regulated by photoperiodic. Previous studies have confirmed that MADS14 is downstream of Hd3a and RFT1 and participates in the transmission of the florigen signal [50]. In this study, MADS14 and RFT1 expression was significantly up-regulated in all three photoperiod-sensitive materials following SD treatment, indicating its involvement in flowering regulation. Under favorable SD conditions, knockdown of Hd3a and RFT1 resulted in almost complete suppression of flowering in rice, suggesting that these two genes have overlapping functions and are required for flowering in rice [51, 52]. Based on KEGG analysis, the circadian rhythm plant pathways were enriched in this process. RFT1 and Hd3a, as key florigen genes, are significantly up-regulated under SD treatment in photosensitive materials and directly regulated early flowering in rice.

Early heading date 1 (Ehd1) promotes flowering under SD by inducing the expression of FT-like genes [53]. The FTL genes are major genetic determinants of flowering in plants. For instance, OsFTL10 regulates Ehd1 and OsMADS51 through a feedback mechanism, thereby influencing early or delayed flowering in rice [54, 55]. Notably, in FTL10 transgenic plants, flowering regulation may differ subtly from that mediated by the core flower-forming factors Hd3a and RFT1 [56]. In the present study, MADS50 expression remained largely unchanged under SD compared to LD conditions. In contrast, RFT1, Hd3a, and FTL9 were significantly up-regulated in photoperiod-sensitive materials under SD vs. LD, underscoring their key roles in flowering regulation. The expression of other FTL genes varied across materials: FTL4 was down-regulated in H17 and H26 after SD treatment, whereas FTL10 was up-regulated. FTL12 showed down-regulation in H17 but up-regulation in H20. This may be due to differences in expression caused by varying material backgrounds. Beyond the FTL family, basic Helix-Loop-Helix (bHLH) and basic leucine zipper (bZIP) transcription factors are also known to regulate rice flowering [57, 58]. For example, OsbZIP65 suppresses Ehd1 expression, delaying heading under both LD and SD conditions [59]. In our analysis of 181 DEGs specifically expressed in the three photoperiod-sensitive lines (125 up-regulated, 56 down-regulated), OsbHLH127 was markedly up-regulated, while two bZIP transcription factors, OsbZIP29 and OsbZIP64, were significantly down-regulated. Thus, these genes were identified as potential candidate regulators of flowering in photoperiod-sensitive rice. It is noteworthy that the Arabidopsis agl12 mutant displays a delayed-flowering phenotype under LD conditions [60]. Nevertheless, in rice, OsMADS26 has so far been confirmed to function as a negative regulator of resistance to both blast fungus and bacterial leaf blight, and also to negatively modulate drought tolerance [61, 62]. However, whether it influences flowering under different photoperiods in rice requires further investigation.

Based on multi-year field phenotyping surveys conducted during the heading date, this study selected one photoperiod-insensitive material along with three varying degrees of photoperiod sensitivity. Gene expression patterns in other photoperiod-sensitive materials may differ from the findings presented here, likely due to variations in their genetic backgrounds. KEGG functional enrichment analysis of differentially expressed genes revealed that they were primarily associated with starch and sucrose metabolism, as well as plant hormone signal transduction. Previous studies have shown that auxin, gibberellin, and other phytohormones indirectly regulate flowering [63, 64]. Based on the above findings, we speculate that components of auxin and GA signaling may be located downstream of the core flowering pathway or act in concert with it, thereby participating in the regulation of flowering in rice. For example, OsSAUR56 influences rice flowering time and heading date by modulating the expression of the clock gene OsGI and two repressors, Ghd7 and DTH8 [65]. The GA1-3 gibberellin-deficient mutant lacks the enzyme responsible for the first step of GA biosynthesis and fails to flower under SD conditions [66–69]. The LFY gene, a central regulator of flowering that controls the transition from vegetative to reproductive development, is known to be induced by gibberellins (GAs) [70]. Our research found that under SD conditions, the Os04g0537100 (OsSAUR19) gene was significantly upregulated in all three photoreceptor tissues. Similarly, gibberellin biosynthesis-related genes GASR1 and OsGA20ox7 also showed marked upregulation. Therefore, we speculate that under short-day conditions, the upregulation of auxin- and gibberellin-related genes may lead to earlier heading by amplifying the photoperiod signal. This interactive mechanism may reveal a potential link between hormone signaling and the core flowering pathway involving Ghd7-DTH8-Ehd1, but this remains to be verified by future studies.

This study identified five DEGs associated with flowering that were specifically expressed in the strong photoperiod-sensitive material H26. Previous studies have revealed that under normal conditions, OsWRKY11 directly binds to the W-box elements in the promoters of the rice flowering-promoting genes OsMADS14 and OsMADS15, thereby activating their transcription and positively regulating rice heading [71]. The dlf1 mutation was found to suppress the transcription of Ehd2/RID1/OsId1 and its downstream flowering genes, including Hd1, Ehd1, and Hd3a, under both LD and SD conditions [71]. In our study, OsWRKY11 was significantly up-regulated under SD conditions, thereby promoting flowering, consistent with previous research findings. The vig1a allele of OsbZIP01 exhibits a late-heading phenotype, which depends on interaction with OsbZIP18 [72]. Thus, our results suggest that OsbZIP18 is involved in flowering regulation and participates in photoperiod-induced responses. OsABF1/OsbZIP12 acts as a negative regulator of flowering transition, exhibits functional redundancy with OsbZIP40. It likely delays flowering by directly activating OsWRKY104 expression, thereby suppressing Ehd1 expression [73]. In this study, the significant downregulation of OsbZIP12 likely promotes Ehd1 expression and accelerates flowering. OsBBX26/OsCOL15 inhibits flowering by upregulating the flowering repressor Ghd7 and downregulating the flowering activator RID1, ultimately leading to down-regulated expression of flowering activators such as Ehd1, Hd3a, and RFT1 [74]. OsAP2-39 is an APETALA-2-like transcription factor in rice. Overexpression of OsAP2-39 induces multiple phenotypic alterations in transgenic rice, such as reduced plant height and delayed heading by 1–2 weeks [75]. In this study, expression level of OsAP2-39 was significantly reduced under short-day conditions, which may indirectly promote earlier flowering. In summary, we speculate that these five flowering-related genes may function as early signaling components or downstream flowering regulators, thereby either promoting or inhibiting heading. Future studies will further investigate their functions.

Overall, the key mechanistic difference between photoperiod-sensitive and insensitive lines is that insensitive lines show little or no response to photoperiod changes. In the photoperiod insensitive line YH, key flowering genes (such as OsMADS14, Ehd1, RFT1, and Hd3a) did not exhibit significant changes in expression under LD or SD conditions, even after 10 days of treatment. In YH, RFT1 and Hd3a expression remained almost unchanged after 5 or 10 days under both photoperiods. We conducted a further analysis of three photoperiod-sensitive lines, including H26. These lines exhibited varying degrees of sensitivity (with H26 being the most sensitive), a difference attributable to changes in the amplitude and response speed of key regulatory factors in the photoperiod pathway under LD and SD conditions. These regulatory factors include Ghd7, Ehd1, Hd3a and RFT1. Under SD conditions in photoperiod-sensitive materials, Ghd7 expression was significantly down-regulated. At the same time, the expression of Ehd1, RFT1, and Hd3a was significantly up-regulated. This promoted heading. Among these genes, the photoperiod-sensitive line H26 exhibited the most significant differences in expression. Therefore, we believe that the essence of photoperiod sensitivity lies in the amplitude and speed of key genes responses to photoperiod change, rather than in their absolute expression levels under a single set of conditions.

Conclusions

Through qRT-PCR validation, we identified the response patterns of Hd3a and RFT1 to the photoperiod (significantly induced under SD conditions). Furthermore, combined with transcriptomic analysis, we identified several candidate genes (such as OsWRKY11 and OsBBX26) in photoperiod-sensitive materials that may be involved in the photoperiod-regulated flowering process. This suggests that these genes may play a potential regulatory role in photoperiod signaling pathways. Functional analysis of these DEGs and related signaling pathways (such as plant hormone signaling and circadian rhythm) provides new insights for further elucidating the regulatory network underlying rice photoperiod sensitivity.

Supplementary Information

Supplementary Material 1. (3.6MB, xlsx)

Acknowledgements

Not applicable.

Authors’ contributions

P.F. performed all experiments, prepared the figures and completed data analysis, and was the main contributor to the manuscript. X.L., J.Z. and Y.Z. provided experimental assistance. P.S., W.Z., H.D., Q.H., and F.S. conceived and provided project support for the research. P.S. and W.Z. designed the experiments and revised the manuscript. All authors reviewed and approved the final manuscript for publication.

Funding

This research was supported by the Top Ten Technical Breakthrough Projects of Hunan Province (Grant No. 2025QK1006).

Data availability

All data generated or analysed during this study are included in this published article and its supplementary information files. The raw data used in this study has been uploaded into China National center for Bioinformation system with the primary accession code GSA: CRA036028.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Huafeng Deng, Email: dhf@hhrrc.ac.cn.

Pingyong Sun, Email: zlspy23@126.com.

Wuhan Zhang, Email: zhangwuhan@hhrrc.ac.cn.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. Sang J, Zou D, Wang F, et al. Genom Proteom Bioinform. 2020;18(02):161–72. 10.1016/j.gpb.2018.12.011. IC4R-2.0: Rice Genome Reannotation using massive RNA-seq data. [DOI] [PMC free article] [PubMed]

Supplementary Materials

Supplementary Material 1. (3.6MB, xlsx)

Data Availability Statement

All data generated or analysed during this study are included in this published article and its supplementary information files. The raw data used in this study has been uploaded into China National center for Bioinformation system with the primary accession code GSA: CRA036028.

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