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Review

Research Progress on Photoperiod Gene Regulation of Heading Date in Rice

by
Jian Song
†,
Liqun Tang
†,
Yongtao Cui
,
Honghuan Fan
,
Xueqiang Zhen
and
Jianjun Wang
*
Institute of Crops and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
*
Author to whom correspondence should be addressed.
†
These authors contribution equally to this work.
Curr. Issues Mol. Biol. 2024, 46(9), 10299-10311; https://doi.org/10.3390/cimb46090613
Submission received: 22 July 2024 / Revised: 6 September 2024 / Accepted: 9 September 2024 / Published: 16 September 2024
(This article belongs to the Special Issue Advances in Multi-Omics for Functional Genomics Studies and Molecular Breeding)
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Abstract

:
Heading date is a critical physiological process in rice that is influenced by both genetic and environmental factors. The photoperiodic pathway is a primary regulatory mechanism for rice heading, with key florigen genes Hd3a (Heading date 3a) and RFT1 (RICE FLOWERING LOCUS T1) playing central roles. Upstream regulatory pathways, including Hd1 and Ehd1, also significantly impact this process. This review aims to provide a comprehensive examination of the localization, cloning, and functional roles of photoperiodic pathway-related genes in rice, and to explore the interactions among these genes as well as their pleiotropic effects on heading date. We systematically review recent advancements in the identification and functional analysis of genes involved in the photoperiodic pathway. We also discuss the molecular mechanisms underlying rice heading date variation and highlight the intricate interactions between key regulatory genes. Significant progress has been made in understanding the molecular mechanisms of heading date regulation through the cloning and functional analysis of photoperiod-regulating genes. However, the regulation of heading date remains complex, and many underlying mechanisms are not yet fully elucidated. This review consolidates current knowledge on the photoperiodic regulation of heading date in rice, emphasizing novel findings and gaps in the research. It highlights the need for further exploration of the interactions among flowering-related genes and their response to environmental signals. Despite advances, the full regulatory network of heading date remains unclear. Further research is needed to elucidate the intricate gene interactions, transcriptional and post-transcriptional regulatory mechanisms, and the role of epigenetic factors such as histone methylation in flowering time regulation. This review provides a detailed overview of the current understanding of photoperiodic pathway genes in rice, setting the stage for future research to address existing gaps and improve our knowledge of rice flowering regulation.

1. Introduction

Flowering (referred to as heading date) represents the transition of plants from vegetative growth to reproductive growth, serving as the pivotal physiological process determining the reproduction of flowering plants. In rice (Oryza sativa L.), the heading date is defined as the time from sowing to when the panicle emerges from the flag leaf, typically indicated when 50% of panicles have emerged. This timing is critical as it affects the period for photosynthetic accumulation, which in turn influences the environmental conditions during the grain filling stage and ultimately impacts rice yield and quality [1]. The heading date of rice is primarily influenced by genetic factors and environmental conditions. Studies in Arabidopsis thaliana have revealed several pathways regulating flowering, including the photoperiodic, circadian clock, vernalization, temperature sensing, autonomous flowering, gibberellin, and age-related pathways. Among these, the photoperiodic pathway plays a pivotal role in rice heading regulation. Understanding the genes involved in this pathway not only sheds light on the molecular mechanisms underlying variation in heading dates, but also offers potential for genetic improvements in rice heading times.
Rice is a short-day plant, and different varieties exhibit diverse responses to the photoperiod. Research has identified several key photoperiod-related genes affecting heading date in rice, including Ehd1, Hd1, DTH2, and OsGI (Table 1) [2,3,4,5]. Additionally, homologous genes to Arabidopsis flowering genes, such as RFT1 and Hd3a, have been found in rice [6,7,8,9,10]. These genes function similarly to their Arabidopsis counterparts, influencing heading by regulating the apical meristem (SAM) during leaf expression. The photoperiodic induction of heading in rice involves pathways such as OsGI-Hd1-Hd3a and Ghd7-Ehd1-Hd3a/RFT1 (Figure 1). Beyond photoperiodic signals, other factors like gibberellins (GA) and abscisic acid (ABA) also contribute to flowering induction.
This review aims to provide a comprehensive overview of the localization, cloning, and molecular regulatory mechanisms of genes associated with rice heading date. It discusses the current understanding of these genes, their interactions, and their applications in genetic enhancement for optimizing heading date in rice. By highlighting recent advancements and identifying areas requiring further research, this review underscores the importance of these genes in improving rice cultivation and adaptation.

2. Photoperiod Gene Regulatory Network for Rice Heading Date

2.1. Hd1 and Regulatory Genes

Rice, a model monocot and a typical short-day plant, shares several similarities with Arabidopsis in its response to photoperiod signals, despite some mechanistic differences. Many rice genes homologous to Arabidopsis photoperiod-induced genes have been identified, such as OsGI, Hd1, Hd3a, and RFT1. OsGI and Hd1 are homologous to Arabidopsis GI and CO (CONSTANS), while Hd3a and RFT1 are homologous to the Arabidopsis florigen gene FT [7,35]. Additionally, rice heading date regulatory genes OsMADS14 and OsMADS15 are homologous to maize MADS box gene ZAP1 [36]. These interactions form a photoperiod regulatory network controlling rice heading date.
Hd1, located on chromosome 6, encodes a B-box zinc finger protein and is the first cloned heading date gene in rice [37,38]. Although Hd1 in rice is highly homologous to CO in Arabidopsis, their mechanisms are not entirely identical. In Arabidopsis, CO controls flowering by regulating FT transcription; under LD conditions, CO activates FT transcription, promoting flowering; and under SD conditions, CO does not affect flowering [39]. In rice, Hd1 regulates heading date differently: under SD conditions, Hd1 promotes heading by increasing Hd3a expression; under LD conditions, Hd1 inhibits Hd3a transcription, delaying heading. Hd1 loss-of-function mutants exhibit early flowering under LD conditions [38]. Despite these differences, Hd1 and CO share significant similarities. Both genes are highly conserved in their regulatory pathways: in Arabidopsis, CO is regulated by the circadian clock gene GI, forming the GI-CO-FT pathway. Similarly, in rice, Hd1 is regulated by the circadian clock gene OsGI, forming the OsGI-Hd1-Hd3a pathway [3,20,39,40,41].
OsGI, homologous to Arabidopsis GI (GIGANTEA), is controlled by the circadian clock and inhibits flowering under LD conditions in rice, a characteristic different from Arabidopsis GI [42]. OsGI antagonizes rice phytochrome genes to regulate Ghd7 protein stability and flowering time [40]. HAF1 (Heading date-associated factor 1), an E3 ubiquitin ligase with a C3H4 ring domain located on chromosome 4, interacts with Hd1 and facilitates its degradation via the 26S proteasome pathway. HAF1 loss-of-function mutants exhibit late heading under both SD and LD conditions. Double mutants for HAF1 and Hd1 exhibit heading phenotypes similar to hd1 mutants under SD conditions and similar to haf1 mutants under LD conditions, indicating that HAF1 affects heading primarily through Hd1 transcriptional activity under SD conditions [43]. OsELF3, a direct substrate of HAF1, is involved in circadian regulation and photoperiod-induced heading. Double mutants for HAF1 and OsELF3 show heading times similar to oself3 plants under LD conditions [32]. SPIN1 (SPL11-interacting protein 1) interacts with the E3 ubiquitin ligase SPL11 and acts as a repressor of rice heading: under SD conditions, SPIN1 delays heading by mediating Hd1 inhibition of Hd3a transcription; under LD conditions, SPIN1 regulates heading independently of Hd1 [44]. RBS1 (RNA-binding and SPIN1-interacting 1) interacts with SPIN1 to regulate heading, inhibiting heading under both SD and LD conditions. RBS1 activates SPIN1 transcription while inhibiting SPL11 expression [45].
The rice heading gene Hd6 encodes the α subunit of protein kinase CK2 (CK2α) and delays heading under LD conditions by inhibiting FT-like gene expression [35]. Hd6 regulation of heading is controlled by Hd1, which modulates Hd6 transcriptional activity based on the photoperiod [46]. SE5 (PHOTOPERIOD SENSITIVITY5) senses light signals by regulating Hd1 transcription [47]. SE5 loss-of-function mutants exhibit early heading under both SD and LD conditions due to altered light signal pathways, making Hd1 insensitive to light [7,48]. Photoperiod sensitivity in rice heading involves major genes such as Hd1, Ghd7, and DTH8. Hd1 promotes heading under all photoperiods when Ghd7 and DTH8 are knocked out, while Ghd7 inhibits heading. Under LD conditions, Hd1 promotes Ghd7 expression, and Ghd7 and DTH8 form inhibitory complexes that partially or completely silence the Ehd1-Hd3a/RFT1 pathway, leading to delayed or absent heading. Under SD conditions, low Ghd7 expression allows Hd1 to compete with the inhibitory complex, promoting Hd3a/RFT1 expression and heading [3]. Therefore, rice photoperiodic flowering is controlled by two interacting modules: the Hd1-Hd3a/RFT1 pathway under SD and the (Hd1/Ghd7/DTH8)-Ehd1-Hd3a/RFT1 pathway under LD. These genetic differences provide a basis for the wide adaptability of rice.

2.2. Ehd1 and Regulatory Genes

Ehd1 is a critical regulator of rice heading date, located on chromosome 10, which encodes a B-type response regulator unique to rice. Under SD conditions, Ehd1 can promote heading independently of Hd1, indicating that Ehd1’s regulation of heading does not rely on Hd1. Moreover, Ehd1 promotes heading under both LD and SD conditions, differing from Hd1 in its response to photoperiod signals. Currently, no direct homologs of Ehd1 have been identified in the Arabidopsis genome. Under SD conditions, Ehd1 promotes rice heading by inducing the expression of Hd3a and RFT1 [49]. Extensive research has been conducted on Ehd1-mediated heading in rice. Ehd1 interacts with an A-type response regulator, OsRR1, forming a heterodimer. Overexpression of OsRR1 results in a late flowering phenotype, suggesting that OsRR1 may inhibit Ehd1 transcription, thereby affecting heading [50]. Cytokinins can induce the expression of OsRR1 and OsRR2, which bind to Ehd1 to form inactive complexes, suppressing Ehd1’s transcriptional activity. This indicates that exogenous cytokinins can delay flowering by inhibiting Ehd1, thereby prolonging the vegetative growth period [2]. While Ehd1 determines heading by regulating the transcription of Hd3a and RFT1, the interaction mechanisms among Ehd1, Hd3a, and RFT1 vary across different rice varieties. Studies involving segregating populations with various allelic combinations of Ehd1, Hd3a, and RFT1 revealed that Hd3a remains silent when Ehd1 is mutated, but RFT1 still exhibits transcriptional activity, albeit at a lower level compared to plants with functional Ehd1. Additionally, a null allele of RFT1 (rft1) was identified in these populations. Plants with homozygous mutations in ehd1 and hd3a/rft1 do not induce heading. Similar to Hd3a, RFT1 can interact with the florigen receptor 14-3-3 protein, but RFT1 null mutants cannot. Furthermore, research on sequence variations and geographical distribution indicates that functional RFT1 alleles were selected during the adaptation of rice to high-latitude regions [51].
Ehd2/RID1/OsId1/Ghd10 is a critical factor in rice flowering transition, encoding a zinc finger transcription factor homologous to the maize flowering promoter ID1 (INDETERMINATE1). In ehd2 mutants, Hd1 is insensitive to photoperiod, showing a late heading phenotype under both LD and SD conditions, indicating that Ehd2 is crucial for heading transition. In ehd2 mutants, the transcription levels of Ehd1, Hd3a, and RFT1 are significantly down regulated under both long and short-day conditions, suggesting that Ehd2 influences heading primarily by promoting the transcriptional activities of Ehd1, Hd3a, and RFT1 [16]. RID1 can directly bind to the promoters of Hd3a and RFT1, activating their expression and maintaining the chromatin accessibility at their transcription start sites through H3K4me3, H3K9ac, and H3K36me3 deposition, thereby promoting flowering [17].
The Ehd3 gene encodes a transcription factor with two PHD-type zinc fingers. Under LD conditions, ehd3 mutants exhibit delayed heading compared to the wild type. In ehd3 mutants, Ghd7 transcription is activated, suppressing the expression of Ehd1, Hd3a, and RFT1, indicating that Ehd3 acts as a promoter of Ehd1 in the rice heading regulatory network [16]. Ehd4 encodes a new CCH-type zinc finger protein and acts as a positive regulator of Ehd1. Ehd4 loss-of-function mutants (ehd4) do not head under LD conditions. The expression pattern of Ehd4 in rice is similar to that of Ehd1, and it regulates the transcription of Hd3a and RFT1 through Ehd1 [18].
OsCOL4 (CONSTANS-like) loss-of-function mutants (oscol4) flower early under both LD and SD conditions, whereas overexpression of OsCOL4 results in late flowering under both conditions. In oscol4 mutants, the transcriptional activities of Ehd1, Hd3a, and RFT1 are increased, while overexpression of OsCOL4 reduces their transcription, indicating that OsCOL4 acts upstream of Ehd1 as a heading repressor [34].
OsMADS51 is a SD heading promoter. OsMADS51 loss-of-function mutants flower 15 days later than wild-type under SD conditions, with minimal impact under LD conditions. In these mutants, the expression levels of Ehd1, OsMADS14, and Hd3a are significantly reduced. Overexpression of OsMADS51 leads to earlier heading under short-day conditions and upregulation of Ehd1, OsMADS14, and Hd3a. These results suggest that OsMADS51 is a SD heading promoter, acting upstream of Ehd1, OsMADS14, and Hd3a. Furthermore, OsMADS51 expression is not affected in Ehd1 RNAi lines, confirming that OsMADS51 acts upstream of Ehd1 [52]. Co-expression of OsMADS51 with OsFLZ2 destabilizes OsMADS51, weakening its transcriptional activation of downstream target genes like Ehd1 [53].
Ehd5, encoding a WD40 domain-containing protein, is light-inducible and exhibits a circadian rhythm in its expression pattern. Transcriptome analysis has identified Ehd5 as an upstream regulator of flowering genes Ehd1, RFT1, and Hd3a [54]. OsCIBL1 interacts with OsCRY2, a member of the rice CRY family (OsCRY1a, OsCRY1b, and OsCRY2), and binds to the Ehd1 promoter, thereby activating the rice-specific Ehd1-Hd3a/RFT1 pathway for flowering induction [55]. OsWRKY11 facilitates the formation of a ternary protein complex involving OsWRKY11, Hd1, and DTH8; this complex subsequently suppresses Ehd1 expression, leading to a delayed heading date [56].

2.3. Ghd7 and Regulatory Genes

Ghd7 is associated with traits such as grain number per panicle, plant height, and heading date in rice. It encodes a nuclear protein with a CCT domain. Under long-day conditions, overexpression of Ghd7 results in significantly delayed heading, increased plant height, and larger panicle size compared to wild-type plants [19]. Ghd7 is induced by phytochromes and suppresses the transcription of Ehd1. The interaction between the heading promoter Ehd1 and the repressor Ghd7 regulates the transcriptional activity of Hd3a, thereby affecting heading [57].
Overexpression of OsMFT1 delays heading by approximately seven days compared to the wild type, and significantly increases the number of spikelets per panicle and branches. In contrast, OsMFT1 knockout mutants show earlier heading and reduced spikelet numbers. Overexpression of OsMFT1 significantly suppresses Ehd1 transcription while activating Ghd7 expression. Additionally, the transcription factor OsLFL1 directly binds to the RY element in the OsMFT1 promoter, activating its transcription. This indicates that OsMFT1 is a heading repressor, acting downstream of Ghd7 and upstream of Ehd1, primarily regulating rice heading at the transcriptional level [31].
Variations in the alleles of Hd1, Ghd7, and DTH8 lead to differences in photoperiod sensitivity among rice populations. Studies indicate that rice photoperiod-sensitive flowering is controlled by the Hd1-Hd3a/RFT1 module under SD conditions and the (Hd1/Ghd7/DTH8)-Ehd1-Hd3a/RFT1 module under LD conditions. These genetic differences provide the basis for rice’s wide environmental adaptability. The Ghd8-OsHAP5C-Ghd7 triple complex directly binds to the Hd3a promoter, downregulating the expression of Ehd1, Hd3a, and RFT1, ultimately leading to delayed heading [21]. OsCOL5, an ortholog of Arabidopsis COL5, is involved in photoperiodic flowering and enhances rice yield through modulation of Ghd7 and Ehd2 and interactions with OsELF3-1 and OsELF3-2 [58]. OsCOL10 encodes a member of the CONSTANS-like (COL) family, which represses the expression of the FT-like genes RFT1 and Hd3a through Ehd1. Transcripts of OsCOL10 are more abundant in plants carrying a functional Ghd7 allele or overexpressing Ghd7 than in Ghd7-deficient plants, thus placing OsCOL10 downstream of Ghd7 [59].

3. Gene Interaction Regulates Rice Heading Together

Gene interactions during the heading stage of rice have elucidated synergistic effects and signaling mechanisms among multiple genes involved in the regulation of rice flowering. These investigations advance our understanding of the complex regulatory networks that govern rice growth and development, while also laying the groundwork for theoretical advancements in breeding new varieties with enhanced agronomic traits [20,60]. The photosensitivity of rice at the heading stage involves several key genes, including Hd1, Ghd7, and DTH8. Irrespective of day length, the single knockout of Hd1 (Ghd7 and DTH8) promotes heading, whereas single Ghd7 inhibits it. Under LD conditions, Hd1 enhances Ghd7 expression and forms distinct inhibitory complexes with Ghd7 and DTH8, thereby partially suppressing (double knockout) or completely silencing (triple knockout) the Ehd1-Hd3a/RFT1 flowering pathway, resulting in varying degrees of delayed or absent heading. Conversely, under SD conditions, Ghd7 expression is significantly reduced, leading to a competitive relationship between Hd1 and the inhibitory complex. This promotes Hd3a/RFT1 expression to varying degrees, thereby influencing heading. Thus, photoperiodic flowering in rice is governed by two modules: HD1-HD3A/RFT1 under SD conditions and (Hd1/Ghd7/DTH8)-Ehd1-Hd3a/RFT1 under LD conditions. Variations in these genes provide the foundation for broad adaptability in rice [3]. The genetic interaction of four major genes Ghd7, Ghd8, OsPRR37/Ghd7.1 and Hd1 in the rice heading stage was analyzed. The four genes had four-gene, three-gene, and gene interactions in both conditions, but were more significant in NLD (natural long-day) conditions. In the context of functional Hd1, Ghd7 had the strongest gene interaction with Ghd8 under NLD conditions, while Ghd7 had the strongest gene interaction with PRR37 under NSD (natural short-day) conditions. Interestingly, PRR37 acts as a flowering suppressor under NLD conditions, while under NSD conditions, it can alternately act as an activator or suppressor depending on the state of the other three genes [61]. OsCOL5, a homologue of Arabidopsis COL5, is involved in photoperiodic flowering and increases rice yield by regulating Ghd7 and Ehd2 and interacting with OsELF3-1 and OsELF3-2 [58]. OsCOL13 negatively regulates the flowering of rice under both long- and short-day conditions and inhibits the floral genes Hd3a and RFT1 by inhibiting Ehd1 [62].
Histone haploidin-1 (OsHUB1) and OsHUB2 are involved in the regulation of heading date through Hd1 and Ehd1 pathways. In both LD and SD conditions, the loss of OsHUB1 and OsHUB2 function resulted in early heading dates. The expression of Hd3a, RFT1, and Ehd1 was induced under LD conditions, and the transcription levels of Hd1, Ghd7, OsCCA1, OsGI, OsFKF1, and OsTOC1 were decreased, while the expression of RFT1 and Ehd1 was induced by the oshub2 mutant under SD conditions [63]. OsFTL12 is an important factor in the regulation of rice heading, and it has antagonistic effects on Hd3a and RFT1. Unlike Hd3a and RFT1, OsFTL12 is not regulated by day length and is highly expressed under both SD and LD conditions, and the heading date is delayed under both SD and LD conditions. OsFTL12 interacts with GF14b and OsFD1, two key components of the anthocyanogen activation complex (FAC), and forms the anthocyanogen inhibition complex (FRC) by competitively binding to GF14b with Hd3a. In addition, OsFTL12-FRC can bind the promoters of the floral identity genes OsMADS14 and OsMADS15 and inhibit the expression of both [64]. OsFLZ2 is a negative regulator at heading stage of rice. It interacts with OsMADS51 and disrupts the stability of OsMADS51, weakening its transcriptive activation of downstream target gene Ehd1 [53]. Therefore, by identifying and utilizing the gene interaction at heading stage, the flowering time and growth period of rice can be accurately regulated, and the yield stability and adaptability can be improved to meet the growing global food demand.

4. Pleiotropy of Rice Heading Date Genes

Recently, with the advancing research on the functional mechanisms of rice heading date genes, a series of pleiotropic genes have been discovered. These genes exhibit a phenomenon known as one gene, multiple effects, where a single gene or gene pair on the chromosome influences multiple phenotypic traits. For example, Ehd1 functions as a pivotal integrative gene in the regulatory network controlling rice heading, with its expression levels negatively correlated with heading date and yield [65]. Using CRISPR-Cas9 technology, the Ehd1 gene was edited in the elite Northeast japonica rice varieties Jiyuanxiang 1 and Yinongxiang 12. Field trials showed that these new ehd1 mutants not only outperformed the wild type in yield under low latitude conditions, but also retained their superior agronomic traits [66]. Both the Ehd1 and the Hd1 genes reduce the number of primary branches in the panicle, resulting in a decreased grain number. These important flowering genes likely regulate rice panicle development by affecting the expression of florigen genes in the leaves, thereby influencing crop yield in the field [67]. DTH7/Ghd7.1/OsPRR37/Hd2 represents a major genetic locus controlling rice photoperiod sensitivity and grain yield, encoding a pseudo-response regulator protein whose expression is regulated by photoperiod [23,68]. DTH8/Ghd8/LHD1, encoding the HAP3H subunit of the transcription factor CCAAT-box binding protein, has been shown to concurrently regulate rice yield, plant height, and heading date [61,69]. Overexpression of DHD1 delays rice heading and enhances agronomic traits such as panicle length, tiller number, and grain number, thereby increasing yield [70]. Ghd7 and PRR37 promote the spikelet number and yield, with a synergistic effect observed in Ghd7–DTH8 or Ghd7–PRR37 combinations, although Hd1 negatively impacts yield [71]. OsMFT1 acts as a flowering inhibitor, operating downstream of Ghd7 and upstream of Ehd1, while also positively regulating rice panicle morphology [31].
The efficiency of nitrogen utilization in plants is primarily regulated by genetic factors, environmental influences, and their interactions. The ARE1 gene serves as a key regulator of nitrogen nutrition and yield. Studies have revealed that Ghd7 binds to the ARE1 gene and suppresses its expression, thereby positively regulating nitrogen utilization and yield in rice. It is noteworthy that the Ghd7 and ARE1 haplotypes are closely associated with soil nitrogen content and exhibit differential distribution patterns among rice subpopulations, making them selected loci in rice breeding processes. Furthermore, the combination of superior alleles from both genes enhances nitrogen use efficiency and yield under low nitrogen conditions, offering genetic markers for breeding nitrogen-efficient materials [72].
Ghd7 regulates the balance between abscisic acid (ABA) and gibberellins (GAs), increasing the ABA/GA3 ratio to inhibit seed germination. During seed germination, the mutant ghd7 exhibits reduced sensitivity to exogenous ABA, leading to decreased ABA accumulation in mature ghd7 seeds due to diminished OsNCED gene expression. Additionally, elevated GA3 levels during seed imbibition in ghd7 seeds are attributed to induction of genes involved in biologically active GA synthesis pathways [73]. Overexpression of OsABF1 in plants results in a late-flowering phenotype. Simultaneous RNAi knockdown of OsABF1 and its most homologous gene, OsbZIP40, causes a significant early-flowering phenotype. Moreover, overexpression of OsABF1 leads to a typical gibberellin-deficient phenotype, semi-dwarfism, and delayed seed germination [74,75,76]. During rice heading, the gene OsSOC1/OsMADS50/DTH3 regulates the number of adventitious roots in rice. OsMADS50 acts as a target gene of OsSPL3 or OsSPL12, which are targets of Osmir156. Thus, the “miR156-OsSPL3/OsSPL12-OsMADS50” module constitutes a regulatory pathway involved in rice adventitious root formation through modulation of auxin transport and signaling [77].

5. Prospects

Research on rice flowering regulation has significantly expanded our understanding of the molecular mechanisms of flowering induction and regulation. As new genes are discovered and the mechanisms of gene interactions are further understood, the molecular regulatory network is becoming increasingly complex. The molecular network for flowering regulation involves hormone pathways, autonomous pathways, and temperature pathways, which interact with the photoperiod pathway to precisely control flowering time, highlighting the complexity of flowering mechanisms.
Despite significant progress in the Hd1 and Ehd1 regulatory pathways, with numerous related genes cloned, the interaction mechanisms among these genes and their responses to environmental signals, as well as the transcriptional and post-transcriptional regulation of Hd1 and Ehd1, remain unclear. The role of histone methylation proteins in the epigenetic regulation of flowering time, such as SDG708, SDG724, SDG725, OsTrx1, and OsVIL2, also requires further investigation. With advancements in genome sequencing, transcriptome analysis, CRISPR gene editing, and large-scale screening of interacting proteins, new flowering genes and genetic regulatory networks will continue to be discovered. This research will provide valuable insights into the ecological and environmental survival strategies of different species.
The study of rice flowering regulation mechanisms has broad applications beyond basic research. Research on pivotal flowering genes such as Hd3a, DTH8, and Ghd7 has illustrated heterosis, with different allele combinations outperforming parental lines in traits like grain number per panicle, seed setting rate, and grain yield. These discoveries are widely applied in hybrid rice breeding. Selecting optimal allele combinations of flowering genes for specific regions from low to high latitudes will provide breeders with effective choices for developing eco-type varieties and lay the foundation for future molecular design breeding.

6. Conclusions

In summary, the regulation of rice heading dates through photoperiodic genes involves a complex network of interactions that govern the timing of flowering. The identification and functional analysis of key genes such as Hd1, Ehd1, Ghd7, and their associated pathways have provided significant insights into the molecular mechanisms that control this crucial developmental stage in rice. The interplay between these genes and their responses to environmental signals, such as day length, highlights the intricate balance required for optimal flowering and, consequently, rice yield.
While much progress has been made, our understanding of the photoperiodic regulation of heading date is still incomplete. Many of the regulatory interactions remain to be fully elucidated, particularly in the context of varying environmental conditions and different rice cultivars. Further research is needed to explore these aspects, which will not only advance our fundamental knowledge of plant biology but also have practical implications for breeding programs aimed at improving rice’s adaptability and productivity under diverse agricultural conditions.
This review consolidates current knowledge on the photoperiodic control of rice heading date and points to future directions for research, emphasizing the need for a more comprehensive understanding of gene interactions and the potential for genetic manipulation to optimize rice cultivation.

Author Contributions

Conceptualization, J.S.and L.T.; data collection, L.T. and J.S.; writing—original draft preparation, J.S.; writing—review and editing, L.T.; data analysis, X.Z., Y.C., H.F. and J.W. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by Zhejiang Provincial Natural Science Foundation of China under Grant No. LQ20C130007 and LQ22C130007, National Key R&D Program of China under Grant No. 2023YFD1200904, National Natural Science Foundation of China under Grant No. 32101791.

Conflicts of Interest

The authors declare no conflicts of interest.

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Cimb 46 00613 g001
Figure 1. Photoperiodic regulatory pathway of rice flowering. (a) Under short-day conditions, OsGI activates Hd1 and Ehd1, which promote the expression of the florigen gene Hd3a, triggering the transition from the vegetative to the reproductive phase. Various genes, such as Ghd8, OsCOL4, and MADS51, regulate Ehd1 and Hd1, either enhancing or repressing their effects. (b) Under long-day conditions, OsGI activates Hd1, which represses Hd3a, while Ehd1 activates Hd3a/RFT1 to promote flowering. Other genes, including Ghd7, DTH7, and OsTrx1, modulate this pathway by controlling Hd1 and Ehd1 activity.
Figure 1. Photoperiodic regulatory pathway of rice flowering. (a) Under short-day conditions, OsGI activates Hd1 and Ehd1, which promote the expression of the florigen gene Hd3a, triggering the transition from the vegetative to the reproductive phase. Various genes, such as Ghd8, OsCOL4, and MADS51, regulate Ehd1 and Hd1, either enhancing or repressing their effects. (b) Under long-day conditions, OsGI activates Hd1, which represses Hd3a, while Ehd1 activates Hd3a/RFT1 to promote flowering. Other genes, including Ghd7, DTH7, and OsTrx1, modulate this pathway by controlling Hd1 and Ehd1 activity.
Cimb 46 00613 g001
Table 1. Key genes involved in the photoperiodic regulation of flowering in rice.
Table 1. Key genes involved in the photoperiodic regulation of flowering in rice.
GeneGene IDPrimary FunctionReferences
Hd3a/FTL2LOC_Os06g06320Promotes flowering; acts as a florigen gene under SD (short-day) conditions.[9,10]
RFT1/FTL3LOC_Os06g06300Promotes flowering; acts as a florigen gene under LD (long-day) constitutive flowering repressor conditions.[11]
OsGILOC_Os01g08700Circadian rhythm gene; activator of Hd1; promotes flowering under SD and inhibits under LD.[4,12]
Hd1LOC_Os06g16370Encodes a zinc finger protein with 395 amino acids; promotes flowering under SD and inhibits under LD; a key integrator in the OsGI-Hd1-Hd3a pathway.[13,14]
Ehd1LOC_Os10g32600Early heading quantitative trait locus (QTL) derived from African cultivated rice (Oryza glaberrima Steud.); promotes heading under SD conditions independently of Hd1.[2,15]
Ehd2/RID1/OsId1/Ghd10LOC_Os10g28330Encodes a zinc finger transcription factor; promotes heading and initiates flowering induction.[16,17]
Ehd3LOC_Os08g01420Promotes flowering; encodes a PHD-type zinc finger protein; induces heading by suppressing Ghd7 or upregulating Ehd1 under LD.[16]
Ehd4LOC_Os03g02160Promotes flowering; encodes a CCH-type zinc finger protein; upregulates florigen genes via Ehd1, without direct binding to the Ehd1 promoter region.[18]
Ghd7/Hd4/E1LOC_Os07g15770A major QTL controlling panicle number per plant, plant height, and heading date.[19,20]
DTH8/Ghd8/LHD1/OsHAP3H/EF8/OsNF-YB11/CAR/LH2LOC_Os08g07740Encodes a polypeptide with 297 amino acids; delays flowering under LD by regulating Ehd1, RFT1, and Hd3a; promotes flowering under SD.[13,21]
DTH7/Ghd7.1/OsPRR37/Hd2LOC_Os07g49460Major locus controlling photoperiod sensitivity and grain yield; encodes a pseudo-response regulator protein regulated by photoperiod.[22,23]
OsCO3LOC_Os09g06464Flowering inhibitor; regulates flowering time mainly under SD, independent of the SD florigen pathway.[5,24]
OsPhyALOC_Os03g51030Affects heading date by regulating OsGI under SD and Ghd7 under LD.[25]
OsPhyBLOC_Os03g19590Regulates Hd1-mediated expression of florigen Hd3a and critical day length.[26,27]
OsELF3/Hd17/Ef7LOC_Os01g38530Circadian gene; promotes flowering under LD.[14,28]
Hd6/CK2αLOC_Os03g55389Delays flowering under LD by inhibiting the expression of FT-like genes.[29]
OsLFL1LOC_Os01g51610Encodes a transcription factor with a B3 domain; regulates heading date by directly binding to the OsMFT1 promoter through the RY motif.[30,31]
HAF1LOC_Os04g55510E3 ubiquitin ligase with a C3H4 ring domain; regulates heading date through interaction with Hd1.[32]
OsCOL4LOC_Os02g39710Constitutive flowering repressor in rice; acts upstream of Ehd1 and downstream of OsphyB.[33,34]
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Song, J.; Tang, L.; Cui, Y.; Fan, H.; Zhen, X.; Wang, J. Research Progress on Photoperiod Gene Regulation of Heading Date in Rice. Curr. Issues Mol. Biol. 2024, 46, 10299-10311. https://doi.org/10.3390/cimb46090613

AMA Style

Song J, Tang L, Cui Y, Fan H, Zhen X, Wang J. Research Progress on Photoperiod Gene Regulation of Heading Date in Rice. Current Issues in Molecular Biology. 2024; 46(9):10299-10311. https://doi.org/10.3390/cimb46090613

Chicago/Turabian Style

Song, Jian, Liqun Tang, Yongtao Cui, Honghuan Fan, Xueqiang Zhen, and Jianjun Wang. 2024. "Research Progress on Photoperiod Gene Regulation of Heading Date in Rice" Current Issues in Molecular Biology 46, no. 9: 10299-10311. https://doi.org/10.3390/cimb46090613

APA Style

Song, J., Tang, L., Cui, Y., Fan, H., Zhen, X., & Wang, J. (2024). Research Progress on Photoperiod Gene Regulation of Heading Date in Rice. Current Issues in Molecular Biology, 46(9), 10299-10311. https://doi.org/10.3390/cimb46090613

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