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. 2022 Oct 6;42(10):63. doi: 10.1007/s11032-022-01334-4

Transcription factor bZIP65 delays flowering via suppressing Ehd1 expression in rice

Tingting Pan 1, Mingliang He 2,3, Hualong Liu 4, Xiaojie Tian 2, Zhenyu Wang 2, Xinglong Yu 5, Xingfen Miao 1,✉, Xiufeng Li 2,✉
PMCID: PMC10248685  PMID: 37313010

Abstract

Flowering time is one of the most fundamental factors that determine the distribution and final yield of rice. Ehd1 (Early heading date 1) is a B-type response regulator which functions as a flowering time activator. Although diverse flowering time genes have been reported as regulatory factors of Ehd1 expression, the potential regulators of Ehd1 largely remain to be identified. Here, we identified a basic leucine zipper transcription factor bZIP65, a homolog of bZIP71, as a new negative regulator of Ehd1. The overexpression of bZIP65 delays flowering, while bzip65 mutants have similar flowering time to SJ2 (Songjing2) in both long-day and short-day conditions. Biochemically, bZIP65 associates with Ehd1 promoter and transcriptionally represses the expression of Ehd1. Moreover, we found that bZIP65 enhances H3K27me3 level of Ehd1. Taken together, we cloned a new gene, bZIP65, regulating rice heading date, and uncovered the mechanism of bZIP65 delaying flowering time, where bZIP65 increases the H3K27me3 level of Ehd1 and transcriptionally represses the expression of Ehd1, similar to its homolog bZIP71.

Supplementary Information

The online version contains supplementary material available at 10.1007/s11032-022-01334-4.

Keywords: Rice, Heading date, Ehd1, bZIP65

Flowering time is one of the most fundamental factors that determine the regional distribution and seasonal adaptability of rice. Currently, two conserved flowering pathways have been found in rice, an evolutionarily conserved OsGI-Hd1-Hd3a pathway and a specific Ehd1-Hd3a pathway (Hori et al. 2016). HEADING DATE1 (Hd1) plays a dual role in regulating flowering time. By regulating the expression of Hd3a and RFT1, Hd1 represses flowering in long-day (LD) conditions and promotes flowering in short-day (SD) conditions (Yano et al. 2000; Hayama et al. 2003; Zhang et al. 2017). Heading date 3a (Hd3a) and RICE FLOWERING LOCUS T1 (RFT1), as florigens in rice, are expressed in the phloem of leaves and transported to the shoot apical meristem to promote flowering (Song et al. 2017). Knockdown of Hd3a or RFT1 in the japonica rice cultivar Norin 8 delays flowering only under SD or LD conditions, respectively, indicating that Hd3a and RFT1 might be specific florigens in rice under SD and LD conditions, respectively (Komiya et al. 2009). Recently, several studies using a set of isogenic lines showed that the dual role of Hd1 is dependent on the allelic variations of its interaction partners, grain number, plant height and heading date 7 (Ghd7), Ghd8, and Ghd7.1 (Zhang et al. 2019; Zong et al. 2021). Genotyping for Hd1 variation in major cultivated rice varieties offers a new strategy for utilizing these preponderant alleles to improve yield and quality of japonica varieties (Leng et al. 2020).

Early heading date 1 (Ehd1) is a B-type response regulator that induces floral initiation by promoting the expression of the florigen genes Hd3a and RFT1 in both LD and SD conditions (Doi et al. 2004). Ehd1, as a central signal integrator of floral transition, is regulated by multiple upstream regulators, such as suppressors (e.g., Hd2/OsPRR37/Ghd7.1, Ghd7/Hd4, Ghd8/DTH8/Hd5, OsCOL4) and activators (e.g., OsMADS50/OsSOC1/DTH3, OsMADS56/GL10, Ehd2/RID1, Ehd4, Hd17/OsELF3) (Matsubara et al. 2008, 2012; Xue et al. 2008; RYU et al. 2009; Lee et al. 2010; Wei et al. 2010; Gao et al. 2013, 2014; Hori et al. 2016). Notably, although many upstream regulators of Ehd1 have been identified, their associations or detailed regulatory mechanisms are largely unknown.

Heading date was found to be subjected to epigenetic regulation. At least 35 genes have been identified to participate in regulating rice heading date by histone modification. For example, SET domain group protein 701 (SDG701) can increase the expression of Hd3a and RFT1 by enhancing H3K4me3 level of their promoters (Liu et al. 2017). Other SDGs involved in heading date regulation include SDG708, SDG723, SDG724, SDG711, and SDG728 (Qin et al. 2010; Sun et al. 2012; Choi et al. 2014; Liu et al. 2014, 2016, 2017; Jiang et al. 2018). Trithorax-like protein 1 (OsTrx1), a homolog of SDG704, can physically interact with transcription factor (TF) interaction protein 1 (SIP1) to activate Ehd1 transcription by altering its H3K4me3 levels, which eventually promotes rice flowering (Choi et al. 2014). Rice WD40-repeat protein 5a (OsWDR5a) can interact with SDG723 to form the core components of the COMPASS-like complex to accelerate flowering via Ehd1-H3K4me3 pathway (Jiang et al. 2018). SDG711 is a component of polycomb-repressive complex 2 (PRC2) complex, which was shown to directly target the Ehd1 locus to mediate H3K27me3 and gene repression, thereby delaying rice flowering (Liu et al. 2014).

Basic leucine zipper (bZIP) family transcription factors, containing a basic region for DNA binding and a leucine zipper for protein–protein interactions, are extensively involved in various biological processes (Nijhawan et al. 2008). There are 89 bZIP members in the rice genome, some of which have been characterized and determined to function in the regulation of rice flowering. For example, OsFD1 interacts with RFT1-14–3-3 complex to form florigen activation complex (FAC) and then activates the transcription of OsMADS15, leading to floral induction (Peng et al. 2021). However, Hd3a BINDING REPRESSOR FACTOR 1 (HBF1) and HBF2 form repressor complexes with Hd3a-14–3-3 and reduce Hd3a and RFT1 expression to delay flowering (Brambilla et al. 2017). OsbZIP40 functions redundantly with ABA-responsive element binding factor 1 (OsABF1) to delay floral transition upon water deficit. Molecular and genetic analyses demonstrated that a drought regime enhances the expression of OsABF1 and its direct target gene OsWRKY104 and then indirectly suppresses the expression of Ehd1 to delay flowering (Zhang et al. 2016). Recently, OsRE1 was reported to interact with OsRIP1, regulating rice heading date by repressing Ehd1 expression (Chai et al. 2021).

Previously, we reported that bZIP71 can recruit PRC2 to the Ehd1 locus to induce its H3K27me3 modification to delay rice flowering (Li et al. 2022). The 89 bZIP TF-encoding genes in rice have been phylogenetically categorized into 10 distinct clades, in which bZIP71 belongs to clade H (Nijhawan et al. 2008). Within this clade, bZIP65 is the closest homolog of bZIP71, showing 98% sequence similarity (Supplemental Fig. 1). To dissect the biological functions of bZIP65, we generated the bZIP65 OE in Songjing2 (SJ2) background (Supplemental Fig. 2A). Phenotype analysis showed that bZIP65 OE delays flowering around 15.9 days in LD condition and around 7.5 days in SD condition (Fig. 1A, B). A RT-qPCR analysis showed that the mRNA levels of the florigen genes Hd3a and RFT1 were markedly reduced in the bZIP65 OE plants relative to SJ2 under LD condition (Fig. 1C, D). Simultaneously, we also generated bzip65 single mutant in SJ2 background (Supplemental Fig. 2B) and found bzip65 mutants have similar flowering time to SJ2 in both LD and SD conditions (Supplemental Fig. 3). Subsequently, we detected expression patterns of bZIP65 and bZIP71 in different organs, and the results showed that the expression level of bZIP65 was lower than that of bZIP71 in various organs except the root, suggesting that the bzip65 mutant might have a small effect (Supplemental Fig. 4A). These results suggest that the overexpression of bZIP65 delays flowering.

Fig. 1.

Fig. 1

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bZIP65 are flowering repressors. A Representative image of bZIP65 OE (SJ2) plants and SJ2 grown in LD conditions at heading stage. B Flowering time of bZIP65 OE (SJ2) plants and SJ2 under LD and SD conditions. Data are means ± standard error (SE) (n = 20). P values were calculated by Student’s t test compared to SJ2; ** is P < 0.01. C and D Rhythmic expression patterns of Hd3a (C) and RFT1 (D) in bZIP65 OE plants and SJ2 under LD conditions. Black and white boxes denote dark and light periods, respectively. Rice UBIQUITIN gene was used as the internal control. Data are means ± SE (n = 3). ZT, zeitgeber time. E Yeast one-hybrid assay showing that bZIP65 binds to the Ehd1 promoter. Left, diagrams of bait constructs comprising full length of bZIP65 fused with pGADT7 vector. Right, plate auxotroph assays showing transcriptional activation activity of each construct. AbA, 100 mM Aureobasidin A. F EMSA assay showing that bZIP65 binds to the A-box containing region of the Ehd1 promoter. An A-box mutated to CCCCCC was used as mutant probe. Unlabeled probe was used as competitive probes. GST was used as a negative control. G Schematic diagram of various constructs used in transient expression assay. 35Spro:bZIP65, 35Spro:REN-Ehd1pro: LUC were used as effector and reporter, respectively. 35Spro:GFP was used as control. H Relative LUC activity expressed with reporters and effectors. Expression level of Renilla (REN) was used as an internal control. The LUC/REN ratio represents the relative activity of the Ehd1 promoter. Data was shown as means ± SE (n = 5). P values were calculated by Student’s t test; ** is P < 0.01. I and J ChIP assays showing that bZIP65 significantly enhances the H3K27me3 in Ehd1 promoter. Immunoprecipitation was performed with anti-H3K27me3 antibody in diverse lines. Immunoprecipitated chromatin was analyzed by qPCR using primers indicated in I. qPCR enrichment was calculated by normalizing to ACTIN of each sample. Data was shown as means ± SE (n = 3). P values were calculated by Student’s t test compared to SJ2; ** is P < 0.01. K Proposed working model for the role of bZIP65 in regulating rice heading date. bZIP65 can enhance the H3K27me3 level of Ehd1 and transcriptionally represses its expression and then delay the flowering of rice

As bZIP71 delays flowering via directly suppressing the expression of Ehd1, we asked whether bZIP65 functions in the same mechanism. To this end, Y1H was performed. Results showed that bZIP65 binds Ehd1 promoter in yeast system (Fig. 1E). Gel shift assay demonstrated that GST-bZIP65 can bind the Ehd1 promoter in an A-box-dependent manner (Fig. 1F). In addition, we performed transient expression assay in rice protoplasts and found that 35SPro:bZIP65 efficiently suppresses Ehd1 promoter-driven LUC activity (Fig. 1G, H). Moreover, we tested whether bZIP65 can recruit the PRC2 complex to Ehd1 loci to mediate H3K27me3 of Ehd1. The ChIP assay showed that the accumulation of H3K27me3 in Ehd1 promoter is significantly increased in bZIP65-OE, while it has no changes in bzip65 mutant (Fig. 1I, J). Collectively, these results suggest that bZIP65 delays flowering via a similar mechanism to bZIP71 (Fig. 1K).

Given that bZIP71 and Ehd1 show opposite expression patterns, we asked whether the diurnal expression patterns between bZIP65 and Ehd1 are also similar to that between bZIP71 and Ehd1 under LD and SD conditions. The results showed that bZIP65 expression is the lowest in the early morning. It gradually increases to the peak along with the sunshine and then decreases after sunset under LD condition. The peak moved back to the evening under SD condition (Supplemental Fig. 4B, C). We also examined the diurnal expression pattern of Ehd1 under LD and SD conditions, revealing that its expression peaked in the morning and was at its lowest in the light (Supplemental Fig. 4B, C). The opposite expression patterns of bZIP65 and Ehd1 suggest that bZIP65 may repress the expression of Ehd1.

In summary, we found a new gene bZIP65 that regulates heading date in rice. bZIP65 inhibited Ehd1 expression by increasing H3K27me3 level of Ehd1 and thus inhibited rice flowering. In the future, double mutant of bZIP71 and bZIP65 will be generated to detect the existence of functional redundancy between them. More bZIP family members involved in the regulation of rice flowering will be explored. The analysis of mechanisms of bZIP TFs regulating rice flowering will improve the gene regulatory network of rice heading date.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 408 KB) (408KB, docx)

Acknowledgements

We thank Dr. Yaoguang Liu for providing the vector pYLCRISPR/Cas9Pubi-H.

Abbreviations

SD

short-day

LD

long-day

Hd1

Heading date1

Ehd1

Early heading date1

Hd3a

Heading date 3a

RFT1

RICE FLOWERING LOCUS T1

Hd2

Heading date 2

Hd4

Heading date 4

Hd5

Heading date 5

COL4

CONSTANS-like 4

DTH3

Days to Heading 3

Ehd2

Early heading date 2

Ehd4

Early heading date 4

Hd17

Heading date 17

SDG

SET domain group protein

OsTrx1

Trithorax-like protein

PRC2

Polycomb-Repressive Complex 2

DHD4

delayed heading date 4

bZIP

basic leucine zipper

FAC

florigen activation complex

HBF1

Hd3a BINDING REPRESSOR FACTOR 1

OsABF1

ABA-responsive element binding factor 1

LUC

Firefly luciferase

REN

Renilla luciferase

Author contribution

XFL and XFM designed and supervised the research. TTP, MLH, and HLL performed the experiments. XJT, ZYW, and XLY analyzed the data. TTP and XFL wrote the paper. The author(s) read and approved the final manuscript.

Funding

This study was supported by the Youth Innovation Promotion Association CAS (Grant No. 2022231), the National Natural Science Foundation of China (Grant No. 31801327), and the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDA28100301).

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

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

Xingfen Miao, Email: byndmxf@126.com.

Xiufeng Li, Email: lixiufeng@iga.ac.cn.

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Associated Data

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Supplementary Materials

Supplementary file1 (DOCX 408 KB) (408KB, docx)

Data Availability Statement

All data generated or analyzed during this study are included in this published article and its supplementary information files.

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