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. 2025 Mar 24;18:21. doi: 10.1186/s12284-025-00773-9

Allelic Variation of Hd17 for Rice Heading Date is Caused by Natural Selection

Zifeng Yang 1,2,#, Yun Li 1,3,#, Jin Liu 3, Shuiqing Wu 3, Xuelin Wang 3, Min Guan 3, Yanyun Li 3, Haitao Zhu 1, Guifu Liu 1, Shaokui Wang 1, Guiquan Zhang 1,✉
PMCID: PMC11933555  PMID: 40126692

Abstract

Heading date is an important agronomic trait of rice, which directly determines adaptability and yield. Selection for natural variated alleles for heading date genes is an important manifestation of rice domestication that allows rice to spread to more broad geographic areas. In this study, three alleles of the Hd17 gene for heading date were identified by sequence analysis of 14 single-segment substitution lines, 6 wild rice species, and 2524 accessions of O. sativa. The Hd17-1 allele is an ancestral type with a middle heading date. The Hd17-2 allele was caused by the functional nucleotide polymorphism (FNP) of C to T at position 1016 of the gene and exhibits delay heading. The Hd17-3 allele was caused by the FNP of C to T in 1673 point of the gene and shows earlier heading. The Hd17-1 allele is mainly distributed in tropical regions, carrying by 5 wild rice species, O. glaberrima, and two O. sativa (Aus/Boro and tropical japonica types). The Hd17-2 allele is mainly distributed in subtropical regions, carrying by O. meridionalis, O. rufipogon, and two O. sativa (indica subspecies and Basmati/Sandri types). The Hd17-3 allele is mainly distributed in temperate regions, carrying only by temperate japonica of O. sativa. Hd17-2 and Hd17-3 had been evolved from Hd17-1, independently. Three different rice growing regions formed three alleles of Hd17, showing that the allelic variation of Hd17 is the result of natural selection. We also found that Hd17 controls heading date by up-regulating Ghd7 and down-regulating Ehd1 under long day conditions. Our findings will help to understand the evolution and the regulation of Hd17 in rice.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12284-025-00773-9.

Keywords: Natural variation, Natural selection, Hd17, Heading date, Rice

Background

Rice is one of the most important crops in the world, and heading date is a critical agronomic trait, which directly determines the adaptation to specific cropping locations and growing seasons, and thus playing key role for producing and expanding of rice varieties (Izawa 2007; Jung and Muller 2009). What’s more, the restructuring of heading date is effective for avoiding the hostile environment, such as drought, flood and extreme low or high temperatures (Takeno 2016). Heading date is a complex conversion from the vegetative period to the reproductive period, which is controlled by a complicated network consisted of numerous genes (Wei et al. 2020).

Photoperiodic flowering, among the most important biological systems regulating floral transition (Wang et al. 2021), is regulated by the involvement of light perception and the circadian clock (Imaizumi and Kay 2006). In Arabidopsis thaliana, EARLY FLOWERING3 (ELF3) plays key roles in controlling circadian rhythm and photoperiodic flowering (Dixon et al. 2011; Nefissi et al. 2011). Rice has two ELF3 homologs, OsELF3.1 (LOC_Os06g05060) and OsELF3.2 (LOC_Os01g38530) (Murakami et al. 2007), while the former has been revealed to play a more predominant role than the latter (Zhao et al. 2012). OsELF3.1 was identified from mutant line HS276, named as Ef7 (Saito et al. 2012). One another homolog of OsELF3.1 was found by QTL analysis of heading date between the Nipponbare and Koshihikari, and named as Heading date 17 (Hd17) (Matsubara et al. 2008). This Hd17 was associated with a small difference in heading date (< 3 days under natural day conditions) between two Japanese rice (Oryza sativa L.) cultivars, Nipponbare and Koshihikari (Matsubara et al. 2008). Then a near isogenic line (NIL) of Hd17 was built from Koshihikari and the recurrent parent Nipponbare, and the heading date in NIL-Hd17 of Koshihikari was same to Nipponbare under short-day (SD) conditions (10 h light/14 h dark), but flower about 8 days later than Nipponbare under long-day (LD) conditions (14.5 h light/9.5 h dark). They revealed that the difference in heading date result from a single nucleotide polymorphism (SNP) at the fourth exon (SNP4: T/C). All indica cultivars and wild rice species carry the Koshihikari SNP (C), indicating that the wild-type allele has the Koshihikari SNP, and the Nipponbare allele is a variant that the amino acid change (serine to leucine), which led to earlier flowering than NIL-Hd17. They also hold that Hd17 takes part in the pathway of photoperiodic flowering, but probably not through affecting circadian rhythms (Matsubara et al. 2012). Hd17 were demonstrated to function as a flowering promoter under LD conditions through reducing the mRNA level of the floral repressor Ghd7 (Matsubara et al. 2012), and participate in the degradation of OsGI (Zhao et al. 2012; Yang et al. 2013). Recent research put forward the clock component OsLUX regulates rice heading date through recruiting OsELF3.1 and OsELF4s to repress Hd1 and Ghd7 (Xu et al. 2023), which suggests OsELF3.1 (Hd17) maybe related to circadian rhythms.

Single-segment substitution line (SSSL), like NIL, which carry only one substitution segment from donors in the recipient genetic background (Zhang et al. 2004; Zhang 2021). Our lab has built a library of 2360 SSSLs, which were derived from 43 donors of seven species in AA genome rice under the genetic background of Hua-jing-xian 74 (HJX74), an indica elite variety in southern China (Zhang et al. 2004; Zhang 2021). To construct the SSSL, donors have been crossed separately with the recipient HJX74. Then the F1 hybrids were backcrossed to HJX74. Each cross was screened with 300 to 400 polymorphic SSR markers to identify substitution segments and genetic background in one segregating population. After backcrossing 3 to 7 times with marker-assisted selection by SSR markers, plants were selected carrying only single substitution segments from the donor in the recipient genetic background. Finally, homozygous SSSLs were developed by selfing (Zhang et al. 2004; Xi et al. 2006; Zhang 2021). Typically, a SSSL contains just a single gene associated with a particular trait. These SSSLs were widely used to detect QTLs for many complex traits in rice (Zhu et al. 2014, 2018; Yang et al. 2018, 2021; Tan et al. 2020, 2021; Huang et al. 2024), and further to clone and analyze the functions of key genes (Wang et al. 2012; Sui et al. 2019; Zhan et al. 2022). In the present study, we detected that Hd17 has three allelic variants by 14 SSSLs carry Hd17. A new allele of Hd17 with a new FNP, was found and named as Hd17-2. Then, we used the abundant genetic resources, including 6 wild rice species from AA genome group and 2524 cultivated rice accessions, for haplotype analysis to confirm this FNP. Moreover, our results also indicated that the natural variations of Hd17 were caused by natural selection.

Results

Heading Dates Controlling by Hd17

In order to test most natural allelic variants of Hd17, we screened out 14 SSSLs of Hd17 from a library including 2360 SSSLs previously established by our lab (Zhang 2021) (Table S1). Heading dates of these SSSLs, ranging from 94 to 103 days, were investigated and divided into three groups, namely P-1, P-2, and P-3, respectively (Table S2). Significant phenotypic differences could be seen among the three groups of Hd17 in both the first cropping season (FCS) and the secondary cropping season (SCS) (Fig. 1a). The heading date of P-1 is delayed by about 3 days compared to P-2 in FCS, and that of P-3 is 4 days earlier than P-2 under both conditions. (Fig. 1b). These results showed that it was different among the heading dates of 14 SSSLs controlled by Hd17.

Fig. 1.

Fig. 1

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Heading date variations of Hd17. a The phenotypes of P-1, P-2 and P-3, Scale bar: 15 cm. b The average heading date of Hd17 in different SSSL materials in FCS (The first cropping season) and SCS (The secondary cropping season). Letters above the bars represent statistically significant differences calculated using one-way analysis of variance (ANOVA) with the method of Duncan, different letters indicate significance at 0.01 level

Haplotypes of the Hd17 Gene

To further investigate the roles of Hd17 in rice heading date, we made haplotype analysis by sequencing 14 SSSLs. Four haplotypes were identified (Fig. 2). Among these sequences, we discovered 15 single nucleotide polymorphisms (SNPs) and ten of them lead to amino acid substitutions. According to heading date of SSSLs-Hd17, four haplotypes of Hd17 were grouped into three (Fig. 2). Studies have shown that a SNP (SNP4: T/C) variant of Hd17 regulates the heading date in rice (Matsubara et al. 2012). Based on this SNP, we designed a marker Hd17-SNP1 to identify different rices by SNP high-throughput detection KASP platform of LGC company (Fig. S1 and Table S3). The Hd17-SNP1 marker can quickly screen and confirm the mutation site, suggesting that the previously reported SNP (SNP4: T/C) at position 1673 of Hd17 is a FNP associated with changes in heading date..

Fig. 2.

Fig. 2

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SNPS and protein variations between different haplotypes of Hd17. NC means no change. SCS, The secondary cropping season. Heading date in SCS means mean ± SD

Apart from the previously reported SNP (1673: C/T), we found another SNP at position 1016 (C/T), which may be the FNP in Hd17 that is associated with the changes in heading date (Fig. 2). This SNP offer approximately three days change in heading date. We could see there are three combinations from SNP at positions 1016 and 1673, as TC, CC and CT. The TC group showed delay heading, while the CT group exhibited earlier flowering, and CC was the middle type. Taken together, the phenotypic differences of SSSLs-Hd17 may be explained by the two FNPs at position 1016 (C/T) and 1673 (C/T).

To examine the evolutionary origin of the Hd17, we sequenced and analyzed the sequences of Hd17 in 6 wild rice species (including O. rufipogon, O. meridionalis, O. nivara, O. barthii, O. glumipatula and O. longistaminata), thereinto O. meridionalis has four haplotypes, which were all collected from Australia by our lab. Six haplotypes were identified in all wild species (Table 1). There were another 3 SNPs except the 15 SNPs mentioned above. O. rufipogon and O. meridionalis-M1 all belong to H1 haplotype. O. meridionalis of Hd17 from Australia has rich variations, O. meridionalis-M3 and O. meridionalis-M4 have two kinds, H5 and H6, respectively. O. nivara and O. meridionalis-M2 belong to H7 haplotype. O. barthii of Hd17 is an independent haplotype, namely H8, which have 3 SNPs comparing with Hd17 in O. rufipogon and O. meridionalis-M1. O. glumipatula and O. longistaminata were grouped into the same haplotype (H9). All these wild species were classified into 2 groups according to the two FNPs positions 1016 (C/T) and 1673 (C/T). Above results suggested that the sequences of Hd17 in wild rice exhibit more different variations than those of cultivated rice.

Table 1.

Six haplotypes of Hd17 in wild rice species

Species Haplotype 15 24 451 751 1016 1223 1342 1464 1468 1492 1560 1673 1794 1849 1941 2129 2130 2164
O.meridionalis-M1 H1 A C C C T G G G G A C C C C T C A G
O.rufipogon H1 A C C C T G G G G A C C C C T C A G
O.meridionalis-M4 H5 A C C C C G G G G A C C C C T C A G
O.meridionalis-M3 H6 A C C C C G A G G A C C C C T T A G
O.meridionalis-M2 H7 A C C C C T G G G A T C C C T C A G
O.nivara H7 A C C C C T G G G A T C C C T C A G
O.barthii H8 A A C C C G G G G A C C C C T T A G
O.glumaepatula H9 A G G C C G G A G A C C C C C C A G
O.longistaminata H9 A G G C C G G A G A C C C C C C A G
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In order to analyze the haplotype variation of Hd17 accurately, we furthermore investigate the sequence of Hd17 in 2524 cultivated rice accessions from RFGB (https://www.rmbreeding.cn/). Five haplotypes of Hd17 were identified in 2524 cultivated rice accessions (Table 2). The number of accessions in haplotype H1 is the largest, followed by H3. H1 to H4 were consistent with the four haplotypes in 14 SSSLs (Fig. 2). Another haplotype from 206 cultivated rice accessions was same to H5, which from O. meridionalis-M4 (Tables 1 and 2). According to the two FNPs positions 1016 (C/T) and 1673 (C/T), five haplotypes were also grouped into three types. So, we could see that there were more allele variations of Hd17 in cultivated rice, and had low similarity to wild rice.

Table 2.

Five haplotypes of Hd17 in 2524 cultivated rice accessions

Haplotype Number 15 24 451 751 1016 1223 1342 1464 1468 1492 1560 1673 1794 1849 1941 2129 2130 2164
H1 1379 A C C C T G G G G A C C C C T C A G
H2 2 G G C C C G G A T G C C T T C C G G
H3 650 A A C C C G A G G A C C C C T T A A
H4 287 A A C C C G A G G A C T C C T T A A
H5 206 A C C C C G G G G A C C C C T C A G
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Taken together, we surveyed the SNP of Hd17 in 14 SSSLs, 6 wild rice species, and 2524 cultivated rice accessions. There were 18 SNPs variations in these materials, which were grouped into nine haplotypes, H1-H9 (Table 3). Of the nine haplotypes, only H1 undergoes a C to T transition at 1016, which is a late-maturing mutation. H1 is identified as a new allele, named Hd17-2. Only H4 undergoes a C to T transition at 1673, which is an early-maturing mutation, named Hd17-3. This mutation is consistent with the predecessors’ result (Matsubara et al. 2012). The remaining seven haplotypes have C at both 1016 and 1673, representing the original type, named Hd17-1 and numbered Hd17-1-1 to Hd17-1-7. We suggested that 1016 and 1673 were two FNPs, with 1016 being a new FNP discovered in this study. All alleles identified could be classified into three groups [Hd17-1 (P-2), Hd17-2 (P-1), Hd17-3 (P-3)] and nine haplotypes (H1-H9) (Table 3). Notably, the variation of Hd17 may be related to rice evolution, which leads to a trend of heading earlier and earlier.

Table 3.

Nine haplotypes of the Hd17 gene

Allele Haplotype Phenotype 15 24 451 751 1016 1223 1342 1464 1468 1492 1560 1673 1794 1849 1941 2129 2130 2164
Hd17-1–1 H2 P-2 G G C G C G G A T G C C T T C C G G
Hd17-1–2 H3 P-2 A A C C C G A G G A C C C C T T A A
Hd17-1–3 H5 A C C C C G G G G A C C C C T C A G
Hd17-1–4 H6 A C C C C G A G G A C C C C T T A G
Hd17-1–5 H7 A C C C C T G G G A T C C C T C A G
Hd17-1–6 H8 A A C C C G G G G A C C C C T T A G
Hd17-1–7 H9 A G G C C G G G G A C C C C C C A G
Hd17-2 H1 P-1 A C C C T G G G G A C C C C T C A G
Hd17-3 H4 P-3 A A C C C G A G G A C T C C T T A A
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Distribution of Three Alleles of Hd17 in the AA Genome Group

To examine the origin of the nucleotide change in Hd17, we surveyed the distribution of five haplotypes of Hd17 in 2524 cultivated rice accessions (Basmati/Sandri, Aus/Boro, indica, Tropical japonica and Temperate japonica, n = 64, 190, 1615, 358 and 297, respectively), among these more than half are indica (Table 4). We found significant differences in five haplotypes of Hd17 distribution. Hd17-1 mainly existed in Aus/Boro and Tropical japonica, accounting for 70–80%. Hd17-2 mainly emerged in indica and Basmati/Sandri, accounting for 77.6% and 65.6%, respectively. Hd17-3 were mainly from Temperate japonica, accounting for more than 50%. These results indicated that different haplotypes distribution of Hd17 were associated to the evolutionary process of cultivated rice.

Table 4.

Distribution of five haplotypes of Hd17 in 2524 accessions of O. sativa

Species Hd17-1–1 Hd17-1–3 Hd17-1–2 Hd17-2 Hd17-3 Total
indica 2 47 235 1254 (77.6%) 77 1615
Basmati/sandri 3 17 42 (65.6%) 2 64
Aus/boro 150 (79.0%) 9 27 4 190
Tropical japonica 1 290 (81.0%) 29 38 358
Temperate japonica 5 99 27 166 (55.9%) 297
Total 2 206 650 1379 287 2524
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Based on all above results, we put forward a network of domestication in the Hd17 gene. The Hd17-1 allele exhibits a medium maturity heading date (P-2), which is the ancestral type, and is mainly found in O. meridionalis, O. glumaepatula, O. longistaminata, O. barthii, O. nivara, O. glaberrima from Africa and Asian cultivated rice (Aus/Boro and Tropical japonica). Hd17-1 is mainly distributed in tropical regions. The Hd17-2 allele is mainly found in O. meridionalis, O. rufipogon and indica, which is mainly distributed in subtropical regions. The subtropical environment results in a C to T mutation at position 1016 of Hd17 with a corresponding late heading date phenotype (P-1). The Hd17-3 allele is mainly found in Temperate japonica, and is mainly distributed in the temperate japonica rice growing area. The temperate environment leads to a C to T mutation at position 1673 of Hd17 with an early heading date phenomenon (P-3). In addition, O. meridionalis has four haplotypes and exhibits genetic diversity. Three different rice growing regions have formed three alleles of Hd17, and different rice varieties carry the same alleles at the same region. Together, the allelic variation of Hd17 is the result of natural selection. Hd17-2 and Hd17-3 have evolved from Hd17-1 independently through separate evolutionary events.

Expression of Hd17 and its Effect on Downstream Genes Under LD Conditions

Hd17 shows abundant variations, suggesting that it plays an important role in regulating the heading date of rice. To ascertain the Hd17 that is the major determinant of the heading date diversity, we first analyzed the expression level of Hd17 and explored possible relationships between their expression levels and heading date. Interestingly, mRNA levels of Hd17 were proportional to heading date. Higher expression levels of Hd17 were correlated with later heading under FCS of LD conditions (Fig. 3a and Table S4). We also analyzed the mRNA level of the major heading date genes Hd3a, RFT1, Hd1 and Ehd1. Results showed that the expression levels of Hd3a, RFT1 and Ehd1 were contrary to that of Hd17 under LD conditions (Fig. 3c-e and Table S4). In contrast, expression levels of Hd1 were uniform among these cultivars, and little correlation with heading date was found (Fig. S2f and Table S5). These results suggested that Hd17 was the major determinant of variation in heading date by down-regulating Ehd1, Hd3a and RFT1.

Fig. 3.

Fig. 3

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Relative expression levels of Hd17, Ghd7, Ehd1, Hd3a and RFT1 in different alleles under LD conditions. a Hd17 RNA levels in different Hd17 allelic materials. b Ghd7 RNA levels in different Hd17 allelic materials. (c) Ehd1 RNA levels in different Hd17 allelic materials. d Hd3a RNA levels in different Hd17 allelic materials. e RFT1 RNA levels in different Hd17 allelic materials. Leaf samples were collected at 6:00 (dawn) of 78 days after germination under FCS conditions (LD conditions). RNA levels were determined by quantitative real-time PCR (qRT-PCR). Letters above the bars represent statistically significant difference using one-way analysis of variance (ANOVA) with the method of Duncan, different letters indicate significance at 0.05 level. Error bars indicate standard deviations

To further explore the photoperiodic pathway that Hd17 is involved in, we detected the expression levels of known upstream regulators of Ehd1. Ghd7 has been reported to play a very important role in the flowering pathway and negatively regulate the expression of Ehd1 (Xue et al. 2008). Similar expression levels of Ghd7 and Hd17 among P-1, P-2 and P-3 plants, indicated that Hd17 functions upstream of Ghd7 under LD conditions (Fig. 3b and Table S4). Furthermore, the expression levels of other Ehd1 regulators, including Ehd2, Ehd3, Ehd4, DTH2, DTH7 and DTH8, were not affected by Hd17 (Fig. S2a-e, g and Table S5). Above results suggested that Hd17 repressed flowering by up-regulating Ghd7 independent of other Ehd1 regulators under LD conditions.

The Expression of Hd17 is Regulated by the Circadian Clock

Hd17 encodes a homolog of the Arabidopsis EARLY FLOWERING 3 (ELF3) protein, which plays important roles in maintaining circadian rhythms (Matsubara et al. 2012). To examine the expression patterns of Hd17, we monitored its expression level in different samples collected during day and night in controlled long-day (CLD) (14 h light and 10 h dark) and controlled short-day (CSD) (10 h light and 14 h dark) conditions by RT-qPCR. It was clearly observed that the expression patterns of Hd17-1, Hd17-2 and Hd17-3 were consistent, gradually increasing from Zeitgeber time (ZT) 12 h and reaching the peal at ZT 16 h (Fig. 4a, f). Obviously, the expression levels among three Hd17 alleles were significantly different under CLD conditions, but remained similar under CSD conditions, suggesting that the difference of Hd17 expression levels in three alleles is induced by the long day conditions (Fig. 4a, f). Hd17 may act as an integrator of photoperiod sensing and circadian clock in rice.

Fig. 4.

Fig. 4

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Expression patterns of Hd17, Ghd7, Ehd1, Hd3a and RFT1 in different Hd17 allelic plants. a, f Expression patterns of Hd17 in different Hd17 allelic materials under CLD and CSD conditions, respectively. b, g Expression patterns of Ghd7 in different Hd17 allelic materials under CLD and CSD conditions, respectively. c, h Expression patterns of Ehd1 in different Hd17 allelic materials under CLD and CSD conditions, respectively. d, i Expression patterns of Hd3a in different Hd17 allelic materials under CLD and CSD conditions, respectively. e, j Expression patterns of RFT1 in different Hd17 allelic materials under CLD and CSD conditions, respectively. CLD, 14 h light/10 h dark conditions. CSD, 10 h light/14 h dark conditions. ZT, Zeitgeber time. Black shade in the plots indicates dark conditions and the rest of blank indicates light conditions. Leaf samples were collected at 60 days and 36 days after germination under CLD and CSD conditions, respectively

Next, we compared the diurnal expression patterns of Hd3a, RFT1, Hd1, Ehd1, Ehd2, Ehd3 and Ghd7 among P-1, P-2 and P-3 plants under both CLD and CSD conditions. Under CLD conditions, the expression pattern of Ehd1 and Ghd7 are similar to that of Hd17, with two expression peaks at ZT 4 h and ZT 16 h. The expression levels of Ghd7 in the three alleles of Hd17 were consistent with that of Hd17 in ZT 4 h, but exhibiting an opposite trend in ZT 16 h (Fig. 4b). On the contrary, the expression levels of Ehd1 in the three alleles of Hd17 were opposite to that of Hd17 in ZT 4 h, but becoming consistent in ZT 16 h (Fig. 4c). The expression levels of flowering activators Hd3a and RFT1 gradually rose from P-1 to P-3, showing two expression peaks at ZT 8 h and ZT 20 h under CLD conditions (Fig. 4d, e). However, the expression pattern of these genes was not affected under CSD conditions (Fig. 4g–j). Moreover, the transcription levels of Hd1, Ehd2 and Ehd3 were not significantly affected among different Hd17 alleles under both conditions (Fig. S3). Taken together, these results suggested that Hd17 functions upstream of Ghd7 through the Ehd1 pathway to regulate the heading date in the CLD conditions.

Discussion

Hd17-2 is a New Allele of Delay Flowering

In Arabidopsis, ELF3 is an important flowering repressor, involved in photoperiod flowering pathways (Anwer et al. 2020). There are two closely related ELF3 homologs, namely OsELF3.1 and OsELF3.2 in rice, and OsELF3.1 has a greater effect on the regulation of heading date than OsELF3.2 (Zhao et al. 2012; Ning et al. 2015). OsELF3.1 was found by QTL analysis of heading date between the Nipponbare and Koshihikari, and named as Heading date 17 (Hd17) or Ef7 (which were identified from mutant line HS276) (Matsubara et al. 2012; Saito et al. 2012). There was no significant difference in heading date between Nipponbare and NIL-Hd17 (from Koshihikari) under SD conditions, but NIL-Hd17 can delay flowering about 8 days than Nipponbare under LD conditions, which is related to a SNP (SNP4: T/C) at position 1673 (Matsubara et al. 2012). In our studies, the Hd17-3 and Hd17-1 are consistent with Hd17 from Nipponbare and Koshihikari, respectively. Furthermore, we found another SNP (C/T) at position 1016 that may be a functional nucleotide polymorphism (FNP) in Hd17-2 (Figs. 1 and 2). The effect of Hd17-2 on heading date can delay about 3 days than Hd17-1, and delay approximately a week than Hd17-3 in FCS (nature long day conditions) (Fig. 1 and Table S2).

We also found that the expression levels of Hd17 were significant difference among three Hd17 alleles, which was inconsistent with the results of previous study (Matsubara et al. 2012). The nucleotide change in Hd17 was reported to not affect its transcription level [a < 1.9-fold change at the maximum, which occurred at Zeitgeber time (ZT) 20]. Nevertheless, there were significant difference among three Hd17 alleles when we tested the Hd17 expression in the sample harvested before dawn (under natural long day conditions) or at ZT 16 (under CLD conditions) (Figs. 3a and 4a). For the Hd17 expression pattern, we can see that the expression levels among three alleles of Hd17 were different at every different Zeitgeber time (Fig. 4a). In our tests, the expression levels of Hd17 were also not different among three Hd17 alleles at ZT 20, which was the same time to obtain RNA sample in previous study (Matsubara et al. 2012). That's probably why our conclusions were different from those of previous research. In addition, it's worth noting that the expression of the three Hd17 alleles were significantly different under long day conditions, whether it is caused by difference CDS sequences or promoter sequences still remaining unclear.

Hd17 Controls Flowering by Up-Regulating Ghd7 Under Long Day Conditions

In Arabidopsis, ELF3 functions as a flowering repressor, but Hd17 in rice is a promoter of flowering regulation (Yu et al. 2008; Zhao et al. 2012; Yang et al. 2013; Itoh et al. 2019). In our study, we can see that the expression level of Hd17 was higher in P-1 than that in P-2, and remained the lowest in P-3 both at dawn (Fig. 3a) and at ZT 4 (Fig. 4a) under long day conditions. There was the same relation of Ghd7 among Hd17 alleles both at dawn and ZT 4 under long day conditions (Figs. 3b and 4b). Our results were consistent with the fact that the level of Ghd7 in Nipponbare is generally lower than that in NIL-Hd17 at ZT 3 (Matsubara et al. 2012). But previous results suggested that the nucleotide change (FNP at 1673) in Hd17 did not appear to affect its transcription level, which was opposite to our conclusion. They supposed that they failed to detect any difference in the abundance of their transcript (Matsubara et al. 2012). Moreover, with expression level of Hd17 and Ghd7 declining, the expression levels of Ehd1, Hd3a and RFT1 were increased under long day conditions (Figs. 3c-e and 4c-e). Therefore, we suggested that Hd17 directly acts on Ghd7, promoting the expression of Ghd7, and then down-regulating Ehd1 and Hd3a/RFT1 through Ghd7, which eventually leads to changes in the heading date of rice under long day conditions (Fig. 5), but not under short day conditions.

Fig. 5.

Fig. 5

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A model for Hd17-mediated photoperiodic control of flowering in rice under LD conditions. Hd17 directly acts on Ghd7, promoting the expression of Ghd7, and then down-regulating Ehd1 and Hd3a/RFT1 through Ghd7, which eventually leads to changes in the heading date of rice under long day conditions. Arrows, positive regulation. Bars, negative regulation

In addition, EARLY FLOWERING 3 (ELF3) is critical for circadian clock in Arabidopsis (Chow et al. 2012; Kolmos et al. 2011; Nusinow et al. 2011; Jiang et al. 2019). Circadian clock assays showed that ELF3 and GI are fundamental that enable the oscillator to synchronize the endogenous cellular mechanisms to external environmental signals (Anwer et al. 2020). In rice, Hd17, a homolog of ELF3, also functions a circadian clock regulator (Matsubara et al. 2012; Saito et al. 2012; Yang et al. 2013; Wang et al. 2021). In our study, we also hold that the expression of Hd17 was associated to the circadian clock, gradually increasing from ZT 12 and reaching the peak at ZT 16 (Fig. 4).

Allelic Variation of Hd17 is Caused by Natural Selection

Mutations of regulatory gene were thought to underlie phenotypic changes, which are associated with crop domestication (Morrell et al. 2011; Swinnen et al. 2016). Intriguingly, heading date variation is considered as a domestication trait by many studies (Paterson et al. 1995; Thomson et al. 2003; Lee et al. 2022; Jing et al. 2023; Osnato et al. 2023). The domestication of cultivated rice (O. sativa) has been achieved by selection of natural alleles of floral regulators. For example, allelic variation of OsPRR37 was linked with geographical distribution, a suppressor of LD-dependent flowering, contributing to the adaptation of rice cultivars to a wide range of latitudes (Koo et al. 2013). SNP (SNP4: T/C) at position 1673 of Hd17 was surveyed in Asian rice cultivars along with their wild progenitors, revealing that the widespread distribution of the Nipponbare SNP, especially in japonica. Besides, the Koshihikari SNP appeared in almost all indica cultivars and wild species (Matsubara et al. 2012). In our study, a novel SNP (C/T) at position 1016 of Hd17 was discovered to associate with rice domestication. Based on the combination of two FNPs, all alleles should be classified into three groups, CC (Hd17-1), TC (Hd17-2) and CT (Hd17-3) (Table 3).

Hd17-1 is the ancestral type, which exhibited a medium maturity heading date (P-2), and mainly found in O. meridionalis, O. glumaepatula, O. longistaminata, O. barthii, O. nivara, O. glaberrima, Aus/Boro and Tropical japonica, distributing in tropical regions. The Hd17-2 allele mainly exists in O. meridionalis, O. rufipogon, and indica, distributing in subtropical regions. The subtropical environment causes the 1016 position of Hd17 to undergo a C to T mutation and exhibit a late heading date (P-1). The Hd17-3 allele mainly distributes in the temperate japonica rice growing area, which is mainly found in Temperate japonica, a C to T mutation at the position 1673 of Hd17 and show an early heading date (P-3). These variations of Hd17 were consistent with rice domestication (Khush 1997; Kovach et al. 2007; Callaway 2014; Choi et al. 2017; Fornasiero et al. 2022; Osnato 2023). Therefore, three different rice growing regions have formed three alleles of Hd17, demonstrating that the allelic variation of Hd17 is the result of natural selection. Abundant allelic variation provides diverse choices for utilizing these preponderant alleles to the molecular design breeding in rice.

Conclusion

Using 14 SSSLs, 6 wild rice species, and 2524 accessions of O. sativa to analyze the allelic variation of heading date Hd17 gene, three alleles were identified. The Hd17-1 is an ancestral type with a middle heading date and mainly distributing in tropical regions. The Hd17-2 is a new allele with a delay heading, which was caused by the FNP of C to T at position 1016, and mainly distributes in subtropical regions. The Hd17-3 allele was caused by the FNP of C to T in 1673 point with earlier heading, and mainly distributes in temperate regions. Hd17-2 and Hd17-3 had been evolved from Hd17-1, which is the result of natural selection.

Methods

Plant Materials and Field Experiments

There were 14 SSSLs and their receptor parent Hua-jing-xian 74 (HJX74) being selected as experimental materials in this study (Table S1). HJX74 is an elite indica variety with a lot excellent properties, which was developed by our laboratory from South China. Each of the 14 SSSLs possesses only single segment substituted from one donor into HJX74 genetic background (Zhang et al. 2004; Xi et al. 2006; He et al. 2017; Zhao et al. 2019; Zhang 2021). The six wild rice species (including O. rufipogon, O. meridionalis, O. nivara, O. barthii, O. glumipatula and O. longistaminata), thereinto O. meridionalis has four haplotypes all from Australia, were collected by our lab. The phenotypic test was conducted at the experimental station in South China Agricultural University, Guangzhou, China (23°07' N, 113°15' E). All 15 materials (14 SSSLs and HJX74) were planted in five cropping seasons from 2015 to 2017, two cropping seasons per year The frst cropping season (FCS) was from late February to middle July, the second cropping season (SCS) was from late July to middle November (Tan et al. 2020; 2021). Germinated seeds were sowed in a seedling bed, and then seedlings were transplanted to a rice field 20 days later with one plant per hill, according to the density of 16.7 cm × 16.7 cm. A completely randomized block design was adopted, in which each plot consisted of four rows with ten plants each row. The heading date was measured as the number of days from sowing to the appearance of the first panicle.

DNA Extraction, PCR Amplification, Cloning and Sequence Analysis

Fresh leaves were collected at the seedling stage and DNA were extracted plants using the CTAB method (Murray and Thompson 1980). The program of polymerase chain-reaction (PCR) amplification was followed a previously described protocol (Panaud et al. 1996). SSR markers labeled ‘RM’ were selected from online resources (https://archive.gramene.org/markers/). The primers of cloning were designed by using the software of primer premier 5.0, and the primers were listed in the Table S6. We cloned Hd17 gene from these SSSLs and wild species. The CDS sequence of Hd17 in 14 SSSLs and six wild species were analyzed by BGI Sequencing.

RNA Extraction and Reverse-Transcription Quantitative PCR (RT-qPCR)

Leaf samples were collected at two hours after sunset, 78 days after germination under FCS conditions, or collected 60 days and 36 days after germination under CLD (14 h light/10 h dark) and CSD (10 h light/14 h dark) conditions, respectively. Total RNA was isolated using TRIZOL reagent (Invitrogen) following the manufacturer’s instruction from leaves. First-strand cDNA was reverse transcribed from DNaseI-treated RNA with oligo-dT as the primer using ReverTra Ace kit (Toyobo). Gene expression was tested by RT-qPCR using the QuantStudio3 Real-Time PCR system (Thermo Fisher Scientific). The RT-qPCR was carried out in a total volume of 20 μl containing 1X SYBR Green Master Mix (Life technologies). We normalized the expression levels by using Ubc gene as internal control. Each experiment was repeated three times, and the ΔΔCT method was used to evaluate quantitative variation. The RT-qPCR program was conducted at 94 ℃ for 3 min, followed by 40 cycles at 94 °C for 30 s, 60 °C for 30 s, and 72 °C for 30 s. The RT-qPCR primers were showed in the Table S6.

Data Analysis

Sequence analysis based on the ‘BioEdit’ and ‘SnapGene’ software. The data of SNP high-throughput detection SNP analysis using ‘IntelliScore’ software. The sequences were aligned using the ClustalW2 software (http://www.ebi.ac.uk/Tools/clustalw2/index.html). The sequence of Hd17 in 2524 cultivated accessions were from RFGB (https://www.rmbreeding.cn/), and detail data showed in Supplementary Material 2. The CDS sequence of Hd17 in 14 SSSLs and 6 wild rice species showed in Supplementary Material 3 and Supplementary Material 4, respectively.

Supplementary Information

Additional file1 (DOCX 3518 KB) (3.4MB, docx)
Additional file2 (XLSX 453 KB) (453.1KB, xlsx)
Additional file3 (PDF 31 KB) (31.2KB, pdf)
Additional file4 (PDF 26 KB) (26.1KB, pdf)

Acknowledgements

Not applicable.

Abbreviations

SSSLs

Single-segment substitution lines

FNP

Functional nucleotide polymorphism

QTL

Quantitative trait locus

SD

Short-day

LD

Long-day

FCS

First cropping season

SCS

Secondary cropping season

SNP

Single nucleotide polymorphism

CLD

Control long-day

CSD

Control short-day

RT-qPCR

Reverse-transcription quantitative PCR

ZT

Zeitgeber time

HJX74

Hua-jing-xian 74

Author Contributions

GZ designed and supervised the works. ZY and YL performed most of the experiments and analyzed the experimental data. JL, SW, XW, MG, YL, HZ, GL and SW conducted a part of experiments. GZ and ZY analyzed the data and wrote the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported by grants from the National Natural Science Foundation of China (91735304 and 91435207).

Availability of Data and Materials

No datasets were generated or analysed during the current study.

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.

Zifeng Yang, Yun Li have contributed equally to this work.

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Associated Data

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

Supplementary Materials

Additional file1 (DOCX 3518 KB) (3.4MB, docx)
Additional file2 (XLSX 453 KB) (453.1KB, xlsx)
Additional file3 (PDF 31 KB) (31.2KB, pdf)
Additional file4 (PDF 26 KB) (26.1KB, pdf)

Data Availability Statement

No datasets were generated or analysed during the current study.

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