Skip to main content

Genome-wide characterization of SDR gene family and its potential role in seed dormancy of Brassica napus L.

Abstract

Rapeseed (Brassica napus L.) with short or no dormancy period are easy to germinate before harvest (pre-harvest sprouting, PHS). PHS has seriously decreased seed weight and oil content in B. napus. Short-chain dehydrogenase/ reductase (SDR) genes have been found to related to seed dormancy by promoting ABA biosynthesis in rice and Arabidopsis. In order to clarify whether SDR genes are the key factor of seed dormancy in B. napus, homology sequence blast, protein physicochemical properties, conserved motif, gene structure, cis-acting element, gene expression and variation analysis were conducted in present study. Results shown that 142 BnaSDR genes, unevenly distributed on 19 chromosomes, have been identified in B. napus genome. Among them, four BnaSDR gene clusters present in chromosome A04、A05、C03、C04 were also identified. These 142 BnaSDR genes were divided into four subfamilies on phylogenetic tree. Members of the same subgroup have similar protein characters, conserved motifs, gene structure, cis-acting elements and tissue expression profiles. Specially, the expression levels of genes in subgroup A, B and C were gradually decreased, but increased in subgroup D with the development of seeds. Among seven higher expressed genes in group D, six BnaSDR genes were significantly higher expressed in weak dormancy line than that in nondormancy line. And the significant effects of BnaC01T0313900ZS and BnaC03T0300500ZS variation on seed dormancy were also demonstrated in present study. These findings provide a key information for investigating the function of BnaSDRs on seed dormancy in B. napus.

Peer Review reports

Introduction

Dormancy has lost in most crops with the long-term domestication [1]. As a consequence, pre-harvest sprouting (PHS), seeds tend to sprout or even germinate on field plants during continuous rainy weather before harvest, occurring on a large scale [2, 3]. And PHS has caused serious yield loss of many crops in China [4]. For decreasing yield loss, the genetic mechanisms of seed dormancy and PHS need to be explored in crops.

Among a series of reported seed dormancy QTLs, the functions of short-chain dehydrogenase/reductase 1 (SDR1) and SDR4 regulating rice seed dormancy have been clarified [5, 6]. OsSDR4, encodes a nucleus located protein, is the dominant genetic factor for the difference in pre-harvest sprouting between japonica and indica rice subspecies [7]. The OsSDR1 encodes an inhibitory protein that acts as a molecular link between the nutritional signaling pathway and plant hormone biosynthesis. And OsSDR1 gene could regulate seed dormancy by interacting with other structural elements [8].

SDRs, one of the oldest and largest superfamily, can regulate growth and development in various species such as archaea, prokaryotes, eukaryotes and viruses [9, 10]. ABA2/GIN1 (AtSDR1), the first identified SDR gene in Arabidopsis, was involved in sugar signaling and ABA biosynthesis. The loss-of-function mutation Atsdr1 leads to a typical ABA-deficient phenotype in Arabidopsis, resulting in reduced seed dormancy. In contrast, overexpressing AtSDR1 Arabidopsis showed increased ABA content, promoted seed dormancy [11]. Thus, SDR genes have played critical role in seed dormancy in plant.

Rapeseed (Brassica napus L.) originated from natural hybridization between B. rapa and B. oleracea > 7,500 years ago [12]. As a young crop, it is an ideal model for seed dormancy investigation. As statistics in recent years, the proportion of rapeseed PHS in the main production area Yangtze River Basin of China was higher than 0.6%. And PHS has been seriously decrease seed weight and oil content in B. napus [13]. However, few report of seed dormancy and PHS mechanism has greatly inhibited the rapeseed breeding progress. It is great significance to clarify whether SDR genes are involved in seed dormancy and PHS in B. napus.

Considering these matters, 142 BnaSDRs were identified in B. napus genome by homology sequence blast in this study. The protein physicochemical properties, conserved motif, gene structure, cis-acting element, and tissue expression profile analysis were also conducted. Furthermore, seven seed dormancy related candidate genes were selected for gene expression and variation analysis. These findings could provide a key information for investigating the function of BnaSDRs on seed dormancy and PHS in B. napus.

Materials and methods

Identification of SDR genes in B. napus genome

Fifty-five AtSDR protein sequences obtained from UniProt database [14] (https://www.uniprot.org/) were employed as reference sequence in present study. Then, blastP [15] were performed in the Brassica napus pan-genome Information Resource (BnPIR) database [16] (http://cbi.hzau.edu.cn/bnapus/). BnaSDRs were screened according to the conserved protein structure by using the Simple Modular Architecture Research Tool (SMART) [17]. Besides, NCBI and Ensemble Plants data source were used to further validate the identified proteins.

The B. napus genome file, chromosome annotation information, and BnaSDR genes’ location information were downloaded from the BnPIR database. And Gene Location Visualize subroutine of TBtools software [18] was used to map the chromosome location of BnaSDR genes.

Evolutionary analysis of SDR family

The full-length protein sequences of 55 AtSDRs, 142 BnaSDRs, 70 BraSDRs and 51 BolSDRs were obtained from UniProt database and BnPIR database, respectively. And these protein sequences were aligned using the ClustalW program [19]. Neighbor-Joining (NJ) phylogenetic tree was constructed by MEGA7.0 [20]. Bootstrap analysis was conducted with 1000 replications [21]. Then the evolutionary tree was visualized by using the online website iTOL (https://itol.embl.de/).

Analysis of collinearity replication relationship of BnaSDR genes

In order to analyze the replication events involved in BnaSDR genes between or within species, the genome and annotation files of Arabidopsis thaliana and B. napus were downloaded from the Ensemble Plants database and BnPIR database, respectively. The OneStepMCScanX program in TBtools was used to analyze the collinearity between or within species of BnaSDR genes.

Protein physicochemical properties and subcellular localization analysis of BnaSDR proteins

The physicochemical properties including amino acid number, molecular weight, theoretical pI, instability index, aliphatic index and grand average of hydropathicity of SDR proteins were analyzed by online software Expasy [22] (https://web.expasy.org/protparam/). Subcellular localization of SDR proteins were predicted by the online software Wolf PSORT [23] (https://wolfpsort.hgc.jp/).

Analysis of conserved motifs of SDR proteins

The online analysis software MEME [24] (https://meme-suite.org/meme/) was used to analyze the conserved motifs of all SDR protein sequences, with the following parameters: distribution of motifs, the optimum width of motif, 6–50; the number of repetitions, any. number of motifs, 12; the number of motif occurrences on each sequence is not limited; Then visualization was conducted by TBtools software.

Analysis of gene structure and cis-acting elements in promoter region of SDR genes

The rapeseed genome and annotation files were downloaded from the BnPIR database. And the BnaSDR gene structure was visualized by the subroutine Gene Structure View function of TBtools software. For cis-acting elements analysis, the upstream 1500 bp promoter sequence of BnaSDR genes were extracted from B. napus genome by TBtools software. Then, cis-acting elements in the BnaSDR promoter regions were predicted by online software Plant CARE [25] (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/).

Analysis of tissue expression profiles of BnaSDR genes

In order to investigate the tissue expression profiles of BnaSDR genes, the gene expression data in root, stem, leaf, bud, filament, petal, pollen, sepal, cotyledon, seed and silique of B. napus were obtained from BnTIR database [26] (http://yanglab.hzau.edu.cn). Considering BnaSDR might relate to seed dormancy, BnaSDR expression level in seeds from 14 to 64 days after flowering were also downloaded from BnTIR database.

RNA extraction and qRT-PCR analysis

Primers were designed using qPrimerDB [27], and the specific primer sequence was shown in Table 1. The fresh harvest seeds of weak dormancy line (T) and nondormancy line (S) divided from a breeding population of our research group were employed for germination test. Seeds of these two lines were kept in rapeseed laboratory of Anhui agricultural university. The total RNA of fresh harvest seeds and soaked with ABA or water for 12 h of T or S line were isolated using plant total RNA extraction Kit (Baori Medical Technology (Beijing) Co., Ltd.,). The PrimeScriptTM RT reagent Kit with gDNA Eraser reverse transcription Kit (Baori Medical Technology (Beijing) Co., Ltd.,) was used to synthesize single-stranded cDNA. The qRT-PCR was conducted by real-time fluorescence quantitative PCR Kit (Baori Medical Technology (Beijing) Co., Ltd.,). The expression level of BnaSDR genes was quantified by 2-Ct method. Each test was repeated for four times. The expression heat map was drawn by TBtools software.

Table 1 Sequences of primers used for qRT-PCR

BnaSDR haplotype variation analysis

In order to analyze the effects of BnaSDR gene variation on seed dormancy, the variation of seven seed dormancy related candidate genes and germination character were investigated in a 143 rapeseed micro-core collections. The sequence variation and haplotype information were extracted from our previous study [12]. In germination experiment, fresh harvest-seeds of 143 rapeseed accessions were employed. Fifty seeds of each accession were sown on the plastic dish with one layer of filter paper. Seeds were germinated at 25 °C, a relative humidity of 60–70%, a 16-h photoperiod, in a growth chamber. Then, the germination rate was measured every day. All the treatments were replicated for three times.

Results

Identification of SDR genes in B. napus genome

A total of 142 BnaSDR genes were identified from B. napus genome by blast with 55 AtSDR sequences. The results of chromosome location shown that there were 141 BnaSDR genes anchored in 19 B. napus chromosomes (Fig. 1). However, Bnascaffold2694G0000200ZS has not been anchored to any chromosome. We also found that 141 BnaSDR genes were unevenly distributed on the A and C sub-genomes. There were 67 and 74 BnaSDR genes located on A and C sub-genomes, respectively. Among them, chromosome C04 contained the maximum number of BnaSDRs (17), and chromosome A06 and C06 had only two BnaSDRs. Furthermore, four BnaSDR gene clusters, contain more than five BnaSDRs in a 20 M region, were identified on chromosomes A04, A05, C03 and C04 (Fig. 1).

Fig. 1
figure 1

The distribution of BnaSDR genes in the B. napus chromosomes | BnaSDR gene clusters were marker as red line

Evolution of SDR family in B. napus

To understand the evolutionary relationships and functions among BnaSDR proteins, a phylogenetic tree was created with 142 BnaSDR protein sequences, its orthologous proteins in B. rapa and B. oleracea, and 55 AtSDR protein sequences by MEGA7.0. Phylogenetic tree results shown that 142 BnaSDR proteins were divided into four distinguishing groups (Group A–D; Fig. 2). The subgroup C contained the least number of SDR members, only 4 AtSDRs, 9 BnaSDRs, 5 BraSDRs and 4 BolSDRs. But Subgroup D, a largest group, contains 28 AtSDRs, 68 BnaSDRs, 34 BraSDRs and 27 BolSDRs. Subgroup A contained 4 AtSDRs, 13 BnaSDRs, 4 BraSDRs and 3 BolSDRs. Subgroup B contained 19 AtSDRs, 52 BnaSDRs, 27 BraSDRs and 17 BolSDRs.

Fig. 2
figure 2

Phylogenetic tree of BnaSDR, BraSDR, BolSDR and AtSDR proteins

Gene replication plays an important role in the evolution of organisms, replicated genes lay the foundation for the physiological and morphological changes of individual plants [28]. In order to study the replication events of the BnaSDR gene family in the B.napus genome and the interspecies of A. thaliana, the interspecies and intraspecies collinearity of A. thaliana and B.napus were investigated by using TBtools software (Fig. 3). Results shown that there were a large number of orthologous SDR genes between B. napus and A. thaliana. Within B. napus genome, the SDR gene has been amplified to a certain extent. These indicating that gene replication plays a very important role in the evolutionary process of B. napus.

Fig. 3
figure 3

Synteny analysis of SDRs among A. thaliana and B. napus (A) Intraspecies collinearity analysis; (B) Interspecies collinearity analysis. The coarse red line in the circle is the collinearity gene of SDR genes among species, and the fine gray line indicates all the collinearity genes contained among species

Physicochemical properties of BnaSDR proteins

In order to clarify the basic characteristics of SDR proteins in B. napus, the physicochemical properties of 142 BnaSDR proteins were analyzed. Results shown that the sequence length of BnaSDR proteins were ranged from 92 to 501 aa, with an average length of 306 aa. The largest relative molecular mass was BnaA04T0077900ZS (55188.59 Da), the smallest relative molecular mass was BnaC05T0510200ZS (9801.25 Da), and the average relative molecular mass was 33170.24 Da. The average theoretical pI was 7.37, and most BnaSDR proteins were alkaline. The instability index of BnaSDR proteins were between 10.35 and 66.84, and only 13.38% BnaSDR proteins were unstable proteins (Table S1). The average hydrophobicity index of BnaSDR proteins was between − 0.603 and 0.381, and 61.27% BnaSDR proteins showed hydrophobicity (Table S2; Fig. 4). Results of subcellular localization showed that most of the BnaSDR proteins (71, 50%) were located in chloroplasts, 33.10% BnaSDR proteins located in cytoplasm, and some BnaSDRs were located in peroxisomes (3.52%), plasma membrane (3.52%), nucleus (2.82%), endoplasmic reticulum (2.82%), cytoskeleton (2.11%) and extracellular matrix (1.41%). Only one BnaSDR protein (BnaC04T0186800ZS), homologous to At2g29330, was located on the Golgi apparatus (Table S1).

By comparing the physicochemical properties between different subgroups (Fig. 4), it was found that the number of amino acids, theoretical pI, molecular weight and instability index of subgroup A were the highest among four subgroups. And the unstable proteins were mainly distributed in subgroup A. The average theoretical pI of subgroup A and subgroup C was greater than 7. This indicated that most of the BnaSDRs in subgroup A and subgroup C were alkaline. BnaSDRs in subgroup D were mostly neutral. BnaSDRs in subgroup B were mostly acidic. The grand average of hydrophobicity of subgroup C was the highest. In addition, the BnaSDRs in B, C and D subgroups were almost hydrophobic proteins. However, BnaSDRs in subgroup A were hydrophilic proteins.

Fig. 4
figure 4

Comparations of protein physicochemical properties between different BnaSDR subgroups

Conserved motifs of BnaSDR proteins

To further understand the protein sequence features of BnaSDRs, the conserved motifs of each protein were identified using the online software MEME. we found that almost all of the BnaSDR proteins contained motif 4 (95.77%), indicating that motif 4 is relatively conserved in the SDR family. However, only 14.79% BnaSDR proteins contained the motif 12 (Fig. 5A, Figure S1).

Results of the distribution of conserved motifs in different groups have shown that proteins in the same group have similar motif distribution. It was found that motif 1 and motif 2 were mainly existed in the members of subgroup B. BnaSDRs containing motif 9, motif 10 and motif 11 are mainly in subgroup D (Fig. 5B). These indicating that the proteins in different subgroups may have large functional differentiation.

Fig. 5
figure 5

Motif distribution map of BnaSDRs. | (A) Conserved motifs in BnaSDRs; (B) Distribution of conserved motifs in different BnaSDR subgroups

Gene structure and cis-acting elements of BnaSDR genes

To character structures of BnaSDR genes, gene length, CDS length, intron number, and cis-acting elements were investigated. By aligning CDS and genomic sequences, we found that the structure and intron number were quite different among BnaSDR genes, but roughly similar among a subgroup. There were 2 to 12 introns distributed in BnaSDR genes. However, the number and location of introns in BnaA09T0182700ZS was very different from other branches in the same subgroup (Figure S2). The functional differentiation of BnaA09T0182700ZS has occurred in B. napus.

To explore cis-acting elements in the promoter region of BnaSDR genes, the online promoter database Plant Care was employed in present study. Results shown that there were 1558 (14 no duplication) cis-acting elements in the BnaSDR promoter regions. There were 856 hormone response regulatory elements (5 no duplication), including auxin-responsive element, gibberellin-responsive element, abscisic acid responsiveness, salicylic acid responsiveness and CGTCA-motif responsive element. There were 42.99% and 36.10% BnaSDR genes containing CGTCA-motif response element and abscisic acid response element, respectively (Table 2, Figure S3). These indicated that the expression of these genes might be regulated by hormone signaling.

Besides, there were 625 (5 no duplication) environmental stress responses elements, including light responsive element, anaerobic induction, defense and stress responsiveness, low-temperature responsiveness, MYB binding site involved in drought-inducibility. And the remaining 77 cis-elements (4 no duplication) are related to tissue expression, including meristem expression, MYB binding site involved in flavonoid biosynthetic genes regulation, endosperm expression and phytochrome down-regulation expression (Table 2, Figure S3). These results indicated that the functional diversity of BnaSDRs has been occured during the growth and development of B. napus.

Table 2 Distribution cis-acting elements in different BnaSDR subgroups

Tissue expression profiles of BnaSDR genes

To explore tissue-specific expression profiles of the BnaSDR genes, the expression data of 37 tissues (including 11 tissues and 26 seeds at the different development stages) were obtained from the BnTIR database. Results shown that the 142 BnaSDR genes widely expressed in different tissues (Figure S4). But the expression pattern of BnaSDR genes in different groups were largely different. The expression level in stem, leaf, bud and cotyledon of genes in subgroup A were higher than those in other groups. BnaSDR genes in subgroup C were highly expressed in root, filament, petal, pollen, sepal and silique, but not in cotyledon. In subgroup D, BnaA02T0152200ZS, BnaC02T0194900ZS, BnaA03T0253100ZS and BnaC03T0300500ZS were only highly expressed in seeds.

The expression level of BnaSDR genes in seeds from 14 to 64 days after flowering were also compared between different subgroups (Fig. 6). As a whole, the expression levels of BnaSDR genes in subgroup A, B and C were gradually decreased, but increased in subgroup D with seed development. Especially, the expression level of BnaA01T0256500ZS, BnaC01T0313900ZS, BnaA05T0476100ZS, BnaA02T0152200ZS, BnaA03T0253100ZS, BnaC03T0300500ZS and BnaC03T0290800ZS in subgroup D were significantly increased at the late stage of seed development (64 days after flowering).

Fig. 6
figure 6

Expression patterns of BnaSDR gene in developing seeds

BnaSDR genes expression level in dormant seed

Based on the phylogenetic and gene expression data, seven promising seed dormancy related BnaSDR genes were selected from subgroup D for further study. Expression level of these seven genes in weak dormancy (T) or nondormancy (S) seeds were analyzed by qRT-PCR. Results shown that the expression levels of six BnaSDRs (BnaC01T0313900ZS, BnaA05T0476100ZS, BnaA02T0152200ZS, BnaA03T0253100ZS, BnaC03T0300500ZS, BnaC03T0290800ZS) in fresh harvest seeds of T line were significantly higher than those in S line (Fig. 7A). These indicating that BnaC01T0313900ZS, BnaA05T0476100ZS, BnaA02T0152200ZS, BnaA03T0253100ZS, BnaC03T0300500ZS, BnaC03T0290800ZS might relate to seed dormancy.

By comparing the gene expression levels of germinated seeds treated with distilled water or ABA, we found that abscisic acid treatment significantly increased the expression levels of seven genes both in T and S lines (Fig. 7B). The delayed germination was also found under ABA treatment (Fig. 7C). Thus, ABA treatment might enhance seed dormancy by upregulating seed dormancy related BnaSDR genes in B napus.

Fig. 7
figure 7

Expression pattern analysis of seven promising seed dormancy related BnaSDR genes. | (A) Expression level of seven promising seed dormancy related BnaSDR genes in fresh harvest seeds of weak dormant line (T) and non-dormant line (S); (B) Expression level of seven promising seed dormancy related BnaSDR genes in germinated seeds treated with distilled water or ABA for 12 h. (C) Phenotype of fresh harvest seeds treated with distilled water or ABA for 12 h. WT: fresh weak dormant seeds treated with distilled water for 12 h; WS: fresh non-dormant seeds treated with distilled water for 12 h; AT: fresh weak dormant seeds treated with ABA for 12 h; AS: fresh non-dormant seeds treated with ABA for 12 h

Effects of BnaSDR variation on seed dormancy

In order to clarify the effects of BnaSDR gene variation on seed dormancy, the variation of seven seed dormancy related candidate genes and germination character were investigated in a 143 rapeseed micro-core collections. Results of sequence variation were shown that there were 1 to 9 variation sites in four BnaSDR genes (BnaC01T0313900ZS, BnaC03T0300500ZS, BnaA02T0152200ZS, and BnaA03T0253100ZS) (Table S3). However no available variation (minor allele frequency > 0.05) be detected of other three candidate genes in present population.

There was one variation site in BnaC01T0313900ZS. Accessions carrying haplotypes 1 (Hap1, T variation) exhibited a higher germination speed and germination rate than that of Hap2 (C variation) (Fig. 8). And we also found that the germination speed and germination rate were significantly different between three haplotypes of BnaC03T0300500ZS. Accessions carrying Hap2 or Hap3 of BnaC03T0300500ZS exhibited higher germination speed and germination rate than that of Hap1 of BnaC03T0300500ZS (Fig. 8). However, there were no difference of germination character between different haplotypes in BnaA02T0152200ZS and BnaA03T0253100ZS (Figure S5).

Fig. 8
figure 8

Effects of BnaSDR gene variation on seed dormancy in B. napus

Discussions

Seed dormancy and its related PHS are complex quantitative traits controlled by multiple genes [29]. It has been demonstrated that SDR genes can regulate seed dormancy and PHS by promoting ABA biosynthesis [7]. In present study, a total of 142 non-repetitive BnaSDR genes were identified in the B. napus genome. Which provide a chance to clarify whether SDR genes are the key factor of seed dormancy in B. napus. The distribution of these 142 BnaSDR genes on B. napus chromosomes was irregular. And four BnaSDR gene clusters were found on chromosomes A04, A05, C03 and C04. As reported in previous studies, gene clusters may emerge on chromosomes when genes replicate. And it plays a special role in rapid stress response, gene coregulation, co-function and co-heredity, they are important for plant environmental adaptation and evolution [30, 31]. Therefore, it is speculated that BnaSDR genes were asymmetrically retained on these chromosomes after whole-genome triplication (WGT) event in Brassica [32]. These indicated BnaSDR genes play vital role in rapeseed growth and development.

We also found that the SDR family can be divided into four groups by phylogenetic analysis. The seed dormancy related protein ABA2 (At1g52340) [11] was distributed in the subgroup D. Members of same group have a similar protein character, conserved motifs, gene structure, cis-acting elements and tissue expression profile. There were also some homologous genes with different motifs and gene struct. These indicating that these genes in different subgroups may have large functional differentiation. Previous studies have reported that, SDR genes also involved in the synthesis and degradation of lipids, sugars, nucleotides and amino acids to regulate plant growth, development and stress defense [33, 34].

The expression pattern plays an important role in gene function [35]. We found that the expression level of seven BnaSDRs (BnaA01T0256500ZS, BnaC01T0313900ZS, BnaA05T0476100ZS, BnaA02T0152200ZS, BnaA03T0253100ZS, BnaC03T0300500ZS and BnaC03T0290800ZS) in subgroup D were rapidly raised at the late stage of seed development (64 days after flowering). The expression of six BnaSDRs (BnaC01T0313900ZS, BnaA05T0476100ZS, BnaA02T0152200ZS, BnaA03T0253100ZS, BnaC03T0300500ZS, BnaC03T0290800ZS) among these seven genes in T line (weak dormancy) was higher than that in S line (non-dormancy). In addition, the expression levels were increased to varying degrees after ABA treatment in both T and S lines. Previous studies have shown that the multi-step reaction of AtSDR1 catalyzing aflatoxin to abscisic aldehyde is a key step in ABA biosynthesis [36,37,38]. And the seed dormancy is enhanced during ABA biosynthesis. Thus, these six BnaSDRs might play an important role in rapeseed seed dormancy. Which provide a critical information for investigating the molecular mechanism of seed dormancy and PHS in B. napus.

The role of ABA and GAs on seed dormancy and germination have been demonstrated by previous studies [39,40,41]. In present study, a large number of hormone response-related elements and abiotic stress-related elements in the upstream promoter region of BnaSDR genes were also identified. And ABA treatment significantly increased the expression levels of seven seed dormancy related candidate genes both in T and S lines in present study. Therefore, BnaSDR genes might regulate seed dormancy as well as growth and development by responding hormone in B. napus as in other plants.

Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Liang Y, Liu H-J, Yan J, Tian F. Natural variation in crops: realized understanding, continuing Promise. Annu Rev Plant Biol 2021, 72(1).

  2. Tai L, Wang HJ, Xu XJ, Sun WH, Ju L, Liu WT, Li WQ, Sun J, Chen KM. Pre-harvest sprouting in cereals: genetic and biochemical mechanisms. J Exp Bot. 2021;72(8):2857–76.

    Article  PubMed  CAS  Google Scholar 

  3. Sheikh FR, Jose-Santhi J, Kalia D, Singh K, Singh RK. Sugars as the regulators of dormancy and sprouting in geophytes. Ind Crops Prod. 2022;189:115817.

    Article  CAS  Google Scholar 

  4. Xu F, Tang J, Gao S, Cheng X, Du L, Chu C. Control of rice pre-harvest sprouting by glutaredoxin-mediated abscisic acid signaling. Plant J. 2019;100(5):1036–51.

    Article  PubMed  CAS  Google Scholar 

  5. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, et al. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell. 2002;14(11):2723–43.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Chen W, Wang W, Lyu Y, Wu Y, Huang P, Hu S, Wei X, Jiao G, Sheng Z, Tang S, et al. OsVP1 activates Sdr4 expression to control rice seed dormancy via the ABA signaling pathway. Crop J. 2021;9(1):68–78.

    Article  CAS  Google Scholar 

  7. Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, et al. Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci U S A. 2010;107(13):5792–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Xu H-B, Xu Q, Lian L, Zhu Y-s, Jiang J-h, Xie H-g, Luo X, Jiang M-r. Zheng Y-m, Xie H-a et al: Cloning and sequence analysis of OsSDR1 gene from Restorer Line of Hybrid Rice Fuihui 7185. Fujian J Agricultural Sci. 2017;32(9):939–45.

    Google Scholar 

  9. Yu S, Sun Q, Wu J, Zhao P, Sun Y, Guo Z. Genome-wide identification and characterization of short-chain Dehydrogenase/Reductase (SDR) Gene Family in Medicago truncatula. Int J Mol Sci. 2021;22(17):9498.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Moummou H, Kallberg Y, Tonfack LB, Persson B, Van Der Rest B. The Plant Short-Chain dehydrogenase (SDR) superfamily: genome-wide inventory and diversification patterns. BMC Plant Biol. 2012;12(1):219.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Lin PC, Hwang SG, Endo A, Okamoto M, Koshiba T, Cheng WH. Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol. 2006;143(2):745–58.

    Article  PubMed  Google Scholar 

  12. Hu J, Chen B, Zhao J, Zhang F, Xie T, Xu K, Gao G, Yan G, Li H, Li L, et al. Genomic selection and genetic architecture of agronomic traits during modern rapeseed breeding. Nat Genet. 2022;54(5):694–704.

    Article  PubMed  CAS  Google Scholar 

  13. Mácová K, Prabhullachandran U, Štefková M, Spyroglou I, Pěnčík A, Endlová L, Novák O, Robert HS. Long-term high-temperature stress impacts on embryo and seed development in Brassica napus. Front Plant Sci. 2022;13:844292.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Rolf A, Amos B, Wu CH, Barker WC, Brigitte B, Serenella F, Elisabeth G, Huang H, Rodrigo L, Michele M. UniProt: the Universal protein knowledgebase. Nucleic Acids Res. 2004;32(Database issue):D115–119.

    Google Scholar 

  15. Carlos F. Susannah, gal: aspartic proteinase content of the Arabidopsis Genome. Curr Protein Pept Sci 2005, 6(6).

  16. BnPIR. Brassica napus Pan-genome Information Resource for 1,689 accessions. Plant Biotechnol J 2020.

  17. Letunic I, Khedkar S, Bork P. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res. 2021;49(D1):D458–60.

    Article  PubMed  CAS  Google Scholar 

  18. Chen C, Chen H, Zhang Y, Thomas HR, Xia R. TBtools: an integrative Toolkit developed for interactive analyses of big Biological Data. Mol Plant 2020, 13(8).

  19. Clh A, Ysl B, Cyl C, Ycc B, Yfc C. CUDA ClustalW: an efficient parallel algorithm for Progressive multiple sequence alignment on Multi-GPUs. Comput Biol Chem. 2015;58:62–8.

    Article  Google Scholar 

  20. Sudhir K, Glen S, Koichiro T. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 2016(7):1870.

  21. Yan G, Zhang M, Guan W, Zhang F, Dai W, Yuan L, Gao G, Xu K, Chen B, Li L, et al. Genome-wide identification and functional characterization of stress related glyoxalase genes in Brassica napus L. Int J Mol Sci. 2023;24(3):2130.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Duvaud S, Gabella C, Lisacek F, Stockinger H, Durinx C. Expasy, the Swiss Bioinformatics Resource Portal, as designed by its users. Nucleic Acids Res 2021: W216–27.

  23. Paul H, Keun-Joon P, Takeshi O, Naoya F, Hajime H, Adams-Collier CJ, Kenta N. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35(Web Server issue):585–7.

    Google Scholar 

  24. Timothy B. James, Johnson, Charles, Grant, William: the MEME suite. Nucleic Acids Res 2015: W39–49.

  25. Lescot M. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Liu D, Yu L, Wei L, Yu P, Guo L. BnTIR: an online transcriptome platform for exploring RNA: eq libraries for oil crop Brassica napus. Plant Biotechnol J 2021.

  27. Chang W, Niu Y, Yu M, Li T, Li J, Lu K. qPrimerDB: a powerful and user-friendly database for qPCR primer design. Methods Mol Biol. 2022;2392(D1):173–82.

    Article  PubMed  CAS  Google Scholar 

  28. Kong HLL, Frohlich MW, Leebens-Mack J, Ma H, dePamphilis CW. Patterns of gene duplication in the plant SKP1 gene family in angiosperms evidence for multiple mechanisms of rapid gene birth. 2007:50(55):873–85.

  29. Sohn S, Pandian S, Kumar T, Zoclanclounon Y, Muthuramalingam P, Shilpha J, Satish L, Ramesh M. Seed dormancy and Pre-harvest sprouting in Rice-An updated overview. Int J Mol Sci. 2021;22(21):11804.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Chen X, Liu F, Liu L, Qiu J, Fang D, Wang W, Zhang X, Ye C, Timko MP, Zhu Q-H, et al. Characterization and evolution of gene clusters for terpenoid phytoalexin biosynthesis in Tobacco. Planta. 2019;250(5):1687–702.

    Article  PubMed  CAS  Google Scholar 

  31. Qiao D, Tang M, Jin L, Mi X, Chen H, Zhu J, Liu S, Wei C. A monoterpene synthase gene cluster of tea plant (Camellia sinensis) potentially involved in constitutive and herbivore-induced terpene formation. Plant Physiol Biochem. 2022;184:1–13.

    Article  PubMed  CAS  Google Scholar 

  32. Xie T, Zhang FG, Zhang HY, Wang XT, Hu JH, Wu XM. Biased gene retention during diploidization in Brassica linked to three-dimensional genome organization. Nat Plants. 2019;5(8):822–32.

    Article  PubMed  CAS  Google Scholar 

  33. Bhatia C, Oerum S, Bray J, Kavanagh KL, Shafqat N, Yue W, Oppermann U. Towards a systematic analysis of human short-chain dehydrogenases/reductases (SDR): Ligand identification and structure-activity relationships. Chem Biol Interact. 2015;234:114–25.

    Article  PubMed  CAS  Google Scholar 

  34. Zhang Y, Li C, Wang S, Yuan M, Li B, Niu L, Shi Q. Transcriptome and volatile compounds profiling analyses provide insights into the molecular mechanism underlying the floral fragrance of tree peony. Ind Crops Prod 2021, 162.

  35. Han Z, Liu Y, Deng X, Liu D, Liu Y, Hu Y, Yan Y. Genome-wide identification and expression analysis of expansin gene family in common wheat (Triticum aestivum L). BMC Genomics. 2019;20(1):101.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Gonzalez-Guzman M, Apostolova N, Belles JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodriguez PL. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell. 2002;14(8):1833–46.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Huijser C, Kortstee A, Pego J, Weisbeek P, Wisman E, Smeekens S. The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses. Plant J. 2000;23(5):577–85.

    Article  PubMed  CAS  Google Scholar 

  38. Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW. Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J. 2001;26(4):421–33.

    Article  PubMed  CAS  Google Scholar 

  39. Barreto LC, Herken DMD, Silva BMR, Munne-Bosch S, Garcia QS. ABA and GA(4) dynamic modulates secondary dormancy and germination in Syngonanthus Verticillatus seeds. Planta. 2020;251(4):86.

    Article  PubMed  CAS  Google Scholar 

  40. Gubler F, Millar AA, Jacobsen JV. Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol. 2005;8(2):183–7.

    Article  PubMed  CAS  Google Scholar 

  41. Huang Y, Song J, Hao Q, Mou C, Wu H, Zhang F, Zhu Z, Wang P, Ma T, Fu K et al. WEAK SEED DORMANCY 1, an aminotransferase protein, regulates seed dormancy in rice through the GA and ABA pathways. Plant Physiol Biochem 2023.

Download references

Funding

This work was supported by the Natural Science Foundation of Anhui Province of China (2208085QC84), the Natural Science Research project of Universities in Anhui Province of China (KJ2021A0198), the Open Project of Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, P. R. China (KF2021003) and the Special Fund for Anhui Agriculture Research System. The funding bodies had no role in study design, data collection and analysis, interpretation of data, decision to publish, or writing the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

K.J. Zhou and F.G Zhang conceived the study. F.G Zhang, T.H. Chen and K.J. Zhou designed the experiments. T.H. Chen, X.Z. Qianand H. Xu identified SDR members from Brassica napus genome. T.H. Chen, L. Wang, Q.A Cai, R. Li, performed the Bioinformatics analysis and data collection. T.H. Chen, N. Liu, X.Z. Hou, carried out the qRT-PCR analyses. F.G Zhang and T.H. Chen wrote the paper. Z.H. Zhu, W.Y. Zheng, Y. Yu participated in the modification of the manuscript. All the authors have read and approved the publication of the manuscript.

Corresponding author

Correspondence to Kejin Zhou.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, F., Chen, T., Liu, N. et al. Genome-wide characterization of SDR gene family and its potential role in seed dormancy of Brassica napus L.. BMC Plant Biol 24, 21 (2024). https://0-doi-org.brum.beds.ac.uk/10.1186/s12870-023-04700-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://0-doi-org.brum.beds.ac.uk/10.1186/s12870-023-04700-2

Keywords