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Transcriptome and WGCNA reveals the potential genetic basis of photoperiod-sensitive male sterility in soybean

BMC Genomics volume 26, Article number: 131 (2025) Cite this article

Abstract

Background

Soybean (Glycine max (L.) Merr.) is a crucial crop due to its high plant protein and oil content. Previous studies have shown that soybeans exhibit significant heterosis in terms of yield and protein content However, the practical application of soybean heterosis remains difficult, as the molecular mechanisms underlying photoperiod-sensitive genic male sterile (PGMS) is still unclear.

Results

This study characterized the PGMS line 88-428BY, which is sterile under short-day (SD) conditions and fertile under long-day (LD) conditions. To elucidate the genetic basis for this trait, we collected anthers, from 88-428BY under SD and LD conditions at three developmental stages, resulting in the identification of differentially expressed genes (DEGs) (2333, 2727 and 7282 DEGs, respectively) using Illumina transcriptome analysis. Using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway analyses, we fund that among the DEGs, enriched genes were associated with photoperiod stress, light stimulus, oxidation-reduction processes, multicellular organism development and protein phosphorylation. Additionally, weighted correlation network analysis identified four modules (blue, brown, red, and yellow) that were significantly correlated with PGMS, revealing co-expressed hub genes with potential regulatory roles. Functional annotation of 224 DEGs with|KME| >0.9 across the four modules in seven databases highlighted their involvement in light stimulus, oxidation-reduction processes, multicellular organism development, and protein phosphorylation, suggesting their importance in soybean PGMS. By integrating fertility-related genes previously identified by other studies with the DEGs from our analysis, we identified eight candidate genes associated with the photosensitive sterility in soybeans.

Conclusions

This study enhances the understanding of PGMS in soybean and establishes the genetic basis for a two-line hybrid seed production system in soybean.

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Introduction

Soybean is considered one of the most economically important leguminous crops due to its high plant protein and oil contents in the seed [1, 2]. Despite significant advancements in soybean breeding in recent decades, increasing yield remains challenging [1, 3]. Studies have shown that hybrid cultivars, which exhibit a 15–50% yield increase compared to inbred cultivars, can harness the heterosis present in soybean [4]. Heterosis, a phenomenon successfully utilized in maize, rice, sorghum, rapeseed and sunflower, is recognized as an effective method to increase crop yields [5,6,7]. However, the application of heterosis in soybean has been limited by factors such as natural outcrossing and a narrow genetic background in male-sterile lines and restorers [8, 9].

Selecting a male sterility (MS) system is a crucial step in hybrid seed production, as it forms the basis for crop heterosis and the identification of sterile genes [10,11,12,13,14]. There are three types of male sterility (MS): genetic or nuclear male sterility (GMS/NMS), cytoplasmic male sterility (CMS), and cytoplasmic genetic male sterility (CGMS) [15]. Approximately 50 cm and 30 N/GMS lines/mutants have been identified in soybean [7, 10, 12,13,14, 16,17,18,19]. GMS systems include structural MS, partially MS, and photosensitive MS, and CMS is primarily utilized in three-line breeding systems, with each line only being viable in specific soybean planting regions. Matched lines are selected from a large number of germplasm resources, especially an abundance of restorers lines for CMS [19, 20]. Inefficient maintenance of pure MS lines has hindered the application of GMS in soybean hybrid seed production. Among GMS, environment-sensitive genic male sterility (EGMS) has shown promise in two-line hybrids compared to three-line hybrids developed from the CMS system [20]. EGMS lines exhibit male sterility induced by specific environmental factors, such as temperature and day length [7, 19]. Understanding its genetic basis and effectively utilizing these genetic tools can accelerate two-line hybrid seed production heterosis in soybean.

In soybean, the first identified EGMS line was MS3, which exhibits male sterility influenced by photoperiod. A recent study revealed that MS3 encodes a homeodomain-finger protein, with natural variations in ms3, leading to pre-termination and loss of the PHD-finger domain [20]. Another EGMS line, 88-428BY, also displayed male sterility induced by photoperiod [21]. To determine the molecular mechanisms and gene networks underlying male sterility in 88-428BY, RNA sequencing (RNA-seq) analysis was conducted to examine the genome-wide expression patterns of relevant genes at three stages of anther development [22] under short-day (SD) and long-day (LD) conditions. Differentially expressed genes (DEGs) in response to photoperiod and light stimulus, oxidation-reduction processes, multicellular organism development and protein phosphorylation were identified. DEGs involved in the chlorophyll metabolization as well as toxicological, forming interactive networks, were also detected using weighted gene co-expression network analysis (WGCNA). The findings of this study enhance our understanding of photoperiod-sensitive genic male sterility in soybean.

Materials and methods

Plant materials and different day-length treatments

Soybean seeds of 88-428BY were provided by Baoguo Wei [21]. Seeds of 88-428BY were cultivated in an experimental field in Taiyuan, and designated as 88-428BY (LD: 14.5–15.0 h light). SD (12 h light/12 h dark) treatments were performed in Taiyuan using a black shading cloth. The 88-428BY seedlings were cultured under SD treatment for 20 days, following which the shade cloth were removed. The SD experiments were also conducted in a paddy field at Sanya, between 2005 and 2022, with an average light duration of 11 h, 5 min, and 30 s during November and December, to validate the PGMS phenotype of 88-428BY.

Phenotype characterization

Plants were photographed using a Nikon D7100 digital camera (Japan). To analyze pollen fertility, anthers were collected from three flower buds (1 day before flowering) per plant and stored in 70% alcohol. Pollen grains and mature pollen were dyed using a 1% potassium iodide solution (I2-KI) and observed under an OLYMPUS CX33 microscope (Japan) to assess the fertility of mature pollen.

Sampling and RNA extraction

Anthers at development stage 4 (S4), stage 8 (S8) and stage 12 (S12) were sampled in soybean 88-428BY (LD) and 88-428BY (SD) and immediately flash-frozen in liquid nitrogen before being stored at −80℃ for further analysis. Ten individual plants were sampled at each stage. Total RNA was extracted using an RNA isolation kit (Tiangen, China), following the manufacturer’s instructions. The RNA quality was evaluated using a Bioanalyzer 2100 (Aligent, USA).

RNA sequencing and data analysis

Illumina Novaseq™ 6000 (LC-BIO, Hangzhou, Zhejiang, China) was utilized for paired-end sequencing of approximately 10 µg of total RNA, obtained from three biological replicates following a standard protocol. A total of 18 cDNA libraries (comprising three biological replicates from three anther stages under both LD and SD conditions) were generated, yielding 150 bp paired-end reads with an average of 45 million raw data points per sample. Sequence quality assessment was conducted using a standard protocol [23]. Raw reads were filtered using Cutadapt to obtain high quality clean reads [24]. The clean reads were subsequently aligned to the reference genome (Glyma.Wm82. a2. v1) using HISAT2.2.4 [25]. The fragments per kilobase of exon model per million mapped reads (FPKM) value was calculated to quantify the gene expression levels [26]. Genes meeting stringent criteria (|log2foldchange|≥2, p < 0.05) were identified as DEGs using edgeR software [27]. These DEGs were then anlyzed to identify their gene ontology (GO) terms and kyoto encyclopedia of genes and genomes (KEGG) pathways, revealing their enriched biological processes and metabolic pathways.

Weighted gene co-expression network analysis and candidate genes related to GMS

This study utilized the WGCNA package in R software (version 4.1.2) to construct gene co-expression networks [28]. The core DEGs were grouped into 16 modules using the WGCNA package in R, and the PGMS for each module was calculated. To determine the correlation between the module and PGMS, an association coefficient was calculated following the method outlined by Chen et al. [29]. A total of 28 genes from plants with known functions related to environment-sensitive genic, male sterility were identified from the NCBI website (https://www.ncbi.nlm.nih.gov/).

Validation of gene expression by qRT-PCR

Total RNA was extracted and followed by reverse transcription using the PrimeScriptTMRT reagent kit (TaKaRa, Japan). The resulting first-strand cDNA was then amplified in accordance with the instructions provided for RealMasterMix (SYBR Green, TIANGEN). The relative expression levels of 10 DEGs across tissues and treatments were determined using the 2−ΔΔCt method [30]. GmActin11(accession number: LOC100781831)was selected as the reference gene to assess the template load [31]. The experiment was conducted with three dependent biological replicates. The primers were designed using Primer 3 software (Table S1).

Results

Phenotype of photoperiod-sensitive genic male sterility line 88-428BY

When exposed to a photoperiod of 14.5–15.0 h (LD), soybean 88-428BY exhibited normal plant height and pollen grain fertility (Fig. 1a, c, e and f). In contrast, under a 12.0–13.0 h (SD) condition, the plants exhibited dwarfism, with less smaller flowers and complete male sterility (Fig. 1b, d, g and h). The consistent observations from 1998 to 2022 indicate that the photoperiod plays a pivotal role in regulating male sterility in 88-428BY.

Fig. 1
figure 1

Comparison of the phenotypes of 88-428BY under long day (LD) and short day (SD) conditions. a, b Whole plants at the flowering stage. c, d Bud phenotype at three anther development stages: 4, 8 and 12. e, g Buds with the petals and sepals removed. f, h Pollen grains stained with I 2 -KI. (Scale bar: a,b = 5 cm; c,d, e and g = 2 cm; f, h = 100 μm.)

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Experiments with varying day lengths (12.5 h, 13.5 h, 15.0 h) and temperatures (24 °C and 32 °C) were conducted to determine whether the fertility phenotype of 88-428BY was specifically caused by photoperiod. As shown in Fig. 2, pollen from 88-428BY plants grown under 12.5 and 13.5 h photoperiods exhibited complete male sterility at both 24 and 32 °C, whereas plants grown under 15.0 /9.0 h photoperiod produced fertile pollen (Fig. 2e, f). These results confirm that the fertility of 88-428BY is predominantly controlled by photoperiod rather than temperature, aligning with previous research findings [21].

Fig. 2
figure 2

I 2 -KI stained pollen grains of 88-428BY grown under different temperature and photoperiods in a growth room. (Scale bars: 100)

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Analysis of the global transcriptome between samples

To investigate the molecular mechanism of male sterility in 88-428BY, transcriptome analysis was conducted at three stages of anther development under SD and LD conditions. Flower buds of 88-428BY at stages 4, 8, 12 were labeled as LD-S4, LD-S8, LD-S12, SD-S4, SD-S8, and SD-S12, depending on the photoperiod treatment. Illumina Novaseqâ„¢ 6000 sequencing generated approximately 830 million reads, with an average of 46 million reads per sample, a Q30 base ratio of over 98%, and GC content of about 42% (Table 1). Nearly 96% of valid data were mapped to the reference genome (Glyma.Wm82. a2. v1), with approximately 83% of these reads located at unique chromosomal positions (Table S2).

Table 1 Statistics of RNA-Seq results and corresponding quality control information of all samples
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Principal component analysis (PCA) was conducted using the FPKM values, and samples were separated into 6 distinct groups along with their replicates (Fig. 3a). Samples from LD_S4, SD_S4, and SD_S8 clustered on the negative side of the x-axis, while LD_S12 was positioned on the positive side of the x-axis. On the other side, samples from SD_S12 and SD_S8 were located on the positive side of the y-axis, whereas LD_S4 and SD_S8 were on the negative side of the y-axis. Except for LD_S4 and SD_S4, which were on the same side of the lactated axis, samples from other stages under LD or SD conditions were distributed across different axes. PCA, further revealed that a significant proportion of the variation (38.89%), was explained by two principal components (PC1: 24.76%, PC2: 14.13%) (Fig. 3b).

Fig. 3
figure 3

a Pearson’s correlation co-efficient analysis (PCC) and (b) principal component analysis (PCA)

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The median expression of all genes in the samples studied, was relatively stable, with minor variations, except for a decline in LD-S12 and SD-S12 (Fig. S1). Analysis of whole-genome FPKMs showed that the sample from the S4 and S8 stages had higher values compared to those from the S12 stage (Fig. S2). The Pearson’s correlation coefficient (PCC) was used to confirm the association with RNA-seq data, revealing a significant positive correlation (≥ 0.97) among the 3 replicates of each sample. There was a relatively high correlation between the other samples (≥ 0.74), except for LD-S12. PCA showed that samples from the S12 stage under two different conditions clustered together but with a greater distance compared to the other samples. These results were consistent with PCC analysis, suggesting that the 88-428BY genotype exhibited high gene expression similarity during the S4 and S8 stages under LD/SD treatments, which may be linked to anther development.

Comparative analysis of differentially expressed genes during anther development under different photoperiod conditions

To identify DEGs across various treatments and anther developmental stages, a comparative analysis was conducted under LD and SD conditions at three distinct stages. The number of DEGs identified varied from 2,011 (comparing SD-S8 to SD-S12) to 10,028 (comparing LD-S4 to LD-S12) (Fig. 4). Interestingly, DEGs, were more abundant at stage 12 than at stages 4 and 8 under both LD and SD conditions. GO analysis was utilized to categorize the DEGs into biological processes, cellular components, and molecular functions (Fig. 5a, Table S3-S5). The comparison of treatments revealed that DEGs were associated with various GO terms, such as transcription regulation process, oxidation-reduction process, multicellular organism development, response to light stimulus, and protein phosphorylation. KEGG enrichment analysis shed light on the pathways enriched with DEGs. The DEGs were found to be enriched in common pathways across the three different anther development stages between 88-428BY under SD and LD conditions. These pathways included plant hormone signal transduction (KO04075), plant-pathogen interaction (KO04626), pentose and glucuronate interconversions (KO00040), MAPK signaling pathway (KO04016), phenylpropanoid biosynthesis (KO00940), galactose metabolism (KO00052), starch and sucrose metabolism (KO00500), glycerolipid metabolism (KO00561), flavonoid biosynthesis (KO00941), and ABC transporters (KO02010) (Fig. 5b).

Fig. 4
figure 4

Up- and down-regulated DEGs between LD and SD at three anther developmental stages

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Fig. 5
figure 5

a Gene Ontology and (b) Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses of all DEGs

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Co-expression network analysis reveals candidate genes regulating photosensitive sterility in soybean

To identify highly associated genes in 88-428BY, we utilized WGCNA with a soft threshold power of 20 to construct a gene co-expression network (Fig. S3). A total of 17 co-expression modules were generated and visualized in a clustergram with distinct colors (Fig. 6a and Fig. S4). The network heatmap, which exhibited topological associations between the identified modules, shows lighter blue colors representing low association and darker red colors indicating strong association. By examining the correlation of eigengenes, we identified three clusters with strong interactions: modules brown and green, blue and red, and black and yellow (Fig. 6b).

Fig. 6
figure 6

WGCNA of high-variance DEGs in 88-428BY at different anther developmental stages. a Cluster dendrogram and network heatmap plot. b Module-sample associations based on Pearson correlations. The color key indicates r 2 values from − 1 to 1 in a gradient from blue to red

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The brown, blue, red, and yellow modules showed significant correlations with the PGMS phenotype (r = 0.58, 0.64, 0.72 and 0.87) in soybean (Fig. 7), indicating that genes within these modules have a positive regulatory effect on PGMS. A total of 244 genes were identified as hub genes in these four modules, based on the criterion of |KME|>0.9. The brown, blue, red, and yellow modules were composed 84, 97, 12, and 33 DEGs, respectively (Table S6). Functional annotation of 224 DEGs (|KME|>0.9) in the four modules was performed using seven databases (Fig. 8). Several DEGs were associated with light stimulus, oxidation-reduction processes, multicellular organism development, and protein phosphorylation, suggesting their importance in the photosensitive sterility process in soybean.

Fig. 7
figure 7

Module-trait relationships plots. The numbers represent the Pearson’s correlation coefficients, with positive correlations in red and negative correlations in blue

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Fig. 8
figure 8

Integration of candidate genes for GMS on the soybean reference genome. The Circos program was used to draw different features in concentric circles, including:â‘  20 soybean chromosomes, â‘¡ 224 genes in the four modules, different colors represent different modules, and â‘¢ 5 cloned genes

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Among the identified genes, Glyma.08G250800 and Glyma.10G240900 encode MADS-box transcription factors. Previous research has highlighted the significant roles of MADS-box transcription factors, such as GmNMH7 and GmMADS28, in reproductive development and plant fertility [32, 33]. The Glyma.19G219000 encodes a MYB2 transcription factor that regulates plant mortality and senescence by inhibiting cytokinin production, leading to less apical meristem under environmental stress and a shortened vegetative stage [34, 35].

Furthermore, 10 hub genes were selected to validate the reliability of the DEGs identified from RNA-seq data. qRT-PCR analysis was conducted to assess gene expression levels at the different anther development stages under two treatments. Figure 9 illustrates that these 10 genes exhibited a consistent trend with the result of RNA-seq. Thus, our study confirms the relevance of the identified hub genes in the soybean response to day-length treatment.

Fig. 9
figure 9

Validation of 10 DEGs by qRT-PCR. The FPKM values of RNA-seq were compared with the relative expression level determined by qRT-PCR. The qRT-PCR results represent the mean ± standard error of the three replicates

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Selection of photoperiod-sensitive genic male sterile candidate genes

A total of 28 cloned genes associated with male sterility in various crops have been identified in the previous studies (Table S7) [12, 18, 20, 36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53]. Among these, 20 genes were found to be expressed in the transcriptome (Table S8). The expression levels of 5 genes exhibited significant differences between LD and SD conditions (Fig. 10), namely cas, CalS5, res3, ms1, and ms6, which validated the reliability of the transcriptome sequencing data in this study. These genes showed significant differences in the transcriptome of the soybean line 88-428BY, suggesting their involvement in the regulation of male sterility in soybeans. The observed variations in gene expression levels may influence the genetic control of male fertility through diverse molecular mechanisms. These findings imply a possible link between the expression of these genes and the development of male sterility in the specific soybean line under study. Investigating the functions of these genes and their regulatory mechanisms may shed light on the genetic basis of male sterility and its manipulation in soybean breeding programs.

Fig. 10
figure 10

FPKM values of five reported genes in RNA-seq

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Discussion

Circadian rhythms and light signals play a crucial role as a key environmental factors in plant growth and development. Plants sense day-length signals to regulate their physiological and developmental responses [54,55,56]. Soybean was the first plant studied for its photoperiod response. It is a classic short day-length plant that is sensitive to day-length, and that is unable to flower when exposed to sunlight beyond a certain threshold. This can lead to photoperiod stress, affecting the flowering, maturity and other biological processes of soybean [57,58,59]. Despite this, there are limited reports on natural variation in soybean sensitivity to photoperiods leading to nuclear sterility. The soybean MS3 gene has been successfully identified and cloned, playing a key role in controlling photoperiod-sensitive genic male sterility [20]. In this study, high-throughput RNA-seq and WGCNA were applied to identify pathways and candidate genes associated with photoperiod sensitivity in another soybean genic male sterile line 88-428BY [21]. A total of 224 core DEGs were identified in pathways responsive to photoperiod stress (Table S6, Fig. 8). GO and KEGG enrichment analysis of these core DEGs revealed involvement in biological processes and pathways related to transcription factors, protein binding, MAPK signaling, starch and sucrose metabolism pathways (Figs. 5 and 6).

The MYB and MADS-box family members were found to play important roles in various plant biological processes including plant growth, development, and abiotic stresses response [60,61,62,63]. Specifically, MYB proteins, including AtMYB2, AID1, and OSMYOXIB, have been highlighted for their roles in anther development and plant growth under photoperiod stress [64,65,66]. The MYB transcription factor Glyma.19G219000 showed significant differential expression during soybean anther development under photoperiod stress. MADS-box family members have been implicated in regulating flowering and maintaining floral organ identity, with studies in rice demonstrating that mutations in these genes, lead to male sterility. GmMADS28 has been identified as a causative factor for male sterility in soybean [61,62,63]. This study identified expression variation in the MADS-box transcription factor gene, Glyma.10G240900, under different day-length conditions.

CSA shared homology with the Glyma.01G049600 located on chromosome 01, showing a similarity of 71.5%. Glyma.01G049600 demonstrated higher expression levels under LD conditions than under SD conditions, with its expression decreasing as anther development progressed. This expression pattern suggests that Glyma.01G049600 is involved in anther development, potentially playing a role in the early stages of this process. The decline in expression during anther maturation indicates that its function is most crucial during the initial phases of development, after which its significance diminishes as the anther matures. This expression profile is indicative of genes, initiating or regulating developmental pathways in anthers. Previous research has revealed that CSA encodes an R2R3 MYB-type transcription factor and is vital in directing sugar allocation from source tissues, where photosynthesis takes place, to the developing anthers, which act as the sink tissues. Mutations in this gene may lead to male sterility in rice plants under short-day (SD) conditions; however, male fertility can be restored under long-day (LD) conditions [43].

The CalS5 gene shared 76.3% similarity with Glyma.04G213100 located on soybean chromosome 04. Glyma.04G213100 exhibited differential expression between LD and SD conditions, with peak expression levels observed in the LD-S12 stage and relatively low or no expression in other developmental stages. This expression pattern indicates that the gene’s function is primarily active during the anther maturation phase. The hypothesis that its function may be associated with pollen viability is supported by its peak expression, which coincided with a crucial period in anther development when pollen maturity was determined. The function of the CalS5 gene is directly linked to male fertility in Arabidopsis thaliana, as the cals5-2 mutant exhibits male sterility under normal conditions, but it can regain fertility under permissive conditions, such as low temperature or SD photoperiod [42]. The res3 gene has been shown to restore fertility in various known P/TGMS lines with pollen wall formation defects [37], and it is homologous to the soybean gene Glyma.09G233700, sharing a 49.4% similarity. Glyma.09G233700 exhibited significantly lower expression levels in SD conditions compared to LD conditions, and its expression gradually decreases as anther development progresses. This expression pattern suggests that Glyma.09G233700 plays a crucial role in anther development, particularly during the early stages of anther growth under LD conditions.

MS1 (Glyma.13G114200) and MS6 (Glyma.13G066600) were identified, and their functions wrer linked to male sterility in soybean. MS1 expression was notably higher under SD than under LD conditions, and its expression gradually decreased as the anthers developed. Previous research generated ms1 mutant through CRISPR/Cas-mediated gene editing, exhibiting a complete male-sterile phenotype [18]. This highlights the crucial role of MS1 in soybean male fertility. The expression pattern of MS6 mirrored that of MS1, with MS6 exhibiting higher expression levels under LD conditions than under SD conditions. Previous studies have indicated that MS6, which was highly expressed in anthers, encodes an R2R3 MYB transcription factor known as GmTDF1-1 [10]. This transcription factor is homologous to Tapetal Development and Function 1 (TDF1), a key factor in anther development identified in Arabidopsis and rice. The homology and role of MS6 suggest its involvement in regulatory pathways crucial for anther and pollen development in soybean.

Overall, these results offer valuable insights into the cloning of the mutated allele of PGMS in 88-428BY and its potential application in enhancing soybean heterosis.

Conclusions

This study identified soybean 88-428BY, which exchibited the PGMS trait. RNA-seq, WGCNA and qRT-PCR were employed to uncover the genes associated with PGMS in 88-428BY under photoperiod stress. Eight candidate genes demonstrated a strong correlation with PGMS in soybean, enhancing our understanding of its genetic foundation and paving the way for future functional validation studies. This research establishes a genetic basis for developing new photoperiod-sensitive nuclear sterile materials in soybean, further utilization of these candidate genes in soybean breeding would provide important gene materials for hybrid soybean varieties cultivation.

Data availability

The original transcriptome sequence data in this publication have been submitted to the National Center for Biotechnology Information under accession number CRA017761.

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Acknowledgements

The authors would like to acknowledge Professor Baoguo Wei for providing the soybean resource 88-428BY used in this study.

Funding

This work was supported by the Major Science and Technology Special Program of Shanxi Province (No.202201140601025), the Natural Science Foundation of Shanxi Province (No.202303021211085), the Science and Technology Innovation Project of Colleges and Universities in Shanxi Province (No. 2021L091), the National Agricultural Science and Technology Major Projects (No.NK202308010403), the China Postdoctoral Science Foundation, Young Scholars of Shanxi Province (No.20210302124152), the Central Guide Local Science and Technology Development Special Project Fund (No.YDZJSX2022C020), and the Modern Agro-industry Technology Research System, Science and Technology Innovation Young Talent Team of Shanxi Province (No.202204051001020).

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Authors and Affiliations

  1. Center of Agricultural Genetic Resources Research, Shanxi Agricultural University, Taiyuan, Shanxi, 030031, China

    Yuhua Yang, Lihong Xu, Minggui Wang, Shuichun Chen, Zhiyuan Bai, Haiping Zhang & Ruijun Zhang

  2. Houji laboratory in Shanxi Province, Shanxi Agricultural University, Taiyuan, Shanxi, 030031, China

    Yuhua Yang, Suqin He, Bo Zhao & Lixiang Wang

  3. College of Agricultural, Shanxi Agricultural University, Taigu, 030801, China

    Suqin He, Lihong Xu, Minggui Wang, Shuichun Chen, Tingting Yang, Bo Zhao & Lixiang Wang

  4. Institute of Bast Fiber Crops, Chinese Academy of Agricultural Sciences, Changsha, 410205, China

    Jiangjiang Zhang

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Contributions

J.Z. and Y.Y. conceived and designed research; S.H., L.X., M.W., Z.B. and B.W. performed the sample collection; Y.Y., J.Z., T.Y., B.Z., H.Z., S.C. and R.Z. collected and analyzed the data; L.W. and Y.Y. wrote the manuscript. All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Yuhua Yang, Jiangjiang Zhang or Ruijun Zhang.

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This article does not contain any studies with human participants or animals.

The collection materials of the plants, complies the relevant institutional, national, and international guidelines and legislation.

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The authors declare no competing interests.

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Supplementary Information

Supplementary Material 1. Fig. S1. Boxplot for FPKM values of all samples.

Supplementary Material 2. Fig. S2. Kernel plot of the overall expression density.

12864_2025_11314_MOESM3_ESM.tif

Supplementary Material 3. Fig. S3. Analysis of network topology for different soft–thresholding powers of 88-428BY in different samples. The x-axis represents the soft-thresholding power. The y-axis represents the scale-free topology model fit index (a) and the mean connectivity (b).

Supplementary Material 4. Fig. S4. Dendrogram of co-expression modules identified by WGCNA.

Supplementary Material 5. Table S1. Makers for qRT-PCR and their related information.

Supplementary Material 6. Table S2.Reference genome comparison read statistics for all samples.

Supplementary Material 7. Table S3. Detailed subcategory GO enrichment analysis SD-S4 vs. LD-S4.

Supplementary Material 8. Table S4. Detailed subcategory GO enrichment analysis SD-S8 vs. LD-S8.

Supplementary Material 9. Table S5. Detailed subcategory GO enrichment analysis SD-S12 vs. LD-S12.

12864_2025_11314_MOESM10_ESM.xlsx

Supplementary Material 10. Table S6. A total of 244 genes were discovered and subsequently defined as hub genes in these four modules.

12864_2025_11314_MOESM11_ESM.xlsx

Supplementary Material 11. Table S7. The 28 cloned male sterility-related genes collected from crops in the reported studies.

Supplementary Material 12. Table S8. Expression of cloned genes in the transcriptome.

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Yang, Y., He, S., Xu, L. et al. Transcriptome and WGCNA reveals the potential genetic basis of photoperiod-sensitive male sterility in soybean. BMC Genomics 26, 131 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12864-025-11314-5

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Keywords

BMC Genomics

ISSN: 1471-2164

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