Comprehensive analysis of IDD family genes and their expression patterns in barley
Chengxin Yin, Junjuan Li, Wenxing Liu, Jianbin Zeng, Wujun Ma, Xue Feng
TL;DR
This study identifies and analyzes the HvIDD gene family in barley, revealing their potential roles in plant growth and stress response.
Contribution
The first comprehensive bioinformatics analysis of the HvIDD gene family in barley, including gene classification, motif identification, and miRNA interactions.
Findings
Thirteen HvIDD genes were identified and classified into three subfamilies.
Ten conserved motifs and various cis-acting elements in HvIDD promoters were discovered.
Six miRNAs were predicted to interact with HvIDD genes, which regulate genes involved in membrane-binding pathways.
Abstract
INDETERMINATE DOMAIN (IDD) is a unique C2H2 zinc finger protein subfamily in plants. It has been thoroughly studied in Arabidopsis and is widely involved in the growth and development of various plants and stress response. Following wheat, maize and rice, barley stands as the fourth major cereal crop. In contrast, there are limited studies on the IDD gene family in Hordeum vulgare. Therefore, this study comprehensively identified and analyzed the barley IDD gene family by bioinformatics methods. A total of 13 HvIDD family genes were detected and classified into three subfamilies. Ten conserved motifs were identified by motif analysis. Through chromosome localization analysis, 13 HvIDD genes were found to be located on multiple chromosomes, of which 4 HvIDDs were found on chromosomes 3 and 4, respectively. In addition, analysis of cis-acting element in promoter revealed a variety of…
Genes, proteins, chemicals, diseases, species, mutations and cell lines named across the full text — each resolved to its canonical identifier and authoritative record.
Click any figure to enlarge with its caption.
Figure 10
Figure 11
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9- —Joint Funds of the National Natural Science Foundation of China
- —Natural Science Foundation of Shandong Province
- —Special Fund of Taishan Scholar Program
- —Young Talent of Lifting engineering for Science and Technology in Shandong, China
Peer Reviews
No public reviews on file for this paper yet. If you reviewed it on a platform where reviews are public (OpenReview, ICLR, NeurIPS, ICML), you can paste yours below so the community can read it here.
Videos
No videos yet. Explain this paper in a talk, walkthrough, or lecture? Add one.
Taxonomy
TopicsPlant Molecular Biology Research · Plant Gene Expression Analysis · Plant responses to water stress
Introduction
In the regulation of gene expression, transcription factors are indispensable components that exert profound impacts on plant growth, development, and adaptive responses to environmental stresses [1, 2]. Through sequence-specific DNA binding, these factors modulate gene transcription, thereby influencing various physiological processes in plants [3, 4]. Among the diverse families of transcription factors in plants, the bZIP (basic leucine zipper) family is known for its role in seed maturation and inflorescence development [5–8]. The AP2/EREBP (APETALA 2/ethylene response element binding protein) family integrates signals to regulate both stress responses and developmental processes [9, 10]. The MYB family centrally directs development and metabolism, while also mediating plant adaptation to abiotic stresses [11–16]. And the WRKY family ranks among the largest transcription factor families in plants, it is widely involved in the regulation of various signaling pathways, as well as seed dormancy and germination [17–19]. Overall, these families have a close association with plant growth and development, environmental adaptation, and gene or genome duplication events.
The INDETERMINATE DOMAIN (IDD) transcription factors are a plant-specific C2H2 (Cys2His2 zinc finger) protein subfamily, exclusively found in land plants [20, 21]. IDD family members play vital roles in multiple developmental processes in plants, including root development, nitrogen metabolism, flowering time regulation, seed development, and germination [2, 22–25]. In Arabidopsis, IDD family members are involved in multiple developmental pathways. For instance, AtIDD14 regulates starch metabolism and cold response in Arabidopsis. Under cold stress, AtIDD14β inhibits the activity of AtIDD14α, thereby modulating starch accumulation [24]. The first identified member of the IDD family is the ID1 gene in maize, which is associated with flowering time regulation, as its mutation effectuates a late-flowering phenotype [26]. Additionally, IDD genes are crucial for endosperm development in maize [27, 28]. In rice, studies on mutant and overexpression lines have elucidated that IDD10 directly binds to and activates the AMT1;2 and GDH2 genes, regulating ammonium-dependent gene expression and affecting root growth and nitrogen metabolism [29, 30]. This research point to a pivotal role for the IDD family in regulating growth, development, and environmental adaptation.
Although research on the IDD family has made some progress in other crops, studies in barley are still relatively limited. Here, the IDD gene family was identified through bioinformatics approaches in barley and analyzed their conserved protein motifs, gene structures, chromosomal distribution, evolutionary relationships, cis-element, and GO (Gene Ontology) enrichment. Additionally, the expression patterns of these genes were examined across a range of developmental stages and stress conditions. These analyses provide valuable references for further functional studies of the HvIDD gene family.
Materials and methods
Identification of HvIDD genes
To identify the HvIDD proteins, we performed BLASTP alignments using AtIDDs, OsIDDs, and ZmIDDs. We used the Hordeum vulgare (MorexV3_pseudomolecules_assembly) database from Ensemble Plants (http://plants.ensembl.org) to retrieve the IDD family genes and protein sequences [31]. We selected the longest transcript for each gene and excluded the incomplete sequences which lack start and stop codons. Additionally, to verify the authenticity of the sequences, we referenced data from SMART [32]. On the basis of the chromosomal positions, the 13 genes were detected and named HvIDD1 to HvIDD13.
Phylogenic analysis of HvIDDs
We conducted a phylogenetic analysis to classify HvIDDs by aligning 13 unique HvIDD amino acid sequences with IDDs from Arabidopsis, rice and maize. Sequence alignment was performed using ClustalW with default settings, and MEGA 7.0 was used to construct a phylogenetic tree by the neighbor-joining (NJ) method with the Poisson model, pairwise deletion, and 1,000 bootstrap replicates [33, 34]. Phylogenetic relationships were visualized using iTOL (https://itol.embl.de/) [35].
Chromosome distribution and gene collinearity analysis
Circos was employed to map the positions of HvIDD genes on barley chromosomes [36]. Collinearity analysis of orthologous IDD genes between barley and wheat, as well as maize, was performed using MCScanX [37]. The ParaAT tool served to compute the the non-synonymous (Ka) and synonymous (Ks) substitution rates of HvIDD genes, and the Ka/Ks ratio was subsequently determined using Calculator 2.0. Additionally, gene duplication time was estimated using Ks/2, with a substitution rate of 1.5 × 10⁸ per year [38].
Gene structure analysis
The Gene Structure Display Server (GSDS) tool (http://gsds.cbi.pku.edu.cn/) was used to analysis the exon and intron structure of HvIDD genes [39]. Conserved motifs were examined via the MEME program utilizing default settings and subsequently annotated by referencing the InterProScan database (http://www.ebi.ac.uk/Tools/pfa/iprscan/) [40, 41]. We employed TBtools to visualize the structures of genes and their associated motifs [42]. The Swiss-Model (https://swissmodel.expasy.org/) was used to forecast the three-dimensional structures of HvIDD proteins, with the structure assessment conducted via the SAVES server [43].
Cis-Elements analysis of HvIDDs
We selected a 1500 bp sequence upstream of the transcription start site of the barley IDD genes to study the cis-elements in their promoter regions, utilizing the PlantCARE software (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) [44]. Additionally, TBtools was employed for the annotation and visualization of their promoter regions.
The regulation network analysis of miRNA-HvIDD
We used the psRNATarget server with default parameters to predict miRNAs that may modulate the expression of HvIDD genes, and then utilized Cytoscape V3.8.2 software to visualize these interactions [45].
Gene expression patterns of HvIDDs
The analysis were performed through the barley expression database (BarleyExpDB: The Barley Expression Database) [46]. Using the Fragments Per Kilobase of transcript per Million mapped reads (FPKM) method, we confirmed the expression levels. For visualizing the level of gene expression, we constructed a heatmap with TBtools software. According to [47], quantitative real-time PCR (qRT-PCR) was performed by a QuantStudio3 PCR system (Thermo, USA). First-strand cDNA synthesis was performed using the PrimeSciptTM RT reagent Kit (Takara, Japan), followed by qRT-PCR using a SYBR Green Supermix (Takara, Japan) with HvActin as a reference. The program included an initial step at 95 ℃ for 30 s, followed by 40 cycles of 95 ℃ for 15 s, 60 ℃ for 30 s, and 72 ℃ for 10 s [48]. We used cultivated barley GP and wild barley XZ5 as the experimental material. All the testing barley seeds were harvested in the summer of 2023 at the Jiaozhou Experimental Station, Qingdao Agricultural University, Jiaozhou, Shandong, China. The seedlings were exposed to drought and salt stress treatments with 25% PEG6000 and 100mM NaCl, respectively. Sampling roots and leaves at 0 h and 24 h treatment. Experiments were replicated three times with 2^−ΔΔCt^ relative quantification method. The primers were given in Table S15.
Statistical analysis
Statistical analyses were performed with the DPS (Data Processing System) software. For significance testing, an Analysis of Variance (ANOVA) was performed, succeeded by Duncan’s Multiple Range Test. We considered the results significant at a P-value threshold of less than 0.05.
Results
Characterization of the barley IDD gene family
Here, we characterized a total of 13 HvIDD genes. Table S1 presents the basic information of these genes including gene names, gene IDs, chromosomal locations, protein amino acid lengths, molecular weights and isoelectric points. The proteins were found to be 391–868 residues in length and 43.3–94.9 kDa in molecular weights. The detailed sequences of genes and proteins are presented in Table S2. To illustrate the evolutionary relationships of the IDD genes, a phylogenetic tree was generated based on the neighbor-joining (NJ) method. By comparing 16 Arabidopsis, 14 rice, 22 maize and 13 barley IDDs, they were classified into three subfamilies. Subfamilies I, II, and III contain four, five and four HvIDDs, respectively (Fig. 1).
Fig. 1. Phylogenetic tree of HvIDD, AtIDD, OsIDD, ZmIDD proteins. Three colored arcuate lines represent different subfamilies of the IDD proteins. The phylogenetic tree was assembled based on the identification of 13 HvIDDs (denoted by squares) in barley, 16 AtIDDs (indicated by asterisks) in Arabidopsis, 14 OsIDDs (marked by circles) from rice, 22 ZmIDDs (represented by triangles) from maize. MEGA7 was utilized to build the unrooted phylogrnetic tree, based on full-length amino acid sequences, with bootstrapping set to 1000 cycles
Structure Analysis of the HvIDD Genes
The MEME tool was utilized and 10 evolutionarily preserved motifs named motif 1 to motif 10 were identified (Fig. 2A). Detailed information was listed in Table S4. According to the Fig. 2A, motifs 1, 2, and 3 were present in all HvIDDs. Motif 5 was absent in HvIDD7/8/11, and Motif 6 is absent in HvIDD8/11. These proteins, HvIDD7/8/11, were all classified into subfamily (I) Motif 4 and Motif 9 were exclusively present in HvIDD1, Motif 7 was only found in HvIDD2/13, and Motif 8 was restricted to HvIDD2/12/13. HvIDD1/2/12/13 are categorized into subfamily (II) The distribution of these distinct motifs reveals the differentiation between subfamilies and their unique functional characteristics. The widespread presence of Motif 5 and Motif 6 highlights their significance in the fundamental functions of the gene family.
Fig. 2. The structure of the conserved protein motifs and gene in the IDD genes from barley. (a) The motif composition of barley IDD proteins, with motifs 1–10 displayed in differently colored boxes, is detailed in Table S2, and the protein length can be estimated using the scale at the bottom with aa units. (b) The exon-intron structure of IDD genes in barley. Yellow boxes illustrate the exons; the green boxes present the untranslated regions and the introns are exhibited by the black lines
The GSDS web server was employed to determine the gene structure of HvIDDs. The results revealed an uneven distribution of 2 to 4 exons among HvIDDs (Fig. 2B). Additionally, we forecast the protein structures of HvIDD1, HvIDD3 and HvIDD6 (Fig. 3), which belong to subfamily II, subfamily III, and subfamily I, respectively. The protein predictions indicate significant structural variations among different IDD proteins.
Fig. 33D structure modeling of HvIDD proteins. The structural image was built by the PyMOL software
Chromosomal localization and duplication of HvIDD genes
Chromosomal distribution analysis demonstrated that all 13 HvIDD genes were successfully mapped to specific genomic loci on barley chromosomes, with the exception of chromosomes 1 and 7. One HvIDD was located on chromosome 6. Two HvIDDs were found on chromosomes 2 and 5, and four HvIDDs were identified on both chromosomes 3 and 4 (Fig. 4). Additionally, using BLAST and MCScanX methods, we detected a duplication event within the HvIDD genes: HvIDD2/HvIDD13 (Fig. 5). To elucidate the evolutionary constraints on their function, we estimated the Ks (synonymous substitution rate), Ka (non-synonymous substitution rate), Ka: Ks ratio, and divergence time for the paralogous IDD genes. We determined that the Ka: Ks ratio for segmentally duplicated HvIDD gene pairs was less than 1. These duplication events are estimated to have occurred approximately 30,400 years ago (Table S5). Furthermore, we performed a collinearity analysis between barley and wheat, as well as between barley and maize. This analysis identified 33 pairs of IDD gene orthologs between barley and wheat, along with 18 pairs between barley and maize (Fig. 6).
Fig. 4. Positions of 13 IDD genes on the barley chromosomes. In the figure, 1 H to 7 H represent the seven barley chromosomes, with black short lines indicating the IDD genes, including their name codes (to the right of the columns) and specific locations (to the left of the columns)
Fig. 5. Synteny analysis of HvIDD family in barley. The gray lines denote all collinear genes within the barley genome, while the red lines indicate duplicated gene pairs within the HvIDD gene family
Fig. 6. Synteny analysis of IDD genes in barley, wheat and maize. Gray lines in the background indicate the collinear blocks within barley and other plant genomes, while the red lines highlight the syntenic gene pairs. The specie names with the prefixes, Ta, Zm and Hv indicate wheat, maize and barley respectively
Cis-elements Analysis of HvIDDs promoters
We analyzed a variety of cis-acting elements in the promoters of 13 HvIDD genes, including the O2-site (a cis-acting regulatory element involved in zein metabolism regulation), TGA-element (auxin-responsive element), MRE (MYB binding site involved in light responsiveness), ARE (a cis-acting regulatory element essential for anaerobic induction) and LTR (low-temperature response element). These elements are involved in the regulation of gene expression during physiological activities such as protein metabolism, anaerobic induction, and low-temperature responses (Table S8). Overall, nine HvIDDs (69%) carried the ARE element, seven HvIDDs (54%) carried both the TGA-element and TCA-element, and six HvIDDs carried the CCAAT-box. Five HvIDDs had the O2-site, CAT-box, TC-rich repeats and RY-element. Four HvIDDs possessed the MBS and GCN4-motif. Additionally, one HvIDD had the MRE, MBSI, MSA-like ACE, Circadian, WUN-motif and AuxRR-core (Fig. 7).
Fig. 7. Predicted of cis-regulatory elements in HvIDD promoters. The 1.5-kb region upstream of the translational start codon (ATG) of 13 barley HvIDD genes was submitted to PlantCARE. Identified elements are indicated by colored symbols; their approximate distance to the translation initiation site can be estimated with the scale bar at the bottom
Expression pattern analysis of HvIDDs
Transcriptome analysis revealed distinct expression patterns of the HvIDD gene family across developmental stages and abiotic stress conditions (Tables S8, S9). Based on developmental regulation, the 13 genes were categorized into three groups. Group 1 contained HvIDD4,* 6* and 10, which exhibited consistently low expression across all tissues. Group 2 included HvIDD7,* 8*,* 9* and 11, which showed low basal expression but were upregulated at specific stages. For example, HvIDD7 showed high expression during early caryopsis development (5 DPA), HvIDD9 showed high expression in 1–1.5 cm inflorescences (INF2), and HvIDD11 exhibited high expression in stage III floral buds. Group 3 contained HvIDD1,* 3* and 13, which maintained high expression across all 16 tested tissues. Notably, the expression pattern of HvIDD2 was peaked during grain quality formation (15 DPA caryopses) but was silenced in stage III floral buds. Similarly, HvIDD5 was silenced in senescent leaves yet highly expressed in floral buds, while HvIDD12 remained inactive during floral organ development (5–6 weeks) but was activated in 15 DPA caryopses and senescent leaves (Fig. 8).
Fig. 8. Heatmap illustrates the expression levels of HvIDD genes across different tissues. The gene names listed on the right and a phylogenetic tree constructed based on full-length protein sequences on the left. The 16 tissues are arranged at the bottom of the figure. The color scale indicates relative expression levels ranging from high (red) to low (blue), with the expression data normalized using the log2 method. The 16 tissues are as follows: EMB, Embryo (germinating); ROO, Root (10cmseedlings); LEA, Shoot(10cmseedlings); INF1, Inflorescence (0.5 cm); INF2, Inflorescence (1–1.5 cm); NOD, Tillers (3rd internode); CAR5, Grain (5 DPA); CAR15, Grain (15 DPA); ETI, Etiolated (10 day seedlings); LEM, Lemma (6 weeks p.a.); LOD, Lodicule (6 weeks p.a.); PAL, Palea (6 weeks p.a.); EPI, Epidermis (4 weeks); RAC, Rachis (5 weeks p.a.); ROO2, Root (4 week seedling); SEN, Senescing leaf (2 months)
Under abiotic stress conditions, drought stress consistently induced the up-regulation of all 13 genes in both root and leaf tissues. Heat stress specifically triggered a twofold increase in HvIDD6 expression in roots. In response to salt stress, gene expression patterns in leaves varied significantly. HvIDD11 was markedly down-regulated (~ 5-fold), whereas HvIDD9 exhibited sustained up-regulation. Notably, HvIDD9 responded positively to both drought and salt stresses, whereas HvIDD11 displayed contrasting regulatory patterns under these two stress conditions (Fig. 9). The results of RT-PCR further validated the expression pattern of HvIDD gene family in response to salt and drought stress. According to Fig. 10, the expression trends of the four genes under salt and drought stress are consistent with the results of expression pattern analysis. HvIDD6 exhibited an increased expression trend in roots and a decreased trend in leaves. Meanwhile, the expression of HvIDD8/11/12 in roots was significantly upregulated under drought stress. These findings suggest that the high expression of HvIDD6/8/11/12 in roots under drought stress may be correlated with the drought tolerance of XZ5 (Fig. 11).
Fig. 9. Heatmap illustrates the expression patterns of HvIDD genes in response to drought, high temperature, and salt stress conditions. The gene names are listed on the right, with a phylogenetic tree constructed on the left. Below the heatmap are the types of stress and the tissues where expression levels were measured. The color scale indicates upregulation (in red) and downregulation (in blue) of gene expression. The numerical values represent the ratios of treated samples to controls
Fig. 10. Bar charts of real-time quantitative PCR results. Panels (A), (B), (C), and (D) represent the drought and salt stress treatment outcomes for HvIDD6, HvIDD8, HvIDD11, and HvIDD12, respectively. The selected tissues were roots and leaves. Black scales indicate the control group, while gray scales represent the treatment groups. Gene names are labeled at the top of each graph, with the X-axis denoting the type of stress and tissue, and the Y-axis showing the level of gene expression. Results were calculated using the 2^^−ΔΔCt^ method
Fig. 11. Bubble map of GO enrichment of HvIDD-target genes. Genes were listed in Table. The X-axis represents the Rich Ratio. Rich Ratio = Term Candidate Gene Number/Term Gene Number. The Y-axis represents the GO Term. The size of the bubble represents the number of different genes annotated to a GO Term, and the color represents the enriched Pvalue. 0 < Pvalue < 1. The smaller the Pvalue, the more significant the GO enrichment
miRNA-targeted HvIDDs and GO Enrichment Analysis of HvIDD Target Genes
We constructed a regulatory network involving 71 known miRNAs in barley and the 13 HvIDD genes. And a total of six miRNAs were predicted to exert cutting effects on HvIDDs (Table S11). There were five HvIDDs (HvIDD4, 5, 7, 9 and 13) which could bind the cis-elements and mediate transcription level of 72 downstream genes in barley. Additional details were presented in Table S12. GO enrichment analysis revealed that four HvIDD-targeted genes which were annotated as being associated with glycosylation, redox, lipid composition and chloroplast outer membrane division. They collaboratively participated in the structural maintenance of the organelle boundary membrane. Notably, except for glycosylation, the remaining three genes were also enriched in organelle outer membrane and outer membrane. It revealed that these three HvIDD-targeted genes were highly specialized for the outer membrane of the organelle in the aspects of localization and function (Fig. 10, S13 ,S14).
Discussion
The efficient expression of genes enable plants to cope with biotic and abiotic stress, such as salt stress and diseases [49]. Indeterminate domain (IDD) proteins constitute a plant-specific family of C2H2/C2HC zinc-finger transcription factors that exert broad regulatory effects on flowering time, nitrogen metabolism, starch biosynthesis, as well as adaptive responses to heat, salinity, and drought stress [2, 50–57]. The genome-wide analyses have been completed in more than ten plant species including maize, rice, tomato, and tobacco, which revealed 7–25 members distributed among three to five clades [58, 59]. In maize, six IDD proteins target to 180 genes which were feedback-regulated by 22 miRNAs. In rice and tomato, IDD can enhance the stress resistance by activating the genes associated with osmoregulation and ROS scavenging directly, such as RD29A-like, LEA3, P5CS and so on [23, 59–61]. There were abundant elements of hormone and stress response in the promoter of IDD genes, including ABRE、MBS and LTR. Meanwhile, expression patterns of IDD indicates high levels in roots, leaves, endosperm, and panicles. Moreover, the genes exhibited significantly differential expression patterns in response to drought, salinity, low temperature and high temperature stress treatments [62, 63]. Besides, the genes display uneven chromosomal distribution across species, which provides insights into their evolutionary relatedness. For example, five SiIDD genes reside on foxtail millet chromosome 5 with none on chromosomes 3, 4, or 8 [64]. Unlike maize IDDs, which are distributed across 5 chromosomes [27], HvIDDs are absent from chromosomes 1 and 7, indicating lineage-specific chromosomal loss or rearrangement during barley evolution. This reveals the lineage-specific evolution within cereal IDD families (Figs. 1 and 4).
MicroRNAs mediate the cleavage of target mRNAs or translational repression, thereby exerting negative post-transcriptional regulation of gene expression and modulating plant development as well as stress-responsive processes [65]. Here, six miRNAs were predicted to interact with the members of HvIDD (Table S11). Previous studies have indicated that hvu-miR6196 were upregulated significantly under salt stress in Hordeum bulbosum. And it has been demonstrated that hvu-miR6196 can enhance the salt tolerance by regulating the metal tolerance proteins and polyamine-metabolism genes in Hordeum bulbosum [66]. Our research predicted that a target interaction between hvu-miR6196 and HvIDD8/9, and qRT-PCR confirmed that salt stress reduced the expression of HvIDD8/9. This result was consistent with the upregulation trend of hvu-miR6196 reported in previous studies, implying that hvu-miR6196 likely mediated salt tolerance in barley by repressing the expression of HvIDD8 and HvIDD9. Dou et al. [67] demonstrated that hvu-miR166a/b/c cleaved HD-ZIP III transcription factors to regulate vascular-bundle differentiation, lateral-root emergence and salt stress responses. In our study, HvIDD1 targeted by hvu-miR166a/b/c exhibits high expression during rapid inflorescence-axis vascular development (INF1/INF2 stages). And hvu-miR5053 was predicted to target HvIDD2/6/7/9/12/13 in our study, but functional characterization remains to be fully elucidated (Table S11).
Additionally, five HvIDD members target to 72 downstream genes in total, and GO terms encompass stress, metabolism and development (Fig. 10,Table S12). Previous work showed that IDD proteins could directly mediate drought, salt and cold responses by ABRE, MBS and other stress-responsive motifs [24, 68]. In rice, OsIDD genes were strongly induced by ABA and multiple abiotic stresses, and they act in coordination with histone-modifying factors [55, 69]. Therefore, it should be presumed that among the 29 GO categories enriched in our dataset, a subset of IDD-regulated targets may participate in stress adaptation via similar mechanisms. These putative interactions await validation via transient transformation assays and mutant-based analyses.
These results not only provide an important basis for understanding the functions of the IDD gene family in barley, but also provide a reference for related research in other cereals. In summary, this study comprehensively analyzed the structure and function of IDD genes in barley through bioinformatics methods, providing help for barley molecular marker-assisted breeding. However, further validation of the functional roles of IDD genes remains critical for a comprehensive understanding of their regulatory mechanisms.
Conclusion
In our research, an exhaustive analysis of the 13 genes in the barley HvIDD gene family were conducted. These 13 genes can be categorized into three subfamilies. We examined the structure of these genes in relation to proteins, summarized their expression levels during various growth and development stages and under different stress conditions, and analyzed the various cis-elements in their promoters. These findings have laid the foundation for manipulating IDD genes and assisting in marker-assisted breeding of barley.
Supplementary Information
Supplementary Material 1.
The reference list from the paper itself. Each links out to its DOI / PubMed record.
- 1Li C, Yu W, Xu J, Lu X, Liu Y. Anthocyanin biosynthesis induced by MYB transcription factors in plants. Int J Mol Sci. 2022;23:11701.10.3390/ijms 231911701 PMC 957029036233003 · doi ↗ · pubmed ↗
- 2Feng X, Yu Q, Zeng J, He X, Ma W, Ge L, Liu W. Comprehensive analysis of the INDETERMINATE DOMAIN (IDD) gene family and their response to abiotic stress in Zea Mays. Int J Mol Sci. 2023;24:6185.10.3390/ijms 24076185 PMC 1009474337047154 · doi ↗ · pubmed ↗
- 3Kozaki A. INDETERMINATE DOMAIN transcription factors in crops: plant architecture, disease resistance, stress response, flowering, and more. Int J Mol Sci. 2024;25:10277.10.3390/ijms 251910277 PMC 1147672939408609 · doi ↗ · pubmed ↗
- 4Kumar M, Le DT, Hwang S, Seo PJ, Kim HU. Role of the INDETERMINATE DOMAIN genes in plants. Int J Mol Sci. 2019;20:2286.10.3390/ijms 20092286 PMC 653943331075826 · doi ↗ · pubmed ↗
- 5Zhang T, Yu X, Liu D, Zhu D, Yi Q. (2024). Genome-wide identification, expression pattern and interacting protein analysis of INDETERMINATE DOMAIN (IDD) gene family in Phalaenopsis equestris. Peer J 12, e 18073.10.7717/peerj.18073 PMC 1143843439346067 · doi ↗ · pubmed ↗
- 6Zou T, Lin R, Pu L, Mei Q, Wang Z, Jian S, Zhang M. Genome-Wide Identification, structure Characterization, expression pattern Profiling, and substrate specificity of the metal tolerance protein family in Canavalia rosea. Sw.) DC. ; 2021. p. 10. Plants (Basel).10.3390/plants 10071340 PMC 830908134209283 · doi ↗ · pubmed ↗
- 7Panahabadi R, Ahmadikhah A, Farrokhi N. (2023). Genetic dissection of monosaccharides contents in rice whole grain using genome-wide association study. Plant Genome 16, e 20292.10.1002/tpg 2.20292 PMC 1280743436691363 · doi ↗ · pubmed ↗
- 8Guo X, Zhou M, Chen J, Shao M, Zou L, Ying Y, Liu S. Genome-Wide identification of the highly conserved INDETERMINATE DOMAIN (IDD) zinc finger gene family in Moso bamboo (Phyllostachys edulis). Int J Mol Sci. 2022;23:13952.10.3390/ijms 232213952 PMC 969577136430436 · doi ↗ · pubmed ↗