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Genome-wide profiling of bZIP transcription factors in Camelina sativa: implications for development and stress response

BMC Genomic Data volume 25, Article number: 88 (2024) Cite this article

Abstract

Background

The bZIP transcription factor family, characterized by a bZIP domain, plays vital roles in plant stress responses and development. While this family has been extensively studied in various plant species, its specific functions in Camelina sativa (False Flax) remain underexplored.

Methods and results

This study identified 71 bZIP transcription factors in C. sativa, classified into nine distinct groups based on phylogenetic analysis. Subcellular localization predicted a nucleus-specific expression for these bZIPs. Analysis of GRAVY scores revealed a range from 0.469 to -1.256, indicating a spectrum from hydrophobic to hydrophilic properties. Motif analysis uncovered 10 distinct motifs, with one motif being universally present in all CsbZIPs. Conserved domain analysis highlighted several domains beyond the core bZIP domain. Protein-protein interaction predictions suggested a robust network involving CsbZIPs. Moreover, promoter analysis revealed over 60 types of cis-elements, including those responsive to stress. Expression studies through RNA-seq and Real-time RT-qPCR demonstrated high expression of CsbZIPs in roots, leaves, flowers, and stems. Specifically, CsbZIP01, CsbZIP02, CsbZIP44, and CsbZIP60 were consistently up-regulated under cold, salt, and drought stresses, whereas CsbZIP34 and CsbZIP35 were down-regulated.

Conclusion

This study presents the first comprehensive genome-wide profiling of bZIP transcription factors in Camelina sativa, providing novel insights into their roles in plant development and stress response mechanisms. By identifying and characterizing the bZIP gene family in C. sativa, this research offers new opportunities for improving stress tolerance and crop resilience through targeted genetic approaches, addressing key challenges in agriculture under changing environmental conditions.

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Introduction

In Brassicaceae family, Camelina sativa is an oil-yielding flowering plant that produces pale yellow cross-shaped flowers. In addition to the common names “Gold of Pleasure,” “False Flax,” “Wild Flax,” and “German Sesame,” it is sometimes called “Siberian Oilseed” [1]. Various regions of North America, Europe, and Central Asia cultivate this plant for oilseeds. Its oil is used for cooking, fuel, and burning in lamps and is well known for its high omega-3 fatty acid content (up to 45%), oil content (up to 43%) with antioxidant properties, protein content (up to 32%), erucic acid (up to 3%), and almost 110 mg of Vitamin E per 100 g [2]. It is also known for its unique almond-like aroma and flavor, and the European Union protects it under the trademark name “Olej Rydzowy Tradycyjny”. This plant grows on light or medium soils in temperate climate zones and has a short cultivation period [3]. Global climate change is significantly affecting the overall performance of C. sativa [4].

Abiotic stress can be caused by several factors including salinity, drought, cold or high temperatures, which are often linked to global climate change [5]. Plants have developed sophisticated regulatory mechanisms to cope with such environmental factors [6]. At the cellular level, transcription factors (TF) are master regulators for these processes. The basic leucine zipper (bZIP) transcription factors are a large family of genes and have been shown to play a critical role in response to various stresses and development of different plant organs [7,8,9,10]. The bZIP proteins have a conserved domain consisting of 60 to 80 amino acid residues [11]. It is further divided into an N-terminal leucine zipper domain and a C-terminal alkaline amino acid domain. Almost 16 to 20 basic conserved amino acid residues constitute the N-terminal that can specifically recognize the ACGT motif in promoter region of gene. The C-terminal is relatively variable and contains single or multiple repeat regions (heptapeptide) creating an α helix [12]. The bZIPs play a crucial role in various functions in plants, including the accumulation of anthocyanins in Malus domestica [13], and sucrose in Arabidopsis thaliana [14]. Moreover, bZIPs are also involved in stress responses including abiotic factors (drought, salt, ROS, temperature) [8, 15,16,17], biotic factors (like Sclerotinia sclerotiorum and Pseudomonas syringae) [18, 19] and the regulation of growth and development of flower in Litsea cubeba [10], and seed in A. thaliana [21]. These are also involved in managing responses to environmental stresses and modulating plant hormone signaling pathways in Helianthus annuus and A. thaliana [22,23,24]. Moreover, a potential association was observed between the expression of six bZIP TFs and oil accumulation in Chlamydomonas reinhardtii under stress conditions [25]. Overexpression of NsbZIP21 enhanced biomass and lipid productivity in Nannochloropsis salina [26]. In Arabidopsis thaliana, bZIP52 modulates the biosynthesis of seed oil through interaction with other genes like WRINKLED1 [27]. Similarly, PfbZIP85 in Perilla frutescens mediates ω-3 fatty acid-enriched biosynthesis of oil [28]. Additionally, bZIP TFs are mostly studied for their involvement in plant stress response. It was reported that AtbZIP11 can regulated the expression of IAA3/SHY2, which is a negative regulator of root development and growth [29]. The VdAtf1 is involved in the regulation of virulence by modulation of nitrogen metabolism in Verticillium dahlia [30, 31]. Similarly, bZIP TFs are involved in abiotic stress responses [16, 20, 22, 24, 25, 32]. Altogether, bZIPs are integral to plants’ ability to adapt to environmental stresses, regulate growth, and modulate key biosynthetic pathways, highlighting their potential in agricultural and biotechnological applications. Therefore, an understanding of the role of bZIPs in C. sativa is expected to guide novel avenues for improvement of this crop.

In this research study, we conducted an in-depth analysis of bZIP transcription factors in C. sativa involving CsbZIP classification, Phylogenetics, gene structure analysis, cis-elements prediction, and expression analysis using NGS and qPCR.

Materials and methods

Plant materials, treatments, and growth conditions

Plants were grown under controlled environmental conditions for three weeks in a growth room (at Government College University Faisalabad, Pakistan), with a 16-hour light and 8-hour dark cycle at a temperature of 20 °C ± 5 °C and a humidity level of 60% [33]. Seeds (Camelinanaheel variety) were obtained from the local market. To provide preliminary treatment, the seedlings were watered daily with the Hoagland solution, which contains essential nutrients for plant growth and development. After two weeks of growth, one group of plants was treated with a 1 M NaCl solution to induce salt stress, while the other group served as the control and was watered daily with the Hoagland solution. For drought stress, no water was given to a separate group of plants, and for cold stress, the plants were exposed to a temperature near the freezing point (0 °C) in the growth chamber. Following the treatments, the plants were watered every other day with NaCl for the salt stress treatment, while the control group continued to receive the Hoagland solution. One week after the treatments were applied, the samples were collected, quickly frozen with liquid nitrogen, and stored at -80 °C until analysis.

Identification of bZIP genes in C. Sativa

Members of the bZIP transcription factor gene family in A. thaliana were identified in the TAIR database (“https://www.arabidopsis.org/”), and their protein sequences were retrieved from the NCBI (https://www.ncbi.nlm.nih.gov/) database using the accession numbers provided in the database. The sequences were annotated using the text editor Notepad++, and homologs in C. sativa were identified using NCBI BLASTp (score value ≥ 100, e value ≤ 1e-10) (https://blast.ncbi.nlm.nih.gov/Blast.cgi). Protein family database PFAM was employed to generate a Hidden Markov Model (HMM) profile with the bZIP domain in HMMER 3.0 [34]. Later on, PFAM (https://www.ebi.ac.uk/interpro/entry/pfam/PF00170/) and SMART program (http://smart.embl-heidelberg.de/) was used to confirm bZIP domains.

Sequence alignment and phylogenetic analysis of CsbZIP gene family

For multiple sequence alignment, protein sequences from Cameline sativa, Arabidopsis thaliana, Helianthus annuus, Sinapis alba, and Lactuca sativa were uploaded to EMBL Clustal Omega (https://www.ebi.ac.uk/jdispatcher/msa/clustalo) following default parameters and Pearson/FASTA as output format. Sequence alignment file was then used to generate phylogenetic tree in IQ-TREE (http://iqtree.cibiv.univie.ac.at/) [35]. The tree was built through 1000 bootstrapping maximum likelihood with default parameters. As a last step, the derived tree was annotated utilizing an online server-based tool called iTOL (https://itol.embl.de/) [36].

Physiochemical properties of CsbZIP proteins

The physicochemical properties of the bZIP transcription factor proteins were predicted using an online server-based tool called ProtParam (https://web.expasy.org/protparam/), hosted by the Swiss Institute of Bioinformatics. To predict the subcellular localization of proteins, an online server-based tool called ProtComp 9.0 (hosted by Softberry) was used (http://www.softberry.com/berry.phtml?topic=protcomppl&group=programs&subgroup=proloc).

Gene structure and motif analysis of CsbZIP proteins

Gene Structure Display Server (GSDS) Tool v2.0 (https://gsds.gao-lab.org/) [37] was used to predict bZIP transcription factor exon and intron arrangements. To predict the structures of genes, this tool used both their coding and genomic sequences. Moreover, to identify motifs within the bZIP transcription factor family proteins, the Multiple EM for Motif Elicitation (MEME) tool (https://meme-suite.org/meme/) [38] was employed. For MEME, parameters were adjusted such that the size distribution was limited to zero or one occurrence per sequence, and the number of motifs was adjusted to 10, with protein sequence input as the only input [39].

Protein-protein interaction and CsbZIP protein domain analysis

The NCBI conserved domain database also called the web CD-Search Tool (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi), was used to identify protein domains present in the bZIP transcription factors. Using a protein batch as input, this tool returns tabular data describing the domains present in the proteins. These domains were then visualized using TBtools [40], which is an open-source tool hosted on GitHub. This allowed us to easily interpret and compare the different domains present in the bZIP transcription factors, providing insight into their potential functional roles. To analyze the protein-protein interactions among the bZIP transcription factors, the STRINGdb [41] was utilized, which is a web-based tool that automatically generates protein interaction networks based on the input sequences. A bZIP transcription factor protein interaction network was generated by parsing all the protein sequences in the search box and clicking the search button. However, some manual adjustments were made to improve the visual representation of the network, such as adjusting the arrangement of protein nodes. Additionally, the strength of the interactions was visually represented by setting the lines between nodes as either dotted or straight, which represented weak and strong interactions, respectively [42].

Cis-regulatory elements and gene enrichment analysis

Promoter and UTR regions (2000 bp upstream) of every bZIP transcription factor gene were retrieved from NCBI nucleotide database [43]. PLANTCARE (https://bioinformatics.psb.ugent.be/webtools/plantcare/html/) was used to predict the cis-regulatory elements of these genes [44], and the results were compiled and visualized using the open-source software TBtools. To perform the gene enrichment analysis, we utilized the ShinyGO [45] database, a web-based tool for gene ontology and KEGG pathway enrichment analysis. We obtained a list of CsbZIP gene IDs from the NCBI database and used it as the input for the analysis.

Gene expression analysis using NGS data

Transcriptomic data from the NCBI Sequence Read Archive (SRA) database were used to study gene expression in the family of bZIP transcription factors. We obtained transcriptomic data from the NCBI Sequence Read Archive (SRA) database about root development (SRR935368), leaf development (SRR935362), stem development (SRR935365), and flower development (SRR935369) [46] (accession number SRP136191). A tool from the Galaxy toolkit called BOWTIE2 was used to map all reads to the C. sativa genome [47]. We determined the expression levels of the bZIP genes by first calculating FPKM values using Galaxy’s Cufflinks tool. These values were then used by TBtools to generate a heatmap of bZIP gene expression.

Real-time RT-qPCR analysis

RNA was isolated from C. sativa leaves [48] using Trizol reagent method and was quantified using Nanodrop 2000 (Thermo Fischer Scientific, Waltham, MA, USA). Subsequently, cDNA was synthesized from 1 µg of RNA using the First-Strand Synthesis kit and stored at -20 °C. Real-time RT-qPCR was performed with iTaq Universal SYBR Green Super-Mix (Bio-Rad Labs, Hercules, CA, USA) and a Real-time RT-qPCR detection system (CFX96 Touch Real-Time PCR Detection System) [49]. Oligo Calculator was used to design gene-specific primers, and Primer-BLAST from the NCBI confirmed their specificity (accessed on 17 July 2023). The actin-2 gene (Csa15g026420) was used as the housekeeping gene, and each sample was tested three times for gene expression in triplicate [50].

Results

Identification and characterization of bZIP genes in C. Sativa

A total of 71 bZIP genes were identified in C. sativa. These bZIPs were named after the genes they were found based on blast results, as the protein homolog was obtained for all the reference bZIP proteins of A. thaliana. After analyzing the CsbZIP proteins, it was found that most of these proteins were predicted to be located inside the nucleus of the cell. The pI values of these proteins ranged from 4.5 to 11.41, indicating their acidic to basic nature. The GRAVY scores, which is a measure of the hydrophobicity of the protein, ranged from − 0.469 to -1.256. The CsbZIP proteins with the highest GRAVY scores were the ones with the most hydrophobic nature, while the ones with the lowest scores were the most hydrophilic. In terms of GRAVY scores, the CsbZIP protein with the highest value was CsbZIP64 with a score of -1.256, while the protein with the lowest value was CsbZIP28 with a score of -0.469. The amino acid counts of the CsbZIP proteins showed that they were predominantly composed of small, polar, and charged amino acids such as Serine, Threonine, Asparagine, and Glutamine. The percentage of small amino acids in these proteins was higher than that of large amino acids, indicating their compact nature. The CsbZIP proteins with the highest and lowest molecular weight were CsbZIP49 and CsbZIP08, with values of 78912.36 and 16267.56 respectively. The physicochemical properties of CsbZIP proteins are presented in tabular form in Table 1.

Phylogenetic analysis

To explore the evolutionary relationship, bZIP proteins from A. thaliana, H. annuus, S. alba, L. sativa and C. sativa were used to generate phylogenetic tree (Fig. 1). The CsbZIPs were grouped into nine groups based on the phylogenetic analysis. Group 1 contained three bZIPs from C. sativa (CsbZIP02, CsbZIP44, and CsbZIP11). Similarly, 7, 4, 13, 13, 5, 14, 6, 6 CsbZIPs were classified into group 2, 3, 4, 5, 6, 7, 8, and 9, respectively.

Fig. 1
figure 1

Phylogenetic analysis of bZIP proteins from various plant species, including C. sativa, A. thaliana, H. annuus, S. alba, and L. sativa. Clustering (Group 1 to Group 9) identifies related CsbZIPs. Orthologs and paralogs indicate functional similarities and gene duplications. Valuable insights for crop improvement

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A total of 41 orthologs pairs of CsbZIPs and AtbZIPs were identified based on their placement in the phylogenetic tree. In G1, there was only one pair as CsbZIP44/AtbZIP44. In group 7, there were nine orthologous pairs involving bZIP19, 20, 21, 26, 46, 47, 50, 57 and 65. Similarly, variable number of orthologous pairs were identified in G2 (bZIP03, 08, 42, 43,70), G3 (bZIP09, 10, 25, 63), G4 (bZIP13, 27, 39, 63), G5 (bZIP18, 30, 51, 52, 59, 61, 71), G6 (bZIP28, 56), G8 (bZIP16, 41, 54, 55, 68), and G9 (bZIP04, 06, 07, 53). Presence of a high number of orthologous pairs indicates that these proteins are likely to have similar functions in both species. Only two paralogs of CsbZIP were also identified as CsbZIP29/CsbZIP71 and CsbZIP31/CsbZIP33. The phylogenetic analysis provides valuable insights into the evolutionary relationship between bZIPs from different plant species and highlights the relationship between bZIPs from C. sativa and other plants. The results could be useful for understanding the functional roles of bZIP proteins and for identifying potential targets for genetic engineering in crop improvement.

Table 1 Physiochemical properties of CsbZIP proteins
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Gene structure and motif analysis of CsbZIP proteins

Gene Structure Display Server 2.0 was used to analyze the intron and exon structures of CsbZIP genes to gain insight into their structural features. The analysis revealed that the Intron count in CsbZIP genes varies from 0 to 19. There were genes with only one intron and others with as many as 20 introns (Fig. 2A). CsbZIP01, 02, 03, 04, 05, 06, 07, 08, 11, 40, 42, 43, 44, 48, 53, 58, and 70 represent intron-less bZIPs. Using the MEME program, conserved motifs were predicted for CsbZIP proteins to investigate their divergence. A total of 10 motifs were selected, with zero to one occurrence in each sequence. Among CsbZIPs, motif 1 was conserved in all sequences. This 29 residue long sequence (EKRQKRMJSNRESARRSRLRKQAYVEELE) represents conserved region of bZIP domain. Similarly, motif 7 was present in all CsbZIPs except for CsbZIP31, 33, 49, 62, and 72. This 19 residue long motif (EVEKLKZENQELQKQLSEL) also represents part of bZIP domain. In all of the CsbZIP proteins, motif 10 was the least conserved (Fig. 2B). The conserved motifs in CsbZIP proteins suggest their distinct functions in various cellular processes.

Fig. 2
figure 2

Gene structure and conserved motif analysis. A) Variation in intron-exon structures of CsbZIP genes. B) Motif analysis predicted conserved motifs in CsbZIP proteins

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Protein-protein interaction and CsbZIP protein domain analysis

Domain analysis of CsbZIP genes revealed that multiple domains were present in most of these proteins, but the bZIP and related domains were present in almost all of the proteins, these domains include bZIP domain, bZIP_1, bZIP_C, bZIP_plant_RF2, bZIP_HBP1b-like, bZIP_plant_GBF1, bZIP_plant_BZIP46, bZIP_HY5-like, bZIP_C superfamily and bZIP superfamily domains (Fig. 3A). Several CsbZIP proteins were found to have domains in addition to the ones discussed earlier, these domains include MFMR domain, BRLZ domain, DOG1 domain, and ZapB domain, indicating the multifunctionality of CsbZIPs and their potential involvement in more than one function within the cell.

The protein-protein interaction analysis of CsbZIP proteins showed the interaction of these proteins among each other in the cell, all the proteins of this family showed very strong interactions among one another indicating the potential complementary action of these proteins for one another (Fig. 3B). Some proteins like CsbZIP17, CsbZIP49, CsbZIP33, CsbZIP72, and CsbZIP04 did not show any interaction indicating their potential involvement in processes other than the ones other proteins are involved in and their potential function as the activator for other genes of the family.

Fig. 3
figure 3

The bZIP domains and protein-protein interaction. A) Domain analysis of CsbZIP genes in C. sativa showed the presence of bZIP and related domains in almost all proteins, along with additional domains (MFMR, BRLZ, DOG1, ZapB) indicating multifunctionality. B) Protein-protein interaction analysis of CsbZIP proteins revealed strong interactions among all family members

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Cis-regulatory elements and gene enrichment analysis

In the context of regulating gene expression and determining an organism’s development and functioning, cis-regulatory elements such as enhancers and promoters play a crucial role. Mutations in these regulatory elements have been found in various species, leading to changes in phenotypic expression. For the current research, the promoter sequences of 2000 base pairs (bp) of 71 bZIP genes in C. sativa were analyzed, revealing the presence of sixty-one different types of cis-regulatory elements. These regulatory elements were found to be enriched in the promoter sequences, with the most prevalent element being the TATA-box, which helps to position RNA polymerase and initiate transcription. Other commonly found regulatory elements include ARE, ABRE, Box-4, G-box, TGACG-motif, CGTCA-motif, TCT-motif, TG1-motif, LTR, MBS, and MRE. Additionally, a few regulatory elements, such as O2-site, CAT-box, AT-rich element, I-box, ACE, and A-box, were present in fewer numbers. In contrast, elements like CAG-motif, AuxRE, L-box, LS7, and HD-Zip 1 were rare (Fig. 4A).

Gene enrichment analysis revealed that the CsbZIP genes are involved in various processes in plants, including seed dormancy control and signaling pathways. These genes function as activators for other genes and more (Fig. 4B). The figure shows the number of genes from this gene family in C. sativa involved in particular functions. The length of each bar indicates the number of genes, while the color of the bars represents the log fold change.

Fig. 4
figure 4

Promoter analysis and enrichment analysis. A) The arrangement of CsbZIP genes’ cis-acting regulatory elements. B) Gene enrichment analysis of CsbZIP genes in C. sativa, indicating their involvement in diverse plant processes. Each bar represents a specific function, with bar length reflecting the number of associated genes, and color indicating the log fold change of gene expression

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Gene expression analysis using transcriptomic data

Transcriptomic data were analyzed to understand the potential functional importance of CsbZIPs. In tissue-specific expression profiling, it was observed that several CsbZIP genes were highly expressed in C. sativa root tissues (including CsbZIP01, CsbZIP02, CsbZIP47, CsbZIP51, and CsbZIP58) as compared to flower, leaf or stem. Interestingly, most of these CsbZIPs were not highly expressed in other tissues (except for CsbZIP02, which is also expressed in stem). It indicated that these bZIPs play an important role in roots (Fig. 5A). Similarly, CsbZIPs were also expressed in other parts of plant including CsbZIP44 in flowers, CsbZIP35/CsbZIP61 in leaves, and CsbZIP 37 in stem. It was noticeable that CsbZIP02 was highly expressed in all samples (Fig. 5A).

Transcriptomic data was also analyzed to study response of CsbZIPs against cold, drought and NaCl (salt) stress (Fig. 5B). A diverse response was observed where CsbZIPs expression changes was observed in distinct groups. In response to cold stress, CsbZIP02 and CsbZIP44 were significantly upregulated, while CsbZIP08, CsbZIP60 and CsbZIP61 were downregulated. In response to drought stress, CsbZIP01, CsbZIP02, and CsbZIP37 were upregulated, while CsbZIP08, CsbZIP60, and CsbZIP61 were downregulated. In response to salt (NaCl) stress, CsbZIP02, CsbZIP37, and CsbZIP60 were upregulated, while CsbZIP35 and CsbZIP60 were downregulated (Fig. 5B).

Fig. 5
figure 5

Transcriptomic analysis. A) The expression patterns of CsbZIP genes across different tissues of C. sativa. B) CsbZIP gene expression under cold, drought, and salt stresses in C. sativa is visualized in a TBtools-generated heatmap. Rows represent genes, columns show control or stress experiments, and colors indicate changes in expression levels

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qRT-PCR analysis

Real time RT-qPCR was used to determine the transcript abundance of nine CsbZIP genes from C. sativa leaves. The genes analyzed were CsbZIP01, CsbZIP02, CsbZIP34, CsbZIP35, CsbZIP37, CsbZIP44, CsbZIP51, CsbZIP60, and CsbZIP61. Under cold, drought, and salt stresses, all CsbZIP genes showed differential regulation. Specifically, CsbZIP01, CsbZIP02, CsbZIP44, and CsbZIP60 were upregulated in response to all three stresses (Fig. 6). Conversely, CsbZIP34 and CsbZIP35 were downregulated under all stress conditions. A very significant upregulation of CsbZIP37 was observed during drought stress, but not much of a change was observed during cold and salt stress. The expression of CsbZIP61 did not change significantly in response to the given stresses, while the expression of CsbZIP51 increased during drought and decreased during cold and salt stress (Fig. 6).

Fig. 6
figure 6

Real-time RT-qPCR analysis of bZIPs in C. sativa leaves under cold, drought, and salt stresses. Each bar represents the mean ± SE from three replicates. (*) and (**) on error bars indicate significant differences (P < 0.0001) between control and stressed samples

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Discussion

Understanding the genetic basis of stress responses and developmental processes in plants is essential for improving crop resilience and productivity [51]. In current study, we focused on Camelina sativa, an important oil-yielding plant known for its high nutritional value and unique aroma. By investigating the bZIP transcription factor family, we aimed to shed light on the molecular mechanisms underlying stress tolerance and organ development in this species. Current findings provide valuable insights that can inform future research and breeding programs to enhance the resilience and productivity of C. sativa under changing environmental conditions [52, 53]. Previously, bZIP gene family has been studied in a diverse range plant species including vitis vinifera [54], Zea mays [55], Legumes [56], Manihot esculenta [57], Ginkgo biloba [58], and many others [20, 31, 59,60,61,62,63,64]. Therefore, understanding the role of bZIPs in C. sativa is particularly important as it contributes to the broader knowledge of plant stress responses and development.

The phylogenetic analysis of bZIP proteins from C. sativa, A. thaliana, H. annuus, S. alba, and L. sativa provided valuable insights into the evolutionary relationships between these genes. The classification of bZIPs was consistent with previous studies [46,47,48, 50]. The grouping of CsbZIPs revealed distinct clades, indicating functional divergence within the bZIP gene family [65]. Some CsbZIPs showed orthology with specific bZIPs from A. thaliana, suggesting functional conservation between these genes in different species [66]. Additionally, paralogs resulting from gene duplication events were also identified, implying potential functional redundancy or specialization within the bZIP family [67]. The physiochemical properties analysis of CsbZIP proteins revealed their diverse nature. These proteins were predicted to be predominantly located in the nucleus, indicating their potential role as transcription factors [68]. The variation in pI values indicated a range of acidic to basic properties among CsbZIPs, which could influence their interactions with other biomolecules. The GRAVY scores reflected the hydrophobicity of the proteins, suggesting their possible roles in membrane-associated processes [58]. The high proportion of small, polar, and charged amino acids in CsbZIP proteins indicated their compact nature, potentially influencing their protein-protein interactions and overall structure [62].

The gene structure analysis revealed variations in the intron-exon organization among CsbZIP genes, indicating their diverse genomic organization [61]. Motif analysis identified conserved motifs, with some motifs present in all CsbZIPs, suggesting functional importance. Other motifs were specific to certain CsbZIP proteins, hinting at potential functional divergence within the gene family [58]. The domain analysis revealed the presence of various bZIP-related domains in CsbZIP proteins, suggesting their involvement in transcriptional regulation. Additionally, the presence of other domains in some CsbZIPs indicated their potential multifunctionality, possibly participating in different cellular processes [11]. The cis-regulatory element analysis of CsbZIP gene promoters identified multiple regulatory motifs associated with transcriptional regulation. The presence of diverse cis-regulatory elements suggested that CsbZIP genes may be involved in the control of various biological processes, including seed dormancy, signaling pathways, and other cellular functions.

Gene expression analysis using RNA-seq data provided insights into the tissue-specific and stress-responsive expression patterns of CsbZIP genes [69]. The higher expression of certain CsbZIP genes in roots indicated their potential role in root development. It was discovered that certain CsbZIP genes respond differentially to abiotic stresses, suggesting that they play an important role in stress responses and adaptation to stress [70]. In addition, qRT-PCR analysis revealed distinct responses to cold, drought, and salt stress in C. sativa leaves. It was observed that under different stress conditions, these CsbZIPs were regulated differently. As a result of all three stressors, CsbZIP01, CsbZIP02, CsbZIP44, and CsbZIP60 were significantly upregulated. Conversely, CsbZIP34 and CsbZIP35 were downregulated in all stress conditions. Notably, CsbZIP37 exhibited a unique pattern, being upregulated during drought stress but under cold and salt stresses showed very little upregulation and downregulation as compared to the control group, and CsbZIP61 showed the slightest change in expression in response to these stresses. Additionally, CsbZIP51 showed upregulation during drought stress but downregulation under cold and salt stresses.

Differential expression patterns of these CsbZIPs suggest they play specific roles in stress-responsive pathways, contributing to the plant’s adaptive mechanisms [8]. Identifying and characterizing these CsbZIP genes will help us to understand the molecular mechanisms that cause C. sativa to tolerate cold, drought, and salinity [22, 23]. By enhancing our understanding of how these bZIP transcription factors function, we can improve the resilience and yield of crops under adverse conditions [71]. Overall, this study highlights the diversity and functional complexity of the bZIP gene family in C. sativa. The identification and characterization of CsbZIP genes, along with their role in development of C. sativa and response to various stresses in the plant.

Conclusion

This study identified and characterized the bZIP transcription factor family in C. sativa and analyzed their expression patterns under different stress conditions and during development. The results showed that some genes were significantly upregulated in response to specific stresses, while others were downregulated or showed no alteration in expression. The study also demonstrated that the bZIP transcription factors play a crucial role in regulating gene expression, response to abiotic stresses, and regulation of plant growth and development in C. sativa. The findings of this research provide valuable insights into the expression pattern of bZIP genes in stress tolerance and plant growth in this important crop species, which can be used to develop strategies for improving crop yields and ensuring food security. Additionally, this study serves as a foundation for future research on the bZIP transcription factor family in C. sativa and other plant species.

Data availability

Data will be made available on reasonable request with the corresponding author.

Abbreviations

C. sativa:

Camelina sativa

bZIP:

Basic Leucine Zipper

NGS:

Next-Generation Sequencing

qPCR:

Quantitative Polymerase Chain Reaction

TF:

Transcription Factor

A. thaliana:

Arabidopsis thaliana

H. annuus –:

Helianthus annuus

S. alba:

Sinapis alba

L. sativa:

Lactuca sativa

pI:

Isoelectric Point

GRAVY:

Grand Average of Hydropathy

RNA-seq:

RNA Sequencing

qRT-PCR:

Quantitative Reverse Transcription Polymerase Chain Reaction

SRA:

Sequence Read Archive

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Acknowledgements

Authors are thankful to Princess Nourah bint Abdulrahman University Researchers Supporting Project number (PNURSP2024R459), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

Funding

No specific funds have been received to conduct the present research.

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Authors and Affiliations

  1. Department of Bioinformatics and Biotechnology, Government College University, Faisalabad, Pakistan

    Shahroz Rahman, Abdul Rehman Ikram, Muhammad Umar Rafique & Farrukh Azeem

  2. Department of Biology, College of Science, Princess Nourah Bint Abdulrahman University, P.O. Box 84428, Riyadh, 11671, Saudi Arabia

    Latifa AlHusnain & Muneera D. F. AlKahtani

  3. Institute of Molecular Biology and Biotechnology, The University of Lahore, Lahore, 54590, Pakistan

    Sajid Fiaz

  4. Department of Plant Pathology, University of Agriculture Faisalabad, Faisalabad, 38040, Pakistan

    Muhammad Amjad Ali

  5. Center of Excellence in Biotechnology Research, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Kotb A. Attia

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Contributions

SR and ARI devised the main idea and supervised the research. SR, ARI, and MUR performed analysis. MAA, FA, and SR wrote the manuscript. SR, ARI, MUR, and FA re-analyzed, the literature review and editing of the article. SF, KAA, LH, and FA provided technical expertise to improve the revised article. FA, SR, SF, MDFA and ARI helped during revision, editing and proof-reading of the revised article. All authors made substantial efforts to improve the article and agreed to submit it.

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Correspondence to Sajid Fiaz or Farrukh Azeem.

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Rahman, S., Ikram, A.R., AlHusnain, L. et al. Genome-wide profiling of bZIP transcription factors in Camelina sativa: implications for development and stress response. BMC Genom Data 25, 88 (2024). https://doi.org/10.1186/s12863-024-01270-6

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BMC Genomic Data

ISSN: 2730-6844

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