1. Introduction
The Short Internodes-Related Sequence (SRS) family, also referred to as the STY (STYLISH) family, encodes proteins that belong to zinc-finger transcription factors unique to plants [1,2]. The SRS family encodes two distinct conserved domains: the RING-like zinc finger domain and the IGGH domain [3,4]. The RING-like zinc finger domain is positioned at the protein’s N-terminal region and mediates the binding of proteins to DNA, RNA, and other biomolecules that are involved in various physiological processes [5,6,7]. Another C-terminal IGGH domain is positioned at the protein’s C-terminus region; this domain is responsible for homo- or heterodimerization between proteins [4]. Moreover, the IXGH domain is not found in other proteins and may be a conserved structural domain unique to the SRS family [2].
Studies on the SRS family began with the identification of LPR1 (Lateral Root Primordia 1). Smith and Fedoroff first identified the LRP1 gene in Arabidopsis (Arabidopsis thaliana), which is closely associated with root formation and flower development and also functions as a signal suppressor in the gibberellin response [8]. The identification of At-LRP1 facilitated research into the SRS family, and 11 AtSRS family members (AtSHI, AtSTY1, AtSTY2, AtLRP1, AtSRS11, and AtSRS3-8) have been found in A. thaliana thus far. Like other transcription factors, SRS family members regulate biological processes, including phytohormone regulation, photomorphogenesis, the adversity stress response, and plant growth and development [4,9,10,11,12]. AtSHI negatively regulates the gibberellin response and can influence stem elongation through transcriptional regulation. Overexpression of AtSHI in A. thaliana, winter pot kalanchoe (Kalanchoe blossfeldiana), and poinsettia (Euphorbia pulcherrima) plants resulted in a dwarf phenotype [1,13,14]. AtLRP1 could regulate lateral root development, and the overexpression of AtLRP1 elevates growth hormone levels and reduces lateral root density [11]. AtSTY1 and AtSTY2 are partially functionally redundant, and they promote stigma development by regulating growth phytohormone homeostasis, affecting the process of pistil development, promoting stigma formation, and also affecting vascular development [9,15]. Furthermore, recent research suggests that the SRS gene family is crucial for abiotic stress. Abiotic stress mainly includes drought, salinity, and low temperature. Plant development is impeded by these stresses, which lower crop yield and quality [16,17,18,19]. MeSRS genes in cassava (Manihot esculenta) react to salt and osmotic stresses and plant hormone stimulation (salicylic acid and methyl jasmonate) [20]. GhSRS21 negatively regulates salt tolerance in cotton (Gossypium hirsutum) [21]. MeSRS expression was stimulated by cold and salt in the fodder plant alfalfa (Medicago sativa), suggesting that SRS genes might be crucial to the tissue-dependent signaling system [22].
The genus Populus, which grows in the northern hemisphere, comprises roughly 30 species and is the fastest-growing of the temperate trees [23,24]. As a model plant for forestry research, Populus has excellent experimental characteristics: ease of interspecific hybridization and asexual propagation; a relatively small genome; and ease of performing genetic research [24,25,26,27]. Additionally, Populus holds significant economic value due to its widespread use, rapid growth, and high yield. Throughout the life cycle of poplar trees, they are often exposed to adversity stresses caused by multiple environmental factors, most notably drought stress and salinity stress. Relevant research has demonstrated that during drought stress, the reduced rate of photosynthesis and the imbalance of intracellular free radical metabolism in poplar produce excess reactive oxygen radicals, which trigger or exacerbate membrane lipid peroxidation and cause damage to the cell membrane system [28,29,30,31,32]. The same photosynthesis of poplar under saline stress is also drastically reduced, and at the same time, due to the large levels of reactive oxygen species buildup in cells under stress, oxidation of nucleic acids, and proteins of other substances in the inner cells of the poplar, which leads to cell damage and death [28,32,33,34,35].
The SRS gene family has been intensively studied in several species, such as soybean (Glycine max) [12], A. thaliana [36], maize (Zea mays) [37], barley (Hordeum vulgare) [38], M. sativa [22], and rice (Oryza sativa) [39]. Recent research on the poplar SRS gene family has only revealed significant functions in controlling wood [40]. Nevertheless, limited information is accessible on the SRS gene family’s evolutionary relationships, its members’ characterization, and its expression patterns under abiotic stress. In this study, we identified 10 SRS family members based on the P. tremula genome. Subsequently, we analyzed chromosomal location, gene duplication events, gene structure and conserved domains, cis-acting elements, evolutionary relationships and expression patterns under drought and salt stress. The findings of this research provide an important basis for exploring genes related to drought and salinity resistance in poplar.
2. Materials and Methods
2.1. Plant Materials and Treatment
In this study, we used 60-day-old Populus davidiana potted seedlings cultivated at the Heilongjiang Forestry Institute. The study site was located at the laboratory of Heilongjiang Forestry Institute at latitude 45°41′59″ N, longitude 126°38′8″ E, at an altitude of 150 m. The following were the conditions in the laboratory: temperature (22 ± 2 °C), light intensity 400 μmol·m−2·s−1, light time 16 h, and relative humidity in the range of 65%–75%. Subsequently, we selected 36 potted seedlings with good growth status and the same growth conditions as the experimental materials for drought stress treatment and salt stress treatment. The natural drought approach was employed to apply the drought stress treatment, and the leaves of the P. davidiana were sampled at six time points (0 d, 2 d, 4 d, 6 d, 8 d, and 10 d). Salt stress was imposed by the soil used for the potted seedlings with a 500 mM NaCl solution, with each pot receiving 200 mL of the solution. Leaves were sampled at (0 h, 3 h, 6 h, 12 h, 24 h, and 48 h) post-treatment for further analysis. Three replicates of each process were wrapped in tin foil, labeled, liquid nitrogen-frozen, and kept at −80 °C. Photographs of drought-stressed poplar and NaCl-stressed poplar are shown in Supplementary Figures S1 and S2.
2.2. Identification of SRS Genes in the P. tremula
The Populus genome database (
2.3. Phylogenetic Analysis
The SRS protein of P. tremula, A. thaliana, Capsella grandiflora, Z. mays, Salix purpurea, and O. sativa underwent sequence alignments, and we used maximum likelihood approach in the MEGA X software to generate a phylogenetic tree [45], every other parameter was set to its default settings, and bootstrap value was set to 1000. The PlantTFDB database (
2.4. Analysis of Gene Structure and Conserved Motifs
Visualization of gene structure was based on obtained genome annotation data using TBtools software [47]. The MEME website (
2.5. Chromosome Localization, Gene Duplication, and Cis-Regulatory Element Analysis
Visualization of gene positioning on chromosomes was based on obtained genome annotation data using TBtools software [47]. The MCScanX [48] function in TBtools was used to examine the evolutionary method of duplication of PtSRS. Visualization was performed using the TBtools software’s Advanced Cicros function [47]. The gene pairs’ Ka/Ks values were computed using the TBtools basic Ka/Ks Calculator. The evolution time is calculated by substituting the value of Ks into the formula T (T = Ks/2λ, λ = 9.1 × 10−9 [49,50]). TBtools was used to extract sequences that were 2000 bp upstream of the PtSRS initiation codon and on the PlantCare website (
2.6. RNA Extraction and qRT-PCR Analysis
With a plant RNA extraction kit (Bio Teke Biotechnology, Beijing, China), RNA was isolated from P. davidiana leaves. The quality of isolated RNA was detected with gel electrophoresis using 2% agarose gel. RNA was transcribed into cDNA with a reverse transcription kit (LABLEAD Biotechnology, Beijing, China). After reverse transcription, cDNA was diluted five times and utilized as a template for two-step amplification under the subsequent reaction conditions: 1 cycle at 98 °C for 30 s, followed by 40 cycles at 95 °C for 10 s and 60 °C for 30 s. Each compound hole was set to three technical repetitions. Levels of gene expression were evaluated using the 2−ΔΔCt approach [51]. Using 18S as the housekeeping gene, primer design was performed using Primer 5 software (primer-specific information is included in Supplementary Table S2).
2.7. Statistical Analysis
We utilized the GraphPad Prism v8.0.2 program for statistical analysis. The means’ differences were compared using a one-way ANOVA. Gene expression during the 0 d/0 h stress treatment served as a control, and the difference was deemed statistically significant if * p < 0.05.
3. Results
3.1. Identification and Physicochemical Characterization Analysis of SRS Family Members in Poplar and Chromosomal Location
In this paper, 10 SRS members were identified in the P. tremula proteins with both HMMsearch and ‘BLASTP’ search methods and named PtSRS01-PtSRS10 based on where they are located on the chromosome. We subsequently conducted a protein-level physicochemical analysis of these identified SRS family members. Information on the physicochemical properties associated with these identified SRS proteins is presented in Table 1. The protein length of family members ranged from 204 (PtSRS05) amino acids to 436 (PtSRS01) amino acids. The range of molecular weights (MWs) was 22.67 kDa (PtSRS05) to 47.92 kDa (PtSRS01), and the theoretical pI (isoelectric points) ranged from 6.5 (PtSRS07) to 9.18 (PtSRS06); of these, only PtSRS07 and PtSRS08 with isoelectric point values less than 7 are acidic proteins, whereas the rest are basic proteins. The aliphatic index ranges from 46.37 (PtSRS03) to 65.55 (PtSRS01). All of the PtSRS proteins’ GRAVY values were less than 0, suggesting they were hydrophilic. Based on the instability index analysis results, it was found that most of the members showed instability. The instability index range was found to be from 32.33 (PtSRS10) to 62.98 (PtSRS08); of these, only PtSRS10 (32.33) and PtSRS02 (36.21) showed instability index ranges of less than 40, indicating greater stability.
According to the data from genome annotation, a map detailing the PtSRS genes’ chromosomal distribution was produced, showing that 10 PtSRS genes were dispersed irregularly throughout seven chromosomes, which are 1, 3, 4, 5, 7, and 9. As shown in Figure 1, there was little difference between the number of SRS gene members on each chromosome, with two SRS genes on chromosomes 1, 5, and 9, and one SRS gene on the other chromosomes.
3.2. Phylogenetic Relationship Analysis of the PtSRS Family
To analysis the affinities of SRS proteins in poplar and other species, we constructed evolutionary trees for SRS proteins of six species: P. tremula (10), A. thaliana (11), C. grandiflora (10), Z. mays (9), S. purpurea (13), and O. sativa (5). As demonstrated in Figure 2, all SRS proteins were categorized into five groups. The number of SRS proteins in each of these five groups was 4, 17, 7, 14, and 16. The SRS proteins of Salicaceae mainly clustered in Group 2 and Group 5; the SRS proteins of Cruciferae mainly clustered in Group 3; and the SRS proteins of Gramineae mainly clustered in Group 4. Poplar and willow SRS proteins were the most homologous, with each poplar SRS protein closely clustered with willow SRS proteins. However, in Group 1, we found that the two S. purpurea SRS proteins from willow are more closely related to A. thaliana and C. grandiflora and less homologous to the SRS proteins from poplar. This difference was inferred to be the result of the divergence of poplar and willow. SRS proteins from all six species are present in Group 5, indicating the possibility these SRS genes have diverged from their common ancestor. In addition, based on the number of SRS proteins in the six species, it was found that the number of SRS proteins was relatively small in different species, indicating that the SRS family is a small transcription factor gene family.
3.3. Gene Structure and Conserved Motifs Analysis
Variation in gene structure indicates the evolutionary relationships among gene families. Simultaneously, the intron–exon arrangement is crucial for gene functionality. Therefore, we investigated the gene structure and conserved motifs of the PtSRS. Figure 3A shows the evolutionary tree and grouping of SRS family members. Based on evolutionary relationships, the 10 PtSRS genes were grouped into five subfamilies (I, II, III, IV, and V). PtSRS motifs were predicted using the MEME website, and in all 10 motifs were found, with motif-specific information summarized in Supplementary Figure S3. The conserved motifs diagram (Figure 3B) displayed comparable composition of motifs in the identical subfamily, indicating functional conservation within subfamilies and functional diversity among subfamilies. Motif 1, 2, and 9 showed significant conservation, and they were distributed among all family members. Motif 6 was found in the Ⅴ subfamily, motif 8 is found only in the IV subfamily, and motif 7 was unique to the III subfamily. Gene functions of PtSRS family members may differ depending on motif composition. The gene structure diagram (Figure 3C) showed that most members of PtSRS had two or three exons, except for PtSRS04 and PtSRS01 (five exons), with all exons separated by introns. The number of UTR structures showed that most PtSRS genes contain two UTRs at the start of the gene; in comparison, PtSRS01 and PtSRS06 had only one UTR structural domain, located at the end of the gene. In addition, there are similarities in gene structure within each subfamily.
3.4. Duplication Events of the PtSRS Gene Family
In plants, previous research has revealed that gene duplication caused by tandem duplication or segmental duplication is the primary cause of gene family expansion [52]. The poplar SRS gene family’s evolutionary events were examined by conducting a collinearity analysis of PtSRS genes. The study’s findings are displayed in Figure 4. In total, four pairs of eight genes were found. All collinear genes were the result of segmental duplication, indicating that the segmental duplication evolution of the PtSRS gene family is dominated by segmental duplication as the main tension. In evolutionary analysis, it is important to understand the incidence of synonymous and non-synonymous mutations. Ka/Ks analysis allows for the measurement of the effect of selective pressure on the evolution of genes or clusters of genes, in addition to the inference of the duplication time of collinearity gene pairs based on the formula. For this purpose, we analyzed the Ka, Ks, and ratios of these collinear gene pairs. The findings of the calculations are shown in Table 2; the calculated Ka values ranged from 0.045453 to 0.085775, and Ks values ranged from 0.213091 to 0.275154. Using the formula T (T = Ks/2λ, λ = 9.1 × 10−9 [49,50]), the calculation results indicated that duplication transpired between 15.12 million and 11.71 million years ago. In addition, the Ka/Ks ratios of duplicated gene pairs were below 1, suggesting that purifying selection was applied to the PtSRS gene family during evolution.
3.5. Cis-Acting Element Analysis of the PtSRS Gene Family
Cis-acting elements are essential for regulating gene expression and responding to environmental changes during different phases of plant growth and development [52]. We extracted coding sequences (CDSs) upstream of 2000 bp of the P. tremula SRS gene to study the cis-acting elements; 33 cis-acting elements in all were discovered. Based on their function, these cis-acting elements were grouped into four classes: light response, stress response, phytohormone response and tissue-specific expression. As demonstrated in Figure 5, numerous cis-acting elements connected with the light response are present in each gene; it is hypothesized that its function is related to the light response pathway. The phytohormone-responsive elements include methyl jasmonate (MeJA), salicylic acid (SA), growth hormone (Auxin), gibberellin (GA), and abscisic acid (ABA). The stress response consists of four stresses: low-temperature stress, drought stress, defense, and anaerobic induction. In addition, PtSRS genes were found to be connected to the cell cycle regulation, metabolism regulation, seed-specific regulation, endosperm expression, and meristem expression during the investigation of tissue-specific expression patterns of cis-acting elements. The above results indicate that the PtSRS family members contain abundant cis-acting elements, which are hypothesized to participate in a variety of important metabolic activities and have a very extensive array of biological functions.
3.6. Analysis of the Expression Pattern of the PtSRS Gene During Drought and Salt Stress
Plant SRS genes are crucial in responding to abiotic stress. In this study, we analyzed the expression patterns of the PtSRS gene family under drought stress and salt stress. As demonstrated in Figure 6A, after subjecting P. davidiana to natural drought treatment for six periods (0 d, 2 d, 4 d, 6 d, 8 d, and 10 d), the expression of most SRS genes increased, whereby PtSRS02 gene’s expression was significantly increased in all periods; PtSRS01, PtSRS03, PtSRS04, PtSRS05, and PtSRS08 all showed a peak in gene expression at 8 d. The expression of PtSRS04 was the highest, with it increased by more than 700-fold at 8 d, suggesting that the PtSRS04 gene may be able to resist drought stress by increasing gene expression. In addition, PtSRS06 only showed a significant difference at 10 d; in comparison, PtSRS07, PtSRS09, and PtSRS10 showed significantly lower gene expression after being subjected to drought stress.
The results for NaCl stress are shown in Figure 6B. After P. davidiana was subjected to NaCl treatment for six periods (0 h, 3 h, 6 h, 12 h, 24 h, and 48 h), some PtSRS genes had a similar pattern of expression. The expression of PtSRS03, PtSRS04, PtSRS05, PtSRS06, PtSRS07, and PtSRS09 was significantly elevated at 48 h; among them, the relative expression of PtSRS05 was the highest, with a 38-fold increase in relative gene expression levels at 48 h. PtSRS01, PtSRS02, and PtSRS08 showed decreased gene expression after stress; PtSRS10 gene expression first increased at 3 h and 6 h and then decreased significantly at 12–48 h.
4. Discussion
4.1. Characterization of the PtSRS Gene Family
Due to their inherent properties, plants are not able to avoid adverse environmental factors as effectively as animals; thus, when faced with abiotic stress, a complex regulatory network is formed in plants to help them resist adversity, and transcription factors are crucial in this process [53,54]. As a key transcription factor, the SRS gene family is significant in adversity stress and has great potential for the genetic improvement of plant resistance [12,22,55]; nevertheless, the SRS gene family of poplar has not been systematically and comprehensively investigated.
In this paper, we conducted a thorough analysis of the poplar SRS gene family, and the findings revealed that 10 SRS genes in the P. tremula genome, distributed unevenly among seven chromosomes (Figure 1). The number of poplar SRS family members is similar to A. thaliana (11) [2], quinoa (Chenopodium quinoa) (10) [56], and tomato (Solanum lycopersicum) (8) [57], suggesting that most species have a low number of SRS gene family members and that gene retention and duplication largely conform to similar evolutionary constraints [58].
The different exon and intron splicing states are essential for the evolution of the PtSRS gene. Although introns are spliced out during transcriptional expression and do not participate in protein formation, their relative positions provide an insight into the evolution of genes and the proteins that correspond to them, besides contributing to an enhanced comprehension of the diversity of gene structure [59]. In this study, we found similar gene structures in each subgroup. We found a small number of introns in groups Ⅰ and Ⅱ, most of which were recorded as one (Figure 3), which may be the result of the loss of introns throughout the evolution of PtSRS genes. The structural diversity of genes accelerates the development of gene families and facilitates the production of genes with new roles, thus improving the plants’ capacity to adjust to changing environment [60]. In all, 10 conserved motifs were discovered, and it was found that PtSRS genes from the same subfamily exhibited the same motif composition, indicating that they serve comparable functions in the life activities of plants. The gene structure and motifs show similarities between each subfamily, providing a further basis for subfamily classification.
4.2. PtSRS Gene Family Expansion Is Determined by Segmental Duplication
Regarding the evolutionary aspect of gene duplication, it is a major factors propelling genetic systems and genome evolution [61]. Gene families arise through a common ancestor via gene duplication, and the most common types of gene family expansion are segmental duplication and tandem duplication [52]. We examined SRS gene duplication events in poplar and found eight pairs of genes in collinearity and that these duplication gene pairs were the result of segmental duplication (Figure 4), this aligns with the findings of earlier research [20,39,55]. Thus, it may be shown that the primary mechanism of the SRS gene family’s evolution may be segmental duplication in higher plants. Gene positive selection analysis is a common method for molecular evolutionary studies. The size relationship (Ka/Ks) between synonymous and non-synonymous substitutions is compared to determine the selective pressure acting on target protein-coding genes and to determine the type and strength of natural selection. Based on our Ka/Ks analysis results (Table 2), all duplication genes have a Ka/Ks ratio below 1, indicating that the PtSRS undergoes purifying selection upon duplication; it is possible that these duplicated genes may have maintained their ancestral functionality.
4.3. Biological Functions of PtSRS
Cis-acting element analysis helps to understand the role that genes play in transcription and expression in plants [62,63,64]. The cis-acting element of PtSRS mainly contains light-responsive acting elements, tissue-specific expression acting elements, phytohormone-responsive acting elements, and stress-related acting elements (Figure 5). Light-responsive acting elements are key determinants of molecular changes in addition to the biochemical composition of plants in a wide range of biological processes [65]. A significant quantity of light response-related action elements have been found in this family member. For example, the G-box (CACGAC) element is distributed in each family member, suggesting that the PtSRS are connected to the growth and development of plants. In the phytohormone response element, most PtSRS genes contain ABRE cis-acting elements, indicating that they may be associated with salt tolerance [66,67]. In addition, the cis-regulatory elements of PtSRS in response to stress are abundant and, in particular, the MBS (CAACTG) element has been identified in most of the family members, suggesting that PtSRS family members may regulate the drought response through possible interactions with drought-inducible, abscisic acid, gibberellin, and other transcription factor binding sites.
Members of the SRS family participate in physiological processes, such as lateral root formation [12,68], phytohormone response [2,11], floral organ development [3,9], and the regulation of photomorphogenesis [69]. The SRS gene family has been implicated in environmental stress tolerance through cis-acting element analysis and related research in recent years, demonstrating the value of its potential role in genetic improvement efforts for crop resistance. GmSRS18, as a negative regulator, significantly increases resistance to salinity and drought in transgenic A. thaliana [12]. GhSRS21 increases cotton’s tolerance to salt stress by regulating the homeostasis of reactive oxygen species [21]. In Melilotus albus and M. sativa, several SRS genes can react to salt stress and low temperatures [22,55]. Understanding the expression patterns of genes under adversity stress is essential for functional gene mining. In this study, we used qRT-PCR to analyze the PtSRS gene expression pattern under salt and drought stress. The findings indicated that some of the PtSRS genes exhibited significant changes in relative gene expression levels after being subjected to stress; for example, the relative gene expression level of PtSRS04 gene was increased 700-fold after 8 d of drought stress treatment, and the relative gene expression level of PtSRS05 gene was increased 38-fold after 48 h of salt stress treatment., inferring that they may help the poplar resist adversity by increasing gene expression levels. Therefore, PtSRS04 and PtSRS05 can serve as important candidate genes for stress tolerance, and their functions need to be verified through future in-depth studies.
5. Conclusions
In conclusion, 10 SRS genes were found in the P. tremula genome. These 10 genes were distributed unevenly among seven chromosomes, and based on our systematic analysis results, they are categorized into five subfamilies. The genes within the same subfamily have analogous structures and motif compositions, indicating that they likely perform comparable functions in biological processes. The results of our evolutionary study of the gene family indicated that the expansion of the poplar SRS gene family is attributable to segmental duplication. Studies on cis-acting elements revealed that PtSRS genes are abundant in cis-acting elements connected to plant growth, development, and abiotic stress, and they will probably play significant roles in the development of plants and during stress. Research on the expression patterns of PtSRS in drought stress and NaCl stress demonstrated that most of the PtSRS participated in the stress response, and that the relative gene expression levels of PtSRS04 and PtSRS05 were the most significant, suggesting that they may be able to resist adversity by regulating the level of gene expression in the presence of abiotic stress and can be utilized as candidate genes for molecular breeding in poplar. To summarize, the findings of this study present a theoretical groundwork for further in-depth investigation of the biological functions of PtSRS and the study of poplar stress tolerance.
Conceptualization, H.B. and Y.W. Validation, Z.Y., H.L. and J.L. Formal analysis, Z.L., H.Z. and H.W. Data Curation, Z.Y., H.L. and C.G. Writing—original draft preparation, Z.Y. and H.L. Writing—review and editing, H.B., Y.W. and J.L. Supervision, H.B. and Y.W. Constructive suggestions, T.S. and P.S. All authors have read and agreed to the published version of the manuscript.
All data supporting the findings of this study are available within the paper and
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 2. SRS protein phylogenetic relationship from P. tremula, A. thaliana, C. grandiflora, Z. mays, S. purpurea, and O. sativa. SRS subfamilies are classified using different colors to differentiate them, and SRS proteins of different species are represented using different shapes and colors.
Enlarge this image.Figure 3. The PtSRS family’s conserved motifs and gene structure: (A) the PtSRS family’s unrooted phylogenetic tree and members were categorized into five subfamilies; (B) conserved motif distribution of PtSRS proteins; (C) gene structure of PtSRS genes.
Enlarge this image.Figure 4. Collinearity mapping of PtSRS. The outer circle represents the 19 chromosomes of the P. tremula, and the inner circle represents the density of genes on the chromosomes. The blue curve represents the collinear gene pairs in PtSRS.
Enlarge this image.Figure 5. Statistics and analysis of cis-elements of the PtSRS gene. The figures within the box denote the quantity of cis-acting elements.
![View Image - Figure 6. The PtSRS gene expression pattern in potted seedlings of P. davidiana: (A) drought treatments and (B) NaCl treatments. Use of 18S as the housekeeping gene. The X-axis shows stress time and the Y-axis shows gene expression. The values are represented by the mean ± standard deviation (n = 3). An asterisk means that there was a notable difference between the gene expression levels before treatment and the levels at each time point following stress treatment (* p [less than] 0.05).](https://media.proquest.com/media/hms/THUM/12/G48jb?_a=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&_s=KBfwev5qd4SMavwr6a4L8ybvJUQ%3D "View Image - Figure 6. The PtSRS gene expression pattern in potted seedlings of P. davidiana: (A) drought treatments and (B) NaCl treatments. Use of 18S as the housekeeping gene. The X-axis shows stress time and the Y-axis shows gene expression. The values are represented by the mean ± standard deviation (n = 3). An asterisk means that there was a notable difference between the gene expression levels before treatment and the levels at each time point following stress treatment (* p [less than] 0.05).")
Enlarge this image.Figure 6. The PtSRS gene expression pattern in potted seedlings of P. davidiana: (A) drought treatments and (B) NaCl treatments. Use of 18S as the housekeeping gene. The X-axis shows stress time and the Y-axis shows gene expression. The values are represented by the mean ± standard deviation (n = 3). An asterisk means that there was a notable difference between the gene expression levels before treatment and the levels at each time point following stress treatment (* p [less than] 0.05).
Detailed information on the 10 PtSRS proteins.
| Gene Id | Gene Name | Protein Length (aa) | Predicted Mw (kDa) | Theoretical pI | Aliphatic Index | Gravy | II |
|---|---|---|---|---|---|---|---|
| Potra2n1c228.5 | PtSRS01 | 436 | 47.92 | 9.03 | 65.55 | −0.498 | 47.02 |
| Potra2n1c2350.1 | PtSRS02 | 348 | 36.31 | 8.13 | 64.51 | −0.488 | 36.21 |
| Potra2n2c6186.1 | PtSRS03 | 314 | 34.46 | 8.55 | 46.37 | −0.816 | 59.04 |
| Potra2n3c6709.1 | PtSRS04 | 370 | 40.59 | 8.48 | 60.95 | −0.572 | 50 |
| Potra2n4c9865.1 | PtSRS05 | 204 | 22.67 | 8.98 | 53.58 | −0.636 | 55.17 |
| Potra2n5c10747.1 | PtSRS06 | 391 | 42.8 | 9.18 | 60.46 | −0.605 | 61.88 |
| Potra2n5c11757.1 | PtSRS07 | 374 | 41.21 | 6.5 | 65 | −0.579 | 48.86 |
| Potra2n7c16484.1 | PtSRS08 | 332 | 35.93 | 6.65 | 58.83 | −0.613 | 62.98 |
| Potra2n9c19050.1 | PtSRS09 | 205 | 22.93 | 9.02 | 54.78 | −0.593 | 61.86 |
| Potra2n9c19538.1 | PtSRS10 | 353 | 36.84 | 8.73 | 61.08 | −0.48 | 32.33 |
Ka/Ks analysis of PtSRS duplication gene pairs.
| Gene 1 | Gene 2 | Ka | Ks | Ka/Ks | Duplication Type | T (MYA) |
|---|---|---|---|---|---|---|
| PtSRS07 | PtSRS08 | 0.077616 | 0.275154 | 0.282082 | Segmental Duplication | 15.12 |
| PtSRS09 | PtSRS05 | 0.085775 | 0.213091 | 0.40253 | Segmental Duplication | 11.71 |
| PtSRS03 | PtSRS06 | 0.079848 | 0.234788 | 0.340087 | Segmental Duplication | 12.9 |
| PtSRS02 | PtSRS10 | 0.045453 | 0.222736 | 0.204068 | Segmental Duplication | 12.24 |
Supplementary Materials
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References
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; Li, Haixia 1 ; Li, Jing 1 ; Guo, Chengbo 1 ; Li, Zhenghua 1 ; Zhang, Haifeng 1 ; Wang, Hongmei 1 ; Tuya Siqin 2 ; Sun, Peilin 2 ; Wang, Yanmin 1 ; Bai, Hui 1 1 Forestry Research Institute of Heilongjiang Province, Harbin 150081, China;
2 Heilongjiang Institute of Atomic Energy, Harbin 150086, China;