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Article

Identification and Analysis of SOD Family Genes in Peanut (Arachis hypogaea L.) and Their Potential Roles in Stress Responses

by
Shutao Yu
1,2,
Chuantang Wang
1,3,*,
Qi Wang
3,
Quanxi Sun
3,
Yu Zhang
1,2,
Jingchao Dong
2,
Yechao Yin
2,
Shihang Zhang
2 and
Guoqing Yu
2,*
1
College of Agronomy, Shenyang Agricultural University, Shenyang 110161, China
2
Institute of Sandy Land Management and Utilization of Liaoning, Fuxin 123000, China
3
Shandong Peanut Research Institute, Qingdao 266100, China
*
Authors to whom correspondence should be addressed.
Agronomy 2023, 13(8), 1959; https://doi.org/10.3390/agronomy13081959
Submission received: 15 June 2023 / Revised: 14 July 2023 / Accepted: 23 July 2023 / Published: 25 July 2023
(This article belongs to the Special Issue Advances in the Industrial Crops)
Browse Figures
Versions Notes

Abstract

:
Superoxide dismutases (SODs) are crucial in safeguarding plants against reactive oxygen species (ROS) toxicity caused by abiotic or biotic factors. Although recent research has revealed the involvement of the SOD gene family in plant biological processes, the understanding of the SOD gene family in peanut remains inadequate. This study comprehensively characterizes the SOD gene family in the peanut genome. A total of 25 AhSOD genes were identified and subsequently categorized into three subfamilies: sixteen AhCSDs, six AhFSDs, and three AhMSDs according to the phylogenetic tree. A comprehensive analysis revealed that the AhSOD genes underwent segmental duplications. The majority of AhSOD genes exhibited conserved exon–intron and motif structures within the same subfamily. The examination of cis-acting elements within the promoter regions of SOD genes revealed that the expression of AhSOD was subject to regulation by plant hormones, as well as responses to defense and stress. RNA-seq analysis showed expression diversity of AhSOD genes in various tissues and cold, drought, and salt stresses. Furthermore, the regulation of AhSOD gene expression is anticipated to involve numerous transcription factors. The gene ontology annotation results validate the role of AhSOD genes in various stress stimuli, SOD activity, reactive oxygen species metabolic processes, and cellular oxidant detoxification processes. This investigation serves as the initial genome-wide analysis of the AhSOD gene family, providing a basis for comprehending the function of the AhSOD gene family and enhancing plant tolerance to cold, drought, and salt stresses.

1. Introduction

Abiotic stresses such as drought, salt, cold, and heavy metal poisoning negatively affect plant development and crop yield. These stresses induce the overproduction of toxic reactive oxygen species (ROS), which leads to oxidative stress and eventual cell death [1,2]. Plants have developed intricate enzymatic antioxidant defense systems, including the superoxide dismutase (SOD) system, peroxidase (POD) system, catalase (CAT) system, and ascorbate peroxidase (APX) system, in order to deal with these overwhelming toxic ROS [3]. The SOD enzymes have a significant function in protecting plants from oxidative stress. They are capable of catalyzing the dismutation of the harmful superoxide anion (·O2−) into molecular oxygen (O2) and hydrogen peroxide (H2O2) within plant cells when exposed to oxidative stress [4,5,6].
Metalloenzymes called plant SODs have been found in different parts of plants, such as roots, leaves, fruits, and seeds. These enzymes play vital roles in protecting against oxidative stress. Plant SODs can be classified into three subgroups depending on the metal ions they bind, which are Cu/Zn-SOD (CSD), Fe-SOD (FSD), and Mn-SOD (MSD) [7,8]. Arabidopsis thaliana has three members (CSD1-3, FSD1-3) in both the Cu/Zn-SOD and Fe-SOD subfamilies, while the Mn-SOD subfamily has two members (MSD1-2) [9]. Previous studies showed that SODs localized in various cellular organs. CSD primarily occurred in the cytoplasm, chloroplasts, peroxisomes, and also in the extracellular region [10]. The localization of FSD is mainly in the chloroplasts, while MSD is typically found in the mitochondria, although a small number of proteins can be found in the peroxisomes [11,12].
Exposure of plants to diverse environmental pressures, such as low temperatures, water scarcity, and salinity, triggers an elevation in the levels of reactive oxygen species (ROS), resulting in varied biochemical responses within plant cells. Scavenging ROS, SOD is commonly recognized as the initial component of the antioxidant defense system, serving a protective function. Multiple research studies have shown that the SOD individuals can participate in the reaction to non-living pressures and control the aging process of plants [13,14]. For example, an increase in SOD activity helps Brassica juncea plants exhibit high resistance to abiotic stress, including salt and drought stress [15], and cold caused oxidative damage to tomato (Solanum lycopersicum) [16]. Moreover, various environmental pressures can trigger the activation of the SOD genes. During periods of drought, the expression of the MnSOD gene in wheat (Triticum aestivum) was significantly increased [17]. It is worth mentioning that according to reports, the overexpression of SikCuZnSOD3 has been found to enhance the resistance of cotton (Gossypium hirsutum) to drought, salt, and cold stresses [18]. In rice (Oryza sativa), transgenic plants’ overexpression of OsMSD1 displayed higher tolerance to heat, whereas knock-out msd1 mutants was notably susceptible to the same stress [19]. Moreover, the overexpression of MeCu/ZnSOD and MeCAT1 has been observed to significantly improve cold and drought tolerance in cassava (Manihot esculenta) [20]. Notably, overexpression of AtHDG11 and AhWRKY75 improved drought and salt tolerance in peanut by increasing the activity of SOD [21,22]. Collectively, these investigations have demonstrated that enhanced SOD activity and increased expression of genes encoding SOD can serve as mechanisms for enhancing plant resilience to various environmental stressors.
The complete determination of the SOD gene family has been conducted in different plant species, encompassing monocots like rice (Oryza sativa) [23], wheat (Triticum aestivum) [24], and sorghum (Sorghum bicolor) [25], as well as dicots such as cotton (Gossypium hirsutum) [26], alfalfa (Medicago truncatula) [10], and rapeseed (Brassica napus) [27]. Cultivated peanut (Arachis hypogaea L.) is a globally significant crop that plays a vital role in the economy. It serves as a valuable source of oils and proteins for human consumption. During the growing phase, peanut experienced various environmental pressures such as cold, high salinity, and drought. Numerous reports have been published on various gene families of peanuts since the release of the peanut genome database [28,29,30]. However, we have very limited knowledge about the SOD gene family. Considering significant roles of the SODs in participating in stress responses, a total of 25 peanut SOD members were identified from the peanut database in this study. The identified AhSODs were comprehensively analyzed for phylogenetic relationship, gene structure, cis-acting elements, chromosomal location, duplication event, and expression patterns. The findings indicate that peanut SOD members potentially fulfill significant functions in peanut development and in the adaptation to diverse environmental challenges.

2. Materials and Methods

2.1. Identification and Sequence Analysis of the AhSOD Gene Family

Two methods were carried out to identify the SOD family members in peanut. The peanut genome data and Arabidopsis genome data were obtained from Peanut Base (https://legacy.peanutbase.org/peanut_genome, accessed on 20 March 2023) and The Arabidopsis Information Resource (TAIR, https://www.arabidopsis.org/, accessed on 20 March 2023), respectively. First, the HMM profiles of CSD (PF00080) and FSD/MSD (PF00081, PF02777) were employed to search for peanut protein sequences using the HMMER program (version 3.0; Robert D Finn, Ashburn, VA, USA, 2015), with a designated E-value threshold of 0.001. Second, the BLASTP program was utilized to search the peanut protein database using the published protein sequences of Arabidopsis SOD [9] as queries, with a cutoff E-value of 0.001. Subsequently, all candidate sequences of SOD protein were verified with CDD (https://www.ncbi.nlm.nih.gov/Structure/cdd/, accessed on 20 March 2023), SMART [31], and InterProScan databases [32]. Candidate protein sequences without SOD domains were manually deleted. Using the online tool ProtParam [33], the peanut SOD proteins were analyzed for their physical and chemical characteristics, such as the number of amino acids, molecular weight (MW), and theoretical isoelectric point (pI).

2.2. Construction of Phylogenetic Trees and Alignment of Multiple Sequences

Utilizing MAFFT [34] with default parameters, a multiple sequence alignment (MSA) of Arabidopsis SOD and recently found peanut SOD proteins was performed in the current investigation. The MEGA software (version 6.06) [35] was utilized to create a neighbor-joining (NJ) tree using pairwise deletion, Poisson model, and 1000 bootstrap tests, based on the obtained sequence alignment.

2.3. Conserved Motifs and the Structure of Exons-Introns

The structure of peanut SOD genes, including the 5′-UTR, CDS, intron, and 3′-UTR, was analyzed using the online software GSDS 2.0 [36], by examining their mRNA and genomic sequences. The preserved patterns of peanut SOD proteins were examined utilizing the MEME software (version 5.5.3) [37], employing particular settings such as distribution of sites, either zero or one instance per sequence (zoops), a maximum of 15 patterns, and a pattern width varying from six to 50 residues.

2.4. Chromosomal Distribution and Gene Duplication Event

Peanut Base provided the chromosomal location data for SOD genes in peanuts. The online tool MG2C v2.1 (http://mg2c.iask.in/mg2c_v2.1/, accessed on 25 March 2023) was used to create the physical map. Genes that exhibited a similarity of more than 70% and were situated within a 200 kb segment of a chromosome were recognized as tandem duplication genes and were visualized on the peanut chromosomes. MCScanX [38] and TBtools (version 1.120) [39] were utilized to examine and display the genes involved in segmental duplication. Subsequently, the duplication genes’ Ka and Ks values were calculated using the DnaSP 5.0 program [40].

2.5. Analysis of cis-Elements within the AhSODs Promoter

To identify the cis-acting regulatory elements present in the promoter regions of the AhSODs, a segment of 2000 bp from the promoter regions, which are situated before the ATG start codon of the peanut SOD genes, was extracted and then sent to PlantCARE [41].

2.6. Tissue Expression Pattern Analysis of AhSOD Genes

The transcriptome (RNA-Seq) data (accession: PRJNA291488) for peanut SOD genes across various tissues were downloaded from the Peanut Base. A total of 22 tissues, including leaf 1, leaf 2, leaf 3, veg shoot, repr shoot, root, nodule, perianth, stamen, pistil, peg tip 1, peg tip 2, peg tip Pat. 1, fruit Pat. 1, fruit Pat. 3, pericarp Pat. 5, seed Pat. 5, and seed Pat. 7, were selected for expression analysis. TBtools (version 1.120) [39] was used to generate the heat map.

2.7. Prediction of Transcription Factors Involved in Controlling AhSOD Expression

To gain a deeper comprehension of the transcription factors that regulate AhSODs expression, the promoter sequences were utilized to examine potential binding sites for transcription factors. Specifically, the promoter sequences of AhSOD genes, with a length of 2 kb, were submitted to the PlantRegMap database, and the Binding Site Prediction tool was employed to predict the transcription factors that regulate AhSODs expression with a p value of ≤10−5 [42].

2.8. GO Enrichment Analysis

To perform the Gene Ontology (GO) annotation analysis, the protein sequences of all AhSODs were submitted to the eggNOG website [43]. GO enrichment analysis was conducted using TBtools (version 1.120) [39].

3. Results

3.1. Identification and Characterization of AhSODs

The BLASTP method and HMM search were employed to identify SOD gene family members from the peanut genome. After checking the presence of SOD domains (PF00080, PF00081, and PF02777) in each candidate, a total of 25 AhSOD members were identified. The distribution of these genes was observed across 13 chromosomes in peanuts and were designated as AhSOD01 to AhSOD25, based on their respective chromosomal locations. The characteristics of the peanut SOD members including the number of amino acids, Mw, and pI were analyzed (Supplementary Table S1). The amino acid count of the 25 AhSOD members varied between 103 (AhSOD04) and 414 (AhSOD05) in terms of protein length. The molecular weight of the AhSOD proteins varied between 11.02 kDa (AhSOD04) and 46.95 kDa (AhSOD05). The pI ranged from 5.04 (AhSOD01) to 9.63 (AhSOD05).

3.2. Phylogenetic Tree Construction

In order to examine the evolutionary relationships among the peanut SOD gene family members, a neighbor-joining tree was created utilizing the complete amino acid sequences of SOD from both peanut and Arabidopsis (Figure 1). The results of the phylogenetic analysis indicated that the peanut SOD proteins can be categorized into three subfamilies, along with the previously reported eight Arabidopsis SODs. Specifically, there are sixteen AhCSDs, six AhFSDs, and three AhMSDs. Furthermore, it is observed that the FSD subfamily and MSD subfamily exhibit distinct clustering, indicating that these subfamilies might have originated from a shared ancestor through early replication. It is noteworthy that all subfamilies encompass representatives from both peanut and Arabidopsis, implying that the divergence of peanut and Arabidopsis occurred subsequent to that of the SOD gene family.

3.3. Conserved Motifs and the Structure Exon–Intron

The analysis of gene structure has the potential to yield significant insights into the evolutionary history of the SOD family in peanut. In order to generate a comprehensive understanding of the gene structures, both mRNA and genome sequences were utilized (Figure 2). The results indicated that the number of introns present in the peanut SOD gene family ranged from two (AhSOD01/14/16/24) to eleven (AhSOD19). It is noteworthy that the peanut SOD genes within the same subfamily exhibited a similar structure, thereby corroborating the results of our evolution analysis. The online software MEME (version 5.5.3) was subsequently employed to examine motif composition in the peanut SOD family. A total of ten unique motifs were identified (Figure 2, Supplementary Figure S1). Notably, motifs 2, 5, and 7 correspond to the SOD domain, and all SOD members identified possess at least one of these motifs. Additionally, members belonging to the same subfamily exhibit similar motifs.

3.4. Chromosomal Localization and Duplication Events

The result of chromosome localization showed that 25 peanut SOD genes were positioned on 13 peanut chromosomes (Figure 3). The peanut SOD genes were most abundant in Chr16 and Chr20, with a total of four genes. In contrast, Chr5, Chr6, Chr11, Chr13, Chr15, and Chr19 only had one peanut SOD gene each. It is interesting to note that most peanut SOD genes were close to the chromosome terminal. Furthermore, there were no instances of tandem duplication events detected within the SOD gene family of peanuts.
Moreover, we conducted a study on the duplication events of SOD genes in peanuts. A total of nine segmental duplication events were identified between 16 peanut SOD genes (Figure 4). These findings indicated that certain peanut SOD genes are possibly generated by gene duplication, and the segmental duplication events may have served as a significant driving force for peanut SOD evolution (Supplementary Table S2). In order to assess the potential impact of selective pressure on the SOD gene family, the Ka/Ks values were computed for the nine SOD gene pairs. Analysis revealed that nine segmental duplicated peanut SOD gene pairs exhibited Ka/Ks ratios below 1, indicating that a purifying selection pressure was imposed on these SOD genes throughout the course of evolution.

3.5. Analysis of AhSOD Genes Syntenic

To better understand the phylogenetic relationship among the SOD genes in peanut, three syntenic maps were generated for peanut and three other plant species, including Arabidopsis, soybean, and tomato (Figure 5). The analysis revealed that 11 peanut SOD genes exhibited a syntenic relationship with the SOD genes in soybean, followed by Arabidopsis (eight), and tomato (six). The numbers of predicted orthologous pairs between the other three species (soybean, Arabidopsis, and tomato) were twenty-one, eight, and six, respectively. Moreover, it was discovered that certain peanut SOD genes exhibited a minimum of three collinear gene pairs with soybean, including AhSOD03, AhSOD07, and AhSOD18, suggesting their potential importance in the evolution of the SOD gene family in peanut. Moreover, it was discovered that there are four gene pairs that are in a straight line between peanut and the other three species. This suggests that these SOD genes already existed before the species diverged (Supplementary Table S3).

3.6. Promoter Analysis of AhSOD Genes

The importance of SOD genes in the plant response to abiotic stress is supported by accumulating evidence. To gain insight into the potential regulatory mechanisms of AhSOD genes in abiotic stress or hormonal responses of peanut, the cis-acting elements in the promoter regions of the AhSOD genes were analyzed using plantCARE. We have chosen 11 cis-acting elements for the purpose of visualization (Figure 6). Four types of hormone-responsive elements, including ABRE, CGTCA-motif, GARE-motif, and TCA-element, were detected in two peanut SOD genes (AhSOD01 and AhSOD18). These cis-elements are involved in abscisic acid (ABA) response, methyl jasmonate (Me-JA) response, gibberellin (GA) response, and salicylic acid (SA) response, respectively. The results suggested that ABA, Me-JA, GA, and SA might regulate the expression of these genes. Additionally, any hormone-responsive elements were not identified in two genes (AhSOD14 and AhSOD20). Moreover, the promoters of peanut SOD genes were found to contain seven different types of elements associated with environmental stress. Various stress responses may involve these peanut SOD genes as the anaerobic induction elements (ARE) were found in twenty-one genes, low temperature responsive elements (LTR) in six genes, drought-inducibility elements (MBS) in eight genes, stress response elements (STRE) in fifteen genes, defense- and stress-responsive elements (TC-rich repeats) in seven genes, wound-responsive elements (WUN motif) in sixteen genes, and WRKY binding site (W-box) in eleven genes.

3.7. Tissue Expression Pattern of AhSOD Genes

In order to comprehend the potential roles of the peanut SOD genes, an examination of their expression patterns in different tissues was conducted utilizing RNA-Seq data sourced from the Peanut Base. A total of 22 distinct tissues, including but not limited to the leaf, shoot, root, nodule, fruit, and seed, were selected for analysis. (Figure 7). Expression patterns showed that 84% (21 out of 25) of genes were expressed in most of these selected tissues, such as AhSOD02, AhSOD10, AhSOD11, AhSOD13, AhSOD18, and AhSOD25. Certain peanut SOD genes exhibited expression patterns specific to particular tissues. For instance, the expression of AhSOD14 was only detected in the seed. Furthermore, AhSOD08 and AhSOD20 were highly expressed in leaves compared to the other tissues. It is worth mentioning that none of the tissues tested showed expression of four SOD genes, including AhSOD01, AhSOD04, AhSOD16, and AhSOD17.

3.8. Expression Patterns of AhSOD Genes under Stress Treatments

To clarify the expression patterns of peanut SOD genes under abiotic stresses, we analyzed transcriptome data obtained from NCBI after exposure to cold (unpublished data), drought, and salt stresses [44,45]. Various expression patterns were observed in the majority of peanut SOD genes (Figure 8). Cold stress resulted in up-regulation of 68% (17 out of 25) genes. Furthermore, the expression of AhSOD18 was found to be increased significantly under all three stresses and suggested that this gene may play a crucial role in response to these abiotic stresses. Various peanut SOD genes exhibited contradictory expression patterns in response to these stressful conditions. For instance, AhSOD11, AhSOD24, and AhSOD25 were insensitive to salt and drought stresses, whereas they were significantly induced by cold stress. Furthermore, there were no notable alterations in the expression of certain AhSOD genes, such as AhSOD14 and AhSOD17, following exposure to cold, drought, and salt stress treatments. The diverse patterns of expression observed in peanut SOD genes signify their distinct functions in response pathways to abiotic stresses.

3.9. Analysis of Possible Regulatory Interactions between Transcription Factors and AhSODs

To predict possible regulatory connections between transcription factors (TFs) and AhSOD genes, the PlantRegMap online software (version 5.0) was employed. A total of 17 TFs were identified as potential regulators of AhSOD gene expression. TBtools was used to determine and visualize the number of possible binding motifs for transcription factors (TFs) in the promoters of AhSOD genes (Figure 9). The regulatory patterns of AhSOD07, AhSOD21, and AhSOD23 were found to be similar, as they were all regulated by ERF, MYB, and Dof. Furthermore, a distinct group comprising AhSOD12, AhSOD20, and AhSOD25 exhibited comparable regulatory patterns, which were governed by AP2, MIKC_MADS, and TALE. It is noteworthy that the promoter of AhSOD14 contains only one binding site for NAC transcription factors, indicating that AhSOD14 may not be subject to regulation by transcription factors other than NAC.

3.10. GO Enrichment Analysis of AhSOD Genes

The AhSODs genes’ functions were predicted via GO enrichment analysis, which encompassed the biological process (BP), molecular function (MF), and cellular component (CC) categories. The GO enrichment outcomes unveiled a multitude of significantly enriched terms. The analysis of BP annotations showed that these genes mainly participated in responses to superoxide (GO:0000303), responses to oxidative stress (GO:0006979), responses to stress (GO:0006950), responses to salt stress (GO:0009651), responses to abiotic stimulus (GO:0009628), response to toxic substance (GO:0009636), detoxification (GO:0098754), reactive oxygen species metabolic process (GO:0072593), etc. (Supplementary Figure S2). In summary, the GO enrichment analysis substantiated the involvement of AhSODs in various stress stimuli responses, cellular detoxification of oxidants, and SOD activity.

4. Discussion

Previous studies reported that SOD (superoxide dismutase) genes have been found to play crucial roles in both abiotic stress responses and plant development processes by scavenging ROS [46]. Given that cultivated peanut (Arachis hypogaea L.) is a crucial crop for the economy and oil production, it is also susceptible to various abiotic stresses such as cold, drought, and salt. The identification and analysis of SOD genes in peanut would hold significant implications for various stress responses. Thus far, various plant species have been found to possess SOD family genes, including Zostera marina with five genes [47], Medicago truncatula and barley (Hordeum vulgare) with seven genes [10,48], sorghum (Sorghum bicolor) with eight genes [25], tomato (Solanum lycopersicum) with nine genes [49], grape (Vitis vinifera) with ten genes [50], cotton (Gossypium spp.) with eighteen genes [26], banana (Musa spp.) with twenty-five genes [51], wheat (Triticum aestivum) with twenty-six genes [24], and Brassica juncea with twenty-nine genes [52]. However, a comprehensive analysis of the SOD gene family in peanut remains to be carried out. The Arabidopsis genome contains only eight SOD genes, whereas the present study identified a total of twenty-five SOD genes in peanut, which is likely attributed to its allopolytraploid nature. The classification of SOD genes in peanut is consistent with that of other plant species, such as tomato [49] and wheat [24]. Based on their domains and motifs, the peanut SOD members were divided into three subfamilies, which consisted of sixteen AhCSDs, six AhFSDs, and three AhMSDs (Figure 1).
The gene structure and conserved motifs have a significant impact on the evolution of the SOD gene family. The Arabidopsis ERECTA gene, for instance, requires the presence of multiple introns for proper expression [53]. By examining the gene structure, it was found that the peanut SOD genes exhibited variations in the quantity of exons and introns (Figure 2). Specifically, the Fe-SOD subfamily exhibited a range of seven to eleven exons and six to ten introns, with the exception of AhSOD24, which contained three exons and two introns. The Mn-SOD subfamily, on the other hand, consistently exhibited six exons and five introns, with the exception of AhSOD01 that possessed three exons and two introns. Within the Cu/Zn-SOD subfamily, ten genes exhibited a range of six to twelve exons and five to eleven introns, while six genes contained three to five exons and two to four introns. Seven TaSOD genes were identified to contain seven introns in wheat [24], while the number of introns in sorghum ranged from five to seven [25]. Notably, the SOD genes within each cluster exhibited comparable exon–intron associations and conserved motifs (Figure 2). Additionally, the protein structure of AhSOD members is highly conserved within a same subfamily. The findings suggested that these genes may be involved in similar functions related to various abiotic stresses. Similar results have been reported in sorghum (Sorghum bicolor) [25], tomato (Solanum lycopersicum) [49], cotton (Gossypium spp.) [26], and wheat (Triticum aestivum) [24].
The expansion of gene families in plant genomes is attributed to segmental duplication and tandem duplication events [54,55]. The present study reveals that the AhSOD genes expansion in peanut is primarily due to segmental duplication, no tandem duplication. Nine pairs of segmental duplication were identified (Figure 4), and all of the Ka/Ks ratios associated with these duplication pairs were less than one (Supplementary Table S2). This finding suggested that the duplicated SOD genes in peanut may have undergone purifying selective pressure during the course of peanut evolution. Furthermore, the duplicated SOD genes in peanuts were found to be part of the same subfamily, such as AhSOD02/11 in Cu/Zn-SOD subfamily, AhSOD08/20 in Fe-SOD subfamily, and AhSOD09/22 in Mn-SOD subfamily. Notably, AhSOD05 and AhSOD13, as a segmental duplication pair, displayed uniform expression patterns across various organs and tissues (Figure 7).
In order to gain a deeper comprehension of the function of AhSOD genes in response to various environmental stresses, prophesying cis-acting elements in the promoter regions were conducted. The findings of this study revealed the identification of two distinct types of cis-acting elements, including stress- and hormone-responsive. The majority of the identified cis-acting elements were found to be associated with ABA, MeJA, GA, SA, drought, low temperature, and anaerobic induction. It was reported that cis-acting elements contribute to plant stress responses [56,57]. These consequences were corroborated by the results of the GO enrichment analysis (Supplementary Figure S2). Additionally, various researchers have reported similar results in various agricultural crops, where SOD genes were observed to play a crucial role in diverse stress conditions [24,52]. These findings can enhance our comprehension of AhSOD genes under varying environmental conditions. Furthermore, the regulation of SOD gene expression in plants in response to stress is mediated by transcription factors. Overexpression of MuWRKY3 in transgenic peanut resulted in significant up-regulation of SOD gene expression and subsequently improved drought stress tolerance in the transgenic plants [58]. Compared to wild-type plants, the expression levels of SOD, POD, and CBF genes in BpERF13 transgenic lines were dramatically up-regulated under cold stress [59]. Under salt treatment, the up-regulation of stress-related genes, including SOD, POD, APX, and P5CS, was observed in IbMYB308 transgenic plants [60]. Soybean (Glycine max) NAC2 transcription factor negatively regulates drought resistance in transgenic tobacco through the suppression of plant SOD genes expression, resulting in the accumulation of ROS [61]. Notably, the promoter region of the AhSOD genes was found to contain multiple predicted transcription factor binding sites, such as ERF, MYB, Dof, and NAC (Figure 9). This finding suggests that the AhSOD genes possess diverse regulatory mechanisms to adapt to the intricate external environment.
Previous studies have indicated that the expression of SOD genes differs across tissues [51,62]. Therefore, we utilized RNA-seq data to evaluate the tissue-specific expression levels of AhSOD genes in 22 distinct developmental tissues (Figure 7), which corroborated previous findings [26]. Notably, certain genes exhibited higher expression across all tested tissues, suggesting their potential involvement in the growth and development of peanut. In addition, crops are negatively impacted by three primary abiotic stresses: cold, drought, and salt stresses, which hinder their growth, development, and yields [63]. Under conditions of these abiotic stresses, plant cells will accumulate reactive oxygen species (ROS), and an excess of ROS will induce oxidative stress [1]. It should be emphasized that several SOD members have been documented to participate in the response to plant environmental pressures by scavenging ROS [46]. In the current study, the RNA-seq data of peanut under abiotic stresses showed that several genes were induced by cold, drought, and salt treatments (Figure 8). These findings are consistent with previous reports, which demonstrated elevated expression of multiple SOD genes in response to stresses. For example, some SOD genes were found to be up-regulated in response to cold, heat, salinity, and drought stresses in grape [64]. All SOD genes exhibited significant up-regulation in tomato when subjected to salt and drought treatments [49]. Similarly, the activity of SOD was notably enhanced in rapeseed when exposed to cold stress [65]. These results offer compelling evidence that SOD genes exhibit a conserved function in mitigating abiotic stresses across various plant species.

5. Conclusions

In this study, a total of 25 AhSOD members were identified from peanut, which were categorized into three subfamilies based on their Arabidopsis homologs. Our investigation of the SOD genes in both peanut and Arabidopsis demonstrated their variability in terms of member count, evolutionary connections, gene structure, chromosomal positions, gene duplication, collinearity, tissue-specific expression patterns, and responses to cold, drought, and salt stresses. The findings suggest that the AhSOD genes play a crucial role in modulating peanut response to abiotic stresses and growth.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy13081959/s1, Figure S1: The putative conserved motifs in AhSOD proteins; Figure S2: GO enrichment analysis of AhSOD genes; Table S1: The detail information of identified peanut SOD family members; Table S2: The detail information of segmental duplication gene pairs; Table S3: The syntenic pairs between peanut and other three plant species.

Author Contributions

C.W. and G.Y. conceived this research, designed the experiments. S.Y. conducted the research and drafted the manuscript. Q.W., Q.S., Y.Z., J.D., Y.Y. and S.Z. assisted in data collection and analysis. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the China Agriculture Research System of MOF and MARA (CARS-13), and the Liaoning BaiQianWan Talents Program (2021921070).

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, Guoqing Yu, upon reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Phylogenetic tree construction of peanut SOD proteins. The phylogenetic tree was constructed by aligning the SOD proteins from peanut and Arabidopsis, followed by 1000 bootstrap replicates using the neighbor-joining (NJ) method. The resulting classification of the peanut SOD members and their Arabidopsis homologs revealed the existence of three subfamilies.
Figure 1. Phylogenetic tree construction of peanut SOD proteins. The phylogenetic tree was constructed by aligning the SOD proteins from peanut and Arabidopsis, followed by 1000 bootstrap replicates using the neighbor-joining (NJ) method. The resulting classification of the peanut SOD members and their Arabidopsis homologs revealed the existence of three subfamilies.
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Figure 2. The exon–intron structure and conserved motif composition of AhSOD members.
Figure 2. The exon–intron structure and conserved motif composition of AhSOD members.
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Figure 3. Chromosomal distribution of peanut SOD genes. A total of 25 AhSOD genes were positioned on 13 peanut chromosomes in peanut.
Figure 3. Chromosomal distribution of peanut SOD genes. A total of 25 AhSOD genes were positioned on 13 peanut chromosomes in peanut.
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Figure 4. Duplication events of peanut SOD genes. MCScanX was used to investigate the nine presumed pairs of AhSODs that are segmental duplications, which are connected by the red lines.
Figure 4. Duplication events of peanut SOD genes. MCScanX was used to investigate the nine presumed pairs of AhSODs that are segmental duplications, which are connected by the red lines.
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Figure 5. Comparative analysis of the arrangement of SOD genes in peanut and three additional plant species. The collinear blocks between peanut and three other plant species were represented by the gray line in the background, whereas the syntenic SOD gene pairs were exhibited by the red line.
Figure 5. Comparative analysis of the arrangement of SOD genes in peanut and three additional plant species. The collinear blocks between peanut and three other plant species were represented by the gray line in the background, whereas the syntenic SOD gene pairs were exhibited by the red line.
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Figure 6. Cis-acting elements in the promoter regions of AhSOD genes.
Figure 6. Cis-acting elements in the promoter regions of AhSOD genes.
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Figure 7. The expression patterns of AhSOD genes in 22 different tissues. TBtools was used to normalize and cluster the FPKM values of each AhSOD gene.
Figure 7. The expression patterns of AhSOD genes in 22 different tissues. TBtools was used to normalize and cluster the FPKM values of each AhSOD gene.
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Figure 8. The gene expression profiles of AhSODs under cold, drought, and salt stress treatments. TBtools was used to normalize and cluster the FPKM values of each AhSOD gene.
Figure 8. The gene expression profiles of AhSODs under cold, drought, and salt stress treatments. TBtools was used to normalize and cluster the FPKM values of each AhSOD gene.
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Figure 9. Predicted transcription factors controlling the expression of AhSOD genes.
Figure 9. Predicted transcription factors controlling the expression of AhSOD genes.
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Yu, S.; Wang, C.; Wang, Q.; Sun, Q.; Zhang, Y.; Dong, J.; Yin, Y.; Zhang, S.; Yu, G. Identification and Analysis of SOD Family Genes in Peanut (Arachis hypogaea L.) and Their Potential Roles in Stress Responses. Agronomy 2023, 13, 1959. https://doi.org/10.3390/agronomy13081959

AMA Style

Yu S, Wang C, Wang Q, Sun Q, Zhang Y, Dong J, Yin Y, Zhang S, Yu G. Identification and Analysis of SOD Family Genes in Peanut (Arachis hypogaea L.) and Their Potential Roles in Stress Responses. Agronomy. 2023; 13(8):1959. https://doi.org/10.3390/agronomy13081959

Chicago/Turabian Style

Yu, Shutao, Chuantang Wang, Qi Wang, Quanxi Sun, Yu Zhang, Jingchao Dong, Yechao Yin, Shihang Zhang, and Guoqing Yu. 2023. "Identification and Analysis of SOD Family Genes in Peanut (Arachis hypogaea L.) and Their Potential Roles in Stress Responses" Agronomy 13, no. 8: 1959. https://doi.org/10.3390/agronomy13081959

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