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Article

Genome-Wide Identification of Superoxide Dismutase (SOD) Gene Family in Cymbidium Species and Functional Analysis of CsSODs Under Salt Stress in Cymbidium sinense

by
Ruyi Li
1,†,
Songkun Lin
2,†,
Yin Yan
1,2,
Yuming Chen
1,2,
Linying Wang
1,
Yuzhen Zhou
1,
Shuling Tang
1,3,* and
Ning Liu
1,*
1
Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2
College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China
3
Zhangzhou Institute of Technology, Zhangzhou 363000, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Horticulturae 2025, 11(1), 95; https://doi.org/10.3390/horticulturae11010095
Submission received: 6 December 2024 / Revised: 30 December 2024 / Accepted: 13 January 2025 / Published: 16 January 2025
(This article belongs to the Special Issue Orchids: Advances in Propagation, Cultivation and Breeding)
Browse Figures
Versions Notes

Abstract

:
Superoxide dismutase (SOD) enzymes are essential for reducing oxidative damage resulting from overabundant reactive oxygen species under abiotic stress. While the SOD gene family has been extensively studied in many species, research focusing on Cymbidium species remains limited. In this study, a comprehensive analysis of the SOD gene family in three Cymbidium genomes was conducted. A total of 23 SOD genes were identified, with nine SODs in C. sinense, eight in C. ensifolium, and six in C. goeringii. These SOD genes were categorized into three clades: Cu/Zn-SOD, Fe-SOD, and Mn-SOD, with the Cu/Zn-SOD being the most abundant in these three types. This classification was supported by analyses of conserved domains, motifs, and phylogenetic relationships. Cis-element prediction showed that stress-responsive elements were identified in most SODs. Transcriptomic data revealed that seven CsSODs exhibited a border expression in all sequenced tissues, while two exhibited undetectable expression levels. Further qRT-PCR analysis showed that all CsSODs were upregulated under salt stress, with some exhibiting significant changes in expression. These findings all highlight the crucial role of CsSODs in the salt stress response and provide valuable insights for further breeding salt-tolerance varieties of C. sinense.

1. Introduction

Abiotic stress contains adverse non-living environmental factors such as drought, heat, and salt, which negatively impact plant growth and development [1,2]. In response to these stresses, plants generate reactive oxygen species (ROS) as part of their defense mechanisms [3]. However, overproduction of ROS under abiotic stresses can damage proteins, disrupt cell membranes, and even result in cell death [4,5]. Plants evolved an intricate antioxidant defense system to reduce the harmful effects of ROS [6]. This system contains both antioxidant enzymes like superoxide dismutase (SOD) and catalase (CAT), and non-enzymatic antioxidants, such as flavonoids [6,7,8].
The SOD enzyme is regarded as the first line of the antioxidant defense system [9,10]. It facilitates the dismutation of superoxide radicals into hydrogen peroxide and molecular oxygen [11,12]. Based on their metal cofactor, SOD enzymes are classified into four main types: Cu/Zn-SOD (CSD), Fe-SOD (FSD), Mn-SOD (MSD), and Ni-SOD [13,14]. Ni-SOD is predominantly found in prokaryotes [15], whereas the first three types are more commonly observed in plants. Among these, CSD is the most widely distributed in plants and is localized in the chloroplast, mitochondria, and cytoplasm, while FSD and MSD are primarily found in the chloroplast and mitochondria, respectively [13].
The SOD gene family has been widely identified in different species based on the whole genome. For example, seven SODs were identified in Hordeum vulgare L. (comprising four CSDs, two FSDs, and one MSD) [16], and five were identified in Zostera marina L. (two CSDs, two FSDs, and one MSD) [17]. Functional studies have demonstrated the roles of SOD genes in defense against abiotic stresses, such as cold, heat, salinity, and drought. Compared to the wild-type, transgenic cotton (Gossypium hirsutum L.) cultivar ‘Xinluzao 33’ overexpressing SikCuZnSOD3 exhibited enhanced survival and growth under low temperature, PEG6000, and NaCl treatments [18]. Similarly, SOD genes in Phaseolus vulgaris L. exhibited an upregulated expression level under drought stress [19], and ZmSODs from Zea mays L. exhibited a higher expression level under both slat and drought stresses [20]. Functional studies have also been conducted in Brassica juncea (L.) Czern. [21], Solanum lycopersicum L. [22], and other species. Collectively, these studies indicated the key role of SOD genes in mediating plant defense mechanisms against abiotic stresses.
Cymbidium SW. species are ornamental plants in Orchidaceae, valued for their dark green leaves, fragrant flowers, and diverse floral morphologies [23]. Several species, such as C. ensifolium (L.) Sw., C. goeringii (Rchb. f.) Rchb. F., C. sinense (Jack. ex Andr.) Willd., have a long history of cultivation and have been extensively used as parents to cultivate numerous varieties, including ‘Dharma’ [24] and ‘Yu-Qi-Lin’ [25]. These species are primarily sold as potted plants or cut flowers, making them among the most important and commercially popular orchids [26]. Previous studies showed that the fresh weight and dry weight of protocorms from Cymbidium hybrid ‘Twilight Moon’ significantly decreased when cultivated in medium with NaCl solution [27], indicating the substantial challenges salt stress posed to Cymbidium cultivation. Salt-affected soils are widely distributed, and their area continues to expand [28]. Therefore, understanding the molecular mechanisms underlying salt stress response is critical.
Recently, genomic sequencing has been performed for several Cymbidium species [23,29,30], providing valuable resources for functional genomic studies. Here, a systematic analysis of the SOD gene family was performed in three Cymbidium genomes (C. ensifolium, C. goeringii, and C. sinense) using bioinformatics approaches. The expression pattern under salt treatment of CsSODs was also studied as potential salt-resistant candidate genes. These findings provide valuable insights for breeding salt-tolerance varieties of C. sinense.

2. Materials and Methods

2.1. Data Sources and Analysis Workflow

Three Cymbidium genomes were retrieved from public databases. The genome of C. ensifolium was downloaded from the National Genomics Data Center (NGDC) (https://ngdc.cncb.ac.cn/?lang=zh, accessed on 13 October 2024) under accession number PRJCA005355. The genomes of C. goeringii and C. sinense were obtained from the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/, accessed on 13 October 2024) with accession numbers PRJNA749652 and PRJNA174386, respectively. Additionally, eight SOD protein sequences from Arabidopsis thaliana (L.) Heynh. were downloaded from TAIR (https://www.arabidopsis.org/, accessed on 13 October 2024). The Hidden Markov Model (HMM) of the SOD gene family (PF00080, PF00081, and PF02777) was obtained from the website Pfam database (http://pfam.xfam.org/, accessed on 13 October 2024). The analysis workflow is presented in Figure 1.

2.2. Identification and Characterization of SOD Gene Family

The SOD proteins in three Cymbidium genomes were identified using AtSODs and HMMs of the SOD gene family (PF00080, PF00081, PF02777) from the Pfam database. BLASTp and the Simple HMM Search module in TBtools v2.131 [31] were employed to perform the search. Results from both methods were combined, and incomplete or redundant sequences were excluded. Candidate SODs were further confirmed using the Batch CD-search module of NCBI (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi, accessed on 13 October 2024) [32].
The online software ExPASy (https://www.expasy.org/, accessed on 13 October 2024) [33] was used to analyze the physicochemical properties of candidate SODs. The online tool Plant mPloc (http://www.csbio.sjtu.edu.cn/bioinf/plant-multi/, accessed on 13 October 2024) [34] was used to predict the subcellular localization of SODs.

2.3. Sequence Alignment and Phylogenetic Analysis of Candidate SOD Genes

The SOD proteins of three Cymbidium species and A. thaliana were aligned by the MUSCLE module in MEGA7 [34] with default parameters. The phylogenetic relationship was performed by the neighbor-joining (NJ) method in MEGA7 [35] with 1000 bootstrap replicates. The result was further refined and polished using the online website tvBOT (https://www.chiplot.online/tvbot.html, accessed on 15 October 2024) [36].

2.4. Gene Structure, Conserved Motifs Analyses of Candidate SOD Genes

The conserved motifs of candidate SODs were identified by the online software MEME Suite v5.5.7 (https://meme-suite.org/meme/tools/meme, accessed on 15 October 2024), with a maximum of ten motifs. The visualization of motif patterns and gene structures was conducted by the Gene Structure View program in TBtools v2.131 [31].

2.5. Chromosomal Location and Collinearity Analysis of Candidate SOD Genes

The chromosomal locations of candidate SOD genes were determined using genome annotation files and chromosomal length data from the three Cymbidium species. Gene positions were visualized with MapGene2Chrom v2.1 [37]. Collinearity analysis was performed using the One Step MCScanx-SuperFast and Advanced Circo’s modules in TBtools v2.131 [31].

2.6. Cis-Acting Elements Prediction of Candidate SOD Genes

Promoter regions (2000 bp upstream of candidate SODs) were extracted using TBtools v2.131 [31] based on genomes. Cis-acting regulatory elements were predicted with PlantCARE (https://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 18 October 2024) [38] software, and the results were visualized using TBtools v2.131 [31].

2.7. GO Enrichment Analysis

The functional enrichment of CsSODs was assessed using GO enrichment analysis performed with eggNOG-mapper (http://eggnog-mapper.embl.de, accessed on 20 October 2024) [39]. The results were processed and visualized using the eggNOG-mapper Helper, GO Enrichment, and Enrichment Bar Plot modules in TBtools v2.131 [31], focusing on the top 15 GO terms.

2.8. Plant Materials, Growth, Treatments and Sampling

The plant materials were grown in a greenhouse at Fujian Agriculture and Forestry University. The environmental temperatures ranged from 25 °C during the day to 30 °C at night. Salt stress was applied by immersing the plants below the stem in a 300 mmol/L NaCl solution for ten minutes, followed by removal. Leaf samples were harvested at 0, 6, and 12 h following salt treatment.

2.9. Expression Profile and qRT-PCR Analyses

Transcriptome datasets from the stem, leaf, sepal, flower, and other tissues of C. sinense were obtained from OrchidBase (https://cosbi.ee.ncku.edu.tw/orchidbase6/home/, accessed on 30 October 2024) [40]. Fragments per kilobase of exon per million mapped reads (FPKM) method was used to calculate expression levels of CsSODs. Heatmap of CsSODs were generated using TBtools v2.131 [31].
RNA was extracted using the Biospin Plant Total RNA Extraction Kit (Bioer Technology, Hangzhou, China). cDNA was synthesized using the TransScript® All-in-One First-Strand cDNA Synthesis SuperMix for quantitative PCR (qPCR; TransGen Biotech, Beijing, China). RNA extraction and cDNA synthesis procedures followed the kit instructions.
The online software Primer-Blast (https://www.ncbi.nlm.nih.gov/tools/primer-blast/, accessed on 14 November 2024) and Primer Check module in TBtools v2.131 [31] were used to design and further verify the primer sequences of CsSODs and the reference gene (CsACT), respectively (Table S1). The QuantStudio™ Real-Time PCR (Applied Biosystems, Waltham, MA, USA) was used to conduct qRT-PCR experiments. The kit used in qRT-PCR experiments was PerfectStart™ Green qPCR SuperMax (TransGen Biotech, Beijing, China). The relative expression analysis of CsSODs was calculated by the 2−ΔΔCT method.

3. Results

3.1. Genomic Identification and Characterization of SOD Genes in Three Cymbidium Species

A total of 23 SOD proteins were identified in three Cymbidium genomes, with nine members in C. sinense, eight in C. ensifolium, and six in C. goeringii, and the corresponding protein sequences were provided in Table S2. The detailed information on these SODs is listed in Table 1. The identified SODs were renamed based on their conserved domains and homologs in A. thaliana.
The physicochemical properties of these 23 SOD proteins are also listed in Table 1. Protein lengths ranged from 146 aa (CeCSD3;2) to 309 aa (CsFSD1), and molecular weight ranged from 15,353.05 Da (CeCSD1) to 35,557.93 Da (CsFSD1). Most SODs were predicted to be stable proteins, as indicated by an instability index ≤ 40. Additionally, the majority of the SODs were characterized as acidic proteins (pI < 7) and hydrophilic (GRAVY < 0).
Subcellular localization predictions showed that CSDs were localized to the chloroplast, cytoplasm, and mitochondrion; FSDs were found in the chloroplast and mitochondrion; and MSDs were exclusively found in the mitochondrion. Notably, the localization of CeCSD2 and CgCSD3;2 was predicted in both the chloroplast and cytoplasm, while other SODs were assigned to a single location.

3.2. Sequence Alignment and Phylogenetic Analysis

Protein sequence alignment and phylogenetic analysis were constructed using 23 SODs from Cymbidium and eight SODs from A. thaliana to clarify their evolutionary relationships. The sequence alignment of the 424 aa SOD fragments showed 29 conserved sites, 317 variable sites, 256 parsimony-informative sites, and 54 singleton sites.
The phylogenetic analysis grouped the 23 Cymbidium SOD proteins into three distinct clades (Figure 2): Cu/Zn-SOD (15 proteins, accounted for 65.21%), Fe-SOD (6, 26.09%), and Mn-SOD (2, 8.70%). The clade Cu/Zn-SOD contained the highest number of SODs from Cymbidium species, followed by Fe-SOD and Mn-SOD. Within the clade, Cu/Zn-SOD, C. ensifolium, C. goeringii, and C. sinense contained five, four, and six genes, respectively. Each species contained two genes in the clade Fe-SOD. The Mn-SOD clade included one gene each in C. ensifolium and C. sinense, while no SOD from this clade was identified in C. goeringii. Furthermore, compared to the clade Cu/Zn-SOD, clades Fe-SOD and Mn-SOD shared closer relationships.

3.3. Motifs and Gene Structure Analysis

Motif prediction for SODs in three Cymbidium species was conducted by the online software MEME Suite with an upper limit of ten motifs. As shown in Figure 3, the motif patterns were conserved within each clade. For example, the Cu/Zn-SOD clade exhibited a conserved motif arrangement consisting of motif 3, motif 1, motif 2, and motif 7. In contrast, distinct motif patterns were observed in three clades. The Fe-SOD clade showed a conserved pattern comprising motifs 5, 4, 6, and 10, while the Mn-SOD clade displayed a motif arrangement of motifs 8, 10, 4, and 6. Notably, the motif patterns were more conserved between the Fe-SOD and Mn-SOD clades compared to the clade Cu/Zn-SOD. These two clades shared common motifs, including motifs 4 and 6.
The exon–intron composition analysis was conducted to gain insights into the structural evolution of SODs in these Cymbidium species (Figure 4). The gene structure of these SOD genes showed two to nine exons and one to eight introns, exhibiting substantial variability. Four genes, CeCSD3;1, CeCSD3;2, CsCSD3;2, and CsCSD3;3, were characterized by a simple structure with two exons and one intron. In contrast, other SODs exhibited more complex structures, such as CeCSD3;3, which contained eight exons and seven introns. In addition, a significant degree of variability in intron length was observed among these SOD genes.

3.4. Chromosomal Location and Collinearity Analysis

To further elucidate the homologous relationships of SOD genes in Cymbidium species, gene chromosomal localization and collinearity analyses were conducted (Figure 5). The SOD genes from C. goeringii were evenly distributed on six chromosomes, while the other two species showed uneven chromosomal localization. However, in the other two species, chromosomal localization was uneven. Most SOD genes were located on different chromosomes, with a small subset found on the same chromosome. In C. ensifolium, eight CeSODs were unevenly localized on six chromosomes. Specifically, CeCSD3;1, CeCSD3;2, and CeFSD3 were distributed on chr08, while the remaining CeSODs were distributed on the different chromosomes independently. In C. sinense, three SODs were located on chr 02 (CsCSD3;1, CsCSD3;4 and CsFSD1), and two on chr 03 (CsCSD3;3 and CsFSD3), while other four SODs localized on four different chromosomes.
Collinearity analysis among three Cymbidium species was performed using TBtools to explore gene duplication or loss events of interspecies. A total of 12 gene pairs were found (Figure 6), including CeCSD1 and CsCSD1, CeCSD2 and CsCSD2, CeCSD3;2 and CsCSD3;3, CeFSD3 and CsFSD3, CeMSD and CsMSD, CgCSD1 and Ce-CSD1, CgCSD2 and CeCSD2, CgCSD3;2 and Ce-CSD3;3, CgCSD1 and CsCSD1, CgCSD2 and CsCSD2, CgCSD3;1 and CsCSD3;1, CgCSD3;1 and CsCSD3;4. These gene pairs were identified as duplicated genes. There are displayed one-to-one duplicated relationships between two species, except for CgCSD3;1, CsCSD3;1, and CsCSD3;4. Furthermore, these duplicated genes were regarded as the result of WGD or segmental duplication.

3.5. Cis-Element Prediction of SOD Gene Family in the Promoter Region

Here, the 2000 bp promoter region of SODs in Cymbidium species was extracted to predict the cis-element. A total of 497 putative cis-elements were identified, including 43 types and 17 functions (Figure 7A, Supplementary Table S1). Four main types of cis-elements, light responsive, phytohormone responsive, stress-responsive, and plant growth and development, were found in these 23 SODs. CeMSD (50 elements in total) has the maximum elements in all 23 SODs, whereas CgCSD3;1 (eight elements in total) has the minimum elements (Figure 7B).
Light-responsive cis-elements (204 in total) were the most abundant in Cymbidium SODs and found in promoter regions of each SODs. Notably, CgCSD3;1 contained only a light-responsive element. The second most abundant type was the phytohormone-responsive elements, such as auxin-responsive and MEJA-responsive elements. A total of 21 SODs contained cis-elements of phytohormone responsive with 58 elements, 66, and 44 in C. ensifolium, C. goeringii, and C. sinense, respectively. Stress-responsive elements were the third one, such as cis-elements of anaerobic induction, defense, and stress-responsive. This type was also observed in 21 SODs, with 31 elements, 20, and 27 in Phylogenetic, C. goeringii, and C. sinense, respectively. Besides that, a total of 14 cis-elements of plant growth and development were predicted in C. ensifolium, 17 in C. goeringii, and 16 in C. sinense.

3.6. The Expression Profile of CsSODs in Different Tissues

To clarify the function of SODs in C. sinense, the expression patterns of different tissues were observed based on transcriptome datasets (Figure 8, Table S3). The expression heatmap showed that not all SODs were expressed in tissues of C. sinense under normal growth environment. Among these SODs, seven SODs exhibited high expression levels in different tissues, while two SODs (CeCSD3;2 and CeCSD3;3) were not expressed in any tissues. CsCSD1 exhibited the highest expression level in most tissues except the labellum, petal, and sepal. CsMSD is expressed at the highest level in these three tissues. In general, the expression patterns all indicated that SODs played a crucial role in plant growth and development.

3.7. GO Enrichment Analysis and qRT-PCR of SODs in Cymbidium Sinense Under Salt Stress

GO enrichment analysis was used to elucidate the potential function of CsSODs (Figure 9A). The results showed that CsSODs were enriched in molecular function (such as antioxidant activity) and biological function (such as cellular response to oxidative stress and superoxide metabolic process). These findings highlighted the key role of CsSODs in stress responsiveness.
To validate the GO enrichment result, qRT-PCR experiments were performed under salt treatment (Figure 9). The expression pattern of CsSODs revealed two main expressive changes: an initial upregulation at six hours post-treatment followed by downregulation at 12 h (CsCSD1, CsCSD2, and CsCSD3); sustained upregulation throughout the treatment (CsCSD3;1, CsCSD3;2, CsCSD3;3, and CsFSD1). Notably, CsCSD3;4 exhibited an expression pattern of initial downregulation followed by upregulation. After salt treatment, the expression of CsMSD remained stable at six hours but showed significant upregulation at 12 h. These results all indicated that CsSODs were actively involved in the salt stress response. Furthermore, two genes, CsCSD3;2 and CsCSD3;2, which were not detected as expressed in the transcriptome, also responded to salt stress. These two genes exhibited sustained upregulation following treatment.

4. Discussion

SOD enzyme is regarded as a core enzyme in protecting oxidative stress by overproduced ROS under abiotic stresses [9,10]. The identifications and functional characterization of the SOD gene family have been reported in numerous species [41,42,43]. In this study (Figure 1), we identified nine, eight, and six SODs in C. sinense, C. ensifolium, and C. goeringii, respectively (Table 1). The relatively conserved number of SOD genes in the Cymbidium genus aligned with findings in other species, such as Medicago truncatula Gaertn (seven SODs) [44], Daucus carota L. (nine SODs) [45], and Solanum lycopersicum L. (nine SODs) [46]. The variation in SOD numbers in the three Cymbidium species suggested gene duplication or loss events during evolution, as supported by chromosomal localization and collinearity analyses (Figure 5 and Figure 6). Similar evolutionary dynamics have been observed in previous studies [45,47].
Phylogenetic analysis showed that the SODs of Cymbidium were grouped into three subfamilies: Cu/Zn-SOD (CSD), Fe-SOD (FSD), and Mn-SOD (MSD) (Figure 2). This classification was consistent with other studies [42,48]. A previous study reported that the CSD clade contains the largest number of SOD members. For example, 17 CSDs, six FSDs, and three MSDs were identified in Triticum aestivum L. [43], and six CSDs, five FSDs, and two MSDs were identified in Zea mays L. [20]. Here, we identified five CSDs, two FSDs, and one MSD in C. ensifolium; four CSDs and two FSDs in C. goeringii; six CSDs, two FSDs, and one MSD in C. sinense, aligning well with prior findings.
Algae and bryophytes are reported to contain only FSD and MSD clades, suggesting that these two clades evolved earlier than the CSD clade [49]. Phylogenetic studies of Salvia miltiorrhiza Bunge and other species consistently showed that FSD and MSD clades clustered together, while the CSD clade evolved independently [20,43,50]. The phylogenetic results also supported these views. The function and evolution of members in CSD clades are probably more complex than FSD and MSD clades [47,51].
Motif analysis revealed a high degree of conservation among Cymbidium SODs (Figure 3), similar to findings of Camellia sinensis (L.) Kuntze [48] and B. napus L. [52]. In contrast, gene structure exhibited greater variability, with exon numbers ranging from two to nine (Figure 4). This variability was consistent with observations in B. napus, where exon numbers ranged from three to nine [52]. In addition, the cis-element prediction showed that each SODs contained light-responsive cis-elements (Figure 7), highlighting the importance of light in regulating SOD expression. And most SODs of three Cymbidium species contained stress-responsive elements. This corresponded with reports of other species [19,20].
Tissue-specific expression analysis showed that most CsSODs are highly expressed in various tissues, including flowers, leaves, and roots, with CsCSD1 showing particularly high expression (Figure 8). This indicated an important role of SODs in C. sinense. GO enrichment analysis further demonstrated the involvement of CsSODs in oxidative stress protection (Figure 9A). The expression pattern under salt stress of CsSODs showed that all nine SODs responded to salt stress (Figure 9), including two genes that barely expressed under normal conditions. This suggested the crucial role of SODs for responding to the salt stress. Furthermore, two different expression patterns of CsSODs after salt treatment were observed, indicating that CsSODs are regulated by distinct mechanisms.
These findings contribute to understanding the key roles of CsSODs in protecting C. sinense from salt stress. However, their response to other abiotic stresses, such as cold and heat, remains unknown. Future studies should conduct a broader functional analysis of the SOD gene family by exploring their responses to diverse abiotic stresses.

5. Conclusions

Here, 23 SOD genes were identified using the BLASTp and Simple HMM search modules. Specifically, five CSDs, two FSDs, and one MSD were identified in C. ensifolium (eight SODs in total). C. goeringii contained four CSDs and two FSDs (six SODs in total). In C. sinense, six CSDs, two FSDs, and one MSD were found (nine SODs in total). Bioinformatics analyses revealed that most SODs were localized on different chromosomes and conserved in sequence characterization. These genes can be classified into three clades: Cu/Zn-SOD, Fe-SOD, and Mn-SOD, supported by the phylogenetic tree and domain analyses. Cis-elements analysis identified stress-responsive elements in most SOD genes. Transcriptome showed that seven SOD genes were expressed in various tissues of C. sinense. qRT-PCR analysis indicated that all CsSODs responded to salt stress, with significant expression changes in some genes. Two main expressive patterns were observed: an initial upregulation followed by downregulation and sustained upregulation. These findings provide valuable insight into the potential functions of SOD genes in abiotic stress responses, particularly in C. sinense.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae11010095/s1, Table S1: The primers of CsSODs for qRT-PCR; Table S2: SOD protein sequences from A. thaliana, C. ensifolium, C. goeringii, and C. sinense; Table S3: The FPKM values of CsSODs in different tissues.

Author Contributions

Conceptualization, S.T. and N.L.; methodology and software, R.L. and S.L.; validation, Y.Y. and L.W.; formal analysis and visualization, R.L., S.L. and Y.Y.; resources and data curation, Y.C. and L.W.; writing—original draft preparation, R.L. and S.L.; writing—review and editing, R.L., Y.Z. and N.L.; supervision, S.T. and N.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China, grant number 2023YFD1600504.

Data Availability Statement

Data is contained within the article and Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The analysis workflow used in this study.
Figure 1. The analysis workflow used in this study.
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Figure 2. The phylogenetic tree of SODs from Cymbidium species. Different colors in nodes represented bootstrap values. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
Figure 2. The phylogenetic tree of SODs from Cymbidium species. Different colors in nodes represented bootstrap values. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
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Figure 3. The arrangement and architecture of motif pattern in SOD proteins from Cymbidium species. (A) The arrangement of motif patterns; (B) The sequence information for Motifs 1–10, respectively. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
Figure 3. The arrangement and architecture of motif pattern in SOD proteins from Cymbidium species. (A) The arrangement of motif patterns; (B) The sequence information for Motifs 1–10, respectively. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
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Figure 4. The gene structures of 23 SODs from Cymbidium species. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
Figure 4. The gene structures of 23 SODs from Cymbidium species. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
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Figure 5. The chromosomal location map of 23 SODs in Cymbidium species. Different colors represented different species. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
Figure 5. The chromosomal location map of 23 SODs in Cymbidium species. Different colors represented different species. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
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Figure 6. The collinearity analysis of SODs among three Cymbidium species. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
Figure 6. The collinearity analysis of SODs among three Cymbidium species. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
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Figure 7. The putative cis-elements of 23 SODs. (A) The distribution map of cis-elements in promoter regions; (B) The number of cis-elements in each SODs, different colors represented different types. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
Figure 7. The putative cis-elements of 23 SODs. (A) The distribution map of cis-elements in promoter regions; (B) The number of cis-elements in each SODs, different colors represented different types. Different symbols represented different species. Ce: C. ensifolium; Cg: C. goeringii; Cs: C. sinense.
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Figure 8. Expression pattern of CsSODs in different tissues. Cs: C. sinense.
Figure 8. Expression pattern of CsSODs in different tissues. Cs: C. sinense.
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Figure 9. The GO enrichment and qRT-PCR results of CsSODs under salt stress. (A) GO enrichment result, green represented the class Molecular function, and pink represented the class Biological process; (B–J) qRT-PCR visualizations. Cs: C. sinense.
Figure 9. The GO enrichment and qRT-PCR results of CsSODs under salt stress. (A) GO enrichment result, green represented the class Molecular function, and pink represented the class Biological process; (B–J) qRT-PCR visualizations. Cs: C. sinense.
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Table 1. The information of 23 SOD proteins.
Table 1. The information of 23 SOD proteins.
Gene Name aGene IDAmino Acid
(aa)		Molecular Weight
(Da)		pI bInstability IndexGRAVY cSubcellular Localization
CeCSD1JL00614815215,353.055.1516.45−0.143Chloroplast
CeCSD2JL02090916416,644.406.0921.40−0.215Chloroplast, Cytoplasm
CeCSD3;1JL00172019421,155.739.0624.99−0.507Chloroplast
CeCSD3;2JL00171914615,657.424.8213.18−0.182Chloroplast
CeCSD3;3JL01196222122,651.917.1335.110.124Chloroplast
CeFSD1JL02190630935,557.895.2454.51−0.501Chloroplast
CeFSD3JL00697826430,702.237.7647.51−0.368Mitochondrion
CeMSDJL01873926429,840.906.627.62−0.371Mitochondrion
CgCSD1GL0173415215,389.135.4615.28−0.141Chloroplast
CgCSD2GL0916116416,720.516.0922.64−0.212Mitochondrion
CgCSD3;1GL0814227228,404.015.6835.440.035Chloroplast
CgCSD3;2GL2070222022,461.717.1335.410.134Chloroplast, Cytoplasm
CgFSD3;1GL2277723026,684.666.5043.23−0.292Chloroplast
CgFSD3;2GL2277626430,692.117.7646.06−0.412Chloroplast
CsCSD1Mol00978315215,477.235.1813.31−0.122Mitochondrion
CsCSD2Mol02148416416,605.325.9221.92−0.207Mitochondrion
CsCSD3;1Mol01183721421,928.956.1821.170.125Chloroplast
CsCSD3;2Mol00134825227,368.126.224.13−0.106Chloroplast
CsCSD3;3Mol00016523625,620.175.3527.870.044Chloroplast
CsCSD3;4Mol02768024626,106.465.1329.620.074Chloroplast
CsFSD1Mol00822230935,557.935.3255.00−0.504Chloroplast
CsFSD3Mol00973926430,749.237.1844.19−0.383Chloroplast
CsMSDMol02092123826,895.577.1729.04−0.407Mitochondrion
a Ce: C. ensifolium, Cg: C. goeringii, Cs: C. sinense; b pI: Theoretical isoelectric points; c GRAVY: Grand average of hydropathy.
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Li, R.; Lin, S.; Yan, Y.; Chen, Y.; Wang, L.; Zhou, Y.; Tang, S.; Liu, N. Genome-Wide Identification of Superoxide Dismutase (SOD) Gene Family in Cymbidium Species and Functional Analysis of CsSODs Under Salt Stress in Cymbidium sinense. Horticulturae 2025, 11, 95. https://doi.org/10.3390/horticulturae11010095

AMA Style

Li R, Lin S, Yan Y, Chen Y, Wang L, Zhou Y, Tang S, Liu N. Genome-Wide Identification of Superoxide Dismutase (SOD) Gene Family in Cymbidium Species and Functional Analysis of CsSODs Under Salt Stress in Cymbidium sinense. Horticulturae. 2025; 11(1):95. https://doi.org/10.3390/horticulturae11010095

Chicago/Turabian Style

Li, Ruyi, Songkun Lin, Yin Yan, Yuming Chen, Linying Wang, Yuzhen Zhou, Shuling Tang, and Ning Liu. 2025. "Genome-Wide Identification of Superoxide Dismutase (SOD) Gene Family in Cymbidium Species and Functional Analysis of CsSODs Under Salt Stress in Cymbidium sinense" Horticulturae 11, no. 1: 95. https://doi.org/10.3390/horticulturae11010095

APA Style

Li, R., Lin, S., Yan, Y., Chen, Y., Wang, L., Zhou, Y., Tang, S., & Liu, N. (2025). Genome-Wide Identification of Superoxide Dismutase (SOD) Gene Family in Cymbidium Species and Functional Analysis of CsSODs Under Salt Stress in Cymbidium sinense. Horticulturae, 11(1), 95. https://doi.org/10.3390/horticulturae11010095

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