Genome-wide identification and expression analysis of the SET domain-containing gene family in potato (Solanum tuberosum L.)

Suppiyar, Vithusan; Bonthala, Venkata Suresh; Shrestha, Asis; Krey, Stephanie; Stich, Benjamin

doi:10.1186/s12864-024-10367-2

Genome-wide identification and expression analysis of the SET domain-containing gene family in potato (Solanum tuberosum L.)

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Published: 03 May 2024

Volume 25, article number 442, (2024)
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Genome-wide identification and expression analysis of the SET domain-containing gene family in potato (Solanum tuberosum L.)

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Vithusan Suppiyar¹,
Venkata Suresh Bonthala^1,3,
Asis Shrestha^1,3,
Stephanie Krey^1,3 &
…
Benjamin Stich^1,2,3

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Abstract

Genes containing the SET domain can catalyse histone lysine methylation, which in turn has the potential to cause changes to chromatin structure and regulation of the transcription of genes involved in diverse physiological and developmental processes. However, the functions of SET domain-containing (StSET) genes in potato still need to be studied. The objectives of our study can be summarized as in silico analysis to (i) identify StSET genes in the potato genome, (ii) systematically analyse gene structure, chromosomal distribution, gene duplication events, promoter sequences, and protein domains, (iii) perform phylogenetic analyses, (iv) compare the SET domain-containing genes of potato with other plant species with respect to protein domains and orthologous relationships, (v) analyse tissue-specific expression, and (vi) study the expression of StSET genes in response to drought and heat stresses. In this study, we identified 57 StSET genes in the potato genome, and the genes were physically mapped onto eleven chromosomes. The phylogenetic analysis grouped these StSET genes into six clades. We found that tandem duplication through sub-functionalisation has contributed only marginally to the expansion of the StSET gene family. The protein domain TDBD (PFAM ID: PF16135) was detected in StSET genes of potato while it was absent in all other previously studied species. This study described three pollen-specific StSET genes in the potato genome. Expression analysis of four StSET genes under heat and drought in three potato clones revealed that these genes might have non-overlap** roles under different abiotic stress conditions and durations. The present study provides a comprehensive analysis of StSET genes in potatoes, and it serves as a basis for further functional characterisation of StSET genes towards understanding their underpinning biological mechanisms in conferring stress tolerance.

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Introduction

The nucleosome, the fundamental unit of eukaryotic chromatin material, consists of two DNA strands wrapped around an octamer of histone proteins, which comprises two copies of each H2A, H2B, H3, and H4 protein [1]. Post-translational modifications, such as acetylation, methylation, phosphorylation, ubiquitination, and SUMOylation, covalently modify the N-terminal region of core histones [2, 3]. These modifications impact chromatin structure and accessibility and thereby can regulate gene expression [4, 5]. In plants, histone methylation is among the most well-understood histone modifications. This modification plays a crucial regulatory role in plant growth and development, reproductive processes, and response to environmental factors [5,33]

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The length of StSET gene sequences ranged from 430 to 28,651 nucleotides. Three genes, namely StSET21, StSET29, and StSET49, contained a single exon, while the remaining genes contained up to 24 exons (Fig. 2B; Table S1). The length of protein sequences of StSET genes ranged from 112 to 2421 amino acids. The proteins of StSET genes had an average and median molecular weight of 87.7 and 78.2 kilodaltons (kDa), respectively. The protein of StSET43 had the highest molecular weight of 276.5 kDa, while the protein of the StSET17 gene had the lowest molecular weight of 13 kDa. The StSET proteins had a theoretical pI spectrum of 4.51 to 9.47. We predicted that about 84% of the StSET proteins (48 StSETs) are unstable. Amino acid composition analysis showed that Serine (Ser), Glycine (Gly), Leucine (Leu), and Lysine (Lys) are the predominant amino acid residues of StSET proteins. The grand average of hydropathicity (GRAVY) values indicated that StSET proteins are hydrophilic (Table S2).

We found 23 unique protein domains in the protein sequences of StSET genes, including the SET domain (Fig. 2C; Table 1). About 38% of protein sequences of StSET genes (22 genes) contained only the SET domain, while the remaining genes contained diverse combinations of multiple protein domains along with the SET domain. For example, about 17% of protein sequences of StSET genes contained the combination of the SET, Pre_SET, and SAD_SRA protein domains, while one contained a combination of eight protein domains, such as SET, PWWP, FYRN, FYRC, PHD, PHD_2, zf-HC5HC2H_2, and zf-HC5HC2H (Table 2).

Table 1 List of protein domains identified in SET domain-containing genes across Solanum tuberosum, Solanum lycopersicum, Arabidopsis thaliana, and Oryza sativa. ✓indicates presence of a specific protein domain, while X indicates absence of a specific protein domain in the respective plant species

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Table 2 The number of SET genes in which a unique combination of protein domains identified in SET domain-containing genes is observed for Solanum tuberosum, Solanum lycopersicum, Arabidopsis thaliana, and Oryza sativa

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The gene ontology (GO) enrichment analysis identified significantly enriched GO terms (p < 0.05) involved in various biological processes (56 GO terms), molecular functions (57 GO terms), and cellular components (55 GO terms). For example, 100% and about 82.5% of StSET genes were predicted to be involved in catalytic activity and response to stimulus, respectively (Figure S2; Table S3).

We predicted for approximately 93% of StSET genes a localisation in the nucleus, while for the others a localisation in the mitochondria (StSET1) or the chloroplast (StSET8 and StSET41) (Table S1) was predicted. Three genes (StSET28, StSET45, and StSET53) were predicted to have transmembrane helices (Table S1).

Identification of duplicated StSET genes

We found four tandemly duplicated gene (TDG) clusters in StSET genes with cluster sizes from 2—5 genes. The TDG clusters contained about 23% of StSET genes. We found two TDG clusters with StSET genes on chromosome 3, while one was on chromosomes 7 and 8 (Fig. 1). We estimated the non-synonymous (Ka) and synonymous (Ks) substitution ratios (Ka/Ks) for each pair of tandemly duplicated StSET genes, and the ratios ranged from 0.39—0.99.

Phylogenetic analysis of StSET genes

We estimated a phylogenetic tree that clustered all StSET genes into six clades denoted as C1—C6 (Fig. 2A). The largest clades, C1 and C2, contained an equal number of StSET genes (14 genes in each clade), while the smallest clade (C6) contained four StSET genes. Further, we estimated a phylogenetic tree for SET domain-containing genes from Solanum tuberosum, Solanum lycopersicum, Oryza sativa, and Arabidopsis thaliana, and this phylogenetic tree also clustered all the genes into six clades denoted as C1—C6 (Fig. 3).

Identification of cis-elements and conserved motifs

We identified 41 unique cis-elements in the non-overlap** 1 Kb region upstream (potential promoter sequence) to the transcription start site of StSET genes (Table 3; Table S4). Among these, we identified several cis-elements described previously in the context of various environmental factors. For example, the promoter sequences of 53 StSET genes contained cis-elements described previously in the context of light-responsiveness. In addition, we found several drought-responsive, abscisic acid-, salicylic acid-, methyl jasmone acid- and auxin-responsive elements (Fig. 4). In addition, we identified 20 conserved motifs with a length range of 28—100 nucleotides within the potential promoter sequences of StSET genes (Table S5). Motifs 7 and 2 were conserved in 44 and 32 StSET genes, respectively, while motifs 1, 8, and 15 were conserved in two StSET genes (Table S5).

Table 3 List of cis-elements identified in promoter sequences of StSET genes. The sequence column indicates the cis-element identified in the promoter sequences. The count column indicates the number of cis-elements identified in promoter sequences across the StSET genes. The genes column indicates the number of StSET genes in which a specific cis-element is identified

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Tissue-specific expression of StSET genes

We investigated the expression patterns of all the identified StSET genes in 15 tissues, namely pollen, style, flower, fruit, leaf, petiole, stem, shoot, root, stolon, tuber, tuber meristem, tuber periderm, tuber flesh, and tuber sprout using the expression data retrieved from the StCoExpNet database [37]. A detectable expression, i.e., an average transcript per million (TPM) > 1 across samples of respective tissues, was observed in at least one tissue for 47 out of 57 StSET genes (Fig. 5). In addition, we found that about 84% of the StSET genes were assigned to 27 different co-expression clusters. We observed variation in expression between members of a phylogenetic clade and across phylogenetic clades (Figure S3). We found that seven of 13 tandemly duplicated StSET genes were expressed at least in one tissue. Moreover, three StSET genes belonging to TDG3, StSET37, StSET38, and StSET40, showed tissue-specific expression in pollen with an average Tau index of 0.9928 (Fig. 5; Table S6). In contrast, the remaining two genes, StSET36 and StSET39, revealed a low expression across tissues but showed slightly increased expression in flower and pollen, respectively. Two genes of TDG4, StSET44 and StSET45, were expressed in all tissues except pollen (Fig. 5; Table S6).

Expression profiling of StSET genes in response to abiotic stress conditions

We investigated the relative expression of four StSET genes (StSET13, StSET30, StSET48 and StSET52) in three different potato genotypes: Karlena (drought-tolerant), Kolibri (drought-tolerant), and Laura (drought-sensitive and heat-tolerant), under drought and heat stress. We examined two-time points—9 days (T3) and 18 days (T6) in stress—plus four days after recovery (T7) for expression analysis.

The RT-qPCR results showed a change in expression for all four genes under heat and drought stress in a genotype dependent manner. Compared to the control conditions the relative expression of all four genes increased 9 days after heat stress. Under prolonged exposure to heat stress (18 days), the relative expression of the investigated genes went down in Laura (heat tolerant) while the reverse was true for Karlena and Kolibri (heat sensitive) (Fig. 6). Compared to the control conditions, the relative expression of all StSET genes decreased under extreme drought stress (18 days after stress, 2.8% VMC). The relative expression of either gene increased (StSET13, StSET52) or remained at similar levels (StSET30 and StSET48) compared to control conditions in drought tolerant cultivars. The relative expression all four genes was comparable with those in control conditions after stress release in all cultivars (Fig. 6).

Comparative analysis of SET domain-containing genes

To derive orthologous relationships of StSET genes, a comparative map** approach was followed wherein we compared the physically mapped SET domain-containing genes of potato with those of nine other species, namely Arabidopsis thaliana, Camellia sinensis, Gossypium raimondii, Malus domestica, Oryza sativa, Populus trichocarpa, Setaria italica, Solanum lycopersicum, and Triticum aestivum. In this study, we defined the orthologous SET domain-containing genes between potato and the species mentioned earlier based on the following criteria: If the SET domain-containing genes of the other nine species showed at least 50% of sequence identity and query coverage against StSET in BLASTP search, they were considered orthologs to StSETs. Based on these criteria, we observed a considerable variation in the number of orthologous SET domain-containing genes between potato and the species mentioned earlier (Table S7). For example, Solanum lycopersicum contained the highest number (about 79%) of orthologous SET domain-containing genes with potatoes. In contrast, Oryza sativa contained the lowest number (about 37%) of orthologous SET domain-containing genes with potatoes (Table S7; Fig. 7).

We observed the presence and absence of protein domains in SET domain-containing genes between potato and three other species (Table 1). For example, the protein domain, TDBD (PFAM ID: PF16135), was identified only in potato. In contrast, the protein domain, GYF_2 (PFAM ID: PF14237), was not detected in potato. Further, we observed the presence and absence of a unique combination of protein domains in SET domain-containing genes between potatoes and three other species (Table 2). For example, the protein domain combination, SET, Pre-SET, SAD_SRA, and Iso_dh, was only identified in potato, while the protein domain combination, SET, SAD_SRA, was absent in potato.

Discussion

SET domain-containing gene family in potato

SET domain-containing proteins that catalyse histone methylation on lysine residues are vital players for dynamically regulating the chromatin condensation [39], which in turn is essential to regulating genes in various developmental and physiological processes, such as floral organogenesis [40], root development [41], seed development [42], and plant responses to abiotic stress conditions [5, 22, 24]. However, information about the gene family that comprises the SET domain in potatoes was missing. Therefore, identifying members of this gene family will aid in comprehending the epigenetic mechanism that regulates gene expression in potato and, thus, potentially contribute to the phenotypic variation of agronomically important traits.

We identified 57 StSET genes in the potato genome and systematically characterised them (Fig. 1; Table S1). The number of StSET genes significantly exceeded the number of SET domain-containing genes identified in other plant species, including the potato's closest relative species used in this study, Solanum lycopersicum [28]. However, the number observed for potato was lower than in three species, including Triticum aestivum [29] (Table S7). Variation in the number of SET domain-containing genes among the species used in this study reflects the lineage-specific expansion of the gene family [43]. Further, we observed a significant variation in the number of orthologous SET domain-containing genes between potato and other species used in this study (Table S7), which is in accordance with the phylogenetic distance between potato and other species [44].

Our study identified six clades for SET domain-containing genes (Fig. 2A). This number is inconsistent with the number of clades identified in SET domain-containing genes of Solanum lycopersicum (Table S7), which belongs to the same genus as potato [28]. Although a phylogenetic clade is well defined, the criteria and datasets used to infer the phylogenetic clade vary among studies, which explain the observed variation in the number of clades among species. Interestingly, our phylogenetic analysis using the combined list of the StSET genes and SET domain-containing genes of three other species, including Solanum lycopersicum [28], identified six clades (Fig. 3). This result supports that the six phylogenetic clades for StSET genes are acceptable, following the number of clades identified for SET domain-containing genes of Malus domestica [24], Populus trichocarpa [26], and Triticum aestivum [29] (Table S7).

The analysis of cis-elements in the promoter regions allowed the prediction of potential mechanisms of StSET gene regulation. Our results showed that a diverse set of cis-elements were present in most StSET genes (Table 3), indicating that the StSET genes are involved in several diverse biological processes, including drought [45], anaerobic induction, auxin responsiveness, defense, stress responsiveness, wound, and low-temperature responsiveness (Fig. 4). Further, most of these cis-elements were reported to be present in the promoters of SET domain-containing genes of other plant species as well, including Triticum aestivum [29], Solanum lycopersicum [28], Oryza sativa [25], and Arabidopsis thaliana [21], indicating the conservation of regulatory mechanism to control various biological processes mentioned above across species.

Tandem duplication marginally contributes to the expansion of StSET genes

The duplication of genes has played a substantial role in eukaryotic evolution by contributing significantly to the genetic and morphological diversity and speciation [46]. Two whole-genome duplication events have occurred during potato genome evolution [47], and they generated tandemly duplicated genes (about 18% of genes) by sub-functionalisation and neo-functionalisation in the potato reference genome [48]. In this study, we found that about 23% of StSET genes were tandemly duplicated (Fig. 1; Table 4). As this rate is slightly higher than the genome-wide duplication rate, no particular expansion can be reported due to tandem duplication of the StSET genes. We observed similar expression patterns between StSETs of the same tandemly duplicated gene cluster while dissimilar expression patterns between members of different tandemly duplicated gene clusters was observed (Fig. 5). Further, we found that most tandemly duplicated StSET genes contained identical protein domains, showed an expression divergence across tissues (Fig. 5), and a neutral or purifying selection, i.e., Ka/Ks < 1 (Table 4). Altogether, these results indicate that retention of duplicated StSET genes occurred through sub-functionalisation, where the ancestral gene functions have become divided among the daughter copies, and both daughter copies must remain functional [48]. The proportion of tandemly duplicated StSET genes in potato is significantly higher than those identified in Setaria italica [27] and Malus domestica [24], which indicates the expansion of a gene family with tandemly duplicated genes in one species lineage tends to be coupled with losses in the other due to lineage-specific selection of tandemly duplicated genes [49].

Table 4 List of tandemly duplicated gene (TDG) clusters identified in StSET genes. Gene 1 and Gene 2 indicates a pair of tandemly duplicated genes. Ka and Ks indicate the number of non-synonymous substitutions per non-synonymous sites and synonymous substitutions per synonymous sites, respectively. Ka/Ks indicates the ratio of Ka and Ks. Time indicates the estimated time of divergence for tandem duplicated gene pairs calculated based on the Ka/Ks ratio

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Presence and absence of protein domains in StSET genes

Understanding protein domains is crucial for comprehending proteins' biological functions and evolutionary mechanisms, as they are the fundamental units that can function and evolve independently [50]. Thus, we performed a comparative analysis of protein domains identified in StSET genes against SET domain-containing genes of three species to identify the presence and absence variation of protein domains. The protein domain analysis highlighted the absence of three protein domains, such as AT hook (PFAM ID: PF02178), DUF4371 (PFAM ID: PF14291), and GYF_2 (PFAM ID: PF14237), in StSET genes (Fig. 2C; Table 1). In contrast, the StSET genes contain several protein domains absent in SET domain-containing genes of Solanum lycopersicum [28], although the species belongs to the same genus as potato (Table 1). These results indicate the evolution of novel biological functions of StSET genes by incorporating new protein domains with the existing ones. For example, the study identified a new protein domain, TDBD (Tify domain binding domain) (PFAM ID: PF16135), in the StSET45 gene absent in other plant species (Fig. 2C, Table 1). This domain binds with the Tify domain of JAZ1 proteins to play a role in stress-related and growth-related signalling cascades [51].

Recombination effects, such as duplication, insertion, deletion, and transposition, mainly determine the emergence of different domain combinations within proteins [52, 53]. The evolutionary selection of the newly created domain combinations is then influenced by the functional advantage it provides to the organism [54]. Thus, identifying novel protein domain combinations helps to better understand SET domain-containing proteins’ biological functions. In this study, we identified several protein domain combinations within SET domain-containing proteins across species (Fig. 2C; Table 2). For example, the SET domain-containing proteins of potato (StSET52) and Oryza sativa [25] comprised a unique combination of eight protein domains, such as SET, PWWP, FYRN, FYRC, PHD, PHD_2, zf-HC5HC2H_2, and zf-HC5HC2H. In contrast, this combination is absent from Solanum lycopersicum [28] and Arabidopsis thaliana [21]. Similarly, a unique combination of seven protein domains, such as SET, zf-HC5HC2H_2, zf-HC5HC2H, FYRN, FYRC, PWWP, and PHD_2, was identified in two SET domain-containing proteins of Arabidopsis thaliana [21], while being absent in other species, including in potato (Fig. 2C; Table 2). The SET domain-containing proteins with a unique combination of multiple protein domains might be involved in several biological processes in addition to catalysing the histone methylation on lysine residues in respective species.

Pollen-specific expression of StSET genes

Due to the critical roles of SET domain-containing genes in various plant developmental processes, the expression of these genes in different tissues has been studied in many species, including Solanum lycopersicum [28], Setaria italica [27], and Triticum aestivum [29]. We observed the expression of about 82% of StSET genes in at least one tissue (Fig. 5). In addition, most of the genes showed a high expression in all tissues except pollen and indicated key roles of SET domain-containing genes in diverse tissues. Notably, three tandemly duplicated genes, namely StSET37, StSET38, and StSET40, exhibited a pollen-specific gene expression with an average Tau index of 0.9928 (Fig. 5; Table S6). The tissue-specific expression of StSET genes in pollens might indicate that these genes are involved in pollen development. For example, SDG4, a SET domain-containing gene, regulates the pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollens of Arabidopsis thaliana [55]. In addition, our study highlights the expression divergence across tissues between members of a phylogenetic clade and across phylogenetic clades (Figure S3).

Expression profiling of StSET genes in response to abiotic stress

Recent studies suggest that SET domain-containing genes are involved in plant stress responses [16, 22, 24, 27]. Thus, we assessed the expression patterns of four candidate StSET genes, StSET13, StSET30, StSET48, and StSET52, under heat and drought stresses using RT-qPCR in three potato clones. The RT-qPCR results showed that the four candidate StSET genes showed extensive variation in drought and heat-stress-induced gene expression changes across three potato genotypes: Karlena and Kolibri (drought-tolerant), and Laura (drought-sensitive and heat-tolerant).

StSET13 exhibited a consistent pattern of increased expression from early (T3) to late-stage (T6) drought stress in the drought-tolerant genotypes Karlena and Kolibri. This trend, however, was not observed in the drought-sensitive genotype Laura where the relative expression was even down-regulated compared to control conditions under extreme drought. This observation indicated a potential difference in their genotype-specific stress response mechanisms under drought (Fig. 6). Similarly, drought-induced SET domain-containing genes have been reported in many plant species. For example, 21 SET domain-containing genes exhibited a differential expression in response to drought stress in a drought-tolerant Setaria italica genotype [27].

Under heat stress, all four genes showed high expression during the early stage of heat stress (T3) in the heat-tolerant genotype Laura. In comparison, all four genes showed high expression during either early or late-stage heat stress in drought-tolerant genotypes Karlena and Kolibri, respectively (Fig. 6), suggesting a potential difference in their genotype-specific stress response mechanisms under varying durations of heat stress. Similarly, SET domain-containing genes of Gossypium raimondii showed differential expression in response to heat stress to affect the methylation status of stress-responsive genes to further regulate in response to heat stress [23].

Furthermore, most of these genes showed a decline in expression after recovering from the stress (Fig. 6). The high expression of StSET genes under stress and a decline during recovery from stress might be caused by the histone modifications regulating various stress-responsive genes to withstand the abiotic stress, followed by reverting histone modifications to their normal levels once the stressor is no longer present [17, 56, 57]. Therefore, StSET genes may be crucial in conferring drought and heat stress tolerance in potatoes. It is important to validate the observed expression patterns through independent experiments and analyses, such as using additional genotypes, different abiotic stress conditions or complementary techniques like RNA-Seq.

Conclusion

In conclusion, this study provides valuable insights into the SET gene family in Solanum tuberosum. We identified a total of 57 StSET genes in the potato genome, with a majority of StSET genes distributed among 11 chromosomes. Phylogenetic analysis classified the structurally diverse StSET genes into six groups. Gene duplication analysis indicated that tandem duplication played only a marginal role in the expansion of StSET genes. We examined the distinct protein domain combinations of the SET domain and other protein domains and compared them between potato and other plant species. We performed in silico tissue-specific expression analysis of StSET genes among 15 potato tissues to unravel their biological activity in different organs. RT-qPCR assessed the expression profiles for StSET genes under abiotic stress conditions to infer their genetic role in stress tolerance. Overall, this study presents a comprehensive analysis of the SET gene family in potato and will contribute to further characterization and elucidation of the epigenetic regulatory mechanisms of the SET gene family in different potato genotypes and related plant species.

Materials & methods

Identification of StSET genes in Solanum tuberosum

The protein sequences of SET domain-containing genes reported in Arabidopsis thaliana [21], Camellia sinensis [22], Gossypium raimondii [23], Malus domestica [24], Oryza sativa [25], Populus trichocarpa [26], Setaria italica [27], Solanum lycopersicum [28] and Triticum aestivum [29], were retrieved and used as input sequences to identify StSET genes in potato using sequence- and profile-based approaches. Here, we used the genomic sequence and annotation data of the diploid clone derived from the potato cultivar Agria (dAg) [48, 58] as a reference genome to identify the SET domain-containing genes in potato. In the sequence-based approach, the above-retrieved protein sequences were searched against the protein sequences of dAg using BLASTP [59] with an e-value cut-off of 1e⁻¹⁰. In the profile-based approach, we computed a multiple-sequence alignment (MSA) using the above-retrieved protein sequences using ClustalW with the default parameters [60]. We created a Hidden-Markov Model (HMM) profile by feeding the above-computed MSA to hmmbuild with the default parameters [61], and we searched for StSET genes in the protein sequences of dAg using hmmsearch with the default parameters [61] with an e-value cut-off of 1e⁻¹⁰ using the above-computed HMM profile as a query. Finally, we combined the list of putative StSET genes obtained from both approaches. We fed the corresponding protein sequences of the unique putative StSET genes to InterProScan [62] and Pfam [63] to confirm the presence of the SET domain (InterProScan ID: IPR001214; PFAM ID: PF00856). In addition, we have performed a BLASTP search [59] using the confirmed StSET protein sequences as a query against the proteome of dAg to identify additional SET domain-containing proteins in the reference genome except those obtained by the above search. BLASTP [59] hits with e-value cut-off of 1e⁻¹⁰ and > = 50% of sequence similarity and query coverage were fed to InterProScan [62] and Pfam [63] to confirm the presence of the SET domain (InterProScan ID: IPR001214; PFAM ID: PF00856). Overrepresented gene ontology terms were identified for identified StSET genes using WEGO 2.0 [64].

Physical map**, gene structure, and domain organisation of StSET genes

We extracted the chromosomal location of individual StSET genes from the annotation (gff) of the potato reference genome [48]. We visualised the physical map** of StSET genes using MapChart v2.32 [33]. We extracted the coordinates of the exon, intron, and UTR regions of individual StSET genes from the annotation of dAg, and we visualised the gene structure as well as protein domain organisation using TBTools v1.098696 [58] and considered it the putative promoter sequence. Using the MEME Suite web server [68], we identified the top 20 conserved motifs in the promoter sequences of StSET genes. The parameters used were motif width: 5 to 100 bases; site distribution: any number of repetitions. We identified cis-elements within the promoter sequences using the PlantCARE database with a frequency cut-off of three for each cis-element [36].

Identification of duplicated StSET genes

We identified duplicated StSET genes by performing an all versus all BLASTP search between protein sequences of all StSET genes, followed by feeding the BLASTP results to MCScanX with the default parameters [69]. We aligned the protein sequences of each pair of duplicated StSET genes using MAFFT v7.453 with the default parameters [70], and we calculated the non-synonymous (Ka) and synonymous (Ks) substitutions and their ratios (Ka/Ks) using PAL2NAL with the default parameters [71]. Finally, we highlighted the duplicated StSET genes on the physical map** of StSET genes created earlier.

Phylogenetic analysis of StSET genes

We computed an MSA for StSET genes using respective protein sequences by feeding to the MAFFT program v7.453 [70] with default parameters. We computed a mid-rooted phylogenetic tree for StSET genes by feeding the above-computed MSA to RAxML v8.2.12 [72] with the PROTGAMMAAUTO and JTT models and 100 iterations. Similarly, we computed a phylogenetic tree by feeding the protein sequences of StSET genes and SDGs reported in Arabidopsis thaliana [21], Oryza sativa [25], and Solanum lycopersicum [28]. We visualised the computed phylogenetic trees using TBTools [25], and Solanum lycopersicum [28]. We visualised the syntenic relationship of SET genes using Circos v0.69–8 [38]. Further, we compared the StSET genes against SET domain-containing genes of the above mentioned three selected species regarding the presence and absence of protein domains and protein domain combinations.

Availability of data and materials

All data generated or analysed during this study are included in this published article and can be found in Supplementary Tables S1 – S7.

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Acknowledgements

We would like to sincerely thank Böhm-Nordkartoffel Agrarproduktion GmbH & Co. OHG (BNA) and NORIKA GmbH for providing the potato tubers of this study. We are grateful to our former student assistant Charlotte Streitferdt, and CEPLAS intern Susanna Schmitz for their great lab support.

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Institute for Quantitative Genetics and Genomics of Plants, Heinrich Heine University, Düsseldorf, 40225, Germany
Vithusan Suppiyar, Venkata Suresh Bonthala, Asis Shrestha, Stephanie Krey & Benjamin Stich
Cluster of Excellence On Plant Sciences, From Complex Traits Towards Synthetic Modules, Heinrich Heine University, Düsseldorf, 40225, Germany
Benjamin Stich
Present Address: Julius Kühn-Institut (JKI), Institute for Breeding Research On Agricultural Crops, Rudolf-Schick-Platz 3a, OT Groß Lüsewitz, Sanitz, 18190, Germany
Venkata Suresh Bonthala, Asis Shrestha, Stephanie Krey & Benjamin Stich

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Vithusan Suppiyar
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Venkata Suresh Bonthala
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Asis Shrestha
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Benjamin Stich
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BVS conceived the research and designed and supervised the experiments. BS and AS designed the wet lab experiments. VS and SK performed the experiments and analysed the data. AS supervised wet lab experiments. VS and BVS wrote the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Venkata Suresh Bonthala.

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Suppiyar, V., Bonthala, V.S., Shrestha, A. et al. Genome-wide identification and expression analysis of the SET domain-containing gene family in potato (Solanum tuberosum L.). BMC Genomics 25, 442 (2024). https://doi.org/10.1186/s12864-024-10367-2

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Received: 25 September 2023
Accepted: 30 April 2024
Published: 03 May 2024
DOI: https://doi.org/10.1186/s12864-024-10367-2

Genome-wide identification and expression analysis of the SET domain-containing gene family in potato (Solanum tuberosum L.)

Abstract

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Introduction

Identification of duplicated StSET genes

Phylogenetic analysis of StSET genes

Identification of cis-elements and conserved motifs

Tissue-specific expression of StSET genes

Expression profiling of StSET genes in response to abiotic stress conditions

Comparative analysis of SET domain-containing genes

Discussion

SET domain-containing gene family in potato

Tandem duplication marginally contributes to the expansion of StSET genes

Presence and absence of protein domains in StSET genes

Pollen-specific expression of StSET genes

Expression profiling of StSET genes in response to abiotic stress

Conclusion

Materials & methods

Identification of StSET genes in Solanum tuberosum

Physical map**, gene structure, and domain organisation of StSET genes

Identification of duplicated StSET genes

Phylogenetic analysis of StSET genes

Availability of data and materials

References

Acknowledgements

Funding

Author information

Authors and Affiliations

Contributions

Corresponding author

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Competing interests

Additional information

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Supplementary Information

Supplementary Material 1.

Supplementary Material 2.

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