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Article

Deciphering the Roles of Peanut (Arachis hypogaea L.) Type-One Protein Phosphatase (TOPP) Family in Abiotic Stress Tolerance

by
Qi Wang
and
Shihua Shan
*
Shandong Peanut Research Institute, Qingdao 266100, China
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(10), 2444; https://doi.org/10.3390/agronomy13102444
Submission received: 3 September 2023 / Revised: 19 September 2023 / Accepted: 19 September 2023 / Published: 22 September 2023
(This article belongs to the Special Issue Genes: Important Functions in Plant Stress Tolerance)
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Abstract

:
Dephosphorylation is one of the important mechanisms regulating signal transduction in plant growth and development and in response to abiotic stresses. Type-one protein phosphatases (TOPPs) catalyze a significant number of important dephosphorylation events in cells, and play essential roles in plant developmental regulations and multiple stress responses. Nevertheless, the knowledge regarding the peanut’s TOPP gene family remains extremely restricted. Thirteen TOPP genes (AhTOPP1-13) were discovered in the peanut genome database through the utilization of HMMER and BLASTP methods in this research. The thirteen AhTOPP genes were classed into three clades together with their Arabidopsis homologs based on phylogenetic tree, and mapped on nine of twenty chromosomes. The examination of gene compositions and protein patterns indicated resemblance in the structure of exons and introns, as well as the arrangement of motifs within the identical clade, which further reinforces the findings of phylogenetic analysis. All AhTOPP proteins possessed STPPase_N, Metallophos domains, and the core catalytic sites. Promoter analysis showed that the AhTOPP genes may be widely involved in peanut development, hormones, and stress response. The RNA-seq data revealed the presence of AhTOPP genes in twenty-two tissues, suggesting potential variations in the functionality of AhTOPP genes. Furthermore, drought and salt stresses induced the expression of multiple AhTOPP genes, including AhTOPP1, AhTOPP4, AhTOPP7, AhTOPP9, and AhTOPP13. It is worth mentioning that the AhTOPP genes’ expression could potentially be controlled by various transcription factors with different functions, including ERF, WRKY, MYB, and Dof. We will conduct specific functional studies on the peanut TOPP genes through transgenics in future research.

1. Introduction

In nature, plants are constantly threatened by several abiotic stresses, including extreme temperature, drought, and salt, which seriously affect plant growth and crop yield [1]. Plants have developed multiple molecular mechanisms and defense systems over time to deal with these adverse growth conditions. Upon sensing environmental stresses, plants initiate a signaling event within their cellular network, leading to the reprogramming of cellular processes and subsequent changes in gene expression. Moreover, the involvement of plant transporter proteins and channel proteins is essential in the response to various stresses [2]. Phosphorylation and dephosphorylation of crucial regulatory mechanisms in eukaryotic organisms serve as a binary toggle for governing cellular processes [3,4]. This essential mechanism is controlled by protein kinases and protein phosphatases. Protein kinases catalyze phosphorylation of substrate proteins by transferring phosphates from ATP, while protein phosphatases regulate signaling pathways and participate in multiple biological processes by catalyzing the dephosphorylation of substrate proteins [5].
Multiple types of phosphoprotein phosphatase (PPP) can be found in plants, such as PP1 (also known as type-one protein phosphatase, TOPP), PP2A, PP2B, PP2C, PP4, PP5, PP6, and PP7 [6]. TOPP functions as a hub protein with a single domain, where its catalytic subunit (PP1c) interacts with a regulatory subunit to generate an active enzyme. The regulatory subunits determine the catalytic activity, subcellular localization, and substrate specificity [7,8]. Presently, the TOPP gene family has been discovered in different plant species, such as wheat (Triticum aestivum) with a total of eighteen genes [9], soybean (Glycine max) with fifteen genes [10], Arabidopsis thaliana with nine genes [11], Brachypodium with eight genes [9], rice (Oryza sativa) with five genes [12], and Vicia faba with four genes [13].
Research has demonstrated that TOPPs play a crucial part in controlling different aspects of plant growth, development, and stress responses [14]. In Arabidopsis, TOPP1 was reported to be involved in the ABA signaling pathway by inhibiting SnRK2 kinase activity together with Arabidopsis Inhibitor-2 (AtI2). AtI2 is acknowledged as a suppressor of TOPP functions, operating in this capacity to enhance the interaction between SnRK2 and TOPP1 [15,16]. Notably, topp1 and ati-2 mutants exhibited hypersensitivities to ABA and salt stress [15]. TOPP4 positively regulates the gibberellins (GA) signaling pathway by dephosphorylation of the two DELLA proteins, REPRESSOR OF ga1-3 (RGA) and GA INSENSITIVE (GAI) [17]. TOPP4 is also involved in phytochrome B-mediated hypocotyl elongation [18], and regulates pavement cell interdigitation by dephosphorylating PIN-FORMED1 (PIN1) [19]. In addition, rice OsPP1a and wheat TdPP1a have been reported to possibly participate in response to salt stress [9,20]. Overexpression of OsPP1a could enhance salt tolerance in transgenic rice [20]. The TdPP1a was significantly induced by salt stress in wheat leaves [9]. The drought tolerance was significantly enhanced in tobacco plants through the overexpression of GmTOPP13 [10].
Peanut (Arachis hypogaea L.) holds significant economic value as a vital crop for both oil production and overall global economy. It offers a plentiful source of proteins and oils for humanity. Peanut growth, development, and yield are significantly impacted by drought and salt stresses. To manage environmental pressures, cultivating resilient cultivars is an optimal and cost-efficient approach. The peanut genome database has been used to conduct numerous studies on different gene families of peanuts [21,22,23,24]. However, our comprehension of the peanut TOPP gene family remains significantly constrained. In the present study, a total of thirteen TOPP genes were identified from the peanut genome. A thorough examination was conducted to analyze the gene structures, composition of cis-regulatory elements, chromosome distribution, phylogenetic relationships, expression patterns, and potential regulators. Our findings are expected to provide further understanding of how peanut TOPP proteins can enhance plant resistance to drought and salt stresses, leading to potential applications in this area.

2. Materials and Methods

2.1. Identification and Annotation of TOPPs from Peanut

The genome sequence data of peanut (Arachis hypogaea L.) were downloaded from the PeanutBase (https://legacy.peanutbase.org/peanut_genome (accessed on 2 July 2023)). The reported amino acid sequences of TOPP proteins from Arabidopsis thaliana were obtained from TAIR (The Arabidopsis Information Resource, https://www.arabidopsis.org/ (accessed on 2 July 2023)). Using the HMMER program (version 3.0), a thorough search was conducted in the peanut protein database to find all possible TOPP protein sequences. The queries used were the HMM profiles of TOPP (pfam: PF16891 and PF00149). The significance threshold was set at an E-value of 0.001 and the Arabidopsis TOPP protein full-length sequences were also as queries against the peanut protein database using the BLASTP program (E-value = 0.001). All output peanut TOPP proteins were examined using the SMART (http://smart.embl-heidelberg.de/ (accessed on 8 July 2023)) [25] and Pfam (http://pfam.xfam.org/search (accessed on 8 July 2023)) [26]. The isoelectric point (pI) and molecular weight (Mw) of the peanut TOPP proteins were calculated using the ProtParam tool (https://web.expasy.org/protparam/ (accessed on 10 July 2023)) [27]. LocTree 3 (https://rostlab.org/services/loctree3/ (accessed on 10 July 2023)) was utilized to forecast the subcellular protein position [28].

2.2. Multiple Sequence Alignment and Analysis of Phylogenetics

Multiple sequence alignments (MSA) of TOPP members from peanut and A. thaliana were conducted using MAFFT [29] with the default parameters. The construction of phylogenetic trees was carried out using the neighbor-joining (NJ) method in MEGA software (version 6.06) [30] based on the result of MSA. The parameters for phylogenetic tree construction by NJ analysis were Pairwise Deletion, Possion correction, and 1000-replicate bootstrap analysis.

2.3. Gene Structure Analysis and Identification of Conserved Domains

Alignment of the mRNA with their genomic sequences using GSDS 2.0 online software [31] illustrated the untranslated region (UTR), coding sequence (CDS), and intron of the TOPP genes in peanut. The MEME program (version 5.5.3) [32] was utilized to identify the conserved domain arrangement of TOPP proteins in peanuts. The parameters employed were as follows: site distribution limited to zero or one occurrence per sequence (zoops), eight motifs, and a motif width ranging from 6 to 50 amino acid residues.

2.4. Chromosomal Location and Gene Duplication

By referencing PeanutBase, the chromosome locations were determined and the genes were mapped to specific chromosomes using the MG2C v2.1 (http://mg2c.iask.in/mg2c_v2.1/ (accessed on 11 July 2023)), which involved identifying their physical positions on the chromosomes. A gene tandem duplication was defined based on the following set of criteria: (1) located within a 200 kb segment of a chromosome; and (2) a similarity of more than 70% between two genes [33]. The MCScanX program [34] was employed to identify the tandem and segmental gene duplications, while the visualization of the results was accomplished using Circos [35]. Using TBtools (version 1.120) [36], the syntenic analysis of orthologous genes derived from peanut and four other plant species was investigated. Afterwards, DnaSP (version 5.0) [37] was utilized to calculate the rates of nonsynonymous (Ka) and synonymous (Ks) (Ka/Ks), taking into account the identification findings of duplicated peanut TOPP genes.

2.5. Prediction of cis-Regulatory Elements

The 2000 bp sequence upstream of the ATG (start codon) start codon of each peanut TOPP gene was retrieved using TBtools (version 1.120) [36]. To analyze the cis-acting elements, the PlantCARE software (http://bioinformatics.psb.ugent.be/webtools/plantcare/html (accessed on 13 July 2023)) [38] was utilized.

2.6. Expression Analysis of Peanut TOPP Genes

To analyze the expression patterns of peanut TOPP genes, the RNA-seq data (accession: PRJNA291488, SRR8177741, and SRP093341) in 22 tissues and under different stress treatments (salt and drought) were obtained from NCBI. The cultivar Fenghua3 and J11 were used for salt and drought treatment, respectively [39,40,41]. The fold changes between the treatment and control data for each sample were subjected to log2 transformation. Subsequently, a heatmap was generated using TBtools (version 1.120) [36], with data normalization performed through row scaling.

2.7. Prediction of TFs Involved in Controlling Peanut TOPP Expression

In order to enhance the understanding of the transcription factors (TFs) responsible for regulating the expression of peanut TOPP genes, the promoter sequences were employed to investigate potential binding sites for TFs. The promoter sequences of peanut TOPP genes, which had a length of 2000 bp, were submitted to the PlantRegMap database (http://plantregmap.gao-lab.org/ (accessed on 15 July 2023)). Subsequently, the Regulation Prediction tool (http://plantregmap.gao-lab.org/regulation_prediction.php (accessed on 15 July 2023)) was utilized to forecast the TFs that control the expression of peanut TOPP genes, employing a p value of ≤10−5 [42].

2.8. GO and KEGG Enrichment Analysis

The protein sequences of all peanut TOPP members were submitted to the eggNOG website (http://eggnog-mapper.embl.de/ (accessed on 18 July 2023)) for the purpose of conducting the Gene Ontology (GO) annotation analysis [43]. Subsequently, TBtools (version 1.120) [36] was employed to perform the GO and KEGG (Kyoto Encyclopedia of Genes and Genomes) function enrichment analysis.

3. Results

3.1. Identification and Sequence Analysis of the Peanut TOPP Genes

In the present study, a total of thirteen TOPP genes in peanut were confirmed from the PeanutBase. The nomenclature of these genes ranged from AhTOPP1 to AhTOPP13, with each designation being derived from their respective chromosomal positions. In order to comprehensively characterize all peanut TOPPs, we systematically gathered related information including the chromosomal position, the number of amino acids (AAs), molecular weight (Mw), isoelectric point (pI), and predicted subcellular location of the protein (Table S1). The 13 TOPP protein sizes varied from 318 (AhTOPP11) to 387 (AhTOPP8) AAs. The Mw of the TOPP proteins ranged from 36016.49 (AhTOPP4 and AhTOPP9) to 43774.15 (AhTOPP8) Da, and the pI ranged from 5.27 (AhTOPP5 and AhTOPP11) to 6.97 (AhTOPP7 and AhTOPP13). Except for AhTOPP4, AhTOPP5, AhTOPP9, and AhTOPP11, another nine genes encoding proteins were predicted to localize predominantly to the cytoplasm.
In order to elucidate the conserved structure of thirteen AhTOPP proteins, multiple sequence alignments were performed using the DNAMAN tool. The results showed that AhTOPP proteins possess the typical features of serine–threonine protein phosphatases such as serine–threonine protein phosphatase N-terminal domain (STPPase_N domain) and calcineurin-like phosphoesterase (Metallophos domain). Significantly, the core catalytic sites in the AhTOPP family members were found to be conserved (Figure 1).

3.2. Phylogenetic Analysis of Peanut TOPP Genes

To enhance the investigation of the evolutionary correlation among peanut TOPP proteins, a neighbor-joining (NJ) phylogenetic tree was constructed using alignments of thirteen peanut TOPP proteins, fifteen soybean TOPP proteins, and nine Arabidopsis TOPP proteins (Figure 2). According to the result of the phylogenetic tree, the peanut TOPP gene family was classified into three major clades. Specifically, there are nine AhTOPPs in clade I, two AhTOPPs in clade II, and two AhTOPPs in clade III. It is worth mentioning that all clades include members from peanut, soybean, and Arabidopsis, suggesting that the separation of peanut, soybean, and Arabidopsis happened after the divergence of the TOPP gene family.

3.3. Conserved Motifs and Gene Structure

A total of eight conserved motifs were identified in peanut TOPP proteins using the MEME online server. Among the thirteen TOPP proteins analyzed, eleven AhTOPPs exhibited the presence of these eight motifs in a consistent arrangement. However, AhTOPP5 and AhTOPP11 were found to lack motif 8 (Figure 3). Additionally, the analysis of gene structure is important for the evolutionary history of TOPP gene family in peanut. An examination of the peanut TOPP gene structure was conducted using the GSDS online tool to investigate the distribution of exons and introns. We observed that three genes (AhTOPP5/10/11) possessed three exons, and eight genes (AhTOPP1/3/4/6/7/9/12/13) possessed four exons. AhTOPP2 and AhTOPP8 possessed five and six exons, respectively. Notably, a similar structure was found in the similar clade of the peanut TOPP genes (Figure 3).

3.4. Chromosomal Localization and Duplication Events

In order to enhance comprehension of the precise arrangement of genes on chromosomes, we generated chromosome distribution maps for members of the TOPP gene family in peanut. The results of chromosome localization analysis indicted that thirteen peanut TOPP genes were distributed on nine chromosomes (Figure 4A). Chr06, Chr09, Chr16, and Chr19 possessed the maximum number of two peanut TOPP genes, whereas only one peanut TOPP gene was found in Chr02, Chr03, Chr07, Chr13, and Chr17. Notably, no occurrences of tandem duplication events were identified in the peanut TOPP gene family.
In order to investigate the evolutionary relationships of TOPP genes, duplication event analysis of peanut TOPP genes was carried out. Five segmental duplication gene pairs were found among a set of ten peanut TOPP genes (Figure 4B). The results of duplication analysis suggested that specific peanut TOPP genes may have arisen through gene duplication, and that segmental duplication events could have played a crucial role in the evolutionary process of peanut TOPP genes. Furthermore, to investigate the role of selective pressure on peanut TOPP duplicated gene pairs, the non-synonymous levels (Ka) and synonymous levels (Ks) from five TOPP gene pairs were calculated. It is generally believed that Ka/Ks > 1 represents positive selection, Ka/Ks = 1 represents neutral selection, and Ka/Ks < 1 represents purification selection. We found that all of the five gene pairs showed Ka/Ks < 1, suggesting that these peanut TOPP genes were subjected to purification selection during the process of evolution (Table S2).

3.5. Analysis of Peanut TOPP Genes Syntenic

To examine the evolutionary connection between the TOPP genes in peanuts, a comparative analysis was conducted on peanuts and four other plant species. These species included three dicots (Arabidopsis, soybean, and tomato) and one monocot (rice) (Figure 5). The findings showed that nine of the AhTOPP genes displayed a syntenic connection with the TOPP genes in soybean, while five AhTOPP genes exhibited this relationship in tomato. Additionally, four AhTOPP genes in Arabidopsis and two AhTOPP genes in rice also showed a syntenic relationship with the TOPP genes. Peanut and soybean, tomato, Arabidopsis, and rice had a total of twenty-two, six, six, and two collinear pairs, respectively. Furthermore, it was observed that specific peanut TOPP genes, such as AhTOPP3, AhTOPP6, and AhTOPP10, displayed at least three collinear gene pairs with soybean. This finding implies the potential significance of these genes in the evolutionary process of the peanut TOPP gene family. It is worth mentioning that AhTOPP11 exhibited collinear pairs with TOPP genes from Arabidopsis, soybean, tomato, and rice, implying that the potential preexistence of this TOPP gene prior to the divergence of these five plant species. The comprehensive data pertaining to syntenic gene pairs can be found in Table S3.

3.6. Cis-Regulatory Elements Analysis of Peanut TOPP Genes Promoter

To investigate the potential role of peanut TOPP genes in stress responses and plant growth and development, the cis-regulatory elements (phytohormone responsive, abiotic/biotic stress, and development) of AhTOPP gene promoters were predicted via the plantCARE tool. The results indicated that the promoters of peanut TOPP genes exhibited a diverse array of cis-regulatory elements, ranging from eleven cis-regulatory elements in AhTOPP1 to thirty-eight in AhTOPP13 (Figure 6). In the majority of peanut TOPP gene promoters, eight plant hormone-responsive elements were discovered, including ABRE, CGTCA-motif, TGACG-motif, ERE, P-box, GARE, TCA-element, and TGA-element. These elements are responsible for regulating the plant’s responses to abscisic acid (ABA), methyl jasmonate (MeJA), ethylene (ETH), gibberellin, salicylic acid (SA), and auxin, respectively. The results suggest that a considerable amount of AhTOPP genes is probable to be involved in plant hormone-mediated signal transduction. Additionally, the advocates of peanut TOPP genes had numerous cis-regulatory components associated with environmental pressures, including the wound-responsive element (AS-1 and WUN-motif), defensive and stress-responsive element (W-box, TC-rich repeats, and STRE), drought-responsive element (MBS and MYB), flavonoid production (MBSI), low temperature stress element (LTR), and anaerobic stimulation element (ARE). This implies that AhTOPP genes are involved in the mechanism of addressing environmental stress. Additionally, several cis-regulatory elements associated with the growth and development of plants were discovered in peanut TOPP genes (excluding AhTOPP1). These elements include those linked to meristem expression (such as CAT-box and A-box) as well as transcription-factor-binding sites associated with growth and development (such as CCAAT-box and AT-rich element). Therefore, we hypothesize that AhTOPP genes can be triggered by various stresses and have a significant impact on the growth and development of plants.

3.7. Transcriptome Profiling of AhTOPPs in Different Tissues and in Response to Stress Treatments

Based on the transcriptome data publicly available in the PeanutBase [39], it was observed that the expression of AhTOPP genes was evident across twenty-two tissues that were tested, including leaf, shoot, root, nodule, perianth, stamen, pistil, fruit, and seed (Figure 7A). AhTOPP1, AhTOPP7, and AhTOPP13 were highly expressed in root, perianth, and pistil, whereas the expression levels of the three genes were lower in leaf, shoot, and seed. AhTOPP2, AhTOPP3, AhTOPP4, AhTOPP8, AhTOPP9, and AhTOPP10 displayed relatively high expression levels in peg tip Pat. 1 compared to other tissues. The expression levels of AhTOPP5 and AhTOPP11 were higher in early seed development. Notably, AhTOPP genes from the same clade exhibited a resemblance of tissue expression. The diverse profiles of gene expression suggested that AhTOPP genes in peanut growth and development may have very diversified functions.
To obtain further insights into the response of peanut TOPP genes to abiotic stresses, RNA-seq data under drought and salt stresses were downloaded from the NCBI database [40,41]. The results indicated that there was a distinct difference in AhTOPP genes’ response to drought and salt treatments (Figure 7B). Overall, 84.6% (eleven out of thirteen) AhTOPP genes were up-regulated under drought, whereas only 38.5% (five out of thirteen) genes were up-regulated under salt. AhTOPP2, AhTOPP3, AhTOPP6, AhTOPP8, AhTOPP10, and AhTOPP12 were insensitive to salt treatment but significantly induced by drought treatment. Notably, AhTOPP1, AhTOPP4, AhTOPP7, AhTOPP9, and AhTOPP13 displayed up-regulation under drought and salt treatments, suggesting that these five TOPP genes might play important roles in peanut responses to drought and salt stresses.

3.8. Prediction of Regulatory Network

The PlantRegMap server (version 5.0) was utilized to forecast potential regulatory associations between transcription factors and peanut TOPP genes. The analysis results showed a total of thirty-two types of transcription factors were predicted as possible regulators of peanut TOPP gene expression. The number of potential transcription factors that bind the peanut TOPP gene promoters were determined and visualized using TBtools software (version 1.120) (Figure 8A). ERF, C2H2, MIKC_MADS, MYB, and Dof transcription factors might be able to regulate almost all of the peanut TOPP genes. The regulatory patterns of AhTOPP6 and AhTOPP12 exhibited similarity, as these two genes might be regulated by ERF, WRKY, MYB, and Dof transcription factors. Notably, AhTOPP6 was regulated by the most transcription factors (fifteen), whereas AhTOPP3 was regulated by the least (eight). Additionally, we constructed and visualized the transcription regulation diagram using Cytoscape software (version 3.9.1) [44] between potential transcription factors and peanut TOPP genes (Figure 8B).

3.9. GO and KEGG Analysis of Peanut TOPP Genes

The roles of the peanut TOPP genes were anticipated by employing GO and KEGG enrichment analysis, which covered the domains of biological process (BP), molecular function (MF), and cellular component (CC). The GO enrichment analysis yielded a diverse array of terms that exhibited significant enrichment. The analysis of MF and BP annotations revealed that the primary function of these peanut TOPP genes is related to protein serine/threonine phosphatase activity (GO: 0004722), catalytic activity involving proteins (GO: 0140096), dephosphorylation of proteins (GO: 0006470), modification process of proteins (GO: 0036211), metabolic process of proteins (GO: 0019538), metabolic process of macromolecules (GO: 0043170), and metabolic process of nitrogen compounds (GO: 0006807) (Figure 9A). Furthermore, the KEGG enrichment analysis indicated that these peanut TOPP genes were mainly involved in translation, mRNA surveillance pathway, transcription machinery, and spliceosome (Figure 9B).

4. Discussion

Previous studies have suggested that TOPP (type-one protein phosphatase) genes function as Ser/Thr protein phosphatases and have significant involvement in governing abiotic stress responses and plant growth [14]. Considering the economic significance and oil production potential of cultivated peanut (Arachis hypogaea L.), it is also prone to a range of abiotic stresses, including low temperatures, drought, and high salinity. Therefore, it is important to identify and analyze peanut TOPP genes in response to multiple abiotic stresses. To date, TOPP genes have been identified in a variety of plant species, including wheat (Triticum aestivum) [9], soybean (Glycine max) [10], Brachypodium [9], rice (Oryza sativa) [12], and Vicia faba [13]. It has been reported that only nine TOPP genes were present in the Arabidopsis genome [11]. In this study, a total of thirteen TOPP genes were identified on nine chromosomes of the peanut genome (Table S1, Figure 4A), which might be because the peanut is an allotetraploid. All of the TOPP members share the same catalytic mechanism and structural folding and catalytic core [45]. Our results demonstrate that all TOPP members in peanut indeed possess the conserved residues necessary for the formation of the core catalytic domain, indicating their potential as active enzymes (Figure 1). Furthermore, all thirteen peanut TOPP proteins were predicted to localize in the cytoplasm and nucleus (Table S1), which has similar results to the TOPP proteins in Arabidopsis [45].
The distribution of conserved motifs and gene structure have a very important role in the course of gene evolution. Analysis revealed that the majority of the peanut TOPP genes contained eight conserved motifs and two–three introns with similar motif distribution and exon/intron structure, suggesting a close relationship of these genes within the same clade (Figure 2 and Figure 3). Additionally, tandem duplication and segmental duplication events have very important roles in the expansion of gene families in plants [46]. In our study, segmental duplication was the major force that contributed to the expansion of peanut TOPP genes, not tandem duplication. Furthermore, five pairs of peanut TOPP members were identified as segmental duplication genes (Figure 4B), with the Ka/Ks values of these gene pairs being lower than one (Table S2), indicting that these TOPP gene pairs might have experienced purifying selective pressure during peanut evolution. In addition, we found that duplicated TOPP genes existed within the same clade, such as AhTOPP5/AhTOPP11 in clade I, AhTOPP2/AhTOPP8 in clade II, and AhTOPP4/AhTOPP9 in clade III. However, duplication gene pairs for three genes (AhTOPP1, AhTOPP3, and AhTOPP10) were not discovered. This may be due to the loss of genes during the duplication process. Notably, two segmental duplication pairs (AhTOPP6/AhTOPP12 and AhTOPP7/AhTOPP13) showed similar expression patterns in peanut tissues (Figure 7A).
To better appreciate the potential functions of the TOPP genes in peanut growth and development, as well as responses to environmental stresses, we analyzed the cis-regulatory elements of peanut TOPP genes in detail. It was found that many cis-regulatory elements related to plant hormones, stresses, and plant growth and development were extensively distributed in the promoter regions of peanut TOPP genes (Figure 6). Previously, it was suggested that ABRE and MBS elements are involved in the response to abiotic stresses [47,48]. Specifically, the distribution of cis-regulatory elements within the promoters of the peanut TOPP gene exhibited a partial correlation with the level of gene expression. For example, AhTOPP1, AhTOPP4, and AhTOPP9 containing the ABRE in their promoters were up-regulated under drought and salt stresses (Figure 7B,C). Additionally, unequal amounts of ARE elements were found in 77% (ten out of thirteen) of the peanut TOPP genes. The presence of ARE elements was initially detected in the promoter region of the maize Adh-1 gene, which exhibited induction in response to dehydration and cold stresses [49]. It is noteworthy that TOPP1 has been demonstrated to interact with the AUX/IAA transcription factor family member AXR3, which suggests an involvement in auxin signaling [11]. The ethylene response element (ERE) was found in eleven family members, indicating the defense response of peanut TOPP genes. The recent genetic analysis conducted on Arabidopsis has indicated the potential role of TOPP genes in plant immunity [50]. However, additional experiments are required to determine whether TOPP members serve as regulators of plant immunity in peanut. Moreover, in promoters of twelve peanut TOPP genes, the developmentally related element AAGAA motif was detected. In conclusion, the analysis of promoter cis-regulatory elements indicates that TOPP genes may play a role in regulating peanut growth and development in response to various environmental stresses.
In order to examine the expression patterns of the peanut TOPP genes, we analyzed expression levels of AhTOPP genes in different tissues and under drought and salt stresses using RNA-seq data (Figure 7A). Members of the peanut TOPP family displayed different tissues expression patterns, indicating that these genes might be involved in the growth and development of peanut. Furthermore, several peanut TOPP genes were up-regulated under drought and salt conditions. The results are in agreement with previous studies of elevated expression of multiple TOPP genes in response to stresses. For instance, it was observed that certain TOPP genes exhibited up-regulation in response to cold, drought, heat, and salt stresses in Brachypodium [9]. All TOPP genes were involved in early response to drought stress in soybean (Glycine max) roots or leaves [10]. The findings presented in this study provide persuasive evidence that TOPP genes demonstrate a conserved role in alleviating abiotic stresses across diverse plants. Additionally, we found that more peanut TOPP genes are up-regulated under drought stress rather than salt stress. At the transcriptional level, the expression of almost all genes is regulated by transcription factors in plant biological processes. WRKY53 transcription factors promote leaf senescence by repressing SENRK1 gene expression [51]. Overexpression of ZmERF21 could improve drought resistance in maize seedlings by directly regulating stress-responsive genes [52]. Notably, multiple predicted transcription factor binding sites, including ERF, WRKY, MYB, and Dof, were identified within the promoter region of the peanut TOPP genes (Figure 8).

5. Conclusions

In conclusion, a total of thirteen AhTOPP genes were identified in peanut genome, which were divided into three clades based on evolutionary tree. The comprehensive information of AhTOPP members, including evolutionary relationship, gene structure and conserved motif, chromosome localization, duplication event, collinearity, cis-regulatory elements, and expression patterns, were systematically analyzed using bioinformatics and comparative genomics methods. The findings of this study have the potential to contribute to the comprehensive investigation of the specific functionalities of the AhTOPP genes.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy13102444/s1, Table S1: The detail information of identified peanut TOPP family members; Table S2: The detail information of segmental duplication gene pairs; Table S3: The syntenic pairs between peanut and other four plant species.

Author Contributions

S.S. conceived this research and designed the experiments. Q.W. conducted the research and drafted the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Shandong Natural Science Foundation (ZR2023QC057) and the Innovation Project of SAAS (CXGC2023F20).

Data Availability Statement

All data supporting the findings of this study are available within the paper and within its Supplementary Materials published online.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Multiple sequence alignment of 13 peanut TOPP proteins revealed conserved and divergent residues. The red and yellow boxes represent STPPase_N domain and Metallophos domain, respectively.
Figure 1. Multiple sequence alignment of 13 peanut TOPP proteins revealed conserved and divergent residues. The red and yellow boxes represent STPPase_N domain and Metallophos domain, respectively.
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Figure 2. Analysis of peanut TOPP proteins using phylogenetics. Using the neighbor-joining (NJ) method, the phylogenetic tree was created by aligning the TOPP proteins of peanut, soybean, and Arabidopsis, and then conducting 1000 bootstrap replicates.
Figure 2. Analysis of peanut TOPP proteins using phylogenetics. Using the neighbor-joining (NJ) method, the phylogenetic tree was created by aligning the TOPP proteins of peanut, soybean, and Arabidopsis, and then conducting 1000 bootstrap replicates.
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Figure 3. The gene structure and conserved patterns of peanut TOPP members.
Figure 3. The gene structure and conserved patterns of peanut TOPP members.
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Figure 4. Chromosomal distribution and duplication events of peanut TOPP genes. (A) Nine chromosomes contained a total of thirteen peanut TOPP genes that were mapped. (B) MCScanX was utilized to examine the segmental duplications of the five pairs of peanut TOPP genes, which are linked by the red lines.
Figure 4. Chromosomal distribution and duplication events of peanut TOPP genes. (A) Nine chromosomes contained a total of thirteen peanut TOPP genes that were mapped. (B) MCScanX was utilized to examine the segmental duplications of the five pairs of peanut TOPP genes, which are linked by the red lines.
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Figure 5. Comparative analysis of TOPP genes in peanut and Arabidopsis, soybean (Glycine max), tomato (Solanum lycopersicum), and rice (Oryza sativa) using synteny. The collinear blocks between peanut and four other plant species are represented by the gray line in the background, whereas the remaining lines show the syntenic TOPP gene pairs.
Figure 5. Comparative analysis of TOPP genes in peanut and Arabidopsis, soybean (Glycine max), tomato (Solanum lycopersicum), and rice (Oryza sativa) using synteny. The collinear blocks between peanut and four other plant species are represented by the gray line in the background, whereas the remaining lines show the syntenic TOPP gene pairs.
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Figure 6. Promoter regions of peanut TOPP genes contain regulatory elements. The number and abundance of each cis-acting element are also illustrated.
Figure 6. Promoter regions of peanut TOPP genes contain regulatory elements. The number and abundance of each cis-acting element are also illustrated.
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Figure 7. Expression patterns of peanut TOPP genes in different tissues (A) and in response to salt and drought stresses (B). CK, control untreated samples. TBtools was used to normalize and cluster the FPKM values of each peanut TOPP gene.
Figure 7. Expression patterns of peanut TOPP genes in different tissues (A) and in response to salt and drought stresses (B). CK, control untreated samples. TBtools was used to normalize and cluster the FPKM values of each peanut TOPP gene.
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Figure 8. Possible transcription regulators of peanut TOPP gene expression. (A) The number of potential transcription factors that bind the peanut TOPP gene. (B) Brief diagram of the regulatory network.
Figure 8. Possible transcription regulators of peanut TOPP gene expression. (A) The number of potential transcription factors that bind the peanut TOPP gene. (B) Brief diagram of the regulatory network.
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Figure 9. GO (A) and KEGG (B) enrichment analysis of peanut TOPP genes.
Figure 9. GO (A) and KEGG (B) enrichment analysis of peanut TOPP genes.
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Wang, Q.; Shan, S. Deciphering the Roles of Peanut (Arachis hypogaea L.) Type-One Protein Phosphatase (TOPP) Family in Abiotic Stress Tolerance. Agronomy 2023, 13, 2444. https://doi.org/10.3390/agronomy13102444

AMA Style

Wang Q, Shan S. Deciphering the Roles of Peanut (Arachis hypogaea L.) Type-One Protein Phosphatase (TOPP) Family in Abiotic Stress Tolerance. Agronomy. 2023; 13(10):2444. https://doi.org/10.3390/agronomy13102444

Chicago/Turabian Style

Wang, Qi, and Shihua Shan. 2023. "Deciphering the Roles of Peanut (Arachis hypogaea L.) Type-One Protein Phosphatase (TOPP) Family in Abiotic Stress Tolerance" Agronomy 13, no. 10: 2444. https://doi.org/10.3390/agronomy13102444

APA Style

Wang, Q., & Shan, S. (2023). Deciphering the Roles of Peanut (Arachis hypogaea L.) Type-One Protein Phosphatase (TOPP) Family in Abiotic Stress Tolerance. Agronomy, 13(10), 2444. https://doi.org/10.3390/agronomy13102444

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