Next Article in Journal
Effects of Different Irrigation Rates on Remontant Strawberry Cultivars Grown in Soil
Previous Article in Journal
Evaluation of the Inhibitory Efficacy of Eugenol against the Pathogen of Fusarium Wilt in Ginger Seedlings
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 9
Issue 9
10.3390/horticulturae9091025
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Identification and Expression Analysis of Adenylate Kinase Gene Family in Potato

by
Xiang Li
,
Chengcheng Lyu
,
Jun Song
,
Yifei Lu
,
Fuchun Zeng
,
Liming Lu
and
Liqin Li
*
College of Agronomy, Sichuan Agricultural University, Chengdu 611130, China
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(9), 1025; https://doi.org/10.3390/horticulturae9091025
Submission received: 7 August 2023 / Revised: 23 August 2023 / Accepted: 6 September 2023 / Published: 11 September 2023
(This article belongs to the Section Genetics, Genomics, Breeding, and Biotechnology (G2B2))
Browse Figures
Review Reports Versions Notes

Abstract

:
Adenylate kinase (ADK) is a key enzyme that is widely distributed in animals and plants. It plays an important role in growth and stress response. However, ADK genes in potato (StADK) have been little reported. It is of great significance to identify ADK members and understand the molecular mechanism of stress response and tolerance. Based on the potato genome data, 23 StADK genes were identified at a genome-wide level. We then performed a comprehensive study using a bioinformatics method. The results of the evolutionary tree showed that StADK proteins were divided into four groups, and they were highly homologous to the Arabidopsis thaliana ADK members. Meanwhile, our study found that they existed on eight chromosomes, and we obtained three pairs of fragment duplications. Furthermore, we detected the six selected StADK genes using qRT-PCR, and the results confirmed that the genes are involved in the regulation of cold, ABA, salt, H2O2 and drought stresses. Our study provides a theoretical basis for studying the function of the potato ADK genes and lays a solid foundation for further understanding the molecular mechanism of the potato ADK genes under various environmental stresses.

1. Introduction

Adenylate kinase (ADK) is a widespread and abundant enzyme found in almost all living organisms. The synthesis of adenylate is usually accompanied by the release of energy in the organism, and its change is also an important factor affecting cell metabolism [1], which is related to cell growth and development [2]. ADK, as a monomer phosphotransferase, can catalyze the reversible transfer of phosphate groups from ATP to AMP through ATP + AMP ⇌ 2ADP [3] and plays a crucial part in adenosine concentration [4]. ADK has three domains, which are composed of CORE, ATP binding domain LID, and NMP binding domain NMP [5]. It is highly conserved in plants and animals, and its activity has been confirmed in rice, corn, tomato, alfalfa and other plants. It is also expressed in different subcells, for example, cytoplasm, mitochondria and nucleus [6,7,8]. Previous studies showed that after StADK expression was inhibited in potato, the content of adenylate and starch would be significantly increased [9]. During cell death, cytochrome C in ADK and mitochondria is released into the cytoplasm [10]. Under salt stress, both the expression level and activity of adenosine kinase change, and the DNA methylation level will be affected [11]. These studies provide important clues for us to explore the function of ADK in plant growth, development, and resistance to different stresses further.
Potato originated in the Andes Mountains and has been cultivated for over 7000 years [12]. At present, the potato has become the fourth major food crop in the world [13]. However, the function of the members of the ADK family in potato has not been thoroughly reported. In light of the significance of the ADK family and the economic benefits of potato, it is meaningful to have an overview of the identification and analysis of that. Using bioinformatic methods, this study identified 23 ADK members in potato. And our research found that the ADK members of potato are highly homologous to Arabidopsis thaliana, suggesting that they may perform similar functions under various stress. Moreover, in order to determine whether the StADK genes were involved in plant response to abiotic stresses (cold, ABA, salt, H2O2 and drought stresses), we selected six genes (StADK11, StADK12, StADK13, StADK14, StADK15, StADK18) to detect their expression using qRT-PCR. Our results suggested that StADK genes play an important part in responding to abiotic stress. In conclusion, our results not only preliminarily explored the function of StADK genes but also laid a foundation for the selection and breeding of potato with high tolerance.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

Potato tissue culture seedling was used in this study, the variety is Chuanyu No. 10, provided by the potato research center of Sichuan Agricultural University (Wenjiang District, Chengdu, Sichuan Province, China). High quality potato was selected to be cultured into seedlings and subjected to stress treatment (Table S1).

2.2. Acquisition of ADK Gene Sequence in Potato

Searching sequences contains ADK domain structure domain in the whole potato protein database by Hmmer3.0 software, setting the HMM file as the retrieval condition (http://pfam.xfam.org/, accessed on 15 June 2023). Then, the CDD (Conserved Domains Database, accessed on 15 June 2023) software (Batch CD-search) of NCBI website was used to remove incomplete sequences and error sequences.

2.3. Physicochemical Properties and Subcellular Localization Prediction of Potato ADK Protein

The properties of ADK proteins and subcellular localization of the potato ADK protein sequence have been predicted by using the ExPASy ProtParam tool (http://expasy.org/tools/protparam.html, accessed on 15 June 2023) and ProtComp 9.0 (http://linux1.softberry.com, accessed on 15 June 2023), respectively.

2.4. Amino Acid Sequence Analysis and Phylogenetic Tree Construction of ADK Protein

A total of 23 ADK potato genes were analyzed using MEGA7.0 software [14], and phylogenetic trees were constructed using a neighbor-joining method. Parameters were set up with missing data, a P-distance model and Bootstrap test with 1000 instances of pairwise deletion.

2.5. Analysis of ADK Motifs and Gene Structure in Potato

Gene structure information was extracted and displayed visually using TBtools (v1.120) [15]. Using the online software MEME [16] (http://meme.sdsc.edu/meme/meme-intro.html, accessed on 16 June 2023) to forecast motifs of candidate genes, the base sequence length was set as 6~50 and the base sequence number was 20.

2.6. Analysis of Location on Chromosomes, Gene Duplication

We acquired the annotation profile from the Potato Genomics Resource (http://spuddb.uga.edu/, accessed on 16 June 2023). Next, based on the annotated map and gene distribution of the potato genome, the location of the StADK family was visualized by using TBtools software (v1.120).

2.7. Collinearity of ADK Family Genes in Potato

To explore the evolutionary relationship of ADK in different species, we visualized the collinearity of the ADK family in rice, Arabidopsis thaliana and potato using MCScanX (on TBtools v1.120).

2.8. Expression Pattern Analysis of ADK Genes in Potato

The transcriptome data of the potato ADK family were downloaded from the Solanaceae Genomics Resource database [17]. The expression patterns and functions of ADK family members in potato were analyzed using cluster analysis and the evolutionary relationship.

2.9. Verification of Expression of ADK Genes in Potato

According to the cluster heat map drawn, six genes with a high response to abiotic stress were selected, and primers (Table S2) were designed according to their CDS sequences. One control group and five stress treatment groups were set up. The control group was without stress, and the treatment groups were low temperature (4 °C), ABA (1 μmol/L), drought (5%PEG-6000), high salinity (200 mmol/L) and H2O2 (10 mmol/L), respectively. Total RNA was extracted using the TRIzol method, and cDNA was synthesized using a Servicebio reverse transcription kit. SYBR®Premix Ex Taq II (Code No. RR820A/B) was selected for real-time PCR reaction. Then, we calculated the relative expression of genes using the 2−ΔΔCT method.

3. Results

3.1. Identification of ADK Gene Family Members in Potato

We used Hmmer3.0 software in the whole potato protein database to search sequences contains ADK domain by taking the HMM file as the retrieval condition (http://pfam.xfam.org/). In total, 23 StADK genes were identified in potato and were then renamed from StADK1 to StADK23.

3.2. Physicochemical Properties and Subcellular Localization Prediction of Potato ADK Protein

In conclusion, these StADK proteins range in length from 138 to 316 amino acids (aa) and in molecular weight from 15.5 (StADK23) to 35.9 (StADK15) kDa (Table 1). The predicted isoelectric points varied from 4.34 (StADK20) to 9.18 (StADK18), and the GRAVY values ranged from −0.702 (StADK10) to −0.078 (StADK23), respectively. Moreover, all the proteins were defined as hydrophilic proteins and unstable proteins according to our results. The results of subcellular localization showed that 14 StADK proteins were forecasted in the mitochondria, 5 proteins in the cytoplasm, and 4 proteins in the nuclei.

3.3. Phylogenetic Analysis of ADK Genes

Based on the ADK protein sequences of Arabidopsis thaliana and potato, we constructed a phylogenetic tree to observe the classification and the evolutionary characteristics of the ADK proteins (Figure 1). All 44 sequences, including 21 AtADK and 23 StADK, were mainly divided into four groups according to their homology. Group A contained four StADK members (StADK20, StADK21, StADK22, StADK23). Group B consisted of three StADK members, StADK 16/17/19. Group C included relatively many ADK members, StADK4, StADK5, StADK6, StADK7, StADK8, StADK10, StADK10, StADK12, StADK13, StADK14, StADK15, and StADK18. Group D was mainly composed of StADK1, StADK2, StADK3, StADK9, and StADK11. According to the aforementioned results, it can be predicted that the ADK members between potato and Arabidopsis thaliana may have similar biological functions.

3.4. Analysis of Motifs and Gene Structures of StADK

To explore the function of StADK genes, we analyzed their motifs and gene structures. By using MEME, the distribution of conserved motifs in the StADK proteins was visualized by TBtools (Figure 2). It can be seen in Figure 2 that all the ADK proteins included motif 1 and most of the StADK proteins comprised motif 3, except for StADK20, StADK21, StADK22, and StADK23. However, these four StADK proteins are all in group A, including motif 5 and motif 6. In addition, we analyzed the exon and intron compositions of the individual StADK genes. As shown in Figure 2, it can be seen that 2–9 exons in each StADK and most of the StADK genes (18 out of 23) had untranslated regions, except for StADK9, StADK10, StADK11, StADK15, and StADK21.

3.5. Location of Chromosomes and ADK Family Genes in Potato

As shown in Figure 3, StADK family members were distributed on 8 chromosomes, except ch02, ch07, ch10 and ch12. Seven StADK genes, including StADK2, StADK12–StADK15 and StADK19, in potato were gathered on chromosome ch03. And on chromosome ch11, ch06 and ch08, there are three (StADK3, StADK9 and StADK22), four (StADK11, StADK20, StADK21 and StADK23) and five(StADK5, StADK8 and StADK10) StADK genes were also found, respectively. In addition, on the other four chromosomes only one gene exsited, respectively. Gene duplication events play a necessary role in plant evolution. We used TBtools software to analyze all StADK gene replication events to clarify the replication mechanism. The result showed that 3 pairs of fragment duplication were identified, including StADK3/StADK11, StADK4/StADK6 and StADK21/StADK22, but found no tandem duplications in Figure 4.

3.6. Collinearity of ADK Family Genes in Potato

To examine the collinearity of the ADK family genes, we analyzed it between potato, Arabidopsis thaliana and rice. As shown in Figure 5, there were seven pairs of collinearity between potato and Arabidopsis thaliana. However, there was only one pair of collinearity between potato and rice.

3.7. Expression Pattern Analysis of ADK Genes in Potato

To further explore the function of the ADK gene family in potato, we made the heat map (Figure 6) using TBtools according to the transcriptome data. This indicated that StADK genes are highly expressed in the roots and stem. Meanwhile, some genes were mainly distributed in the leaves, such as StADK3, StADK9 and StADK11. Moreover, under abiotic stress, StADK genes mostly had a remarkably up-regulated expression, especially drought and salt stress. Among them, StADK11 and StADK15 had the highest expression under drought and salt stress, respectively. As for ABA treatment, there was a slight change in their expression.

3.8. Verification of Expression of ADK Genes in Potato

To further verify the function of the ADK family, according to the cluster heat map drawn, six genes with a high response to abiotic stress were selected (StADK11, StADK12, StADK13, StADK14, StADK15, and StADK18). One control group and five stress treatment groups were set up to analyze their expression in different tissues or under abiotic stress. The results are shown in Figure 7 and Figure 8. In Figure 7, most of the genes (four out of six) had the highest expression in the roots. As for other genes, StADK15 and StADK18 had the highest expression level in the stems and leaves, respectively.
Further, we summed up the data from qPCR to study the function of the StADK genes responding to abiotic stress. Under cold treatment (Figure 8A), all members were significantly upregulated; among them, StADK11 and StADK14 were significantly induced at 9 h and 24 h, StADK13 at 9 h and 12 h at the same time. Moreover, the expression pattern of StADK11 and StADK14 showed a consistent trend (declined–increased–declined–increased–declined). The StADK12 gene only showed a significantly induced expression level at 12 h, and the StADK15 gene at 9 h. On the contrary, StADK18 was significantly overexpressed at 3 h, 12 h and 24 h. As for ABA treatment, the expression of StADK11, StADK13 and StADK14 reached the top at 3 h; StADK13, StADK15 and StADK18 at 3 h, 12 h and 9 h, respectively. Also, StADK12 in the treatment remarkably expressed more than one in the control group the whole time. In addition, the expression pattern of StADK11, StADK12, StADK13, StADK14 and StADK18 exhibited consistent trends in change (first increased and then declined with the top at 3 h). Also, StADK15 increased at a peak of 12 h and then declined. Under salt stress, StADK11 and StADK14 were inhibited conspicuously all the times selected. As for StADK12, the expression level of it decreased, but not significantly. On the opposite, StADK18 was significantly overexpressed throughout the process. StADK13 was remarkably induced at 12 h while StADK15 was at 24 h. Under H2O2 treatment, the expression levels of the majority increased, among them mostly reached at the peak at 24 h, except for StADK15 at 12 h. In addition, StADK12 was remarkably inhibited at 9 h; on the contrary, StADK13 and StADK18 were significantly induced at 12 h and 3 h, respectively. In addition, the expression pattern of StADK11, StADK12, StADK13, StADK14 and StADK18 exhibited similar change tendencies (increased–declined–increased–declined–increased). Under drought stress, the expression levels of StADK11 and StADK18 significantly rose at 24 h. Meanwhile, the expression levels of StADK13 and StADK15 increased remarkably at both 9 h and 12 h. Moreover, StADK12 was induced significantly at all the times selected. StADK14 was remarkably expressed at 9 h, 12 h and 24 h, except for 3 h.

4. Discussion

The content change of adenylate compounds in vivo is considered to be the main factor causing the energy metabolism of cells. Adenylate kinase is the key enzyme to generate ADP and balance the phosphorylation reaction [7,18]. For example, The T-DNA of Arabidopsis thaliana ADK (At2g37250) gene was inserted into a homozygous mutant, which lead amino acid content rises and roots grow [19]. However, as a solanaceous plant, there are few reports about ADK family in potato. Through replication, gene produce two or more copies of a it [20,21], and they are resemblant in structure and function, coding for similar protein products, and because of this, we can find similar gene family members in different species. In recent research, there are 11 ADK genes in tomato [7], 11 in alfalfa [8], 13 in rice [20] and so on.
Duplication or loss of genes can lead to imparities in the number of gene family members during gene evolution [22,23]. In our study, we indentified 23 genes in the potato, and there are more members than any other plants mentioned. And all of them were hydrophilic proteins and unstable protein. The predicted subcellular localizations of these proteins showed that majority of StADK proteins were located in the Mitochondrial, where the activity of them will significantly affect the metabolic balance of free and bound magnesium ions in cytoplasm and in adenylate library. In the previous research ADK in plants is mainly distributed in the chloroplast matrix and mitochondrial membrane space, which is similar with our results [24,25].
In the phylogenetic tree(Figure 1), most of the ADK proteins show a deep homology among the two different plants, and 23 StADK proteins were divided into four groups. It is speculated that ADK is highly conserved between different species and existed before the separation of monocotyledonous plants. Further, we obtained 10 conserved motifs and found that the distribution of these Motifs of StADK was different between groups, but similar within groups. For example, most of StADK proteins comprised motif 3, except for StADK20, StADK21, StADK22, StADK23. However, these 4 StADK proteins are all in group A, including motif 5 and motif 6. In general, genes with common motifs have functional redundancy, while specific motifs may lead to functional differentiation [26]. Moreover, the pattern of gene organization [21], and exon structure plays a important role in comprehending evolutionary mechanisms of gene families [27]. In the Figure 2, it can tell that majority of the StADK genes had untranslated regions and the number of exons ranges from 2 to 9. There is a certain correlation between gene structure and motif arrangement, which further confirms the classification of StADKs.
In Figure 3, 23 StADK genes were widely distributed on 8 chromosomes, except ch02, ch07, ch10 and ch12. This is similar to the result in rice [22]. Through gene duplication, genes with new functions are produced, which is very important in plant evolution [28]. Fragment replication, tandem replication and translocation events are the main models of plant evolution and gene family expand usually through the first two modes [29,30]. In the Figure 4, it showed that there was collinear relationship between the gene pairs and they were divided into the same subclass. At the same time, these genes are also similar in structure, so it is speculated that they may perform similar functions during the growth and development of plants. Then, we identified 3 pairs of fragment duplication, but found no tandem duplications in Figure 3. Our findings suggest that the above gene pairs were formed through genome-wide replication and that may lead to the expansion of the StADK gene family, which might be the reason why there are more ADK genes in potato than other species. And in Figure 5, we found that there existed 7 pairs of collinearity between Arabidopsis thaliana and potato. This showed that in the evolutionary process, the ADK gene family is highly related to the two species, and there are certain similarities in the number of family members, gene structure and other aspects. Thus, we speculated that they may form similar functions. However, there was only one pair of collinearity between potato and rice (Figure 5), which indicated that there are evolutionary differences between monocotyledonous and dicotyledonous on ADK gene family.
In many species, the expression patterns of the ADK gene in different tissues have been reported [7,20,21]. In Figure 6, the heat map showed that the expression peak of 13 StADK genes was in stem and 7 in roots. Besides, StADK3, StADK9 and StADK11 were mainly expressed in leaves. To assess the potential roles of StADKs throughout potato development, we conducted detailed qRT-PCR to detect transcription in different tissues. In the Figure 7, StADK12, StADK13 and StADK14 expressed highest in the roots and the expression peak of StADK18 was both in roots and leaves, which were basically consistent with the heat map draw by transcriptome data [17]. It is worth mentioning that StADK11 and StADK15 expressed mostly in roots and stems, respectively. These results indicated that StADK genes played different roles in regulating the growth and development of potato.
Abiotic stresses are major causes of crop loss worldwide [31]. The previous study showed that ADKs not only regulate growth and development, but also widely are involved in abiotic stress response in plants [32,33,34]. Meanwhile, ABA plays an important role in plant resistance to abiotic stress [35]. Besides, cultivating crops with high stress resistance can effectively improve the yield and quality of that. For example, salt stress will destroy plant somatic cell membrane, causing damage to membrane structure, and change the permeability of plasma membrane to varying degrees, resulting in the leakage of intracellular substances, leading to the normal stable state of plant cells and a series of changes at the physiological and biochemical level [36]. Low temperatures damage the integrity of plant cell membranes, and some organelles such as the mitochondrial Golgi apparatus are also affected. The selective absorption ability of the cell membrane is lost, and the relative conductivity of the cell membrane is increased, which can reflect the degree of stress [37]. Under drought stress, the cell membrane may be destroyed and loses its semi-permeability, resulting in the exosmosis of amino acids and sugars inside the cell. [36]. Therefore, it is necessary to study the resistance of plants to abiotic stress. In our study, under the abiotic stress, mostly StADK genes in potato had a remarkable up-regulated expression, which were basically consistent with the results in other species [7,22,23]. Under cold treatment, they were induced significantly mostly at 24 h, and under ABA treatment at 3h. Also, StADK11 and StADK14 exhibited similar change tendencies, which means they may perform the same function to response to the stresses. In additions, under salt stress StADK11 and StADK14 were inhibited remarkably while the expression level of StADK12 decreased slightly. And other genes induced significantly at 12 h or 24 h. As for H2O2 treatment, all the genes reached the top at 24 h except for StADK15 at 9 h. It is worth noting that StADK11 and StADK14 exhibited similar change tendencies, even the expression was similar too. At last, under drought treatment, they were significantly at 9 h, 12 h or 24 h. In conclusion, we had further confirmation that StADK family genes do play an important role in potato developement and response to the abiotic stresses.

5. Conclusions

In conclusion, we identified 23 StADK proteins in potato at the whole-genome level, which were divided into four groups. Moreover, our results showed that there is a highly homologous relationship between Arabidopsis thaliana and potato. At the same time, StADKs were localized on eight chromosomes, and three pairs of fragment duplications were identified. Further qRT-PCR analysis confirmed that the six selected StADK genes showed diverse expression patterns, indicating their involvement in the regulation of cold, ABA, salt, H2O2 and drought stresses. All in all, the StADK gene is highly conserved in the evolutionary process and is involved in regulating potato growth and development and plays an important part in the response to stresses. This study will provide a certain basis for the genetic improvement of potato based on genetic engineering to verify the function of StADK members.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae9091025/s1, Table S1: Different stress treatments; Table S2: Primer of StADK genes selected.

Author Contributions

L.L. (Liqin Li) and X.L. designed the experiments and wrote the first draft of the manuscript; C.L. and J.S. performed the experiments; Y.L. and L.L. (Liming Lu) analysed the data; F.Z. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Science and Technology Department of Sichuan Province (Program No. 2022NSFSC0178) and the State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China (SKL-ZY202217).

Data Availability Statement

The data presented in this study are available within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Atkinson, D.E. The Energy Charge of the Adenylate Pool as a Regulatory Parameter. Interaction with Feedbac k Modifiers. Bioc Hemistry 1968, 7, 4030–4034. [Google Scholar]
  2. Ching, T.M.; Crane, J.M.; Stamp, D.L. Adenylate Energy Pool and Energy Charge in Maturing Rape Seeds. Plant Physiol. 1974, 54, 748–751. [Google Scholar] [CrossRef] [PubMed]
  3. Pradet, A.; Raymond, P. Adenine Nucleotide Ratios and Adenylate Energy Charge in Energy Metabolism. Annu. Rev. Plant Physiol. 1983, 34, 199–224. [Google Scholar] [CrossRef]
  4. Park, J.; Gupta, R.S. Adenosine Meta Bolism, Adenosine Kinase, and Evolution; Springer: New York, NY, USA, 2012. [Google Scholar]
  5. Arora, K.; Brooks, C.L. Large Scale allosteric conformational transitions of adenylate kinase appear to involve a population-shift mechanism. Proc. Natl. Acad. Sci. USA 2007, 104, 18496–18501. [Google Scholar] [CrossRef] [PubMed]
  6. Birkenhead, K.; Walker, D.; Foyer, C. The Intracellular Distribution of Adenylate Kinase in the Leaves of Spinach, Wheat and Barley. Planta 1982, 156, 171–175. [Google Scholar] [CrossRef]
  7. Yang, L.; Cao, H.; Zhang, X.; Gui, L.; Chen, Q.; Qian, G.; Xiao, J.; Li, Z. Genome-wide identification and expression analysis of tomato ADK gene family during development and stress. Int. J. Mol. Sci. 2021, 22, 7708. [Google Scholar] [CrossRef]
  8. Wang, Y.; Lei, Y.; Xu, J.; Wei, Z.; Wei, J.; Min, X. Identification and analysis of ADK gene family members in alfalfa (Medicago sativa). Caoye Kexue 2022, 39, 1803–1814. [Google Scholar]
  9. Regierer, B.; Fernie, A.R.; Springer, F.; Perez-Melis, A.; Leisse, A.; Koehl, K.; Willmitzer, L.; Geigenberger, P.; Kossmann, J. Starch Content and Yield Increase as a Result of Altering Adenylate Pools in Transgenic Plants. Nat Biotechnol. 2002, 20, 1256–1260. [Google Scholar] [CrossRef]
  10. Single, B.; Leist, M.; Nicotera, P. Simultaneous Release of Adenylate Kinase and Cytochrome C in Cell Death. Cell Death Differ. 1998, 5, 1001–1003. [Google Scholar] [CrossRef]
  11. Weretigk, E.A.; Alexander, K.J.; Drebensteat, M.; Ssnider, J.D.; Summers, P.S.; Mofratt, B.A. Maitaning Mtlyation Actvties Durng Salt Stess, the Ivovement of Adenosine Kinase 1. Plant Physiol. 2001, 125, 856–865. [Google Scholar]
  12. Hawkes, J.G. The potato, evolution, biodiversity and genetic resources. Am. Potato J. 1990, 67, 733–735. [Google Scholar]
  13. Chen, W.; Cai, R.; Lin, L. Strategic conception of boosting potato staple food normalization. Guizhou Agric. Sci. 2016, 44, 182–185. [Google Scholar]
  14. Sudhir, K.; Glen, S.; Koichiro, T. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 7, 1807. [Google Scholar]
  15. Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. Tbtools: An Integrative Toolkit Developed for Interac tive Analyses of Big Biological Data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
  16. Bailey, T.L.; Boden, M.; Buske, F.A.; Frith, M.; Grant, C.E.; Clementi, L.; Ren, J.; Li, W.W.; Noble, W.S. Meme Suite: Tools for Motif Discovery and Searching. Nucleic Acids Res. 2009, 37, 202–220. [Google Scholar] [CrossRef]
  17. Xu, X.; Pan, S.; Cheng, S.; Zhang, B.; Mu, D.; Ni, P.; Wang, J. Genome sequence and analysis of the tuber crop potato. Nature 2011, 475, 189–195. [Google Scholar] [PubMed]
  18. Igamberdiev, A.U.; Kleczkowski, L.A. Equlibration of adenylates in the mitochondrial intermembrane space maintains respiration and regulates cytosolic metabolism. J. Exp. Bot. 2006, 57, 2133–2141. [Google Scholar] [CrossRef]
  19. Carrari, F.; Coll-Garcia, D.; Schauer, N.; Lytovchenko, A.; Palacios-Rojas, N.; Balbo, I.; Rosso, M.; Fernie, A.R. Deficiency of a plastidial adenylate kinase in Arabidopsis results in elevated photosynthetic amino acid biosynthesis and enhanced growth. Plant Physiol. 2005, 137, 70–82. [Google Scholar] [CrossRef]
  20. Luo, Z.; Liu, Z.; Liu, C.; Li, L.; Xu, D. Bioinformatics analysis of rice ADK gene family. Mol. Plant Breed. 2023, 1–10. Available online: https://www.cnki.com.cn/Article/CJFDTotal-FZZW20230523008.htm (accessed on 6 August 2023).
  21. Xu, G.; Guo, C.; Shan, H.; Kong, H. Divergence of duplicate genes in exon-intron structure. Proc. Natl. Acad. Ences 2012, 109, 1187–1192. [Google Scholar] [CrossRef]
  22. Tang, C.; Zhu, X.; Qiao, X.; Gao, H.; Li, Q.; Wang, P.; Wu, J.; Zhang, S. Characterization of the Pectin Methyl Esterase Gene Famiy and its Function in Cntrlling Pllen Tube Growth in Pear (Pyrus Bretschneiden). Genomics 2020, 112, 2467–2477. [Google Scholar] [CrossRef] [PubMed]
  23. De Grassi, A.; Lanave, C.; Saccone, C. Genome duplication and gene-family evolution: The case of three OXPHOS gene families. Gene 2008, 421, 1–6. [Google Scholar] [CrossRef] [PubMed]
  24. Hampp, R.; Goller, M.; Ziegler, H. Adenylate levels, energy charge, and phosphorylation potential during dark-light and light-dark transition in chloroplasts, mitochondria, and cytosol of mesophyll protoplasts from Avena sativa L. Plant Physiol. 1982, 69, 448–455. [Google Scholar] [CrossRef] [PubMed]
  25. Stitt, M.; Lilley, R.M.; Heldt, H.W. Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol. 1982, 70, 971–977. [Google Scholar] [CrossRef]
  26. Wang, X.; Xue, S.; Chen, S.; Ma, C.; Xu, S. Evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution. Front. Plant Sci. 2018, 9, 71. [Google Scholar] [CrossRef]
  27. Rose, A.B. Intron-Mediated Regulation of Gene Expression; Springer: Berlin/Heidelberg, Germany, 2008. [Google Scholar]
  28. Moore, R.C.; Purugganan, M.D. The early stages of duplicate gene evolution. Proc. Natl. Acad. Sci. USA 2003, 100, 15682–15687. [Google Scholar] [CrossRef]
  29. Kong, H.; Landherr, L.L.; Frohlich, M.W.; Leebens-Mack, J.; Ma, H.; DePamphilis, C.W. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: Evidence for multiple mechanisms of rapid gene birth. Plant J. 2007, 50, 873–885. [Google Scholar] [CrossRef]
  30. Cannon, S.B.; Mitra, A.; Baumgarten, A.; Young, N.D.; May, G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004, 4, 10. [Google Scholar] [CrossRef]
  31. Zhang, H.; Zhu, J.; Gong, Z.; Zhu, J. Abiotic stress responses in plants. Nat. Rev. Genet. 2022, 23, 104–119. [Google Scholar] [CrossRef]
  32. Peterson, T.A.; Nlieman, R.H.; Clark, R.A. Nucleotide metabolism in salt-stressed Zea mays L. Root tips: I. Adenine and uridine nucleotides. Plant Physiol. 1987, 85, 984–989. [Google Scholar] [CrossRef]
  33. Zhou, S.; Wei, S.; Boone, B.; Levy, S. Microarray analysis of genes affected by salt stress in tomato. Afr. J. Environ. Sci. Technol. 2007, 1, 14–26. [Google Scholar]
  34. Raveneau, M.P.; Benamar, A.; Macherel, D. Water content, adenylate kinase, and mitochondria drive adenylate balance in dehydrating and imbibing seeds. J. Exp. Bot. 2017, 68, 3501–3512. [Google Scholar] [CrossRef]
  35. Lee, S.C.; Luan, S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012, 35, 53–60. [Google Scholar] [CrossRef]
  36. Bita, N. Linkages of Farmers Operations with Rhizoctonia Root Rot Spread in Bean Crops on a Regional Basis. J. Phytopathol. 2013, 161, 814–822. [Google Scholar]
  37. Bita, N.; Mozhgan, V. How variable characteristics of bean cropping systems affect Fusarium and Rhizoctonia root rot epidemics? Arch. Phytopathol. Plant Prot. 2019, 52, 1–15. [Google Scholar]
Horticulturae 09 01025 g001
Figure 1. Phylogenetic tree of the ADK gene family in potato and Arabidopsis thaliana.
Figure 1. Phylogenetic tree of the ADK gene family in potato and Arabidopsis thaliana.
Horticulturae 09 01025 g001
Horticulturae 09 01025 g002
Figure 2. Phylogenetic relationships, motifs, and gene structures of ADK family members from potato.
Figure 2. Phylogenetic relationships, motifs, and gene structures of ADK family members from potato.
Horticulturae 09 01025 g002
Horticulturae 09 01025 g003
Figure 3. Chromosome location of the StADK genes.
Figure 3. Chromosome location of the StADK genes.
Horticulturae 09 01025 g003
Horticulturae 09 01025 g004
Figure 4. Collinearity analysis of potato ADK family.
Figure 4. Collinearity analysis of potato ADK family.
Horticulturae 09 01025 g004
Horticulturae 09 01025 g005
Figure 5. Collinearity analysis of the ADK family genes in Arabidopsis thaliana, potato and rice.
Figure 5. Collinearity analysis of the ADK family genes in Arabidopsis thaliana, potato and rice.
Horticulturae 09 01025 g005
Horticulturae 09 01025 g006
Figure 6. Expression profile of ADK genes in potato (A) Expression profile in different tissue; (B) Expression profile under different abiotic stress.
Figure 6. Expression profile of ADK genes in potato (A) Expression profile in different tissue; (B) Expression profile under different abiotic stress.
Horticulturae 09 01025 g006
Horticulturae 09 01025 g007
Figure 7. Expression analysis of four StADK genes selected in roots, stems and leaves.
Figure 7. Expression analysis of four StADK genes selected in roots, stems and leaves.
Horticulturae 09 01025 g007
Horticulturae 09 01025 g008aHorticulturae 09 01025 g008b
Figure 8. Expression analysis of four StADK genes selected under abiotic stress. Note: (A) for cold, (B) for ABA, (C) for salt, (D) for H2O2, and (E) for drought.
Figure 8. Expression analysis of four StADK genes selected under abiotic stress. Note: (A) for cold, (B) for ABA, (C) for salt, (D) for H2O2, and (E) for drought.
Horticulturae 09 01025 g008aHorticulturae 09 01025 g008b
Table 1. Location of conserved sequence and physicochemical properties of potato ADK gene family.
Table 1. Location of conserved sequence and physicochemical properties of potato ADK gene family.
IDSequence
ID		Number of
Amino Acid		Molecular WeightpIInstability IndexAliphatic IndexGrand Average of HydropathicityLocalization Prediction
PGSC0003DMT400003152StADK124226,522.516.9742.7989.42−0.348Cytoplasmic
PGSC0003DMT400039275StADK224426,614.838.5744.3191.93−0.282Cytoplasmic
PGSC0003DMT400036202StADK329732,605.377.0646.9691.92−0.285Cytoplasmic
PGSC0003DMT400004310StADK420922,984.225.6134.5484.83−0.28Mitochondrial
PGSC0003DMT400062218StADK518921,725.058.6645.5574.71−0.579Mitochondrial
PGSC0003DMT400062217StADK621624,492.228.7645.3678.43−0.59Mitochondrial
PGSC0003DMT400062219StADK721624,492.228.7645.3678.43−0.59Mitochondrial
PGSC0003DMT400062220StADK821624,492.228.7645.3678.43−0.59Mitochondrial
PGSC0003DMT400036200StADK929732,821.928.247.5697.17−0.178Mitochondrial
PGSC0003DMT400062216StADK1021324,141.598.851.0570.85−0.702Mitochondrial
PGSC0003DMT400067159StADK1129733,695.818.6957.3284.01−0.32Mitochondrial
PGSC0003DMT400049088StADK1223626,728.798.9947.184.66−0.358Mitochondrial
PGSC0003DMT400049089StADK1323626,728.798.9947.184.66−0.358Mitochondrial
PGSC0003DMT400049087StADK1423726,815.878.9946.9584.3−0.359Mitochondrial
PGSC0003DMT400049085StADK1531635,929.98.4833.9476.84−0.551Cytoplasmic
PGSC0003DMT400071737StADK1628831,268.746.0344.8797.85−0.157Mitochondrial
PGSC0003DMT400074574StADK1727030,145.766.942.9294.96−0.288Mitochondrial
PGSC0003DMT400049086StADK1820323,120.19.185790.74−0.141Cytoplasmic
PGSC0003DMT400034809StADK1928331,788.096.0945.490.95−0.407Mitochondrial
PGSC0003DMT400019372StADK2017719,962.224.3458.1585.88−0.289Nuclear
PGSC0003DMT400019370StADK2118320,694.094.3557.8985.19−0.283Nuclear
PGSC0003DMT400070488StADK2217720,075.484.6365.5686.95−0.424Nuclear
PGSC0003DMT400019371StADK2313815,559.514.5157.6886.88−0.078Nuclear
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Li, X.; Lyu, C.; Song, J.; Lu, Y.; Zeng, F.; Lu, L.; Li, L. Identification and Expression Analysis of Adenylate Kinase Gene Family in Potato. Horticulturae 2023, 9, 1025. https://doi.org/10.3390/horticulturae9091025

AMA Style

Li X, Lyu C, Song J, Lu Y, Zeng F, Lu L, Li L. Identification and Expression Analysis of Adenylate Kinase Gene Family in Potato. Horticulturae. 2023; 9(9):1025. https://doi.org/10.3390/horticulturae9091025

Chicago/Turabian Style

Li, Xiang, Chengcheng Lyu, Jun Song, Yifei Lu, Fuchun Zeng, Liming Lu, and Liqin Li. 2023. "Identification and Expression Analysis of Adenylate Kinase Gene Family in Potato" Horticulturae 9, no. 9: 1025. https://doi.org/10.3390/horticulturae9091025

APA Style

Li, X., Lyu, C., Song, J., Lu, Y., Zeng, F., Lu, L., & Li, L. (2023). Identification and Expression Analysis of Adenylate Kinase Gene Family in Potato. Horticulturae, 9(9), 1025. https://doi.org/10.3390/horticulturae9091025

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop