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Article

Genome-Wide Identification and Expression Profiling of the α-Amylase (AMY) Gene Family in Potato

by
Yudan Duan
and
Liping Jin
*
State Key Laboratory of Vegetable Biobreeding/Key Laboratory of Biology and Genetic Improvement of Tuber and Root Crops of Ministry of Agriculture and Rural Affairs/Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China
*
Author to whom correspondence should be addressed.
Genes 2024, 15(6), 793; https://doi.org/10.3390/genes15060793
Submission received: 22 May 2024 / Revised: 5 June 2024 / Accepted: 9 June 2024 / Published: 17 June 2024
(This article belongs to the Section Plant Genetics and Genomics)
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Abstract

:
Starch degradation provides energy and signaling molecules for plant growth, development, defense, and stress response. α-amylase (AMY) is one of the most important enzymes in this process. Potato tubers are rich in starch, and the hydrolysis of starch into sugar negatively impacts the frying quality of potato. Despite its importance, the AMY gene family has not been fully explored in potatoes. Here, we performed a detailed analysis of the StAMY gene family to determine its role in potato. Twenty StAMY genes were identified across the potato genome and were divided into three subgroups. The promoters of StAMY genes contained an array of cis-acting elements involved in growth and development, phytohormone signaling, and stress and defense responses. StAMY8, StAMY9, StAMY12, and StAMY20 were specifically expressed in mature tubers. Different StAMY gene family members tended to be upregulated in response to β-aminobutyric acid (BABA), Phytophthora infestans (P. infestans), benzothiadiazole (BTH), heat, salt, and drought stress. In addition, different StAMY gene family members tended to be responsive to abscisic acid (ABA), indole-3-acetic acid (IAA), gibberellic acid (GA3), and 6-benzylaminopurine (BAP) treatment. These results suggest that StAMY gene family members may be involved in starch and sugar metabolism, defense, stress response, and phytohormone signaling. The results of this study may be applicable to other starchy crops and lay a foundation for further research on the functions and regulatory mechanisms of AMY genes.

1. Introduction

Potatoes (Solanum tuberosum L.) are the world’s third most important food crop [1,2]. Potatoes are cultivated in 160 countries around the world and are critically important to food security [3]. The starch content of potato tubers is considered one of the most critical agronomic traits in potato breeding. It typically ranges from 10% to 25% of the tuber’s fresh weight. The interconversion between starch and sugar affect potato quality, particularly the frying quality [4,5,6]. Light chips are a basic requirement for the potato processing industry. However, the consistent production of light chips throughout the year remains a major challenge [7]. Processing potatoes directly from cold storage (2–4 °C) into chips can reduce disease losses, extend marketability, and eliminate the need for dormancy-prolonging chemicals. Unfortunately, at low temperature, potato tubers are susceptible to cold-induced sweetening [8]. This phenomenon is an undesirable physiological process in which the rate of conversion of starch to reducing sugars (such as glucose and fructose) is accelerated in potato tubers [9]. As precursors of the Maillard reaction, a high concentration of reducing sugars such as glucose and fructose in potato tubers negatively affects frying quality. During frying, reducing sugars react with free amino acids (mainly asparagine), resulting in dark-colored, bitter-tasting substances. However, the more dangerous product of the Maillard reaction is acrylamide, a neurotoxin and suspected carcinogen [10,11]. Therefore, to reduce acrylamide content during frying, one effective way is to limit the accumulation of reducing sugars [12].
Starch is stored in almost all plant tissues, including leaves, roots, stems, flowers, and tubers. Extensive studies have shown that starch metabolism involves a series of enzymes, among which, amylases play an essential role in starch degradation [13,14,15]. The products of starch degradation provide essential support for plant growth and development and confer increased stress tolerance [16,17]. Starch degradation involves α-amylase (AMY) and β-amylase (BAM) [18]. AMY, as an endonucleoside hydrolase, hydrolyzes the α-1, 4-glycosidic bonds of polysaccharides (including starch) to generate oligosaccharides such as dextrin, maltotriose, maltose, and glucose [19,20,21]. Structurally, AMY possesses a (β/α)8-barrel catalytic domain, composed of three major domains [22,23,24]. The AMY family contains three subfamilies specific to the endosperm (subfamily I), cytoplasm (subfamily II), and chloroplast (subfamily III). Members of endosperm-specific subfamily I typically contain signal peptides which target the protein secretion pathway. In contrast, the functions of cytoplasm-specific subfamily II members are poorly characterized. Members of subfamily III typically contain a 400–500 amino acid (aa) expansion region and are predicted to act as chloroplast transport peptides. Research suggests that members of subfamily III are involved in the degradation of starch in leaves [25,26,27]. The transcription and enzymatic activities of AMY are regulated by a complex network that involves light, phytohormones, and stress factors [28,29]. Notably, AMY genes are controlled by gibberellin via gibberellin-induced MYBGA [30]. Furthermore, reports indicate that salt-stress-induced gibberellin-stimulated transcript (OsGASR1) regulated AMY gene expression [31]. Additionally, the AMY3 gene participates in stress-induced starch degradation via abscisic acid, particularly through the AREB/ABF-SnRK2 kinase signaling pathway [32].
The research on potato starch and sugar metabolism is relatively comprehensive, particularly concerning metabolic enzymes [33,34,35]. Genetic engineering can be utilized to regulate starch and sugar metabolism by targeting these enzymes for inhibition or overexpression [36,37]. Starch degradation plays a pivotal role in the cold-induced sweetening process of potatoes. Within the potato genome, 77 loci have been identified to encode enzymes involved in starch metabolism [38]. Research suggests that AMY activity increases concomitantly with the accumulation of reducing sugars in potato tubers during the initial weeks of low-temperature storage [39]. Furthermore, the manipulation of StAMY23 expression alters amylase activity and reducing sugar content in stored potato tubers [40,41]. The interaction between StAmy23 and the amylase inhibitor gene (SbAI) regulates cold-induced sweetening in potato tubers by modulating amylase activity [42]. Improving potato tuber starch dynamics can be achieved through cloning and functionally characterizing genes related to starch synthesis and degradation, analyzing the promoter sequence regulatory elements of key starch metabolism genes, and elucidating the regulatory mechanism controlling various aspects of starch metabolism.
Despite its importance, the AMY gene family has not been fully characterized in potato. In this study, we identified 20 StAMY genes across the potato genome. We analyzed the sequences, protein physicochemical properties, subcellular localizations, gene structures, conserved motifs, and phylogenetic evolution of each of the StAMY family genes. In addition, we investigated the functions and evolutionary characteristics of the StAMY gene family through promoter cis-acting element analysis and expression profiling. These results help to elucidate key genes involved in starch metabolism in potato tubers, lay the foundation for further research on StAMY genes, and provide a reference for starch improvement engineering in potato.

2. Materials and Methods

2.1. Identification of StAMY Genes

The whole-genome sequence and GFF3 annotation file were obtained from the Spud Database (http://spuddb.uga.edu/, accessed on 22 April 2024). Members of the StAMY gene family were identified via BLAST search using Arabidopsis thaliana AMY protein sequences as queries. To avoid missing any putative StAMY members, the potato protein sequences were queried using the Hidden Markov Model (HMM) file obtained from the Pfam database (http://pfam-legacy.xfam.org/, accessed on 22 April 2024), with default parameters. Following integration and redundancy elimination, the remaining sequences were used for further analyses. The chromosomal location map was created using TBtools. Coding sequence (CDS) length, isoelectric point (PI), and molecular weight (MW) were predicted using the Expasy website (https://www.expasy.org/resources/protparam, accessed on 22 April 2024). Protein subcellular localization was predicted using the WoLF PSORT Protein Subcellular Localization Prediction tool (https://wolfpsort.hgc.jp/, accessed on 22 April 2024).

2.2. Multiple Sequence Alignment and Phylogenetic Analysis of StAMY Genes

The A. thaliana AMY family genes were obtained from the NCBI database (https://www.ncbi.nlm.nih.gov/, accessed on 22 April 2024). All sequences of AtAMY and StAMY family genes were aligned, and a phylogenetic tree was constructed using the maximum likelihood (ML) method with default parameters in MEGA11.

2.3. Gene Structure and Conserved Motif Analysis of StAMY Genes

The structures and conserved domains of the StAMY genes were analyzed using Batch search (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi, accessed on 22 April 2024). Conserved motifs were analyzed using the MEME online tool (https://meme-suite.org/meme/, accessed on 22 April 2024), with the following parameters: the number of repetitions was set to zero or one and the maximum number of motifs was set to 10. Gene structures and conserved motifs were visualized using TBtools.

2.4. Promoter cis-Element Analysis of StAMY Genes

TBtools was used to extract the 2000 bp upstream sequences of StAMY genes. Cis-acting elements in the promoters of StAMY genes were predicted using the PlantCARE database (https://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 22 April 2024). Finally, TBtools was used for visualization following statistical scanning.

2.5. Expression Analysis of StAMY Genes

The expression analysis of StAMY genes was performed using data obtained from the Spud Database (http://spuddb.uga.edu/, accessed on 22 April 2024). TBtools was used to construct heatmaps using log2-normalized fragments per kilo base of transcript per million mapped fragments (FPKM) values. The expression datasets included data from S. tuberosum-group Tuberosum RH89-039-16 (RH; mature tuber, young tuber, stolon, root, stem, leaf, flower) and S. tuberosum-group Phureja DM1-3 516 R44 (DM; heat-treated whole plant, salt-treated whole plant, mannitol-treated whole plant, β-aminobutyric acid [BABA]-treated leaves, P. infestans-treated leaves, benzothiadiazole [BTH]-treated leaves, abscisic acid [ABA]-treated whole plant, indole-3-acetic acid [IAA]-treated whole plant, gibberellic acid [GA3]-treated whole plant, 6-benzylaminopurine [BAP]-treated whole plant).

3. Results

3.1. Genome-Wide Identification of StAMY Genes

A total of 20 StAMY genes were identified across the potato genome. The gene IDs, CDS lengths, start and end positions, protein lengths, MWs, and PIs of the AMY genes can be found in Table 1. The 20 StAMY proteins ranged in length from 373 aa to 1332 aa and ranged in weight from 41,687.07 Da to 150,181.53 Da. Their predicted theoretical PIs ranged from 4.9 to 6.89. The StAMY genes were found to be localized variously to the cytosol, vacuole, nucleus, chloroplast, mitochondrion, and peroxisome. Phylogenetic analysis of 20 StAMY and 15 AtAMY proteins revealed the presence of three distinct clades. As shown in Figure 1, the yellow clade included 14 members, including 8 StAMY and 6 AtAMY proteins; the pink clade included 11 members, including 6 StAMY and 5 AtAMY proteins; and the green clade included 10 members, including 6 StAMY and 4 AtAMY proteins.

3.2. Chromosomal Locations of StAMY Genes

The 20 StAMY genes were found to be variously located on Chr02, Chr03, Chr04, Chr05, Chr06, Chr07, and Chr09 (Figure 2). Specifically, StAMY1 was mapped to Chr02; StAMY2 and StAMY3 were mapped to Chr03; StAMY4, StAMY5, StAMY6, StAMY7, StAMY8, and StAMY9 were mapped to Chr04 (which contained the greatest number of StAMY genes); StAMY10 was mapped to Chr05; StAMY11, StAMY12, and StAMY13 were mapped to Chr06; StAMY14, StAMY15, StAMY16, and StAMY17 were mapped to Chr07; and StAMY18, StAMY19, and StAMY20 were mapped to Chr09.

3.3. Gene Structures and Conserved Motifs of StAMY Genes

Exon–intron analysis can help researchers to understand the structural evolution of gene families. Here, we studied the exon–intron structures of StAMY genes using both genomic and coding DNA sequences. Overall, the number, length, and distribution of exons and introns differed among genes. StAMY2, StAMY3, StAMY5, StAMY6, StAMY7, StAMY8, StAMY9, StAMY11, StAMY12, StAMY13, StAMY14, StAMY15, StAMY16, StAMY17, StAMY18, and StAMY19 exhibited similar sequence lengths but different numbers of exons.
In addition, StAMY family protein architecture was investigated using amino acid sequences. According to MEME motif analysis, the common motifs tended to cluster into the same groups, and many of the motifs were clade- and group-specific (Figure 3). Group I (StAMY1, StAMY2, StAMY3, StAMY4, StAMY5, StAMY6, StAMY7, and StAMY10) contained seven of the same motifs, including motifs 1, 2, 3, 4, 5, 8 and 9. Group II (StAMY11, StAMY12, StAMY13, StAMY14, StAMY15, and StAMY20) contained motifs 2, 3, 5, 6, 7, and 8. Group III (StAMY8, StAMY9, StAMY16, StAMY17, StAMY18, and StAMY19) contained motifs 2, 3, and 5.

3.4. Promoter cis-Acting Elements of StAMY Genes

Analyzing cis-acting elements present in the promoters of genes can help researchers to understand both gene function and regulation. A total of 13 cis-acting elements were identified across StAMY gene family promoters, including those associated with plant growth and development, phytohormone signaling, defense, and stress response. Specifically, the promoters of StAMY genes were found to contain 70 phytohormone-responsive cis-elements (including those responsive to ABA, methyl jasmonate [MeJA], salicylic acid [SA], auxin [Aux], and GA3), 44 light-responsive cis-elements, 3 low-temperature-responsive cis-elements, 6 drought-responsive MYB binding sites, 4 defense- and stress-responsive cis-elements, 8 circadian control cis-elements, 3 zein metabolism-regulating cis-elements, and 3 meristem-specific cis-elements. The most common elements were those related to the response to light and MeJA (Figure 4).

3.5. Tissue-Specific Expression Profiles of StAMY Genes

To study the tissue-specific expression of StAMY genes, we analyzed publicly available RNA-seq data obtained from the Spud Database (https://spuddb.uga.edu/, accessed on 22 April 2024). In general, the various StAMY genes exhibited tissue-specific expression (Figure 5). Specifically, StAMY8, StAMY9, StAMY12, StAMY15, and StAMY20 were highly expressed in mature tubers; StAMY2, StAMY7, and StAMY13 were highly expressed in stems; StAMY6 and StAMY11 were highly expressed in roots; StAMY16 and StAMY17 were highly expressed in stolons; StAMY10 was highly expressed only in flowers; StAMY5 and StAMY18 were highly expressed in young tubers; and StAMY4, StAMY18, and StAMY19 were highly expressed in leaves. Notably, StAMY3 was not found to be expressed in any of the tested tissues.

3.6. Changes in StAMY Gene Expression in Response to Biotic and Abiotic Stress

Changes in StAMY gene expression were evaluated in whole plants or leaves exposed to BABA, BTH, P. infestans, heat, salt, and mannitol (Figure 6). StAMY10 exhibited upregulated expression in response to BABA treatment, whereas StAMY1, StAMY3, StAMY7, StAMY8, StAMY9, StAMY12, StAMY14, StAMY17, StAMY18, StAMY19, and StAMY20 were downregulated. StAMY11 and StAMY16 exhibited upregulated expression in response to P. infestans infection, whereas the expression of StAMY4 was downregulated. StAMY2, StAMY5, StAMY6, and StAMY15 exhibited upregulated expression in response to BTH treatment. StAMY3, StAMY4, StAMY8, and StAMY12 exhibited upregulated expression in response to heat treatment, whereas StAMY1, StAMY2, StAMY10, StAMY18, and StAMY20 were downregulated. StAMY6, StAMY14, StAMY16, and StAMY19 exhibited upregulated expression in response to salt treatment. StAMY5, StAMY11, and StAMY15 exhibited upregulated expression in response to mannitol treatment, whereas StAMY6, StAMY7, StAMY9, StAMY14, and StAMY19 were downregulated.

3.7. Changes in StAMY Gene Expression in Response to Phytohormones

Changes in StAMY gene expression were evaluated in whole plants exposed to BAP, ABA, IAA, and GA3 (Figure 7). StAMY7 exhibited upregulated expression in response to BAP treatment, whereas StAMY1, StAMY4, StAMY6, StAMY10, StAMY12, StAMY14, StAMY16, and StAMY19 were downregulated. StAMY5, StAMY9, StAMY15, and StAMY20 exhibited upregulated expression in response to ABA treatment, whereas the expression of StAMY17 was downregulated. StAMY3 and StAMY17 exhibited upregulated expression in response to IAA treatment, whereas StAMY2 and StAMY11 were downregulated. StAMY18 exhibited upregulated expression in response to GA3 treatment.

4. Discussion

In order to minimize processing losses caused by cold-induced sweetening during the low-temperature storage of potato tubers, preventing the conversion of starch into reducing sugars plays a crucial role in improving the processing quality of potato chips [43]. Since α-amylase (AMY) is the primary starch-degrading enzyme in potato, it is critically important to identify, functionally characterize, and study its role in potato tuber quality. In this study, we used whole-genome sequencing data to identify members of the StAMY gene family. In addition, we evaluated their structures and functions, providing a theoretical basis for further research on the role of the AMY gene family in potato growth and development.
Previous studies have found that many plants, including barley, quinoa, apple, and others, contain multigene AMY families [44,45,46]. Here, we identified 20 AMY genes in the potato genome, which were unevenly distributed on the seven potato chromosomes (Figure 2). In addition, the StAMY proteins exhibited varied conserved motif compositions, likely due to functional differentiation of the StAMY family during evolution. Alternative splicing can result in a polymorphic protein structure, as well as functional and transcriptional differentiation [47]. High sequence similarity and close evolutionary relationships were observed between StAMY2 and StAMY3, StAMY5, StAMY6, and StAMY7; StAMY8 and StAMY9, StAMY11, StAMY12, and StAMY13; and StAMY14 and StAMY15, StAMY18, and StAMY19. However, gene structure analysis indicated that many of these genes exhibited differences in intron–exon structure, resulting in different functions and expression patterns (Figure 3). The phylogenetic tree revealed that the protein structures of the three branches were relatively similar between A. thaliana and potato, suggesting that members of each branch may have originated from a common ancestor (Figure 1).
Analysis of promoter cis-elements can help determine the function of specific genes. Here, we identified a number of defense-, stress-, and phytohormone-responsive cis-elements in the promoters of StAMY genes (Figure 4), suggesting that these genes may be involved in the plant response to stress, as well as hormonal and developmental signaling. We investigated the expression profiles of 20 StAMY genes under biotic and abiotic stress using DM data obtained from the Spud Database (http://spuddb.uga.edu/, accessed on 22 April 2024). Notably, StAMY3, StAMY4, StAMY8, and StAMY12 exhibited upregulation in response to heat stress, suggesting that these genes play a positive role in the heat stress response. StAMY6, StAMY14, StAMY16, StAMY17, StAMY19, and StAMY20 exhibited upregulated expression in response to salt stress, suggesting that these genes similarly play a positive role in the salt stress response. In addition, StAMY5, StAMY11 and StAMY15 were significantly upregulated in response to mannitol treatment, suggesting that these genes play an active role in the drought stress response.
BTH is a synthetic chemical analog of SA and is a potent inducer of plant defenses. BTH has been used to induce protection against diseases in various crops, including potato, tomato, rice, and wheat [48]. We found that StAMY2, StAMY5, StAMY6, and StAMY15 exhibited significantly upregulated expression in response to BTH treatment. BABA is a phytochemical inducer which can induce plant defense responses to an array of biotic and abiotic stressors [49]. We found StAMY10 exhibited significant upregulation in response to BABA, whereas StAMY1, StAMY3, StAMY7, StAMY8, StAMY9, StAMY12, StAMY14, StAMY17, StAMY18, StAMY19, and StAMY20 were downregulated. These results suggest that these genes may play a role in plant defense and stress resistance. P. infestans is one of the most serious pathogens of potatoes, tomatoes, and other solanaceous crops [50,51]. We observed that StAMY11 and StAMY16 exhibited upregulated expression in response to P. infestans infection, indicating that these genes are likely involved in the pathogen defense response.
Phytohormones regulate plant adaptation and defense through a series of signal transduction processes [52]. To investigate the effect of phytohormone signaling on StAMY gene expression, StAMY gene expression was examined in ABA-, IAA-, GA3-, and BAP-treated potato plants. Among these, GA3 and ABA are the most relevant to tuber formation, with GA3 inhibiting and ABA promoting tuber formation [53]. We found that the expression of StAMY5, StAMY9, StAMY11, StAMY15, and StAMY20 was upregulated in response to ABA treatment. In addition, GA3 treatment upregulated the expression of StAMY6, StAMY8, StAMY16, and StAMY18. The promoters of StAMY genes were found to contain a variety of phytohormone-responsive cis-acting elements, including those responsive to GA3 and ABA. The expression of StAMY3 and StAMY17 was upregulated in response to IAA treatment. Notably, StAMY17 was found to be highly expressed in stolons, suggesting that this gene may promote potato tuber growth. However, this hypothesis requires experimental verification. BAP was the first synthetic cytokinin [54]. We observed that the expression of StAMY7 was upregulated in response to BAP treatment, whereas StAMY1, StAMY4, StAMY6, StAMY10, StAMY12, StAMY14, StAMY16, and StAMY19 were downregulated. Taken together, these results suggest that many of the StAMY genes are likely involved in the phytohormone-mediated growth and development of potatoes.
In summary, we identified 20 StAMY genes and analyzed their phylogenetic relationships, gene structures, functional motifs, and expression patterns. StAMY8, StAMY9, StAMY12, and StAMY20 were specifically expressed in mature tubers, suggesting that they may be involved in starch and sugar metabolism. Different StAMY gene family members were significantly upregulated or downregulated in response to a variety of stressors and exogenous phytohormones. Additional studies should be conducted to further investigate the roles of StAMY genes in the regulation of starch metabolism, growth, and development.

Author Contributions

Y.D., methodology, software, writing—original draft. L.J., supervision and funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the Strategic Collaboration Project of the Chongqing Municipal People’s Government and Chinese Academy of Agricultural Sciences.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

α-amylaseAMY; β-aminobutyric acid, BABA; benzothiadiazole, BTH; Phytophthora infestans, P. infestans; abscisic acid, ABA; indole-3-acetic acid, IAA; gibberellic acid, GA3; 6-benzylaminopurine, BAP.

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Genes 15 00793 g001
Figure 1. Phylogenetic tree of AMY protein sequences from A. thaliana (AtAMY) and S. tuberosum (StAMY).
Figure 1. Phylogenetic tree of AMY protein sequences from A. thaliana (AtAMY) and S. tuberosum (StAMY).
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Genes 15 00793 g002
Figure 2. Chromosome location mapping of StAMY gene family in potato.
Figure 2. Chromosome location mapping of StAMY gene family in potato.
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Figure 3. Analysis of gene structures and motifs of StAMY gene family members in potato. CDS, coding sequences. UTR, untranslated region.
Figure 3. Analysis of gene structures and motifs of StAMY gene family members in potato. CDS, coding sequences. UTR, untranslated region.
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Figure 4. Analysis of cis-acting elements in the promoters of StAMY genes in potato.
Figure 4. Analysis of cis-acting elements in the promoters of StAMY genes in potato.
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Figure 5. Tissue-specific expression patterns of StAMY genes.
Figure 5. Tissue-specific expression patterns of StAMY genes.
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Figure 6. Changes in the expression patterns of StAMY genes in response to biotic and abiotic stress.
Figure 6. Changes in the expression patterns of StAMY genes in response to biotic and abiotic stress.
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Figure 7. Changes in the expression patterns of StAMY genes in response to 6-benzylaminopurine (BAP), abscisic acid (ABA), indole-3-acetic acid (IAA), and gibberellic acid (GA3).
Figure 7. Changes in the expression patterns of StAMY genes in response to 6-benzylaminopurine (BAP), abscisic acid (ABA), indole-3-acetic acid (IAA), and gibberellic acid (GA3).
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Table 1. Molecular characteristics of identified StAMY genes in potato.
Table 1. Molecular characteristics of identified StAMY genes in potato.
Gene IDCDS Length (bp)Start–End PositionsProtein Length
(aa)		Molecular Weight
(Da)		Isoelectric Point
(PI)		Subcellular Localization
StAMY1296424230843-24247840987112,118.255.77cytosol
StAMY2132635837209-3584038644149,246.75.43vacuole
StAMY3112235837209-3584038637341,687.075.17cytosol
StAMY4122465328724-6533089440745,723.435.83chloroplast
StAMY5122468257647-6826257140746,346.116.74cytosol
StAMY6122468257647-6826257140746,346.116.74cytosol
StAMY7118868257647-6826257139544,870.426.67cytosol
StAMY8254768516172-6850849784896,766.734.9nucleus
StAMY9274568516457-68508497914104,165.095.09chloroplast
StAMY1039996053915-60372461332150,181.536.05mitochondrion
StAMY111185715327-70027339445,248.836.27peroxisome
StAMY121350715327-70027344951,028.056.1peroxisome
StAMY131143715327-70027338043,513.86.27peroxisome
StAMY1423827370232-735446979389,389.695.54nucleus
StAMY1518667370232-735446962170,484.135.19nucleus
StAMY16194755405743-5538629264873,772.356.89chloroplast
StAMY17270955936361-55953226902103,776.356.4cytosol
StAMY1826313555467-3535898876100,067.775.02chloroplast
StAMY1923163555467-353589877188,867.574.94cytosol
StAMY20263753271759-5326793787897,998.16.8chloroplast
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Duan, Y.; Jin, L. Genome-Wide Identification and Expression Profiling of the α-Amylase (AMY) Gene Family in Potato. Genes 2024, 15, 793. https://doi.org/10.3390/genes15060793

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Duan Y, Jin L. Genome-Wide Identification and Expression Profiling of the α-Amylase (AMY) Gene Family in Potato. Genes. 2024; 15(6):793. https://doi.org/10.3390/genes15060793

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Duan, Yudan, and Liping Jin. 2024. "Genome-Wide Identification and Expression Profiling of the α-Amylase (AMY) Gene Family in Potato" Genes 15, no. 6: 793. https://doi.org/10.3390/genes15060793

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