Role of sweet potato GST genes in abiotic stress tolerance revealed by genomic and transcriptomic analysesAbstract
Glutathione S-transferases (GSTs) are proteins synthesized in plants and responsible for their tolerance to environmental stresses. However, little information is available on the GST gene family of sweet potato, a globally important crop. The genetic evolution of GSTs in sweet potato remains unclear. The present study investigated the GST gene family in sweet potato by transcriptomic and comparative genomic analyses. A total of 51 GSTs were identified. Gene expression analysis showed differential expression patterns of the GSTs between two investigated varieties. Some GST expression levels were either up- or downregulated under oxidative, salinity and drought stresses. The results of the investigation provided new insights on the GST gene family in sweet potato, which may further the understanding of the roles of these genes in regulating abiotic stresses.
Keywords: Gene expression; drought; salinity; oxidative stress; sweet potato
INTRODUCTION
Glutathione S-transferases (GSTs) represent a group of proteins found in various plant species. They mainly function as cytotoxic compounds helping to reduce damages caused by environmental stresses (Estévez and Hernández 2020). Moreover, GST genes can act as carriers of secondary metabolites such as anthocyanins and flavonoids, transporting them to vacuoles for sequestration (Wei et al. 2019). Previously, the GST gene family has been investigated in the genome of different plants and 85, 49, and 52 copies, respectively, were observed in Capsicum annuum (Islam et al. 2019), melon (Wang et al. 2020) and apple (Fang et al. 2020). Glutathione S-transferases could be found in three different subcellular localizations including microsomes, mitochondria and the cytoplasm in which they are most prominent (Hu et al. 2018). The GST gene family can be grouped into eight subfamilies, namely: eukaryotic translation elongation factor 1 gamma (EF1Bγ), Tau (U), Zeta (Z), dehydroascorbate reductase (DHAR), Lambda (L), tetrachlorohydroquinone dehalogenase (TCHQD), Phi (F) and Theta (T) (Liu et al. 2019). Tau and Phi are the most important subfamilies, which are involved in the transport of various secondary metabolites and cell detoxification. The upregulation of these subfamilies reportedly increased plant tolerance to various stresses (He et al. 2016). For example, TaGSTF62 improved the tolerance of wheat to salinity stress (), whereas CmaGSTU14 was shown to enhance cold stress tolerance in pumpkin (Kayum et al. 2018). Other studies also demonstrated the involvement of IbGSTF4 and FaGST73 in anthocyanin accumulation in Arabidopsis (Kou et al. 2019) and strawberry (Lin et al. 2020), respectively.
Sweet potato (Ipomoea batatas), a globally important crop, is affected by various environmental constraints, particularly in a number of developing countries (Zhang et al. 2020). To date, the GST gene family of this crop has not been extensively investigated. However, a recent study based on transcriptomic analysis identified 42 GST genes in sweet potato, which were classified into eight different subfamilies and exhibited varying expression patterns across different varieties and tissues in response to oxidative and metal stresses (Ding et al. 2017). Nevertheless, the genetic evolution of GST genes in sweet potato and their functions under abiotic stress remain unclear. Therefore, a more in-depth analysis of the genome of this crop would be important to better understand the characteristics and transcript accumulation of sweet potato GST genes in stressful environments. In the current study, the GST gene family in the sweet potato genome was investigated using not only transcriptomic technology but also comparative genomic analyses. With a view to providing new insights on GST genes of sweet potato, a number of differentially expressed transcripts were identified and the expression level of 10 GST genes under salinity, drought and oxidative stress conditions determined by RT-qPCR.
MATERIAL AND METHODS
Identification of GST genes in sweet potato
The Arabidopsis thaliana GST protein data were retrieved from the Arabidopsis Information Resource (TAIR release 10 http://www.arabidopsis.org) and used as query to perform a BLASTp search against the Ipomoea triloba genome database NSP323.v3 (http://sweetpotato.uga.edu/), at a cut-off value of ≤e-20. The NCBI-CDD and Pfam databases (El-Gebali et al. 2019) were further employed to examine the presence of conserved domains in the identified candidate proteins, and 55 proteins containing GST domains were obtained. In order to confirm the expression of these 55 GSTs in I. batatas, the genes were compared to those in the transcriptome database, which was constructed based on Illumina High-Seq 2500 sequencing technology (Illumina, Inc.; San Diego, CA, US). The transcriptomic analysis material consisted of leaves of two sweet potato varieties, namely Fushu 7-6 (FS7-6) and EC16 collected from 65- and 85-day-old plants (NCBI SRA, accession number PRJNA592001) (Liu et al. 2021). In the two varieties, 51 GSTs were found. The four not expressed mRNA were manually removed and the remaining 51 were finally confirmed as members of the GST gene family in I. batatas. The FPKM (fragments per kilobase of exon model per million reads mapped) values of these genes were used to generate a heatmap showing the average relative expression of these genes using R packages (https://bioconductor.org/packages/release/bioc/html/ComplexHeatmap.html). The ExPASy Prot-Param tool (https://web.expasy.org/protparam/) was used to determine the molecular weight (Mw), isoelectric points (pI) and polypeptide length of the genes. The tool CELLO v2.5 (http://cello.life.nctu.edu.tw/) served for subcellular localization prediction.
Sequence analysis of sweet potato GST genes
Based on comparison with Arabidopsis GST proteins, the identified sweet potato GSTs were subgrouped with ClustalX2 (Larkin et al. 2007). The Neighbor-Joining method of MEGA7 (Kumar et al. 2016) was used to generate the phylogenetic tree. The online program GSDS (http://gsds.cbi.pku.edu.cn) analyzed the structure of introns and exons of the GST genes, while MEME (http://memesuite.org/index.html) served as motif identification tool. The promoter regions in the GST genes were identified by the database PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html).
Plant material and abiotic stress treatments
The sweet potato varieties FS7-6 and EC16 were used in this study. To identify the GST genes involved in abiotic stress tolerance, the transcript abundance of these genes in the transcriptome database was analyzed. Among the known 51 GSTs, 10 gene transcription levels were relatively high in both varieties and developmental stages. The expression levels of these 10 GST genes were analyzed using real-time PCR under optimum and stressed conditions. Young sweet potato plants were grown in Hoagland hydroponic solution (1%) in a growth chamber at 26±2 ºC under 16 h light/ 8 h dark. Seven days after acclimatization, the plants were treated with 200 mM NaCl, 30% PEG6000 solution and 5% H2O2 for salinity, drought and oxidative stresses, respectively, while unstressed plants grown in 1% Hoagland solution served as control. The test consisted of three replicates. Leaves were collected at 0, 6, 12 and 24 h after stress induction.
Quantitative real-time PCR analysis
Leaf samples of FS7-6 and EC16 were collected and ground in liquid nitrogen. A TransZol Up Kit was used for total RNA extraction and DNase treatment. A TransScript® All-in-One First-Strand cDNA Synthesis SuperMix for PCR served as cDNA synthesis kit and TransStart® Tip Green qPCR SuperMix was used for qRT-PCR analysis. All these kits were purchased from TransGen Biotech (China). The normalized values of the GST gene expression level were assessed using the internal control β-actin gene. The qRT-PCR thermal cycling profile consisted of: 94 °C for 30s, 40 cycles of 94 °C for 5s, 56 °C for 15s and 72 °C for 10s. The experiment was run in independent biological triplicates and the relative expression was calculated by the 2-ΔΔCT method (Livak and Schmittgen 2001). The primer sequences of the selected genes are listed in Additional file 1: Table S1.
RESULTS AND DISCUSSION
Characterization and sequence analysis of GST genes
In a BLASTp search against the I. triloba genome database, 55 putative genes containing conserved GST domains were obtained. These genes were compared with those of the transcriptome database to confirm their expression in I. batatas. Fifty-one GSTs were found in both varieties and finally confirmed as GST members in I. batatas. Among these proteins, itb11g03260 was the largest with 389 amino acids (aa) and itb12g06130 the smallest (110 aa). The isoelectric point (pI) of the GSTs varied widely, from 4.85 (itb06g23080) to 9.19 (itb12g06130) and the molecular weight (MW) from 12.91 to 43.69 kilodalton (kDa). Moreover, 44 GSTs were localized in the cytoplasm, one in the outer membrane and the remaining six in the periplasmic region (Table 1). Previously, a study identified 42 IbGST members and classified them into eight subfamilies in sweet potato (Ding et al. 2017). No similarity was observed between the genes identified in the two studies, except for IbGSTU12 in the previous paper, named itb01g20610 in this study. The sequences of the reported motifs were also different. These results could be explained by the fact that our study was based on the I. triloba GST genes present in the varieties FS7-6 and EC16, while Ding et al. (2017) characterized the GSTs specific to I. batatas. Phylogenetic analysis allocated the 51 GST members to five different subfamilies: Tau, Lambda, Theta, TCHQD and EF1Bγ, according to their similarity to the Arabidopsis GST proteins (Figure 1). However, no GST genes were assigned to the Phi and Zeta classes. A possible explanation is that each GST subfamily followed distinct evolutionary paths and the number of subfamilies varied greatly among plants. The Tau class was the largest, with 40 members. Three proteins were assigned to the Theta, four to the Lambda, two to the TCHQD and two to the EF1Bγ subfamily. The sequence information of sweet potato and Arabidopsis GST proteins is listed in Additional file 2: Table S2 and Additional file 2: Table S3, respectively. Usually, the subfamilies Phi and Tau are the most represented in many plant species, however, in our study Tau (40 GST members) and Lambda (4 GST members) were the most dominant, probably because of the absence of Phi subfamily members in the identified GST genes. This is consistent with Islam et al., who discovered that Tau (57 GST members) and Lambda (7 GST members) were the most prominent GST subfamilies in the tomato genome (Islam et al. 2017). Moreover, the subfamilies EF1Bγ and TCHQD were less represented in the analyzed sweet potato varieties, suggesting few duplication events of these genes during speciation or that duplicated copies were lost during evolution (Abou-Elwafa et al. 2011).
tree representing relationships among sweet potato and Arabidopsis GSTs. The colors indicate distinct subfamilies of the GST gene family. GST proteins in Arabidopsis with the prefix ‘At’ indicate ‘AtGST’. MEGA 7, Neighbor-Joining method and 1000 replicates for the bootstrap test were used to generate the tree. Percentage bootstrap scores of >50% were displayed.
Sequence composition of sweet potato GST genes
The phylogenetic classification of the 51 identified GST genes matched the classification of motifs, domains and structures of these genes (Figure 2A). Online software MEME identified 10 different motifs for all GST genes. These motifs were almost identical within each subfamily, but different among subfamilies (Figure 2B). Motif 3 was the most widely represented in the GSTs. Moreover, motifs 7 and 8 are present in the Lambda, while motif 9 is unique in the Theta subfamily. Motif 4 belongs to Tau and TCHQD, while other motifs (1, 2, 5, 6 and 10) were present in the Tau subfamily. Sequence information for each motif is provided in Additional file 3: Table S4. The GST domains were highly conserved in each subfamily (Figure 2C). Within the subfamilies, they shared a similar structure, although the domains were different among subfamilies. For instance, most members of subfamily Tau comprise GST_C_Tau and GST_N_Tau, except itb15g08160, itb12g06130 and itb08g15850, and most members of subfamily Theta comprise GST_C_Theta and GST_N_Theta, except itb13g03940. In general, the analysis of conserved domains showed 37 GST genes with a highly conserved N-terminal domain. It has been reported that the residue in N-terminal domain regulates the catalytic function of GST genes (Nishida et al. 1998). The gene structure analysis revealed great variation among the genes (Figure 2D). Most GST genes in subfamily Tau contained two exons. The Theta and TCHQD GSTs have seven and six exons, respectively, while the Lambda and EF1Bγ contain approximately 10. Moreover, variations in intron numbers among subfamilies were observed, whereas their positions within subfamilies were conserved.
analysis of sweet potato GST genes. (A) Phylogenetic tree generated using MEGA 7 software, (B) motif pattern of GST genes, (C) conserved domain, (D) GST gene structure. The GST proteins in the four plots (A, B, C, D) are in the same order.
Expression profiling of sweet potato GST genes
To explore the role of the GST genes, the expression of all 51 members was analyzed based on RNA-sequencing data derived from the varieties EC16 and FS7-6, sampled at two developmental stages (from 65- and 85-day-old plants). The 51 GSTs had different expression patterns for the varieties and developmental stages (Figure 3A). Among them, 29 GST genes exhibited constitutive expression (FPKM>1), whereas 22 were expressed with a FPKM value >0 in all analyzed samples. Some GSTs were highly expressed in all samples, while the expression levels of others were extremely low. For example, transcript abundance was highest in itb15g08190 and itb14g03990, and lowest in all analyzed samples of itb01g20560 and itb15g08120. The expression levels of itb15g08190 and itb14g03990 genes were higher in variety EC16 than FS7-6. Moreover, the expression levels of itb13g03940 and itb11g03220 were higher at the sampling of the first developmental stage compared to the second. It can be speculated that the expression of the GST genes is influenced by the genetic constitution and developmental stages of each sweet potato variety.
analysis of the 51 GSTs. Longitudinal direction indicates the varieties EC16 and FS7-6 and developmental stages S1 (stage 1: 65 days) and S2 (stage 2: 85 days). Horizontal direction indicates the 51 sweet potato GST genes. High expression levels are shown in red and low levels in blue (A). GST gene expression levels of sweet potato varieties Lizixiang (L) and ND98 (N) in response to salinity stress. Treatment at 0, 12 and 48 h. L0; Lizixiang at 0 h, L12; Lizixiang at 12 h, L48; Lizixiang at 48 h, N0; ND98 at 0 h, N12; ND98 at 12 h and N48; ND98 at 48 h. The colors represent the gene transcript levels (FPKM value) (B).
Transcript accumulation of sweet potato GST genes under abiotic stress
To determine the functions of GSTs under abiotic stress, transcriptome profiling data of all GST genes from two other sweet potato varieties (Lizixiang and ND98) were retrieved from the NCBI SRA database (accession number SRP092215) (Zhang et al. 2017). These varieties were chosen because no GST transcript levels of EC16 and FS7-6 under abiotic stress conditions were available. Transcriptomic data of 0, 12 and 48 hours after salt stress treatment were extracted from the database. The expression levels of most GSTs were low in Lizixiang and ND98, except for itb12g10540 and itb01g20600, which were upregulated at 12 and 48 h after salinity treatment in both varieties. Some other genes, such as itb15g08200, itb15g08210, itb13g02460, itb14g03990 and itb15g08150, were also found to be downregulated, indicating the non-responsiveness to high salinity conditions of these GSTs in Lizixiang and ND98 (Figure 3B).
To further confirm the abiotic stress-responsiveness of GST genes in the varieties EC16 and FS7-6, the 10 most highly expressed genes in both varieties and developmental stages, i.e., itb01g15260, itb09g30700, itb11g02640, itb11g03220, itb11g07110, itb11g07120, itb13g03940, itb14g03990, itb14g04110 and itb15g08190, were selected from the 51 GST genes (Figure 4A). RT-qPCR experiments were then performed to identify the transcript accumulation of these genes in plants under drought (30% PEG6000), salinity (200 mM NaCl) and oxidative (5% H2O2) stresses. Samples in each treatment were collected at 0, 6, 12 and 24 h after stress induction. The GST genes were significantly up- and downregulated by the induced abiotic stresses. Under salinity, itb11g07110 was significantly upregulated in both varieties throughout the stress period, compared to the control. In addition, itb01g15260, itb09g30700, itb11g02640, itb11g03220, itb11g07120 and itb13g03940 were upregulated only at 6h after treatment, especially in variety FS7-6. The other genes, namely itb14g03990, itb14g04110 and itb15g08190, were mostly downregulated (Figure 4B). Under drought, apart from itb11g07110 and itb13g03940, which were upregulated, the expression of itb11g07120 was remarkable at 24h in variety EC16 (Figure 4C). Under oxidative stress, itb11g07110, itb11g02640 and itb13g03940 were the most responsive genes, whereas itb09g30700 and itb11g07120 were significantly upregulated only at 6h in FS7-6 (Figure 4D). Overall, itb11g07110 responded positively to drought, salt and oxidative stresses, with a significantly higher expression level in FS7-6 compared to EC16. Moreover, the gene itb11g02640 was induced under oxidative stress in both varieties, while itb13g03940 was significantly expressed under drought and oxidative stress. In contrast, itb14g03990, itb14g04110 and itb15g08190 were downregulated in all treatments, indicating that these genes were insensitive to the tested stresses. The differences in stress-regulatory units present in the GST promoter could be the cause of variations observed in the expression pattern of these genes. Additionally, itb15g08190 and itb14g03990, with the highest transcript abundance under unstressed conditions (Figure 3A), were significantly downregulated in all stress treatments. This confirms the non-responsiveness of the genes to abiotic stresses. Various studies have demonstrated the downregulation of GST genes under environmental stress (Islam et al. 2019, Wang et al. 2019). The GSTs of Lizixiang and ND98 were mostly downregulated under salt stress (Figure 3B), even the itb11g07110 gene, which was highly expressed in EC16 and FS7-6 under the same stress condition. The ability of each variety to resist and thrive in a specific growing environment and certain developmental stages could influence the expression of genes responsible for defense against environmental stresses. In numerous studies, GST genes improved tolerance to abiotic factors. For example, VvGSTF13 of grape increased Arabidopsis plant tolerance to drought and salinity stresses (Xu et al. 2018). Likewise, GmGSTU63 enhanced drought tolerance in soybean (Hasan et al. 2020). These studies revealed the significant roles of GST proteins in modulating plant stress pathways. Further investigations may improve our understanding about roles and functions of GST genes in regulating the response of sweet potato to various abiotic stresses.
level of the GSTs. itb01g15260, itb09g30700, itb11g02640, itb11g03220, itb11g07110, itb11g07120, itb13g03940, itb14g03990, itb14g04110 and itb15g08190 had the highest expression levels in the varieties EC16 and FS7-6 and two developmental stages (65- and 85-day-old plants) (A). Expression analysis of GSTs under salinity (B), drought (C) and oxidative (D) stresses. Samples of each treatment were collected at 0, 6, 12 and 24 h after stress induction. Data were normalized to the β-actin gene. * and ** indicate significant differences compared to 0 h at P < 0.05 and P < 0.01 (t-test), respectively.
CONCLUSION
In this study, 51 GST genes were identified. The full-length genomic sequences of these 51 GSTs were characterized and allocated to five distinct subfamilies, based on their similarity with Arabidopsis GSTs. Different conserved motifs and domains were observed in the sweet potato GST genes. The up- and downregulation of the GSTs differed between the two analyzed varieties and abiotic stress treatments. Three genes were upregulated in a stress -specific manner; itb11g07110 was upregulated in all treatments, itb11g02640 was highly expressed under oxidative stress, while itb13g03940 was induced in both drought and oxidative stress. This study provides new perspectives on the GST gene family in terms of its role in regulating abiotic stresses in sweet potato.
ACKNOWLEDGMENTS
This research project was supported by the National Key R&D Program of China (2018YFD1000700, 2018YFD1000705, 2019YFD1001300, 2019YFD1001305), Science and Technology Development Plan Project of Jingzhou City, Hubei Province, China (2018-37), Characteristic Discipline of Hubei Academy of Agricultural Sciences (2015TSXK06) and Science and Technology Innovation Center of Hubei Academy of Agricultural Sciences (2007-620-001-03). Additional Tables S1, S2, S3, S4 and Software and parameters used for RNA-seq data analysis can be required to the main author by e-mail (wyzhang@yangtzeu.edu.cn).
REFERENCES
- Abou-Elwafa SF, Büttner B, Chia T, Schulze-Buxloh G, Hohmann U, Mutasa-Göttgens E, Jung C and Müller AE2011 Conservation and divergence of autonomous pathway genes in the flowering regulatory network of Beta vulgaris. Journal of Experimental Botany 62:3359-3374
- DingNWangAZhangXWuYWangRCuiHHuangRLuoY2017 Identification and analysis of glutathione S-transferase gene family in sweet potato reveal divergent GST-mediated networks in aboveground and underground tissues in response to abiotic stresses. BMC Plant Biology 17:225
- El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA and Smart A2019 The Pfam protein families database in 2019. Nucleic Acids Research 47: D427-D432.
- EstévezIHHernándezMR2020 Plant glutathione S-transferases: An overview. Plant Gene 23:100233
- FangXAnYZhengJShangguanLWangL2020 Genome-wide identification and comparative analysis of GST gene family in apple (Malus domestica) and their expressions under ALA treatment. 3 Biotech 10:1-16
- HasanMSIslamSHasanMNSajibSDAhmedSIslamTGhoshA2020 Genome-wide analysis and transcript profiling identify several abiotic and biotic stress-responsive Glutathione S-transferase genes in soybean. Plant Gene 23:100239
- HeGGuanCNChenQXGouXJLiuWZengQYLanT2016 Genome-wide analysis of the Glutathione S-transferase gene family in Capsella rubella: Identification, expression, and biochemical functions. Frontiers in Plant Science 7:1325
- HuFYeKTuX-FLuY-JThakurKJiangLWeiZ-J2018 Identification and expression profiles of twenty-six glutathione S-transferase genes from rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae). International journal of biological macromolecules 120:1063-1071
- IslamSRahmanIAIslamTGhoshA2017 Genome-wide identification and expression analysis of glutathione S-transferase gene family in tomato: gaining an insight to their physiological and stress-specific roles. PLoS One 12:e0187504
- IslamSSajibSDJuiZSArabiaSIslamTGhoshA2019 Genome-wide identification of glutathione S-transferase gene family in pepper, its classification, and expression profiling under different anatomical and environmental conditions. Scientific Reports 9:9101
- KayumANathUKParkJ-IBiswasMKChoiEKSongJ-YKimH-TNouI-S2018 Genome-wide identification, characterization, and expression profiling of glutathione S-transferase (GST) family in pumpkin reveals likely role in cold-stress tolerance. Genes 9:84
- KouMLiuY-jLiZ-yZhangY-gTangWYanHWangXChenX-gSuZ-xArishaMH2019 A novel glutathione S-transferase gene from sweetpotato, IbGSTF4, is involved in anthocyanin sequestration. Plant Physiology and Biochemistry 135:395-403
- KumarSStecherGTamuraK2016 MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870-1874
- LarkinMABlackshieldsGBrownNPChennaRMcGettiganPAMcWilliamHValentinFWallaceIMWilmALopezR2007 Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948
- LinYZhangLZhangJZhangYWangYChenQLuoYZhangYLiMWangX2020 Identification of Anthocyanins-related Glutathione S-transferase (GST) genes in the genome of cultivated strawberry (Fragaria× ananassa). International Journal of Molecular Sciences 21:8708
- LiuYJiangHZhaoYLiXDaiXZhuangJZhuMJiangXWangPGaoL2019 Three Camellia sinensis glutathione S-transferases are involved in the storage of anthocyanins, flavonols, and proanthocyanidins. Planta 250:1163-1175
- LiuYSuWWangLLeiJChaiSZhangWYangX2021 Integrated transcriptome, small RNA and degradome sequencing approaches proffer insights into chlorogenic acid biosynthesis in leafy sweet potato. PLoS One 16:e0245266
- LivakKJSchmittgenTD2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 25:402-408
- NishidaMHaradaSNoguchiSSatowYInoueHTakahashiK1998 Three-dimensional structure of Escherichia coli glutathione S-transferase complexed with glutathione sulfonate: catalytic roles of Cys10 and His106. Journal of Molecular Biology 281:135-147
- WangJZhangZWuJHanXWang-PruskiGZhangZ2020 Genome-wide identification, characterization, and expression analysis related to autotoxicity of the GST gene family in Cucumis melo L. Plant Physiology and Biochemistry 155:59-69
- WangRMaJZhangQWuCZhaoHWuYYangGHeG2019 Genome-wide identification and expression profiling of glutathione transferase gene family under multiple stresses and hormone treatments in wheat (Triticum aestivum L.). BMC genomics 20:1-15
- WeiLZhuYLiuRZhangAZhuMXuWLinALuKLiJ2019 Genome wide identification and comparative analysis of glutathione transferases (GST) family genes in Brassica napus. Scientific Reports 9:9196
- XuJZhengA-QXingX-JChenLFuX-YPengR-HTianY-SYaoQ-H2018 Transgenic Arabidopsis plants expressing grape glutathione S-Transferase gene (VvGSTF13) show enhanced tolerance to abiotic stress. Biochemistry (Moscow) 83:755-765
- ZhangHZhangQZhaiHLiYWangXLiuQHeS2017 Transcript profile analysis reveals important roles of jasmonic acid signalling pathway in the response of sweet potato to salt stress. Scientific Reports 7:1-12
- ZhangLYuYShiTKouMSunJXuTLiQWuSCaoQHouW2020 Genome-wide analysis of expression quantitative trait loci (eQTLs) reveals the regulatory architecture of gene expression variation in the storage roots of sweet potato. Horticulture Research 7:1-12
Publication Dates
-
Publication in this collection
14 Mar 2022 -
Date of issue
2022
History
-
Received
05 Feb 2021 -
Accepted
14 Jan 2022 -
Published
20 Feb 2022
