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Article

Genome-Wide Identification and Expression Analysis of Sucrose Transporter Gene Family in Wheat Lines under Heat Stress

by
Qiling Hou
†,
Jiangang Gao
†,
Zhilie Qin
,
Hui Sun
,
Hanxia Wang
,
Shaohua Yuan
,
Fengting Zhang
and
Weibing Yang
*
Institute of Hybrid Wheat, Beijing Academy of Agricultural and Forestry Sciences, Beijing 100097, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(7), 1549; https://doi.org/10.3390/agronomy14071549
Submission received: 26 May 2024 / Revised: 8 July 2024 / Accepted: 15 July 2024 / Published: 17 July 2024
(This article belongs to the Special Issue The Stress of Crop Adversity: The Mechanisms and Pathways of Stress Resistance)
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Abstract

:
Sucrose transporters (SUTs) play vital roles in phloem sucrose unloading and transportation in wheat grains. However, the genomic information regarding the SUT gene family and their expression patterns in response to heat stress in grains of male-sterile wheat (Triticum aestivum L.) lines has not been systematically studied. In this study, a thorough examination of the wheat SUT gene family was conducted, focusing on their expression patterns in male-sterile lines under heat stress conditions in grain tissues. A total of 19 SUT genes were identified, with phylogenetic analysis indicating their classification into five distinct groups. Polyploidization was identified as a substantial factor in the expansion of SUT genes, with segmental duplication being the predominant mechanism driving the evolutionary expansion of the SUT gene family in wheat. Transcriptome data indicate that the expression levels of TaSUT1 and TaSUT2 were higher than other SUT genes in grains of male-sterile lines. The TaSUT1 expression showed a gradual decreasing trend, while TaSUT2 showed a reverse trend with the process of grain filling. After heat stress, the TaSUT1 expression in grains of male-sterile lines was first significantly increased and then significantly decreased with the filling stage extension, aligning with the observed trend of sucrose levels, indicating that heat stress may decrease the grain weight by reducing sucrose unloading and transportation process in grains. These results provide a systematic analysis of the SUT gene family and lay a theoretical foundation for us to study the grain filling of male-sterile lines in response to abiotic stress.

1. Introduction

Grain filling is crucial in determining wheat yield, as it is closely associated with the production of photo-assimilates and their subsequent distribution to the developing grains [1,2]. Sucrose is the main form of photosynthetic assimilates’ transfer from source to sink, which is partially mediated by a large number of SUTs. These transporters play a crucial role in regulating the movement of sucrose across cellular membranes, thereby influencing various aspects of plant growth and development [3,4,5,6,7,8]. The SUT gene family in major crop species were typically classified into five distinct groups according to phylogenetic analyses [5,9]. However, Groups 1, 2 and 4 have been extensively characterized [6]. More specifically, SUT genes are members of the glycoside pentose hexuronic ester (GPH) cation symporter family, which is part of the major facilitator superfamily characterized by 12 transmembrane spanning helices [10]. The SUT proteins exhibit high conservation and typically encompass 400–600 amino acids, containing the MFS_2 domain (PF013347) [11].
SUT genes have been identified in some crops, such as rice, barley and maize. OsSUT1 was first identified in rice, and it was not essential for apoplasmic phloem loading of sucrose in rice leaves according to the analysis of the OsSUT1 mutant [5,12], while OsSUT2–OsSUT5 may possess diverse roles in both sink and source tissues [13]. As reported in barley, HvSUT1 is preferentially expressed in caryopses in the cells of the nucellar projection and the endospermal transfer layer, while HvSUT2 is expressed in all sink and source tissues, suggesting that HvSUT1 and HvSUT2 serve distinct functions during grain filling [14,15]. Seven SUT genes were identified in maize; ZmSUT1 has been demonstrated to be essential for efficient sucrose phloem loading, while no evidence proved its apparent function in the unloading process [5,16,17]. In wheat, five SUT genes have been reported [6,18,19]. TaSUT1 is expressed in almost all organs, particularly at high levels in developing grains, suggesting that its key roles are in grain filling via regulation of sucrose unloading in phloem [7]. TaSUT1 also plays a crucial role in stem water soluble carbohydrate remobilization to grain under drought [6,20]. TaSUT2 is involved in the intracellular partitioning of sucrose, particularly between the vacuole and cytoplasm, which was expressed almost equally across vegetative tissues and the grain. TaSUT3 may have specific functions in pollination and seed setting, but so far, the function of TaSUT3 in wheat remains undetermined [6]. TaSUT4 and TaSUT5 displayed lower gene expression levels in grains during the filling stage, suggesting that they do not seem to have an important role during the grain-filling stages [6,19]. Although parts of SUT genes in wheat have been reported, there is very limited information for complete genome identification, evolutionary analysis and expression patterns of SUT genes in grains of male-sterile lines.
Common wheat is an allopolyploid species containing three sub-genomes, A, B and D, which originated from two successive polyploidization events within the genera Triticum and Aegilops. Triticum urartu (diploid, AA) is the progenitor of the A sub-genome of tetraploid (Triticum turgidum, AABB) and hexaploid (T. aestivum, AABBDD) wheat. The hybridization of Triticum dicoccoides and Aegilops tauschii, commonly known as the D genome donor, has led to the evolution of common wheat (T. aestivum) [21]. The assembly and annotation of high-quality genomes of common wheat and its relatives, along with large-scale RNA-seq analysis of wheat genes under various stresses and different developmental stages, facilitate detailed analysis of SUT genes [22].
The technical system of two-line hybrid wheat based on the male-sterile lines in China was first established by our team, which offered the prospects for its application on a commercial scale and has now entered a relatively rapid development stage. Genetically, the male-sterile lines in this study were classified as environmentally sensitive cytoplasmic/genetic male sterility (EC/GMS), which were regulated by the photoperiod and temperature [23,24]. Wheat sterile lines play a crucial role as maternal plants in both self-seed propagation and hybrid seed production. However, they often encounter the impact of high temperatures, leading to insufficient grain filling, which subsequently affects seed quality [25]. In addition, the short grain-filling period can also lead to poor plumpness and low seed vitality of outcrossing grains, which is not conducive to the demonstration and promotion of hybrid wheat. As is well known, SUT genes can illustrate genotypic variations under abiotic stress [6,21]. However, there is almost no relevant research on the effect of heat stress on grain filling of male-sterile lines.
In this study, we performed a genome-wide analysis of the SUT gene family using the recently published wheat reference genome. The chromosomal localization, phylogenetic gene structure, conserved motif, gene duplication, evolution and cis-elements of SUT genes in wheat and its progenitors were also analyzed. Furthermore, SUT gene expressions in grain responses to heat stress are also presented. These will help to better understand the relationship between sucrose unloading and grain filling and provide the candidate genes for breeding wheat varieties with high grain-filling ability. In addition, the sucrose unloading and transport organs in the terminal grains of both cross-pollinated and self-pollinated plants are derived from maternal tissues. This study can also provide a theoretical basis for a deeper understanding of outcrossing grain filling by studying the response of SUT gene expression in self-crossing grains to heat stress.

2. Materials and Methods

2.1. Identification of SUT Gene Family

The genome-wide data for T. aestivum (IWGSC RefSeqv1.1), T. dicoccoides (WEWSeq_v.1.0) and Ae. tauschii (Aet_v4.0) were downloaded from Ensemble Plants (https://plants.ensembl.org/index.html, accessed on 5 July 2023) to construct a local database. The data for T. urartu (Tu 2.0) were downloaded from the MBKBase database (https://www.mbkbase.org/Tu/, accessed on 5 July 2023) [22]. The protein sequences of Arabidopsis and Oryza sativa SUT family members downloaded from Ensemble Plants (https://plants.ensembl.org/index.html, accessed on 5 July 2023) were used as queries for BLASTP searches against wheat and its ancestral species genomes. SUT genes with a score of >100 and an e-value of <10−5 were selected as candidate genes. In order to further verify the accuracy of the above method, we adopted another identification method. The SUT protein sequences of 9 species (Oryza sativa, Zea mays, Arabidopsis thaliana, Glycine max, Hordeum vulgare, Solanum tuberosum, Solanum lycopersicum, Vitis vinifera and Pisum sativum) were downloaded from UniProt (https://www.uniprot.org/uniprotkb? accessed on 5 July 2023), and then, a hidden Markov model (HMMER) file was constructed to search for all protein sequences in the wheat genome using Hmm-search software (3.0) to obtain preliminary identification results (screening e-value < 40 as candidate genes). The results showed that the two methods are consistent.
The longest transcript was selected for subsequent analysis. All candidate proteins were further analyzed using the Pfam database (http://pfam.xfam.org/, accessed on 4 July 2023) [26] and NCBI Batch Web CD-Search Tool (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi, accessed on 5 July 2023). Proteins containing complete SUT conserved domains were reserved for further analysis and named sequentially to their species and location on the chromosomes; all gene names are listed in Table 1. ExPAsy (https://web.expasy.org/compute_pi/, accessed on 5 July 2023) [27] was used to calculate the theoretical isoelectric point (pI) and molecular weight (MW) of each SUT protein. SoftBerry (1.0) (http://www.softberry.com/berry.phtml?topic=protcomppl&group=programs&subgroup=proloc, accessed on 5 July 2023) [28] was used to predict the subcellular location of the SUT proteins.

2.2. Phylogenetic Gene Structure and Conserved Motif Analysis

Multiple sequence alignment of all SUT proteins was performed with ClustalW (2.0.10) using the default options in MEGA-X (10.1.8-1) [29]. Phylogenetic trees were constructed using the maximum likelihood method in MEGAX with 1000 bootstrap replicates [29]. The phylogenetic tree was displayed using the iTOL (v6) [30,31]. Conserved motif analysis was performed using the MEME program (https://meme-suite.org/meme/tools/meme, accessed on 5 July 2023). The parameters were as follows: the maximum number of motifs was set to 20, and the optimum width was 6–50 residues [32,33]. The gene structure and motif composition were visualized using Tbtools (v2.096) [31].

2.3. Chromosomal Localization, Gene Duplication and Synteny Analysis of SUT Genes

Gene annotations of SUTs were extracted from the reference genome annotation information (GFF3) file of T. aestivum (IWGSC RefSeqv1.1), T. dicoccoides (WEWSeq_v.1.0) and Ae. tauschii (Aet_v4.0), which was obtained from Ensemble Plants (http://plants.ensembl.org/index.html, accessed on 5 July 2023) and the MBKBase database (http://www.mbkbase.org/Tu/, accessed on 5 July 2023) [22]. Then, the SUTs in the corresponding chromosomes were visualized using Tbtools (v2.096) [31]. The duplication events of SUT genes were calculated using MCScanX with a threshold e-value ≤ 1 × 10−5 and visualized using Gene Location Visualize from GTF/GFF in Tbtools (v2.096) [31]. Synteny blocks between T. aestivum, T. dicoccoides, Ae. tauschii and T. urartu were determined using Tbtools (v2.096) [31].

2.4. Cis-Element Analysis of SUT Genes

To identify the cis-elements in the promoter sequences of SUT genes, the upstream sequences (1–1500 bp) of SUTs were extracted from wheat and its progenitor species genome files. Not all gene promoters overlap with the 5′ regions of adjacent genes. The PlantCARE website (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 5 July 2023) was used to identify the cis-elements in the promoters [34]. Then, the data were organized and visualized using Simple BioSequence Viewer in TBtools (v2.096) [31].

2.5. Plant Cultivation, Stress Treatments and Sampling

From 2021 to 2022, the male-sterile line BS253 was planted in the experimental field of Beijing Hybrid Wheat Research Institute in Hai Dian, Beijing, China (39°56′ N, 116°17′ E) on 20 October 2021. The photo-thermo-sensitive male-sterile (PTMS) lines are important materials in the two-line system, which exhibit high sterility in hybrid seed production areas (latitude around 32 degrees north), while their fertility can be restored in the reproductive area (latitude around 40 degrees north). This experiment was conducted in the reproductive area. The experimental site features loam soil, with the previous crop being soybean. In three growing seasons, 120 kg N ha−1, 75 kg P2O5 ha−1 and 120 kg K2O ha−1 were applied as basal fertilizer before planting, with 120 kg N ha−1 being top-dressed at the jointing stage. BS253 was planted in six plots, three of which underwent the heat stress treatment, and the others were used as a control. The plot size was 3 m × 1 m (0.25 m between rows), and BS253 was grown with a density of 100 plants m−2. The heat stress treatment method is based on previous studies [35]. A 1.5 m high shed constructed from hollow pipes covered with a white polythene plastic film was built in the plots at 10 days following anthesis (DPA) to raise the temperature. The thickness was 0.1 mm, and the light transmittance was 90% of the plastic film. Four ventilations were opened on both sides of the shed to ensure good ventilation conditions inside. Heat stress was conducted on 15 May from 8:00 to 18:00 and sustained for 4 days, after which the shed was removed. Two temperature sensors were placed 0.3 m above the top of the canopy in the control and heat stress treatment. Data were collected by an automatic temperature recorder every 5 min during the heat stress treatment. The mean daily temperatures between the treatment and control from 08:00 to 18:00 were 35.09 and 27.79 °C, respectively.
Wheat anthesis and maturity were observed on 6 May and 12 June 2022, respectively. Due to the split glumes of male-sterile lines during the flowering stage, about 200 spikes flowered at the same day were selected at the heading stage (GS55) [36] and covered with 20 white bags (12 cm × 20 cm) to prevent pollination (10 spikes per white bag). Five stages were designated for sampling in this experiment: Stage 1 (the first day after heat stress treatment; the heat stress treatment and the control are expressed as HTM1 and NTM1, respectively); Stage 2 (the sixth day after heat stress treatment; the heat stress treatment and the control are expressed as HTM2 and NTM2, respectively); Stage 3 (the eleventh day after heat stress treatment; the heat stress treatment and the control are expressed as HTM3 and NTM3, respectively); Stage 4 (the sixteenth day after heat stress treatment; the heat stress treatment and the control are expressed as HTM4 and NTM4, respectively); and Stage 5 (the twenty-first day after heat stress treatment; the heat stress treatment and the control are expressed as HTM5 and NTM5, respectively).

2.6. Analysis of SUT Gene Expression, Sucrose Content and Grain Weight

Ten labeled spikes (flowered on the same day) from the heat stress treatment and control with three replicates were sampled for each stage described above, and the grains from the spikes were removed for the RNA-seq analysis according to a previous report [37]. The homoeologous SUT gene expression was derived from RNA-seq data, and differential TaSUT expressions in the grains of BS253 at different stages were plotted using Heatmapper. SUT genes with |log2FoldChange| ≥ 0 and padj < 0.05 were assigned as differentially expressed. The sucrose contents in the heat stress treatment and control were determined using the anthrone-sulfuric acid method, and their thousand kernel weights were determined at the mature stage.

2.7. Statistical Analysis

Multivariate analysis of variance for sucrose content and thousand kernel weight was performed using the Data Processing System (DPS) software (Version 7.05, Hangzhou, China), and significant differences were calculated using the least significant difference (LSD) test at p < 0.05 [38].

3. Results

3.1. Identification and Characterization of SUT Genes in Wheat and Its Ancestral Species

In this study, a total of 43 SUT genes with conserved domains were identified from wheat and its three progenitor species, including T. aestivum (19), T. urartu (4), Ae. tauschii (7) and T. dicoccoides (13) (Table 1). The TaSUT genes were named TaSUT1–TaSUT7, according to their orthologs in the rice genes, plus the suffix corresponding to the specific wheat sub-genome identifier (A, B or D). The TuSUT, TdSUT and AetSUT genes were named according to the genome location. If two SUTs were located on the same chromosome, they were sorted based on their physical positions (e.g., TdSUT-5B1, TdSUT-5B2) (Table 1).
The information on the gene name, protein ID and chromosome location was extracted from the reference genome annotation information (GFF3) files. The detailed physical and chemical characterizations of SUT proteins were analyzed using ExPAsy (v1.0) [27,39] (Table 1), including the protein length, molecular weight, theoretical isoelectric point and GRAVY.
The length of TaSUT proteins ranged from 337 (TaSUT6-4A) to 600 amino acid residues (TaSUT4-6D), with the molecular weights ranging from 35.95 kDa (TaSUT6-4A) to 64.00 kDa (TaSUT4-6D), the isoelectric points ranging from 5.75 (TaSUT4-6A) to 9.10 (TaSUT6-4A) and the aliphatic index ranging from 89.86 (TaSUT4-6A) to 108.6 (TaSUT1-4A). The TuSUT proteins ranged in length from 468 (TuSUT-7A) to 599 (TuSUT-6A), with the molecular weights ranging from 48.65 kDa (TuSUT-1A2) to 63.83 kDa (TuSUT-6A), the isoelectric points ranging from 6.63 (TuSUT-7A, TuSUT-6A) to 8.80 (TuSUT-5A) and the aliphatic index ranging from 94.67 (TuSUT-6A) to 108.60 (TuSUT-4A). The TdSUT proteins ranged in length from 413 (TdSUT-4A2) to 557 (TdSUT-2A), with the molecular weights ranging from 44.61 kDa (TdSUT-4A2) to 59.15 kDa (TdSUT-2A), the isoelectric points ranging from 6.02 (TdSUT-1A) to 8.67 (TdSUT-2A) and the aliphatic index ranging from 96.31 (TdSUT-6A) to 110.95 (TdSUT-4A1). The AetSUT proteins ranged in length from 508 (AetSUT-1D) to 600 (AetSUT-6D), with the molecular weights ranging from 53.41 kDa (AetSUT-1D) to 63.98 kDa (AetSUT-6D), the isoelectric points ranging from 5.90 (AetSUT-6D) to 9.42 (AetSUT-5D2) and the aliphatic index ranging from 94.35 (AetSUT-6D) to 109.04 (AetSUT-7D) (Table 1).
Fifteen TaSUT proteins were basic proteins, while only four TaSUTs (TaSUT4-6A/B/D, TaSUT3-1A) were acidic proteins with isoelectric points lower than 7. Three TuSUT proteins were basic proteins, except TuSUT-7A, which was an acidic protein with isoelectric points lower than 7. Ten TdSUT proteins were basic proteins, while only three TdSUT proteins (TdSUT-1A, TdSUT-6B and TdSUT-6A) were acidic proteins with isoelectric points lower than 7. Six AetSUT proteins were basic proteins, while only AetSUT-6D was an acidic protein with isoelectric points lower than 7 (Table 1). The GRAVYs of all SUT proteins were more than zero, indicating that the SUTs were hydrophobic (Table 1). Subcellular localization prediction indicated that 43 SUT proteins in wheat and its three progenitor species were localized in the plasma membrane (Table 1).

3.2. Phylogenetic Analysis of Test Plant SUT Proteins in 13 Plant Species

In this study, except for 43 SUT proteins we identified in wheat and its progenitor species, another 44 SUT proteins, which were previously identified from nine plant species, were collected, including T. aestivum (19), T. urartu (6), Ae. tauschii (8), T. dicoccoides (13), Hordeum vulgare (2), Oryza sativa (5), Arabidopsis thaliana (9), Glycine max (12), Zea mays (5), Pisum sativum (3), Vitis vinifera (2), Solanum lycopersicum (3) and Solanum tuberosum (3) (Table S1). To investigate the evolutionary relationships of the SUT proteins, all the above 87 proteins were used to construct a maximum likelihood phylogenetic tree (Figure 1). Based on the classification of rice SUTs [18], these SUTs were categorized into five main groups (Group 1–Group 5). Among Group 2 and Group 4, the SUTs of monocotyledons and dicotyledons were clustered together, respectively, indicating that the SUT genes of monocotyledons and dicotyledons had experienced great differentiation in the process of evolution. SUT members within the same group of wheat and its progenitor species had a high protein sequence similarity, and the evolutionary process in wheat and its progenitor species was relatively conservative.
The SUT genes identified in wheat and its progenitors were classified into Groups 1 (7 genes), 2 (7 genes), 3 (5 genes), 4 (7 genes) and 5 (17 genes). T. aestivum and T. dicoccoides had 19 and 13 SUT genes, which was about two times that of T. urartu and Ae. tauschii, and four and more than two times that of Oryza sativa and Zea mays, respectively. This indicated that the increased number of SUT genes in polyploid wheat was primarily due to genome polyploidization (Figure 1; Table 2).

3.3. Gene Structure and Conserved Motif Composition Analysis

In order to understand SUT functional divergence, the conserved motifs of these SUT proteins were identified using the MEME software (v5.0). Ten individual motifs were identified (Figure S1). Our results show that (motif numbers ranging from 7 to 10) TaSUT6-4A contained 7 motifs; TdSUT-6A and TdSUT-4A2 contained 8 motifs; TdSUT-5B2, TdSUT-1A, TdSUT-5A, TaSUT4-6B and TaSUT4-6A contained 9 motifs; and the rest of SUT proteins contained all 10 motifs.
The 43 SUT genes analyzed in different Groups from 1 to 5 had a structural divergence. Furthermore, SUT gene members in the same group exhibited a similar exon and intron structure. Variations in the exon and intron structures significantly contribute to the evolution and duplication processes of SUT genes [40].
In Group 1, all seven SUT genes contained 13 exons; the seven SUT genes analyzed in Group 2 all had 5 exons (except for TaSUT2-U). The number of exons of the five SUT genes in Group 3 ranged from 5 to 11. In Group 4, TaSUT4-6B and TdSUT-6A had 11 exons, and all the other five genes had 14 exons. Group 5 contained 17 SUT genes in total: 4 genes had 7 exons, 5 genes had 9 exons, 5 genes had 11 exons, TaSUT6-4A, TdSUT-4A2 and TaSUT5-2A had 4, 6 and 10 exons (Figure 2C). The findings indicate a strong correlation between motifs and the exon and intron structure observed in SUT genes, suggesting a connection with phylogenetic relationships. Additionally, specific motifs in SUT genes may play a significant role in their functional diversity.

3.4. Chromosomal Location and Gene Duplication Analysis of SUT Genes in Wheat and Its Progenitors

To determine the distribution of 43 SUT genes in wheat and its progenitors, we analyzed their chromosomal loci. These genes were assigned to specific chromosomes, but their distribution across the chromosomes was uneven (Figure 3). 2, 3, 4, 4, 3 and 2 TaSUTs were located in the homoeologous group on chromosomes 1, 2, 4, 5, 6 and 7, respectively, while the TaSUT2-U gene was located on the unanchored scaffolds. 1, 1, 1 and 1 TuSUTs were located in 4A, 5A, 6A and 7A, respectively. 1, 1, 1, 2, 1 and 1 AetSUTs were located in 1D, 2D, 4D, 5D, 6D and 7D, respectively. 1, 1, 1, 1, 2, 1, 1, 2, 1, 1 and 1 TdSUTs were located in 1A, 1B, 2A, 2B, 4A, 4B, 5A, 5B, 6A, 6B and 7A, respectively. Most SUT genes were located at the start or end of the chromosomes. No SUT genes were mapped to chromosome 3A, 3B, 3D or 7B in common wheat and its progenitors. Chromosomes 2A in T. aestivum and T. dicoccoides each carried a single SUT gene, whereas chromosomes 1A and 2A in T. urartu contained no SUT gene. Chromosomes 5A in T. urartu and T. dicoccoides each carried a single SUT gene, whereas chromosomes 5A in T. aestivum contained no SUT gene. Thus, the chromosomal location of SUT genes was inconsistent on the corresponding chromosomes among the different species.
Segmental duplication was a crucial process involved in SUT gene family evolution. No tandem repeats were detected in wheat and its progenitors. Sixteen SUT genes in wheat formed six clusters on chromosomes 1A, 2B, 4B, 5B, 6B and 7A. A total of 19 pairs of segmental repeats were identified by MCScanX (Figure 3; Table 3). The Ka/Ks ratios of 19 SUT gene pairs were less than 1, suggesting that SUT genes experienced intense purifying selection during evolution (Table 3). These results suggested that segmental duplication was the main driver of SUT gene evolution involved in expansion of the SUT gene family in wheat and its progenitors. Eighteen SUT genes in T. aestivum were collinear with T. dicoccoides, and seventeen SUT genes were collinear with Ae. tauschii. Collinear genes were much less frequent (ten) between T. aestivum and T. urartu. TaSUT2-U was not collinear with other species (Figure 4; Table S2). TaSUT5-2A in wheat was present in T. dicoccoides (TdSUT-2A) but not in T. urartu, suggesting that this gene evolved after the first polyploidization event. Additionally, TuSUT-5A in T. urartu was present in T. dicoccoides (TdSUT-5A) but not in T. aestivum, implying that this gene emerged subsequent to the initial polyploidization event.

3.5. Cis-Element Analysis of SUT Promoters in Wheat and Its Progenitors

The quantity and arrangement of diverse cis-regulatory elements within gene promoters may suggest variations in their roles and control mechanisms. We found there were many regulatory elements that are involved in plant growth, light responsiveness, stress responsiveness and hormone responsiveness by analyzing the 1.5 kb upstream regions of the 43 SUT genes in wheat and its progenitors (Figure 5). The elements involved in light response accounted for 38.13%; those involved in hormone response accounted for 33.90%; those involved in stress response accounted for 16.46%; and those involved in plant growth accounted for 11.51% (Table S3). The light-responsiveness-related cis-elements were identified in the promoter regions; for example, ACE, Box4, GATA-motif, Sp1, G-box and GT1-motif were found in the promoters of 17, 15, 21, 26, 35 and 24 SUT genes, respectively (Figure 5; Table S3). The I-box, TCT-motif, AE-box, GA-motif and TCCC-motif were observed in 14, 23, 13, 10 and 11 SUT genes, respectively (Figure 5; Table S3). In plant growth response elements, the meristem expression element (CAT-box), MYBHv1-binding-site-related element (CCAAT-box), zein-metabolism-regulation-related element (O2-site), seed-specific-regulation-related element (RY-element) and cell-cycle-regulation-related element (MSA-like element) were found in the promoters of 28, 29, 21, 6 and 8 SUT genes, respectively (Figure 5; Table S3). In stress response elements, anaerobic-induction-related element (ARE) was found in 40 SUT genes. In addition, other stress-related elements, such as anoxic-specific-inducibility-related element (GC-motif), drought-inducibility-related element (MBS), defense- and stress-responsive element (TC-rich repeats) and low-temperature-responsive element (LTR), were also observed in the promoters of 19, 26, 8 and 18 SUT genes, respectively (Figure 5; Table S3). In hormone response elements, the abscisic-acid-responsive element (ABRE), salicylic-acid-responsive element (TCA-element), auxin-responsive element (TGA-element), MeJA-responsive element (CGTCA-motif, TGACG-motif) and gibberellin-responsive element (P-box) were found in the promoters of 41, 23, 22, 42, 42 and 10 SUT genes, respectively (Figure 5; Table S3). Among the 43 transcripts of SUT genes in wheat and its progenitors, the cis-element numbers ranged from 12 (TaSUT7-7A and TdSUT-7A) to 54 (TaSUT2-5D). TaSUT7-7D, TdSUT-6A and AetSUT-7D had no elements distributed in the 1.5 kb promoter regions involved in plant growth. In addition, the distributions in SUT genes of the light response element (G-box), stress response element (ARE) and hormone response elements (ABRE, CGTCA-motif and TGACG motif) were very dense, thus indicating that they may play important roles in regulating SUT genes.

3.6. Expression Pattern of TaSUT Genes under Heat Stress in Grains of Male-Sterile Line

Transcriptome data (FPKM values) were obtained from publicly available RNA-seq data [21,41] for all SUT genes (Figure S2). TaSUTs showed a greatly divergent expression pattern in different developmental stages or tissues. Six genes (TaSUT1-4A/-4B/-4D, TaSUT2-5B/-5D/-U) were highly expressed during the whole growth period of wheat. TaSUT4-6A, TaSUT4-6B and TaSUT4-6D had similar expression patterns and low-level expressions in the whole growth period of wheat. It is important to consider that approximately half of the TaSUTs showed minimal expression in various developmental stages and tissues of wheat, including TaSUT6-4A, TaSUT6-5B, TaSUT6-5D, TaSUT7-7A and TaSUT7-7D. In addition, we found that TaSUT3-1A and TaSUT3-1D were highly expressed in anthers and had a specific tissue expression pattern. Heat stress significantly reduced the grain weight of the male-sterile line BS253 (Figure 6B). Analysis of SUT gene expressions showed that TaSUT1 had the highest expression level, followed by TaSUT2, and other SUT genes had extremely low expression levels. Among the three homeologous genes of TaSUT1 (TaSUT1-4A, TaSUT1-4B and TaSUT1-4D), the expression of TaSUT1-4A was higher than that of TaSUT1-4B and TaSUT1-4D, and the expression of TaSUT1-4A was more sensitive to heat stress compared with TaSUT1-4B and TaSUT1-4D. Compared with the control, heat stress significantly increased the expression levels of TaSUT1 in Stage 1 (HTM1 vs. NTM1) while significantly reducing the expression levels of TaSUT1 in the other stages (Figure 6A). The expression trend of other SUT genes was not significant between the heat treatment and the control. Heat stress significantly increased the sucrose content in Stage 1 and Stage 2 grains while significantly decreasing the sucrose content in Stage 4 and Stage 5 grains, which was consistent with the variation trend of TaSUT1 expression (Figure 6C). TaSUT1 and TaSUT2 exhibited elevated expression levels during the grain-filling stage (Figure S2); this was consistent with their expressions under heat stress. The specific response mechanism of TaSUT1 in wheat sterile lines under heat stress remains to be further investigated.

4. Discussion

Plant SUTs play an important role in the distribution of photosynthetic assimilates in the form of sucrose and have a crucial impact on seed production. Analyzing the evolutionary relationships of the SUT gene family can provide insights into the regulation of sucrose unloading and transportation. With the increasing publication of plant genomes, a growing number SUTs have been found in rice [7], maize [5], wheat [4,6], Hordeum vulgare [15], Glycine max [42], Solanum tuberose [43], Solanum lycopersicum [44], Vitis vinifera [45] and Pisum sativum [46]. The publication of wheat and its progenitor genome sequences provides a good foundation for this study [41]. We identified 43 SUT genes from wheat and its progenitor species for the first time by combining blast and cryptic horse model construction, including T. aestivum (19), T. urartu (4), Ae. tauschii (7) and T. dicoccoides (13). TaSUT2-U and TaSUT2-5A, identified by Al-Sheikh Ahmed et al. [6], may be the same gene because the similarity between the two protein sequences is 80%. SUT genes within the same groups share similar gene structures and conserved domains. This suggests that SUT gene members were functionally conserved during the evolution. Gene duplication events play an important role in genome expansion and evolution [47]. Cis-element analysis of the promoters revealed that light, plant growth, hormone- and stress-related responsive elements were present in the promoters of SUTs. The SUT promoter contains the highest number of light and hormone response elements. The G-box and ARE elements predominate in regulatory elements responsive to light and stress. Within the hormone response elements, ABRE, TGACG- and CGTCA-motifs were present in greater numbers. These elements are essential for the upregulation of SUT proteins and their role in phloem loading and unloading and may directly or indirectly contribute to the regulation of heat stress through SUTs. Therefore, the cis-acting regulatory elements in the promoter region and the expression profiles under heat stress conditions suggest that SUT genes may play a crucial role in plants’ response to various abiotic stresses and plant hormones. Our results showed that segmental duplications played a significant role in the expansion of the SUT gene family. These findings may serve as a valuable reference for analyzing the evolution and predicting the function of SUT genes in wheat. In order to reveal the evolution and function of SUT genes, we analyzed the comparative synteny map between wheat and its ancestor species at the whole-genome level and found that TdSUT-2A was a new gene during the polyploid event, while TdSUT-5A was lost. These results indicated that the polyploidization event led to the variation in SUT gene numbers in the evolution of wheat.
SUT genes are expressed in various parts of the plant, including the roots, stems, leaves, spikes and grains [4]. SUT genes in grains were involved in moving sucrose into the developing grains to support grain growth and starch biosynthesis [7,18]. TaSUT1 may play a role in sucrose transportation from the endosperm to the shield shell in the early stage of wheat germination, and it may function in the progress of long-distance transport in wheat by loading and retrieving sucrose leaked to the phloem apoplasm [7,48]. It has also been proved that TaSUT1 expression might be associated with sucrose levels in leaves [49]. Similar to the high transcription level of TaSUT1 in wheat grain in glasshouse experiments [19], our research also showed that TaSUT1 expression is highest in the grains during the whole grain-filling stage (Figure 6A). Combined with the higher gene expression level of TaSUT1 in grains in comparison to the stem [6], we speculated that TaSUT1 performed an important function in sucrose unloading or transportation. Our results also showed that the expression levels of TaSUT1-4A were higher than those of TaSUT1-4B and TaSUT1-4D during the grain-filling stage. TaSUT1 in wheat grains may be similar to the function of HvSUT1 in barley, since wheat and barley are closely related [14]. Previous studies investigated SUT gene expressions in seedlings under abiotic stress conditions. OsSUT1, HvSUT1, ZmSUT1 and TaSUT1 were all highly upregulated, while the other SUT genes studied were downregulated under drought [6,50]. In our study, compared with the control group, the expression of TaSUT1 showed a trend of first increasing and then decreasing after heat stress, which was consistent with the variation of sucrose content in the grains. Combined with the subcellular localization results for TaSUT1 [4], we speculate that TaSUT1 regulates the grain-filling process by regulating the unloading or post-unloading transport of sucrose under heat stress conditions. Future studies should employ techniques like transgenic or tissue in situ hybridization to elucidate whether the primary role of TaSUT1 is in sucrose unloading, transport to grains following sucrose unloading, or in both processes. Moreover, research on the molecular mechanism of TaSUT1 regulating grain filling under heat stress conditions should also be strengthened.
In barley, the HvSUT2 gene expression level was 25% lower than HvSUT1 expression before 15 DAA in developing grains [51]. The same result was also found in our experiment. Compared with TaSUT1, the gene expression level of TaSUT2 was very low in the early grain-filling stage, and it showed a slight increase in the later grain-filling stage, which was consistent with previous research [52]. Contrary to the expression trend in wheat and barley, both ZmSUT2 and ZmSUT1 showed high expression levels [53], and a diurnal cycling pattern of gene expression was also observed in maize leaves [5], indicating their potential important role in sucrose loading. In our study, the expression level of TaSUT2 was lower than that of TaSUT1 but higher than that of TaSUT3, TaSUT4, TaSUT5, TaSUT6 and TaSUT7. Combining the positive correlations of TaSUT2 expression levels with the grain-filling rate in the mid-grain-filling stage, we concluded that TaSUT2 may compensate TaSUT1 function in the later grain-filling stage in sucrose loading and unloading. Among the three isoforms of TaSUT2 genes, the gene expression levels of TaSUT2-U were higher than those of TaSUT2-5D and TaSUT2-5B. The gene function of TaSUT1 and TaSUT2 during the grain-filling stage needs further investigation. Unlike TaSUT1, TaSUT2 is not sensitive to high temperatures.
TaSUT3 is hypothesized to contribute to pollination and seed setting. TaSUT4 and TaSUT5 do not seem to have an important role during the growth stages of wheat [4]. In this experiment, TaSUT3, TaSUT4, TaSUT5, TaSUT6 and TaSUT7 from RNA-seq data exhibited extremely low expression levels and even levels that were difficult to detect. The expression levels of TaSUT6 and TaSUT7 also indicate a more limited function (Figure 6A). Further research is required to fully explore the differential expressions of organs in wheat in the whole growth stages. Previous studies have indicated that SUT proteins transmitted stress signals through the sugar status [4,54]. Previous research has primarily concentrated on the impact of SUT genes during the seedling stages [4], with limited investigation into their role in heat stress during wheat grain filling. TaSUT1 plays a predominant role in wheat grain weight under drought stress conditions [6,49]. TaSUT1 is highly expressed during mid-seed filling in fertile wheat and might control cytosolic sucrose homeostasis in grains [55,56]. Given the heightened environmental sensitivity of wheat sterile lines relative to fertile wheat lines, the regulatory mechanism of TaSUTs in response to heat stress may exhibit distinct characteristics. Unlike previous studies on wheat seedlings, our experiment showed that TaSUT3, TaSUT4, TaSUT6 and TaSUT7 did not exhibit significant sensitivity to heat stress during the grain-filling stage. Further research should conduct a detailed analysis to elucidate the factors influencing the inconsistent expression patterns of SUT genes, such as the period of heat stress treatment, sampling organs, sampling time and so on. The effects of heat stress on sucrose distribution in sterile lines and common wheat, along with the underlying mechanisms, warrant further investigation.

5. Conclusions

A total of 43 SUT genes were identified from wheat and its three progenitor species, which were categorized into five groups, further supported by highly similar exon–intron structures and motif compositions. Segmental duplication contributed to the expansion of SUT genes in wheat and its progenitors. Analysis of cis-acting elements revealed that light-responsive elements (G-box), stress-responsive elements (ARE) and hormone-responsive elements (ABRE, CGTCA-motif and TGACG motif) may play significant roles in the regulation of SUT genes. Transcriptome analysis showed that TaSUT1, as the main SUT gene, played an important role in the process of sucrose unloading or transfer to the grains after unloading. Heat-stress-induced reduction in TaSUT1 expression led to decreased sucrose content in the grains and reduced grain weight in wheat sterile lines. This study lays the foundation for a deeper exploration of the role of TaSUTs in regulating sucrose distribution in wheat sterile lines.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14071549/s1, Figure S1: Conserved motif sequences of SUTs; Figure S2: Heat map of TaSUT genes expressed in different developmental stages in wheat tissues; Table S1: Ten plant species’ gene ID and protein sequence information; Table S2: Syntenic SUT gene pairs between wheat and its progenitors; Table S3: Promoter analysis of the SUT gene family in wheat and its progenitors.

Author Contributions

Q.H., J.G., F.Z. and W.Y. conceived and designed the research; Q.H., Z.Q., H.W., H.S. and S.Y. performed the experiments; Q.H., Z.Q., H.W. and S.Y. analyzed and interpreted the data; Q.H. and W.Y. wrote the manuscript; Q.H., J.G., F.Z. and W.Y. reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Beijing Natural Science Foundation (6232006), the Youth Fund Project from Beijing Academy of Agriculture and Forestry Sciences, China (QNJJ202225), and the special fund of Modern agricultural industry technology system Construction (CARS-03-3).

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries may be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Phylogenetic relationship analysis of 87 SUT proteins from T. aestivum, T. urartu, Ae. tauschii, T. dicoccoides, Hordeum vulgare, Oryza sativa, Arabidopsis thaliana, Glycine max, Zea mays, Pisum sativum, Vitis vinifera, Solanum lycopersicum and Solanum tuberosum. The phylogenetic tree was built using the maximum likelihood method (ML) with 1000 bootstrap replicates in MEGA X. The diverse subgroups of SUT proteins were marked with different colors. The SUT proteins of T. aestivum, T. urartu, Ae. tauschii, T. dicoccoides, Hordeum vulgare, Oryza sativa, Arabidopsis thaliana, Glycine max, Zea mays, Pisum sativum, Vitis vinifera, Solanum lycopersicum and Solanum tuberosum are represented by red stars, yellow stars, purple stars, blue stars, blue circles, red circles, red squares, purple squares, green circles, blue right-pointing triangles, red right-pointing triangles, red checkmarks and blue left-pointing triangles, respectively. The SUTs identified in this study are represented by stars.
Figure 1. Phylogenetic relationship analysis of 87 SUT proteins from T. aestivum, T. urartu, Ae. tauschii, T. dicoccoides, Hordeum vulgare, Oryza sativa, Arabidopsis thaliana, Glycine max, Zea mays, Pisum sativum, Vitis vinifera, Solanum lycopersicum and Solanum tuberosum. The phylogenetic tree was built using the maximum likelihood method (ML) with 1000 bootstrap replicates in MEGA X. The diverse subgroups of SUT proteins were marked with different colors. The SUT proteins of T. aestivum, T. urartu, Ae. tauschii, T. dicoccoides, Hordeum vulgare, Oryza sativa, Arabidopsis thaliana, Glycine max, Zea mays, Pisum sativum, Vitis vinifera, Solanum lycopersicum and Solanum tuberosum are represented by red stars, yellow stars, purple stars, blue stars, blue circles, red circles, red squares, purple squares, green circles, blue right-pointing triangles, red right-pointing triangles, red checkmarks and blue left-pointing triangles, respectively. The SUTs identified in this study are represented by stars.
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Figure 2. Phylogenetic relationships, conserved motifs, and gene structures of SUT genes in wheat and its progenitors. (A) The phylogenetic tree was constructed using the maximum likelihood method in MEGAX with 1000 bootstrap replicates. (B) The motif composition of SUT proteins. The 10 motifs were indicated by colored boxes and numbered 1–10. (C) Gene structures of SUT genes. Yellow boxes indicate exons; black lines indicate introns.
Figure 2. Phylogenetic relationships, conserved motifs, and gene structures of SUT genes in wheat and its progenitors. (A) The phylogenetic tree was constructed using the maximum likelihood method in MEGAX with 1000 bootstrap replicates. (B) The motif composition of SUT proteins. The 10 motifs were indicated by colored boxes and numbered 1–10. (C) Gene structures of SUT genes. Yellow boxes indicate exons; black lines indicate introns.
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Figure 3. Chromosomal location and duplication events of SUT genes in wheat and its progenitors. The blue lines represent segmental repeats; detailed information on the gene repeats can be found in Table 3. TBtools software was used to draw the chromosomal map of SUT genes.
Figure 3. Chromosomal location and duplication events of SUT genes in wheat and its progenitors. The blue lines represent segmental repeats; detailed information on the gene repeats can be found in Table 3. TBtools software was used to draw the chromosomal map of SUT genes.
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Figure 4. Synteny analysis of SUT genes between wheat and its progenitors. Gray lines in the background indicate the collinear blocks within wheat and its progenitor species, while blue lines represent the syntenic SUT gene pairs.
Figure 4. Synteny analysis of SUT genes between wheat and its progenitors. Gray lines in the background indicate the collinear blocks within wheat and its progenitor species, while blue lines represent the syntenic SUT gene pairs.
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Figure 5. Analysis of promoter cis-acting elements in SUT genes of wheat and its progenitors. (A) The cis-acting elements were classified into four major classes: plant growth, light-responsive, stress-responsive, hormone-responsive-related cis-acting elements. The different colors and numbers on the grid indicate the numbers of different promoter elements in SUT genes. (B) The distributions of different cis-acting elements in SUT gene promoters.
Figure 5. Analysis of promoter cis-acting elements in SUT genes of wheat and its progenitors. (A) The cis-acting elements were classified into four major classes: plant growth, light-responsive, stress-responsive, hormone-responsive-related cis-acting elements. The different colors and numbers on the grid indicate the numbers of different promoter elements in SUT genes. (B) The distributions of different cis-acting elements in SUT gene promoters.
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Figure 6. Response of SUT gene expression, sucrose content and grain weight to heat stress. (A) Response of 19 SUT gene expressions to heat stress during the grain-filling stage after heat stress. (B) Response of grain weight to heat stress at maturity. (C) Response of sucrose content to heat stress during the grain-filling stage after heat stress. The first day after heat stress treatment, the heat stress treatment and the control are expressed as HTM1 and NTM1, respectively. The sixth day after heat stress treatment, the heat stress treatment and the control are expressed as HTM2 and NTM2, respectively. The eleventh day after heat stress treatment, the heat stress treatment and the control are expressed as HTM3 and NTM3, respectively. The sixteenth day after heat stress treatment, the heat stress treatment and the control are expressed as HTM4 and NTM4, respectively. The twenty-first day after heat stress treatment, the heat stress treatment and the control are expressed as HTM5 and NTM5, respectively. The ns symbol represents not significant, and the ** symbol represents significant at p ≤ 0.01.
Figure 6. Response of SUT gene expression, sucrose content and grain weight to heat stress. (A) Response of 19 SUT gene expressions to heat stress during the grain-filling stage after heat stress. (B) Response of grain weight to heat stress at maturity. (C) Response of sucrose content to heat stress during the grain-filling stage after heat stress. The first day after heat stress treatment, the heat stress treatment and the control are expressed as HTM1 and NTM1, respectively. The sixth day after heat stress treatment, the heat stress treatment and the control are expressed as HTM2 and NTM2, respectively. The eleventh day after heat stress treatment, the heat stress treatment and the control are expressed as HTM3 and NTM3, respectively. The sixteenth day after heat stress treatment, the heat stress treatment and the control are expressed as HTM4 and NTM4, respectively. The twenty-first day after heat stress treatment, the heat stress treatment and the control are expressed as HTM5 and NTM5, respectively. The ns symbol represents not significant, and the ** symbol represents significant at p ≤ 0.01.
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Table 1. Members of the SUT gene family in wheat and its progenitor species.
Table 1. Members of the SUT gene family in wheat and its progenitor species.
Gene NameProtein IDChr 1Chr StarChr EndNumber of Amino AcidsMW 1 (Da)pI 1Aliphatic IndexGRAVY 1Subcellular Location 2
TaSUT3-1ATraesCS1A02G134100.11A19709132019713840750252,756.826.92 102.85 0.566 Plasma membrane
TaSUT3-1DTraesCS1D02G135900.11D18013991418017402950352,732.787.91 100.89 0.555 Plasma membrane
TaSUT5-2ATraesCS2A02G505000.12A73356080673356342251755,118.548.49 103.64 0.493 Plasma membrane
TaSUT5-2BTraesCS2B02G533300.12B72962735172963030853056,306.878.16 103.68 0.468 Plasma membrane
TaSUT5-2DTraesCS2D02G505700.12D59991615559991914853056,276.98.48 104.25 0.485 Plasma membrane
TaSUT1-4ATraesCS4A02G016400.14A111829861118852252255,072.568.68 108.60 0.610 Plasma membrane
TaSUT6-4ATraesCS4A02G334500.14A61765238461765433433735,949.449.10 106.29 0.593 Plasma membrane
TaSUT1-4BTraesCS4B02G287800.14B57146867957147408152355,165.688.68 106.90 0.599 Plasma membrane
TaSUT1-4DTraesCS4D02G286500.14D45750093945750658352355,232.88.77 107.46 0.588 Plasma membrane
TaSUT2-5BTraesCS5B02G000100.15B162352135751054,280.318.78 103.88 0.484 Plasma membrane
TaSUT6-5BTraesCS5B02G550700.15B70226832170227141550954,493.28.92 104.68 0.606 Plasma membrane
TaSUT2-5DTraesCS5D02G001200.15D1609486161466450553,859.858.92 104.91 0.499 Plasma membrane
TaSUT6-5DTraesCS5D02G537500.15D55015165355015453853357,281.268.47 101.26 0.522 Plasma membrane
TaSUT4-6ATraesCS6A02G410700.16A61376665661377150156660,581.425.75 89.86 0.217 Plasma membrane
TaSUT4-6BTraesCS6B02G456500.16B71266581171267444953757,907.616.26 92.18 0.237 Plasma membrane
TaSUT4-6DTraesCS6D02G393600.16D46731302146731843760063,999.655.90 94.35 0.287 Plasma membrane
TaSUT7-7ATraesCS7A02G090700.17A553423125534618051954,638.857.87 106.63 0.578 Plasma membrane
TaSUT7-7DTraesCS7D02G086200.17D528496915285311351854,547.758.17 107.39 0.577 Plasma membrane
TaSUT2-UTraesCSU02G136300.1Un12239291112239748748351,441.848.99 101.61 0.414 Plasma membrane
TuSUT-5ATuG1812G0500000064.01.T015A5433346543829750653,942.30 8.80 104.51 0.491 Plasma membrane
TuSUT-4ATuG1812G0400003255.01.T014A57228263757228806952255,072.00 8.38 108.60 0.610 Plasma membrane
TuSUT-7ATuG1812G0700000896.01.T017A475985954760221646348,650.30 6.63 107.30 0.661 Plasma membrane
TuSUT-6ATuG1812G0600004346.01.T016A57102118157102651459963,834.90 6.63 94.67 0.303 Plasma membrane
TdSUT-4BTRIDC4BG049440.3 4B57739201157739744252355,165.20 8.38 106.90 0.599 Plasma membrane
TdSUT-4A1TRIDC4AG002240.34A116371631164286149652,945.70 8.48 110.95 0.632 Plasma membrane
TdSUT-1BTRIDC1BG024620.41B24296018724300642447950,322.5 7.78 101.67 0.581 Plasma membrane
TdSUT-1ATRIDC1AG018920.31A17539717317544439444146,599 6.02 103.58 0.521 Plasma membrane
TdSUT-6BTRIDC6BG073520.106B70293334270306740653356,863.20 6.33 100.15 0.465 Plasma membrane
TdSUT-2BTRIDC2BG076930.12B72548383972548698653056,258.30 7.97 104.23 0.471 Plasma membrane
TdSUT-2ATRIDC2AG071090.12A72672501172672795655759,154.50 8.67 100.77 0.439 Plasma membrane
TdSUT-5B2TRIDC5BG080290.25B69584997569585336050854,242.40 8.47 104.51 0.601 Plasma membrane
TdSUT-6ATRIDC6AG060070.16A61500575361501068844447,429.00 5.32 96.31 0.341 Plasma membrane
TdSUT-7ATRIDC7AG010430.1 7A480199194802384050853,626.17.92 108.54 0.607 Plasma membrane
TdSUT-4A2TRIDC4AG050570.24A60989185560989765141344,613.98.47 99.25 0.529 Plasma membrane
TdSUT-5B1TRIDC5BG000610.15B3299815330439041944,994.9 7.24 104.56 0.522 Plasma membrane
TdSUT-5ATRIDC5AG000570.15A2385745242898446149,473.27.37 108.98 0.563 Plasma membrane
AetSUT-4DAET4Gv20698700.2 4D46365957446366492852355,232.38.48 107.46 0.588 Plasma membrane
AetSUT-1DAET1Gv20346300.2 1D18550780918554290250853,415 7.79 100.67 0.543 Plasma membrane
AetSUT-6DAET6Gv20990400.106D49007143849016124460063,983.595.90 94.35 0.281 Plasma membrane
AetSUT-2DAET2Gv21109000.1 2D59820718959821039153056,276.38.24 104.25 0.485 Plasma membrane
AetSUT-5D2AET5Gv21192100.15D56215628556215950550954,596.68.70 102.77 0.558 Plasma membrane
AetSUT-7DAET7Gv20242500.27D513815235138495051153,905.48.10 109.04 0.598 Plasma membrane
AetSUT-5D1AET5Gv20003000.3 5D1817524182283553657,316.19.42 100.32 0.384 Plasma membrane
1 Chr, chromosome; MW, molecular weight; pI, theoretical isoelectric point; GRAVY, grand average of hydropathicity. 2 The subcellular location results for SUT genes were predicted using SoftBerry (1.0) (http://www.softberry.com/berry.phtml?topic=protcomppl&group=programs&subgroup=proloc, accessed on 5 July 2023).
Table 2. Numbers of SUTs homologs encoded by the surveyed genomes in total and individual subclasses.
Table 2. Numbers of SUTs homologs encoded by the surveyed genomes in total and individual subclasses.
GenomeTotal NumberGroup
Group 1Group 2Group 3Group 4Group 5
T. urartu (AA)411011
Ae. tauschii (DD)711113
T. dicoccoides (AABB)1322225
T. aestivum (AABBDD)1933238
Total43775717
Table 3. Ka/Ks analysis of SUT gene pairs in wheat and its progenitors.
Table 3. Ka/Ks analysis of SUT gene pairs in wheat and its progenitors.
GenomeGene PairKaKsKa/Ks
AABBDDTaSUT3-1A/TaSUT3-1D0.0098 0.0718 0.1370
TaSUT5-2A/TaSUT5-2B0.0230 0.1169 0.1967
TaSUT5-2A/TaSUT5-2D0.0104 0.0970 0.1074
TaSUT5-2B/TaSUT5-2D0.0150 0.1058 0.1422
TaSUT1-4A/TaSUT1-4B0.0035 0.0591 0.0584
TaSUT1-4A/TaSUT1-4D0.0065 0.0767 0.0845
TaSUT6-4A/TaSUT6-5B0.0331 0.0681 0.4856
TaSUT6-4A/TaSUT6-5D0.0444 0.0985 0.4502
TaSUT1-4B/TaSUT1-4D0.0065 0.0552 0.1172
TaSUT6-5B/TaSUT6-5D0.0334 0.0728 0.4591
TaSUT4-6A/TaSUT4-6B0.0335 0.1486 0.2253
TaSUT4-6A/TaSUT4-6D0.0248 0.0997 0.2487
TaSUT4-6B/TaSUT4-6D0.0502 0.1539 0.3259
TaSUT7-7A/TaSUT7-7D0.0184 0.0549 0.3349
AABBTdSUT-1A/TdSUT-1B0.0158 0.1185 0.1334
TdSUT-2A/TdSUT-2B0.0229 0.1146 0.1998
TdSUT-4A1/TdSUT-4B0.0027 0.0543 0.0500
TdSUT-4A2/TdSUT-5B10.0125 0.0554 0.2251
TdSUT-6A/TdSUT-6B0.0040 0.1343 0.0300
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Hou, Q.; Gao, J.; Qin, Z.; Sun, H.; Wang, H.; Yuan, S.; Zhang, F.; Yang, W. Genome-Wide Identification and Expression Analysis of Sucrose Transporter Gene Family in Wheat Lines under Heat Stress. Agronomy 2024, 14, 1549. https://doi.org/10.3390/agronomy14071549

AMA Style

Hou Q, Gao J, Qin Z, Sun H, Wang H, Yuan S, Zhang F, Yang W. Genome-Wide Identification and Expression Analysis of Sucrose Transporter Gene Family in Wheat Lines under Heat Stress. Agronomy. 2024; 14(7):1549. https://doi.org/10.3390/agronomy14071549

Chicago/Turabian Style

Hou, Qiling, Jiangang Gao, Zhilie Qin, Hui Sun, Hanxia Wang, Shaohua Yuan, Fengting Zhang, and Weibing Yang. 2024. "Genome-Wide Identification and Expression Analysis of Sucrose Transporter Gene Family in Wheat Lines under Heat Stress" Agronomy 14, no. 7: 1549. https://doi.org/10.3390/agronomy14071549

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