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Article

Genome-Wide Identification, Characterization, and Expression Analysis of TUBBY Gene Family in Wheat (Triticum aestivum L.) under Biotic and Abiotic Stresses

by
Adil Altaf
1,†,
Ahmad Zada
2,†,
Shahid Hussain
3,
Sadia Gull
4,
Yonggang Ding
1,
Rongrong Tao
1,
Min Zhu
1,5,* and
Xinkai Zhu
1,5,6,*
1
Jiangsu Key Laboratory of Crop Genetics and Physiology, Jiangsu Key Laboratory of Crop Cultivation and Physiology, Wheat Research Center, College of Agriculture, Yangzhou University, Yangzhou 225009, China
2
College of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, China
3
College of Agriculture, Yangzhou University, Yangzhou 225009, China
4
College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China
5
Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China
6
Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education of China, Yangzhou University, Yangzhou 225009, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2022, 12(5), 1121; https://doi.org/10.3390/agronomy12051121
Submission received: 23 March 2022 / Revised: 1 May 2022 / Accepted: 2 May 2022 / Published: 6 May 2022
(This article belongs to the Special Issue Developing Temperature-Resilient Plants: Responses and Mitigation Strategies)
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Abstract

:
The TUBBY gene family is a group of transcription factors found in animals and plants with many functions. TLP genes have a significant role in response to different abiotic stresses. However, there is limited knowledge regarding the TUBBY gene family in T. aestivum. Here we identified 40 TaTLP genes in wheat to reveal their potential function. This study found that TUBBY (TaTLP) genes are highly conserved in wheat. The GO analysis of TaTLP genes revealed their role in growth and stress responses. Promoter analysis revealed that most TaTLPs participate in hormone and abiotic stress responses. The heatmap analysis also showed that TaTLP genes showed expression under various hormonal and abiotic stress conditions. Several genes were upregulated under different hormonal and temperature stresses. The qRT-PCR analysis confirmed our hypotheses. The results clearly indicate that various TaTLP genes showed high expression under temperature stress conditions. Furthermore, the results showed that TaTLP genes are expressed in multiple tissues with different expression patterns. For the first time in wheat, we present a comprehensive TaTLP analysis. These findings provide valuable clues for future research about the role of TLPs in the abiotic stress process in plants. Overall, the research outcomes can serve as a model for improving wheat quality through genetic engineering.

1. Introduction

Global warming has resulted in significant decreases in crop production over the last few decades [1]. Plants are exposed to numerous environmental stresses that disrupt biochemical and physiological processes [2]. Temperature, heat, drought, and salt stress directly reduce the quality and total yield [3,4]. To overcome annual yield losses in crops such as wheat, it is critical to identify and understand new sources of defense biomarkers. The TUBBY-like proteins are a family of bipartite transcription factors discovered in plants [5,6,7]. It was possible to trace the TUBBY-like gene family’s phylogenetic history back to the earliest stages of eukaryotic evolution after discovering TUBBY-like genes in both single-celled and multicellular eukaryotes [7]. TUBBY-like proteins are distinguished from other proteins by the presence of the conserved C-terminal tubby domain, which is composed of 12 antiparallels closed β-barrel strands with a central hydrophobic α--helix [5]. A conserved N-terminal F-box domain and the C terminal tubby domain are found in the TLP family of plants, which is much larger than the TLP family found in animals [8]. The function of TLP genes was studied in various plants such as Arabidopsis thaliana, Oryza sativa, Populus deltoides [9], Malus domestica [8], Zea maize [10], Solanum lycopersicum [11], and cotton [12]. In A. thaliana, 11 TUBBY family genes were identified, whereas in Oryza sativa 14, Malus domestica 15, Zea maize 10, Solanum lycopersicum 11, and cotton 105 TLP genes were previously identified [8,9,10,11,12]. TLP shows different expression levels in tissues in plants in response to various environmental and hormonal stresses [7,8,13]. It was found that AtTLP3 and AtTLP9 play an essential role in abscisic acid and osmotic stress [13], whereas AtTLP9 plays a significant role in salt and drought stress [13,14]. Many TUBBY family genes showed up-regulation in Malus domestica in response to abiotic stresses, suggesting a substantial role of TLP genes in abiotic stresses [8]. Previous observation showed that CaTLP1 in Cicer arietinum plays a vital role in dehydration stress resistance, and its overexpression in tobacco offers salt and drought stress resistance [15]. Thus, TLPs seem to have a significant role in abiotic stress tolerance in plants. However, the function of TLPs and their mode of action in plants is an unexplored topic [11].
Wheat is an important crop providing sustenance to 35% of the world’s population. However, unpredictable climatic conditions have stagnated wheat production in the past two to three decades. Biotic and abiotic stresses affect the growth of wheat crops and have decreased the plant’s output and performance [16]. Wheat crops’ evolutionary diversity allows them to adapt to different environmental conditions, although the molecular basis of this adaptation is unknown. Therefore, we were interested in the evolution of the wheat TUBBY family genes and their function in response to abiotic stress. This research aimed to understand wheat TUBBY family genes to improve wheat production, plant quality, and abiotic stress response.

2. Materials and Methods

2.1. Wheat TUBBY Family Genes Identification

We retrieved the protein sequences of TUBBY genes from the Arabidopsis [17] and wheat [18] using the Hidden Markov Model (HMM). The extracted Triticum aestivum L. protein sequences were analyzed using CD-search NCBI (http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi, http://www.ebi.ac.uk/interpro/search/sequence/) and SMART (http://smart.embl-heidelberg.de/) (accessed on 7 March 2022) databases. Proteins that do not exhibit the TUBBY domain were excluded. The chemical properties of TaTUBBY proteins were examined using the Expasy online server (http://web.expasy.org/protparam/) (accessed on 7 March 2022). The CELLO2GO [19] online server was used to predict the subcellular location of TaTUBBY genes.

2.2. Phylogenetic Tree, Digital Expression, and Motif Analysis

The Mega (version 7.0) program was used to create the maximum likelihood phylogenetic tree [19]. The conserved motif in the TUBBY gene was predicted using the online MEME server (latest Version 4.12.0) (http://meme-suite.org/tools/meme) (accessed on 8 March 2022). In response to biotic and abiotic stress, the gene expression levels were determined at various stages in all available tissue. The RNA-seq data were retrieved in transcripts per million (TPM) from the expVIP wheat Expression Browser (http://www.wheat-expression.com/) (accessed on 8 March 2022) [20,21]. The abiotic stress was comprised of temperature stress ranging from 20 to 40 °C, and biotic stresses were comprised of abscisic acid (ABA), gibberellic acid (GA), and a combination of Fusarium graminearum (FG), ABA, and GA. The ratio of the expression value under treatment to the control was calculated to determine the regulation patterns of a given gene subjected to stress. Ratios greater than or less than 1.0 under a given treatment indicated that the stress treatment had altered gene expression levels. In contrast, a ratio equal to 1.0 showed that the treatment did not affect gene expression levels [20]. The heatmap was created using the Heml 1.0 software tool (http://hemi.biocuckoo.org/faq.php) (accessed on 8 March 2022).

2.3. Chromosomal Location and Protein-Protein Interaction of TUBBY Genes

The chromosomal location of the TUBBY genes was determined using plants from the Ensemble genomes (https://plants.ensembl.org/Triticum_aestivum/Info/Annotation/) (accessed on 9 March 2022) [20]. MAPDraw was also used to map the physical location of TUBBY genes, and nomenclature followed the order in which they appeared on the chromosomes. Analyses of Arabidopsis protein–protein interactions were conducted using the STRING online server (http://string.embl.de) (version. 10) (accessed on 9 March 2022).

2.4. Gene Structure and Conserved Motif Analysis

In the Gene Structure Display server program (http://gsds.cbi.pku.edu.cn/) (accessed on 10 March 2022), genomic and CDS sequences of TaTLPs genes were used to create an exon/intron map [22]. The conserved motifs in the TUBBY proteins were discovered using the online server MEME 4.11.3 (http://meme-suite.org/tools/meme) (accessed on 10 March 2022) [23].

2.5. Gene Ontology and Cis-Elements Analysis of TUBBY Family Genes

A 1.5 Kb genomic DNA sequence upstream of each identified TaTLP gene’s start codon was obtained from the Ensemble Plants database (http://plants.ensemble.org/Triticum_aestivum) (accessed on 11 March 2022) using the Ensemble Plants search engine (ATG). The online Plant CARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) (accessed on 11 March 2022) database was used to identify cis-regulatory elements for all the TUBBY genes. Ontology analysis of the TaTLP protein sequences was performed using the Blast2GO program Ver.2.7.2 (http://www.blast2go.com) (accessed on 11 March 2022), and the groups of GO classification (molecular functions, biological process, and cellular component) were documented.

2.6. RNA Isolation and cDNA Synthesis

Total RNA was isolated from stress-exposed seedlings at selected time points, including 0 (control) and stress using the RNeasy plant mini kit (Qiagen, Redwood City, CA, USA), as per the manufacturer’s instructions. The quantity and quality of isolated RNA were determined by spectrophotometry (Nanodrop 2000, Thermo Fisher Scientific, Waltham, MA, USA) and formaldehyde-based gel electrophoresis, respectively. For cDNA synthesis,1 µg of total RNA was transcribed in 20 µL using Revert Aid First Strand cDNA Synthesis Kit (Fermentas Life Sciences, Waltham, MA, USA) using oligo (dT)primers as per the manufacturer’s instructions.

2.7. Expression Analysis of Different Genes

To examine the temporal expression patterns of selected genes, qRT-PCR was performed. The qRT-PCR was performed in a CFX-96 Real-time PCR Detection 4 System (Bio-Rad, Hercules, CA, USA). Reactions were conducted in a total volume of 20 pl using 50 ng of cDNA, 10 pmol of forward and reverse primers, and 10 L of 2× Sso Fast Eva GreenqPCR Supermix (Bio-Rad, Hercules, CA, USA). The cycling conditions were as per the manufacturer’s protocol with a primer-specific annealing temperature. The threshold cycle (Ct) was automatically determined for each reaction using the system set with default parameters. The transcript levels were normalized to the actin transcript, and the fold differences of each amplified product in the samples were calculated using the 2-AACt method.

3. Results

3.1. Identification and Analysis of TaTLPs Genes

In the current study, 40 TaTLP proteins from wheat were retrieved using the Ensemble Plants (http://plants.ensemble.org/Triticum_aestivum) (accessed on 11 March 2022) database. The genes were named based on their chromosomal position from TaTLPq1 to TaTLP40 (Table 1). Among these, TaTLP2, TaTLP4, TaTLP5, TALP13, TaTLP16, and TaTLP35 genes were located in the Extracellular region, TaTLP14 and TaTLP24 in the mitochondrial region, and TaTLP23 was located in the chloroplast, while the remaining 31 TaTLPs genes were found in the nucleus (Table 1). More details regarding TaTLPs were also recorded, including Locus ID, Proteins, and Molecular weight.

3.2. Phylogenetic Analysis of TaTLPs

We used the Neighbor-Joining method to construct a phylogenetic tree that included Triticum aestivum, A. thaliana, and O. sativa TLPs to investigate their phylogenetic relationship (Figure 1). The results showed that 40 TaTLPs, 15 OsTLPs, and 14 AtTLPs were clustered and further divided into three families, namely, A, B, and C. Furthermore, Family A was divided into two subfamilies, Family AI and Family AII. Family AI was the largest family containing most TLPs including 18 TaTLPs, (TaTLP1, TaTLP6, TaTLP7, TaTLP9, TaTLP11, TaTLP16, TaTLP17, TaTLP20, TaTLP22, TaTLP25, TaTLP27, TaTLP28, TaTLP29, TaTLP30, TaTLP31, TaTLP38, TaTLP39, TaTLP40), six OsTLPs, and three AtTLPs. The subfamily AII contained 14 TLPs including nine TaTLPs (TaTLP2, TaTLP3, TaTLP4, TaTLP5, TaTLP13, TaTLP14, TaTLP18, TaTLP19, TaTLP21), four OsTLPs, and one AtTLP. Family B was the second-largest family, containing 10 TaTLPs including (TaTLP8, TaTLP10, TaTLP12, TaTLP15, TaTLP23, TaTLP24, TaTLP26, TaTLP33, TaTLP35, TaTLP37), four OsTLPs, and five AtTLPs. Family C was the smallest, containing three TaTLPs, including (TaTLP32, TaTLP34, TaTLP36,) one OsTLP, and two AtTLPs. The results confirmed that the evolutionary relationships of A. thaliana, O. sativa, and Triticum aestivum are closer.

3.3. Conserved Motif Analysis of TaTLPs-Genes

A total of 10 conserved motifs were discovered using the MEME online server, and they were found to be appropriate for explaining the TaTLPs’ structure (Figure 2). Among the 40 TaTLPs genes, TaTLP7, TaTLP9, TaTLP22, TaTLP24, and TaTLP39 contained more than seven TLPs motifs.

3.4. Gene Ontology of TaTLP Genes

For the functional prediction of TaTLP genes, we used gene ontology (GO) enrichment pathway analysis to identify potential pathways. Three different processes were studied and predicted in their functional outcomes: molecular, biological, and cellular (Figure 3). The molecular prediction suggested that TaTLP genes participate in many activities such as signal transduction activity, hydrolase activity, lipid binding, ion binding activity, and cytoskeletal protein binding activity. The biological prediction suggested that TaTLP genes participate in various biological processes such as cellular protein modification, signal transduction, vesicle-mediated transport, anatomical structural development, abiotic stresses, cell differentiation, lipid metabolic process, morphogenesis, and embryo development. The cellular prediction suggested that TaTLP genes are located in the plasma membrane, intracellular, cytoplasm, nucleus, and extracellular region. Based on the results, it is suggested that TaTLP genes play an essential role in plant growth regulation by modulating biological, molecular, and cellular activities.

3.5. Protein-Protein Interaction of TaTLPs

The TaTLP protein prediction analysis revealed various other proteins that predictably interact with TaTLP5 (Figure 4 and Figure 2). Thus, TaTLP5 possibly interacts closely with ATG2G20050, which plays a vital role in signal transduction, ATP binding, metal ion binding, and protein serine phosphatase activity, as highlighted by the bit score. The putative bit score of 0.837 closely interacts with our reference gene TaTLP5, a member of the TUBBY gene family. Similarly, it interacted with ATG2G35680, Phosphotyrosine protein phosphatase superfamily protein, and Possesses phosphate activity. Furthermore, these genes interact with AT3G12370, AT3G10330, pBRP2, AT2G45910, ENDOL9, ATGRIP, AT2G04940, and MLO1. The details are given in Table 2.

3.6. TaTLPs Cis-Regulatory Elements

According to the results of the in-silico analyses of the TaTLP-genes, the upstream region of the TaTLP genes contained 13 hormonal, stress, and growth responsive cis-regulatory elements, six of which were responsive to hormones. Seven of these elements were responsive to stress and growth-related changes (Table 3). The hormone-responsive cis-elements were ABRE, which participates in the abscisic acid responsiveness, TCA (cis-acting element involved in salicylic acid responsiveness), TATC-Box (gibberellin-responsive element), AuxRR-Core (auxin-responsive element), CGTCA (cis-acting regulatory element involved in the MeJA-responsiveness), and TGACG (Cis-acting regulatory element involved in the MeJA-responsiveness). The stress and growth responsive cis-elements were ARE (stimulate mRNA decay), ACE (cis-acting element involved in light responsiveness), G-Box (cis-acting element involved in light responsiveness), LTR (Long-terminal repeat), CAT-Box (Cis-acting element involved in meristem development), O2-Site (Cis-acting regulatory element involved in zein metabolism regulation), and MSA-Like (Cis-acting regulatory element involved in the cell cycle). The presence of these cis-elements in the promoter region of TaTLP genes indicates that they regulate gene expression in response to various environmental stimuli at various stages of development.

3.7. Expression Analysis of TaTLP Genes in Different Wheat Cultivars in Response to Fusarium graminum Stress

The gene expression pattern in different wheat cultivars subjected to Fusarium graminum stress was drawn on the heatmap (Figure 5). The TaTLP7, TaTLP22, TaTLP26, TaTLP27, TaTLP35, and TaTLP36 showed dominant expression in all cultivars compared to other TLPs genes, whereas TaTLP9, TaTLP12, TaTLP20, and TaTLP39 showed dominant expression in annonng0771 and zhongmai66 cultivars as compared to the control and sumai3. The TaTLP6 showed low expression levels in annonng0771 and zhongmai66 cultivars compared to the control and sumai3. The TaTLP6 showed lower expression levels for cultivars annonng0771 and zhongmai66 than the control and sumai3 cultivar, which showed low expression levels. Similarly, TaTLP15 and TaTLP30 showed lower expression levels for cultivar zhongmai66, and in comparison, the control, sumai3, and annonng0771 showed higher expression levels. TaTLP10, TaTLP37, and TaTLP24 displayed higher expression levels for annonng0771 and zhongmai66 cultivars, and lower expression levels were recorded for the control and sumai3. The TaTLP1, and TaTLP2, showed lower expression levels in sumai3 than the control, annonng0771, and zhongmai66 cultivars. The TaTLP4 and TaTLP31 showed high expression levels in the control and sumai3 compared to annonng0771 and zhongmai66 cultivars. Furthermore, TaTLP8, TaTLP23, TaTLP29, TaTLP3, TaTLP25, TaTLP38, TaTLP13 and TaTLP28 displayed high expression levels as compared to TaTLP17, TaTLP18, TaTLP5, TaTLP16, TaTLP33, TaTLP32, TaTLP40, TaTLP19, TaTLP11, TaTLP21, TaTLP14, and TaTLP34 which displayed low expression levels, except for TaTLP19, TaTLP11, and TaTLP21 which showed higher expression levels for annong0711 cultivar under Fusarium graminum stress.

3.8. Expression Analysis of TaTLP Genes in Wheat in Response to Different Temperatures

The gene expression pattern in response to temperature stress was drawn on the heatmap (Figure 6). TaTLP10, TaTLP15, TaTLP28, TaTLP2 TaTLP34, TaTLP24, TaTLP26, TaTLP16, TaTLP30, TaTLP7, TaTLP40, TaTLP20, TaTLP31, TaTLP38, TaTLP22, TaTLP14, and TaTLP17 displayed a high expression level under temperatures of 20 and 30 °C, whereas TaTLP24 and TaTLP22 showed the highest expression levels in comparison to other TaTLP genes. Similarly, TaTLP25 and TaTLP39 showed higher expression levels at 30 °C than under 20 or 40 °C.
The role of TaTLP proteins in response to temperature stress is of great interest. To reveal the potential role of TaTLP genes in response to temperature stress, we used qRT-PCR to detect TaTLP expression levels for 0, 3, and 6 h stress at 40 °C (Figure 7). TaTLP genes were found to respond positively to temperature stress. For example, TaTLP1, TaTLP 2, TaTLP6, TaTLP8, and TaTLP15 expression increased at 3 and 6 h temperature stress, indicating that these genes are stress responsive in wheat. Further, TaTLP3, TaTLP12, TaTLP16, and TaTLP32 expression significantly decreased under high-temperature stress. TaTLP4, TaTLP5, TaTLP10. TaTLP17, TaTLP34, and TaTLP36 expression decreased under 3 h temperature stress, and, as temperature stress increased, the expression levels of these genes significantly increased.

3.9. Expression Analysis of TaTLP Genes in Wheat Subjected to Hormonal Treatment

The heatmap analysis showed different expression patterns under various hormonal treatments. TaTLP11, TaTLP2, TaTLP9, TaTLP12, TaTLP34, TaTLP13, TaTLP35, TaTLP30, TaTLP22, TaTLP23, TaTLP29, TaTLP10, TaTLP4, TaTLP37 TaTLP3 TaTLP19, TaTLP38, and TaTLP17 showed high levels of expression in comparison to other TATLP genes under control (CK) and a similar expression patterns were observed for ABA (abscisic acid) treatment, whereas TaTLP11, TaTLP2, TaTLP9, and TaTLP34 showed the highest expression level under CK and ABA treatments (Figure 8). Furthermore, TaTLP40, TaTLP11, TaTLP2, TaTLP9, TaTLP12, TaTLP34, TaTLP13, TaTLP35, TaTLP30, TaTLP22, TaTLP23, TaTLP3 TaTLP19, TaTLP38, TaTLP17, TaTLP1, and TaTLP27 showed a high expression level under GA (gibberellic acid) treatment as compared to other TLP genes. The expression pattern of TaTLP genes in response to the combination of ABA and FG (Fusarium graminum) treatment showed a similar expression pattern as that of GA treatment. The expression pattern of TaTLP genes in response to the combination of GA and FG was different; for example, TaTLP16, TaTLP25, TaTLP7, TaTLP15, TaTLP11, TaTLP12, TaTLP34, TaTLP13, TaTLP35, TaTLP22, TaTLP23, TaTLP37, TaTLP19, TaTLP38, TaTLP17, TaTLP1, and TaTLP27 displayed high expression levels as compared to other TLP genes.

3.10. Expression Analysis of TaTLP Genes in Wheat in Response to Iron Deficiency Stress

The heatmap analysis showed varying expression patterns under iron deficiency conditions in roots and leaf tissues, as shown in Figure 9. TaTLP7, TaTLP17, TaTLP24, TaTLP16, TaTLP22, TaTLP2, TaTLP7, TaTLP710, TaTLP7,14, TaTLP720, TaTLP32, TaTLP35, and TaTLP39 displayed the highest expressions levels as compared to other TLP genes in root-control and root low-Fe conditions, whereas TaTLP26 showed high expression as compared to root-control. The remaining TLP genes’ expression levels were unaffected under root low-Fe conditions. Similarly, TaTLP7, TaTLP17, TaTLP24, TaTLP16, TaTLP22, TaTLP10, TaTLP14, and TaTLP20 showed high expression levels as compared to other TLPSs, but similar expression levels between leaf-control and leaf low-Fe conditions. TaTLP34 showed a high expression level under the leaf low-Fe condition, whereas TaTLP40 and TaTLP1 showed a high expression level in leaf-control compared to the leaf low-Fe condition. The remaining TLP gene expression levels were unaffected under leaf low-Fe conditions.

3.11. Expression Analysis of TaTLP Genes in Different Wheat Tissues

To further study the responses of TaTLP genes against biotic and abiotic stresses, we used qRT-PCR to analyze the expression patterns in various wheat tissues (Figure 10). The results showed that TaTLPs were expressed in different tissues. The TaTLP1 transcript level showed high expression in the leaf compared to other tissues. TaTLP6 and TaTLP16 showed significantly high expression levels in the root, leaf, and spikelet. TaTLP17 and TaTLP6 showed significantly high expression in the stem and leaf, respectively.
Similarly, TaTLP3 and TaTLP4 showed significantly high expression levels in leaf, stem, and spikelet tissues. TaTLP5 was highly expressed in the leaf and stem compared to other tissues, whereas TaTLP8 expression level was higher in the leaf. TaTLP10 was expressed in almost all tissues, and the TaTLP12 expression level was much higher in spikelets than in other tissues. TaTLP15 and TaTLP32 were expressed in all tissues, and the expression level was significantly high in the stem and leaf, respectively. TaTLP34 showed significantly high expression levels in spikelets. TaTLP36 showed a high expression level in the root, stem, and spikelet. The various TaTLPs were expressed in different tissues at varying levels, indicating that they may play a significant role in wheat against various biotic and abiotic stresses.

4. Discussion

Plants contend with various environmental conditions throughout their life cycle that may interfere with their development. TaTLP genes are members of a gene family found in multiple animals. Plants have a smaller number of functionally studied TLPs than animals. TLPs have only been discovered in a few plant species, including Arabidopsis [13], rice [7], maize [10], Solanum lycopersicum [11], and cotton [12]. This study found 40 genes encoding TLP proteins in wheat, which is higher than the numbers found in other plants: 11 in Arabidopsis, 14 in rice, and 15 in maize. This research will advance the knowledge and understanding of their functional characteristics in the future.

4.1. TaTLP Genes Are Distributed Widely in the Wheat Genome

The hexaploid wheat, created by crossing Triticum and Aegilops, is a valuable tool for studying allopolyploidization evolution [24]. An analysis of the phylogenetic tree (Figure 1) shows that the TaTLPs are clustered and divided into three large subfamilies: A, B, and C. The A subfamily has two groups: AI and AII. This grouping matches previous S. lycopersicum reports [8,10,11]. The TLPs within each subfamily share a high degree of homology and have evolved close to one another [25]. Interestingly, we found that TLPs possess the F-box domain related to plant stress resistance [13,26,27]. This finding suggests that TLPs in wheat are highly conserved and may have additional functions, as demonstrated in Figure 3.

4.2. TaTLP Genes Are Thought to Be Involved in Critical Biological and Molecular Processes

The GO analysis revealed that TaTLP genes perform a wide range of biological, molecular, and cellular functions (Figure 3). Many genes are directly involved in cell wall biosynthesis, which is the first line of defense against abiotic and biotic factors [28]. The TUBBY gene family appears to be essential for wheat plant growth in both normal and stressful conditions. Trans-acting elements are required for any biological or molecular process in plants. Multiple signaling pathways regulate plant stress responses, and there is much overlap between the gene expression patterns induced by different stresses [29,30,31]. Several transcription factors influence the expression of stress-related genes in plants. Several closely related transcription factors can frequently activate or repress genes via cis-acting sequences in response to specific stresses [14,32]. In our study, many hormones (ABRE, TCA, TATC-BOX, AUXRR-Core, CGTCA, and TGACG), stress, and growth-related (ARE, ACE, G-Box, LTR, CAT-Box, O2-Site, MSA-Like) cis-elements were identified in the promoter region of TaTLP genes (Table 3). These elements are primarily involved in drought, low-temperature, and hormone responses [33,34].
The CGTCA and TGACG motif were found in nearly all TLP promoters, indicating that they were associated with the jasmonate acid response in most cases. Also found in most TLP promoters where the enzymes ARE (associated with anaerobic reaction) and ABRE (associated with ABA response) [7,8,13,25]. Based on these results, we suggest that TaTLPs may play an essential role in stress responses, but this needs further experimental verification. The PPI analysis demonstrated that TaTLPs interact with other essential proteins, such as ATG2G20050, which play an indispensable role in signal transduction, ATP binding, metal ion binding, and protein serine phosphatase activity. Similarly, the TLP gene interacted with ATG2G35680, AT3G12370, AT3G10330, pBRP2, AT2G45910, ENDOL9, ATGRIP, AT2G04940, and MLO1 (Table 2 and Figure 4).
Plant TLP gene families have been previously studied, and it has been discovered that multiple TLP genes are involved in the responses of plants to biological and abiotic stresses [7,8,10,11,12,13]. According to this, TLP genes can be used as candidate genes in plant resistance breeding.

4.3. TaTLP Genes Control Plant Response to Hormones and Abiotic and Biotic Stresses

To further investigate the response of TaTLPs to abiotic stress, the expression patterns of 40 putative TaTLPs in wheat were determined using a heatmap analysis and confirmed through qRT-PCR to analyze the expression patterns in various tissues and under temperature stress (Figure 7 and Figure 10). TaTLP genes were induced to varying degrees under multiple conditions, including high temperature, GA, exogenous ABA, and low iron deficiency stress. Due to their immobility, plants face abiotic stresses. Abiotic stresses can significantly reduce crop yields by impeding their physiological and biochemical processes [35,36]. Modern research breakthroughs have relied heavily on understanding the impact of changing climate. The underlying mechanism in systematic temporal variation is complex and challenging to comprehend. Our current results showed that many TaTLP genes, such as TaTLP16, TaTLP20, TaTLP22, and TaTLP24, displayed upregulated expression patterns under different degrees of temperature stress. The findings of this study are consistent with those of previous studies [11,12,25]. GA is a plant hormone involved in seed germination, phase transition, flowering, fruit, and grain development [37,38,39]. Here, TaTLP40, TaTLP11, TaTLP2, TaTLP9, TaTLP12, TaTLP34, TaTLP13, TaTLP35, TaTLP30, TaTLP22, TaTLP23, TaTLP3 TaTLP19, TaTLP38, TaTLP17, TaTLP1, and TaTLP27 showed higher expression levels under GA treatment (Figure 8). Our findings suggest that genes may be involved in GA-mediated plant growth activities, but more research is needed. Most TaTLP genes showed a decrease in expression in response to ABA, FG, and a combination of these factors, in addition to low iron deficiency stress.

5. Conclusions

This study identified and analyzed 40 TLPs in wheat (Triticum aestivum L.). We performed a comprehensive analysis of TaTLPs that included gene identification, phylogenetic analysis, chromosomal location, protein–protein interactions, cis-regulatory elements, and expression analysis. Forty TaTLPs were identified and classified into three subfamilies based on their domain and structural characteristics. A heatmap analysis revealed the expression of TaTLPs in different cultivars in response to biotic and hormonal stress. The qRT-PCR analysis showed that the expression patterns under high temperature and in various wheat tissues were significantly high, suggesting that these genes may play a role in wheat resistance mediation. Stress regulation is also a complicated mechanism to comprehend. The in-silico analysis provided valuable information for future functional stress biology studies. More research is needed to fully understand the regulation and pathways of the mechanism of TaTLPs in wheat.

Author Contributions

Conceptualization, formal analysis, investigation, methodology, software, validation, visualization, writing—original draft, A.A.; investigation, formal analysis, software, validation, writing—review and editing, A.Z.; writing—review and editing, S.H.; writing—review and editing, S.G.; writing—review and editing, Y.D.; writing—review and editing, R.T.; conceptualization, methodology, resources, supervision, writing—review and editing, M.Z.; conceptualization, funding acquisition, methodology, project administration, supervision, writing—review and editing, X.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work was jointly supported by the earmarked fund for Jiangsu Agricultural Industry Technology System (JATS[2021]503), the Postgraduate Research & Practice Innovation Program of Jiangsu Province (XKYCX20_020), the National Key Research and Development Program of China (2018YFD0200500), the National Natural Science Foundation of China (31901433, 31771711), Jiangsu Modern Agricultural (Wheat) Industry Technology System, Pilot Projects of the Central Cooperative Extension Program for Major Agricultural Technologies, The Priority Academic Program Development of Jiangsu Higher Education Institutions, and The Science and Technology Innovation Team of Yangzhou University, Yangzhou, China.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 01121 g001 550
Figure 1. TLPs protein phylogeny in three plants: T. aestivum, A. thaliana, and O. sativa. MEGA 7 was used to generate the phylogenetic tree using the following parameters: Bootstrap D 1000 replicates, Neighbor-Joining method, Poisson correction. All group members are divided into four groups, each represented by an assorted color. Different labels are used to identify members of various species.
Figure 1. TLPs protein phylogeny in three plants: T. aestivum, A. thaliana, and O. sativa. MEGA 7 was used to generate the phylogenetic tree using the following parameters: Bootstrap D 1000 replicates, Neighbor-Joining method, Poisson correction. All group members are divided into four groups, each represented by an assorted color. Different labels are used to identify members of various species.
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Figure 2. The TaTLPs genes’ conserved motifs.
Figure 2. The TaTLPs genes’ conserved motifs.
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Figure 3. TaTLP gene GO enrichment analysis shows molecular function, biological process, and cellular component data.
Figure 3. TaTLP gene GO enrichment analysis shows molecular function, biological process, and cellular component data.
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Figure 4. The predicted functional partners of TaTLP protein.
Figure 4. The predicted functional partners of TaTLP protein.
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Figure 5. Heatmap representing expression analysis of TaTLP genes in different wheat cultivars subjected to Fusarium graminum stress.
Figure 5. Heatmap representing expression analysis of TaTLP genes in different wheat cultivars subjected to Fusarium graminum stress.
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Figure 6. Heatmap representing expression analysis of TaTLP genes in wheat subjected to different temperatures.
Figure 6. Heatmap representing expression analysis of TaTLP genes in wheat subjected to different temperatures.
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Figure 7. Expression analysis of TaTLP genes under high temperature at different time points.
Figure 7. Expression analysis of TaTLP genes under high temperature at different time points.
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Figure 8. Heatmap represents expression analysis of TaTLP genes in wheat subjected to hormonal treatment and hormones + Fusarium graminum. ABA (abscisic acid), GA (gibberellic acid), ABA+FG (abscisic acid + Fusarium graminum), GA + FG (gibberellic acid + Fusarium graminum).
Figure 8. Heatmap represents expression analysis of TaTLP genes in wheat subjected to hormonal treatment and hormones + Fusarium graminum. ABA (abscisic acid), GA (gibberellic acid), ABA+FG (abscisic acid + Fusarium graminum), GA + FG (gibberellic acid + Fusarium graminum).
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Figure 9. Heatmap representing expression analysis of TaTLP genes in wheat under iron deficiency stress.
Figure 9. Heatmap representing expression analysis of TaTLP genes in wheat under iron deficiency stress.
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Figure 10. Expression analysis of TaTLP genes in different tissues of wheat.
Figure 10. Expression analysis of TaTLP genes in different tissues of wheat.
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Table
Table 1. The gene features of the wheat TUBBY gene family.
Table 1. The gene features of the wheat TUBBY gene family.
Gene NameLocus IDProteinsMWPISL
TaTLP1Traes_1AL_399C1DBF5269--N
TaTLP2Traes_1AL_45AB9EF3424727,640.249.22EC
TaTLP3Traes_1BL_BDF2FCEC717519,434.989.08N
TaTLP4Traes_1DL_106460E68505544.559.42EC
TaTLP5Traes_1DL_9DE76F00425127,986.789.16EC
TaTLP6Traes_1DL_FAB39637420422,671.219.80N
TaTLP7Traes_2AL_436D234EE47152,097.909.28N
TaTLP8Traes_2AS_11876C29820322,666.819.14N
TaTLP9Traes_2BL_181C4AA2847252,073.749.22N
TaTLP10Traes_2BS_9DCC9CC7A20322,657.809.14N
TaTLP11Traes_2DL_79449BF6D34738,850.309.73N
TaTLP12Traes_2DS_AC89AEF3620322,661.799.14N
TaTLP13Traes_3AL_108550E2812614,455.708.34EC
TaTLP14Traes_3AL_731AE8008606858.8610.08M
TaTLP15Traes_3AL_9B4AF995015217,297.979.37N
TaTLP16Traes_3AL_C3AEDD333829123.3410.72EC
TaTLP17Traes_3B_021E89FE5377--N
TaTLP18Traes_3B_02CE04534119422,052.959.33N
TaTLP19Traes_3B_C967E97B918020,367.299.30N
TaTLP20Traes_3DL_697C6F11721123,933.519.69N
TaTLP21Traes_3DL_C81B58D9827931,811.579.63EC
TaTLP22Traes_4AL_EDE23697844048,793.989.39N
TaTLP23Traes_4AS_0C854209940244,497.049.43C
TaTLP24Traes_4BL_7E9BC637F55961,782.429.73M
TaTLP25Traes_4BS_D5B5C14F644048,817.029.39N
TaTLP26Traes_4DL_7D905B6BC40444,726.349.29C
TaTLP27Traes_4DS_620432A0D44048,833.029.39N
TaTLP28Traes_5AL_83533B97D36140,470.049.54N
TaTLP29Traes_5AL_D38708404647023.984.75N
TaTLP30Traes_5BL_ECCAFFEB444049,017.869.34N
TaTLP31Traes_5DL_FA0200E1343948,856.729.25N
TaTLP32Traes_6AL_058D829C3374--N
TaTLP33Traes_6AS_FB1249AB432135,747.879.70N
TaTLP34Traes_6BL_9F6ACF02D32235,555.869.39N
TaTLP35Traes_6BS_5C281F30317720,314.479.98EC
TaTLP36Traes_6DL_E7A7DAE5C36840,756.929.26N
TaTLP37Traes_6DS_D6AD8C3ED17720,355.529.98N
TaTLP38Traes_7AL_52F3AE87C37341,569.329.80N
TaTLP39Traes_7BL_8312EAB48441--N
TaTLP40Traes_7DL_037F2A4F423826,443.419.69N
CDS: Coding Sequence, MW: Molecular Weight, SL: Sub Cellular Location, EC: Extracellular, N: Nuclear, PM: Plasma membrane, C: Chloroplast.
Table
Table 2. Different predicted protein families interacted with TaTLP genes.
Table 2. Different predicted protein families interacted with TaTLP genes.
Gene NameProtein FamilyPutative Function Interactive-Bit Score
ATG2G20050Protein phosphatase 2C and cyclic nucleotide-bindingSignal transduction, ATP binding, metal ion binding, protein serine phosphatase activity0.837
ATG2G35680Phosphotyrosine protein phosphatase superfamily proteinPossess phosphate activity0.698
AT3G12370EMB3136—Ribosomal protein L10 family proteinThe function is a structural protein0.691
AT3G10330Cyclin-like family proteinDNA-templated transcription, initiation, transcription preinitiation complex assembly0.637
pBRP2Plant-specific TFIIB-related protein 2Regulation of endosperm proliferation, DNA-templated transcription, initiation0.637
AT2G45910U-box domain-containing protein kinase family proteinCellular response to oxygen-containing compound, defense response to the bacterium, flower development, 0.633
ENDOL9Early nodulin-like protein 9electron carrier activity0.623
ATGRIPGolgi-localized grip domain-containing proteinInvolved in Golgi protein trafficking. AtARL1 binds directly to the GRIP domain of AtGRIP in a GTP-dependent manner.0.616
AT2G04940scramblase-like proteinplasma membrane phospholipid scrambling0.603
MLO1Transmembrane domain proteinbarely mildew resistance0.588
Table
Table 3. Analysis of the diverse types and numbers of cis-acting regulatory elements involved in growth, development, stress, and hormonal response.
Table 3. Analysis of the diverse types and numbers of cis-acting regulatory elements involved in growth, development, stress, and hormonal response.
CategoryCis-ElementsAnnotations
HormoneABRECis-acting element involved in the abscisic acid responsiveness.
TCACis-acting element involved in salicylic acid responsiveness.
TATC-BoxGibberellin-responsive element.
AuxRR-CoreAuxin-responsive element.
CGTCACis-acting regulatory element involved in the MeJA-responsiveness.
TGACGCis-acting regulatory element involved in the MeJA-responsiveness.
Stress and GrowthAREStimulate mRNA decay.
ACECis-acting element involved in light responsiveness.
G-BoxCis-acting element involved in light responsiveness.
LTRLong-terminal repeat.
CAT-BoxCis-acting element involved in meristem development.
O2-SiteCis-acting regulatory element involved in zein metabolism regulation.
MSA-LikeCis-acting regulatory element involved in the cell cycle.
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Altaf, A.; Zada, A.; Hussain, S.; Gull, S.; Ding, Y.; Tao, R.; Zhu, M.; Zhu, X. Genome-Wide Identification, Characterization, and Expression Analysis of TUBBY Gene Family in Wheat (Triticum aestivum L.) under Biotic and Abiotic Stresses. Agronomy 2022, 12, 1121. https://doi.org/10.3390/agronomy12051121

AMA Style

Altaf A, Zada A, Hussain S, Gull S, Ding Y, Tao R, Zhu M, Zhu X. Genome-Wide Identification, Characterization, and Expression Analysis of TUBBY Gene Family in Wheat (Triticum aestivum L.) under Biotic and Abiotic Stresses. Agronomy. 2022; 12(5):1121. https://doi.org/10.3390/agronomy12051121

Chicago/Turabian Style

Altaf, Adil, Ahmad Zada, Shahid Hussain, Sadia Gull, Yonggang Ding, Rongrong Tao, Min Zhu, and Xinkai Zhu. 2022. "Genome-Wide Identification, Characterization, and Expression Analysis of TUBBY Gene Family in Wheat (Triticum aestivum L.) under Biotic and Abiotic Stresses" Agronomy 12, no. 5: 1121. https://doi.org/10.3390/agronomy12051121

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