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Article

Exploring the Roles of TALE Gene Family in Maize Drought Stress Responses

by
Buxuan Qian
1,2,†,
Qi Wang
1,†,
Chuang Zhang
1,
Jia Guo
1,
Zhijia Yu
1,3,
Jiarui Han
1,3,
Hanchao Xia
1,2,
Rengui Zhao
2,* and
Yuejia Yin
1,*
1
Institute of Agricultural Biotechnology, Jilin Academy of Agricultural Sciences (Northeast Agricultural Research Center of China), Changchun 130033, China
2
College of Agronomy, Jilin Agricultural University, Changchun 130118, China
3
Agricultural College, Yanbian University, Yanji 133000, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(6), 1267; https://doi.org/10.3390/agronomy14061267
Submission received: 15 April 2024 / Revised: 15 May 2024 / Accepted: 24 May 2024 / Published: 12 June 2024
(This article belongs to the Section Crop Breeding and Genetics)
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Versions Notes

Abstract

:
The TALE gene family plays a crucial role in regulating growth, development, and abiotic stress responses in plants. However, limited studies have been conducted on the functions of the ZmTALE gene family in maize under drought stress. This study identified 40 members of the ZmTALE family within the maize genome through Blast comparisons, distributed unevenly across the first nine chromosomes. Intraspecific collinearity analysis revealed 13 linked pairs. By constructing a phylogenetic tree with Arabidopsis AtTALE members as references, maize members were divided into two subfamilies, KNOX and BEL1-Like, with KNOX further divided into three branches (KNOX Class I, KNOX Class II, and KNOX Class III). The gene structure and motifs of ZmTALE genes within the same subfamily or branch showed similarities, as did their encoded proteins, which possess similar motifs and conserved domains. Analysis of the physicochemical properties of the ZmTALE proteins revealed that the proteins encoded by this family are stable. Expression analysis of ZmTALE genes in maize demonstrated their varied roles in development and drought stress regulation, confirmed through qRT-PCR. The identification, characterization, and expression analysis of ZmTALE genes provide a reference for future gene function research and aid in the genetic enhancement of maize to withstand drought stress.

1. Introduction

The Three Amino acid Loop Extension (TALE) gene family is a distinctive subgroup within the vast landscape of transcription factor superfamilies, notable for its unique 60-amino-acid helix-turn-helix DNA-binding motif that signifies its members’ shared homeodomain (HD) [1]. This conserved structure is a hallmark of the TALE gene family, underscoring its crucial role in the regulation of gene expression through DNA interaction. In eukaryotic organisms, the functional diversity and specialization of the TALE family are further enriched by the integration of the HD with various other structural domains. This integration not only amplifies the functional repertoire of the TALE family members but also aids in their classification into distinct gene families, each characterized by unique structural and functional attributes.
Among these families, HD-Zip, WOX, BELL, KNOX, and SAWADD stand out, each delineated by specific domain configurations that reflect their evolutionary adaptations and functional specializations [2]. The KNOX and BELL families, in particular, exhibit a distinguishing feature within the TALE superfamily—the presence of a homeobox region augmented by an additional three amino acids. This modification introduces a loop structure, aptly named the TALE homeobox domain, which is a critical determinant of their DNA-binding specificity and functional capabilities [3]. This distinctive loop extension within the homeobox domain is not merely a structural peculiarity but a functional innovation that enhances the DNA-binding efficacy and specificity of the KNOX and BELL families, enabling them to execute a wide array of regulatory roles in growth and developmental processes [4].
The KNOX subfamily is meticulously categorized into three classes, each distinguished by specific members and their unique roles within Arabidopsis, a model organism for plant biology research. These KNOX subfamily members are characterized by a signature composition of four domains—KNOX1, KNOX2, ELK, and the KN homeodomain—which together facilitate their critical regulatory functions. Class I of the KNOX subfamily includes AtKNAT1, AtKNAT2, AtKNAT6, and AtSTM, proteins that are integral to the foundational processes governing the shoot apical meristem (SAM) and leaf development [5,6,7,8]. For example, KNAT1 and KNAT2 not only play pivotal roles in the developmental intricacies of Arabidopsis leaves but are also involved in the morphogenesis of male flowers, illustrating the multifaceted nature of their regulatory capabilities [9,10]. Class II, comprising AtKNAT3, AtKNAT4, AtKNAT5, and AtKNAT7, alongside Class III’s sole member AtKNATM, further expand the functional repertoire of the KNOX subfamily [11]. These proteins are intricately involved in various aspects of plant development, from the formation of ovule structures, as seen with KNAT3 and KNAT4’s co-expression in inflorescences, to the significant influence of KNATM on leaf morphology and flowering time. This detailed classification underlines the complexity and specificity with which KNOX proteins contribute to plant developmental processes [12,13,14].
Parallel to the KNOX subfamily, the BELL-like subfamily underscores similar themes of specialization and functional importance in plant development. In rice, a critical staple crop, the BELL1-like transcription factor RI plays a crucial role in normal panicle formation and the establishment of apical meristems [15]. This function is mirrored in the developmental processes of other species, such as pomegranate, where interactions between BELL1, INO, and CRC are indispensable for ovule and seed development. These interactions not only highlight the conserved nature of BELL-like functions across species but also emphasize the integral role of these transcription factors in reproductive organ development and the intricate web of gene regulation that underpins plant morphology and fertility [16].
Expanding the understanding of the TALE superfamily’s functionality, recent research has unveiled a significant extension of their roles beyond the foundational processes of plant growth and development. This exploration into the adaptive mechanisms of plants under environmental pressures has spotlighted the TALE superfamily members as key players in the response to abiotic stresses. In an illustrative study, Yang et al. [17]. embarked on an in-depth examination of the TALE family within plum, a species whose agricultural value and stress resilience are of keen interest. Through their comprehensive analysis, they identified 23 TALE family members, each bearing abiotic stress-responsive elements within their promoter regions. This finding was not just structural but functional; transcriptomic analyses provided concrete evidence of these genes’ responsiveness to a variety of abiotic stresses and hormonal cues. Such responsiveness suggests a sophisticated regulatory network wherein TALE family members mediate plant responses to environmental challenges, enhancing survival and adaptation. Echoing these findings, He et al. [18]. ventured into the tomato genome, focusing on the BEL1-Like subfamily, a significant branch of the TALE superfamily. Their research unearthed cis-elements within the promoter regions of these genes, directly linked to stress responses. The functional analyses underscored the subfamily’s reactivity to extreme temperature fluctuations as well as to drought stresses. This reactivity signifies an intrinsic mechanism through which plants can modulate their gene expression in response to varying environmental conditions, offering a glimpse into the genetic flexibility and resilience that characterize plant survival strategies. Further extending the scope of TALE superfamily research, Wang et al. [11]. identified and analyzed GmTALE genes in soybean, a crop of immense global nutritional and economic value. Through a combination of transcriptomic data and qRT-PCR analyses, they validated the responsiveness of certain GmTALE members to abiotic stress conditions and hormonal signals. This validation not only reinforces the notion of TALE family members as crucial regulatory nodes in stress response pathways but also highlights the potential for leveraging this understanding towards the development of stress-resistant crop varieties. The collective insights from these studies illuminate the TALE superfamily’s intricate involvement in plant responses to abiotic stresses.
With environmental degradation posing increasingly severe challenges to maize growth, the rapid advancement of whole-genome sequencing technologies has facilitated the association of numerous gene families, such as NAC, AP2/ERF, WRKY, and ARM, with stress resilience [19,20,21,22]. However, comprehensive reports on the ZmTALE family’s role in adversity remain scarce. In this study, we identified 40 members of the ZmTALE superfamily in maize, examining their phylogenetic relationships, gene structures, motif compositions, conserved domain patterns, chromosomal distributions, and gene duplication events. Analysis of publicly available transcriptomic data revealed that a majority of ZmTALE members in maize respond to drought stress. Subsequently, representative genes from different ZmTALE subfamilies or branches were selected for qRT-PCR analysis. Our comprehensive examination of the ZmTALE family members under stress conditions lays a foundation for future functional studies of ZmTALE genes, facilitating their potential application in enhancing stress tolerance in crops.

2. Materials and Methods

2.1. Plant Materials and Stress Treatment Procedures

In this study, self-pollinating B73 maize seedlings were grown under controlled greenhouse conditions, maintaining a temperature of 25 °C and a light/dark cycle of 16/8 h. To induce drought stress, maize plants at the three-leaf stage were irrigated with a 15% PEG6000 solution. Leaf samples were collected from the first third segment of the third leaf of maize seedlings at 0, 6, 12, and 24 h after treatment. After the treatment, the third leaf from each selected plant was quickly harvested and immediately flash-frozen in liquid nitrogen, setting the stage for further RNA extraction processes.

2.2. TALE Family Member Identification in Maize

For the identification of TALE family members within maize, the first step involved downloading the maize genome and its annotation files (Zm-B73-REFERENCE-NAM-5.0 https://plants.ensembl.org/Zea_mays/Info/Index, accessed on 11 December 2023) from the Ensembl plants database (plants.ensembl.org). Concurrently, the protein sequences of the AtTALE family in Arabidopsis thaliana were obtained from the same database. Utilizing the AtTALE sequences as query inputs, a BLAST search was performed against the maize genome with an E-value cutoff of 1 × 10−5 using TBtools software (V2.095). This approach facilitated the retrieval of ZmTALE family protein sequences in maize. Following this, the identified ZmTALE protein sequences underwent a conserved domain search using the NCBI Conserved Domain Database (https://www.ncbi.nlm.nih.gov/cdd/?term=, (accessed on 15 December 2023)). Protein sequences missing TALE-related domains, namely those without the POX, Homeobox_KN, Homeodomain, KNOX2, KNOX1, and ELK domains, were eliminated from the dataset. In the final step, the molecular weight (MW), isoelectric point (pI), and amino acid count (aa) of the maize ZmTALE members’ protein sequences were analyzed via the Expasy website (https://web.expasy.org/protparam/, accessed on 16 December 2023). Predicting subcellular localization was conducted using an online website (https://wolfpsort.hgc.jp/, (accessed on 12 May 2024)).

2.3. Phylogenetic Analysis and Categorization of ZmTALE Family Members

To analyze and classify TALE family members from maize and Arabidopsis thaliana, we aligned their protein sequences using the ClustalW algorithm provided by MEGA7 software. Subsequent to the sequence alignment, the results were utilized to construct a phylogenetic tree using the Neighbor-Joining (NJ) method, with an emphasis on robustness achieved through 1000 bootstrap replications. The established classification framework for TALE genes in Arabidopsis served as the benchmark for the systematic categorization of the maize TALE family members.

2.4. Structural and Motif Analysis of ZmTALE Family Genes

For the analysis of gene structures and the identification of conserved motifs among ZmTALE family members, we utilized the MEME Suite version 1.1, available online at (http://meme-suite.org/tools/meme, (accessed on 15 December 2023)). The tool was set to detect up to 10 conserved motifs by adjusting the number of motifs to 10. After identifying these motifs, we employed TBtools for the effective visualization of the motifs identified by MEME. The visualization results were then enhanced for clarity and visual appeal using Adobe Illustrator CC 2022, ensuring that the final images met the high standards required for scientific publication.

2.5. Chromosomal Localisation of the Maize ZmTALE Gene

For the chromosomal positioning of ZmTALE family members within maize, we first calculated the genetic interval densities at 350 kb from the maize gene annotation files. These data were then converted into gradient-colored heatmaps to represent the chromosomal distribution across maize chromosomes. Utilizing TBtools, we displayed the precise chromosomal locations of the ZmTALE genes. These locational data were further merged with the genetic density maps through the application of Adobe Illustrator CC 2022, achieving a comprehensive and visually appealing depiction of ZmTALE genes’ chromosomal localization.

2.6. ZmTALE Gene Collinearity Analysis within the Maize Genome

The analysis of homologous relationships between ZmTALE genes in the maize B73 strain was conducted using the MCScanX tool to explore gene duplication events documented in the maize B73-V5 genome sequence and annotations. Following this, we utilized TBTools to create a diagram representing the intraspecific collinearity among ZmTALE genes. To quantify the evolutionary dynamics of these duplication events, the Simple Ka/Ks Calculator in TBTools was applied to calculate the Ka and Ks parameters, thereby estimating the Ka/Ks ratio, which reflects the balance between neutral, deleterious, and advantageous mutations at the protein level.

2.7. Expression Analysis of ZmTALE Family Genes

The transcriptomic data of maize ZmTALE genes in various tissues, including stamens, embryos, endosperms, unpollinated internodes, unpollinated leaves, pollinated internodes, pollinated leaves, female spikelet filaments, stems, meristematic tissues, complete root systems, and entire seeds, were analyzed using the qTeller tool on MaizeGDB (https://qteller.maizegdb.org/, (accessed on 25 February 2024)), utilizing RNA-Seq data from Kakumanu et al. [23]. In the same manner, the transcriptional expression levels of the maize ZmTALE genes at 6 h and 24 h during drought stress were analyzed using the RNA-Seq data on maize subjected to drought stress treatments by Opitz et al. [24]. Plant RNA was extracted using the Ultrapure RNA Kit (CW Bio, Taizhou, China). The quality of the extracted RNA was verified through electrophoresis, followed by quantification with the NanoDrop ND-2000 Spectrophotometer (Thermo Science, Wilmington, DE, USA). The total RNA was then converted to cDNA using the TransScript® One-Step gDNA Removal and cDNA Synthesis SuperMix (TransGen Biotech, Beijing, China). To investigate the expression patterns of maize ZmTALE genes under drought stress, eight representative ZmTALE genes were randomly selected for qRT-PCR analysis. Specific primers were designed using NCBI’s primer-BLAST (https://blast.ncbi.nlm.nih.gov/Blast.cgi, (accessed on 20 March 2024)). Real-time quantitative PCR was conducted using SYBR™ Green PCR Universal Master Mix (Thermo Fisher Scientific, Guangzhou, China) on the StepOnePlus™ Real-Time PCR System (StepOnePlus™, Thermo Fisher Scientific, CA, USA). Each cDNA sample was subjected to three technical replicates, and the results were analyzed using Relative Quantification (RQ). Finally, the results were subjected to t-tests using GraphPad Prism9 software.

3. Results

3.1. Identification of the ZmTALE Family in Maize

In our quest to identify members of the ZmTALE family in maize, we conducted a BLAST search against the maize genome Zm-B73-REFERENCE-NAM-5.0 using the AtTALE family members from Arabidopsis thaliana as queries. Through detailed screening, we successfully identified 40 ZmTALE gene members within the maize genome, which were subsequently named ZmTALE1 through ZmTALE40 based on their gene loci (Table S1).

3.2. Analysis of Physicochemical Properties of Proteins Encoded by the ZmTALE Gene Family

The physicochemical properties of the proteins encoded by the ZmTALE gene family were thoroughly analyzed through protein parameter calculations (Table 1). This analysis revealed that the amino acid lengths of the encoded proteins range from 93 to 755, and their theoretical isoelectric points vary between pH 4.59 and 9.24. Predominantly, these ZmTALE encoded proteins are acidic, with a minority (nine proteins) being basic. The proteins’ molecular weights span from 1.05 to 7.92 kDa. Furthermore, the aliphatic indexes, which provide insights into protein stability, were found to lie between 62.07 and 104.07, suggesting high stability. The Grand Average of Hydropathicity (GRAVY) values range from −0.038 to −0.762, indicating a universal hydrophilic nature (GRAVY < 0) and implying good aqueous solubility. With all aliphatic indexes exceeding 50, it is deduced that the proteins encoded by the ZmTALE family are notably stable. The predicted subcellular localization of the maize ZmTALE gene shows diversity, covering multiple locations such as the nucleus, cytoplasm, endoplasmic reticulum, chloroplasts, and mitochondria. However, the vast majority of the predicted localizations of the genes were focused on the nucleus.

3.3. Distribution of ZmTALE Genes across Chromosomes

The analysis of chromosomal localization demonstrates that ZmTALE genes are not uniformly distributed, being found on the first nine chromosomes, as well as on scaffold_110 and scaffold_186. Remarkably, chromosome 1 contains the highest number of these genes, totaling 14, whereas scaffold_110 and scaffold_186 each have only a single gene. It was observed that the quantity of ZmTALE genes does not significantly correlate with the lengths of the chromosomes or scaffolds. A color gradient was applied to visualize the gene density across different maize chromosomes and scaffolds, based on the number of genes within 350 kb genetic intervals. It is interesting to note that most identified ZmTALE genes are found to congregate in regions characterized by a higher density of genes (Figure 1).

3.4. Phylogenetic Division and Classification of ZmTALE Family Members

Construct a phylogenetic tree of the selected 40 ZmTALE family members with the known 22 AtTALE genes. Classify maize ZmTALE genes into two main categories, KNOX and BEL1 subfamilies, using a bootstrap value of 95 as a threshold and the classification criteria of Arabidopsis (Table S2). Specifically, 15 ZmTALE genes align with the BEL1 subfamily, while the remaining 25 genes are associated with the KNOX subfamily. Further investigation reveals three distinct clusters within the maize KNOX members: the first cluster comprises 10 members, the second cluster comprises 5 members, and the third cluster also comprises 10 members (Figure 2).

3.5. Gene Structure Analysis of ZmTALE Members

The diversity in gene structure underpins the functional diversity of genes. To gain deeper insights into the potential relationship between gene structure, function, and the evolutionary process of ZmTALE members, we analyzed the gene structures (exon-intron patterns and conserved domain compositions) of the identified ZmTALE members. Regarding the exon-intron pattern, the ZmTALE genes exhibited between 2 to 10 exons, with the majority containing 3–4 exons. Notably, ZmTALE34 and ZmTALE16 contain 2 and 10 exons, respectively. The ZmTALE family members were divided into four subgroups on the phylogenetic tree, with some groups showing diverse arrangements. However, only a few classifications exhibited significant similarity in exon-intron arrangements. Utilizing the MEME Wrapper function of TBTools to scan the amino acid sequences of all ZmTALE family members revealed 10 motifs, with certain motifs appearing or arranging according to a specific pattern based on family classification. In KNOXI and II (except for ZmTALE25 and ZmTALE32), motifs 3, 5, 4, and 1 were consistently present in the same order. However, compared to KNOX I, KNOX II additionally exhibited motif 9, positioned between motifs 5 and 4. KNOX III subgroup members generally had more motifs compared to most KNOX I and II members. The BEL1-like subfamily showed greater diversity in motifs than the KNOX subfamilies, with most arranged in the sequence of motifs 7, 2, 8, 6, 1, and 10. Scanning and visualization of the conserved domains of the ZmTALE gene family revealed that the maize ZmTALE genes possess five conserved domains: KNOX1, KNOX2, Homeobox, ELK, and POX. The KNOX1, KNOX2, and ELK domains were distributed among the KNOX I and II subfamilies, while the POX domain was exclusively found in the BEL1-Like subfamily. Interestingly, the Homeobox_KN domain was absent only in the KNOX III subfamily (Figure 3).

3.6. Collinearity Analysis of ZmTALE Gene Family

Through the application of MCScanX for synteny analysis and TBtools for delineating the linear relationships of the 40 members of the maize ZmTALE gene family, we successfully identified 13 pairs of duplicated genes. These include: ZmTALE14-ZmTALE17, ZmTALE8-ZmTALE23, ZmTALE10-ZmTALE24, ZmTALE14-ZmTALE31, ZmTALE1-ZmTALE38, ZmTALE17-ZmTALE31, ZmTALE19-ZmTALE30, ZmTALE18-ZmTALE35, ZmTALE19-ZmTALE33, ZmTALE22-ZmTALE26, ZmTALE26-ZmTALE37, ZmTALE28-ZmTALE35, and ZmTALE30-ZmTALE33, as illustrated in Figure 4. The identification of these pairs as segmental duplications suggests that such duplications are a key driver in the expansion of the ZmTALE gene family within maize. Further, the Ka/Ks ratios for these segmentally duplicated pairs were computed using the TBtools (Simple Ka/Ks Calculator) to assess the adaptive evolutionary trajectories of their coding sequences. The findings revealed Ka/Ks ratios spanning 0.02 to 0.34, all of which fall below the threshold of 0.5 (Table S3). This indicates a predominant influence of purifying selection across these gene pairs, aimed at the removal of harmful mutations across the species.

3.7. Analysis of ZmTALE Gene Expression

The expression of ZmTALE genes in different tissues and developmental stages was explored through the analysis of transcriptome data, highlighting the expression dynamics of ZmTALE gene family members in selected tissues (Figure 5, Table S4). The analysis indicates that most ZmTALE genes exhibit low or undetectable expression levels in anthers, filaments, embryos, and endosperms, suggesting that the majority of these genes may have minimal involvement in the reproductive processes of maize. Exceptions include ZmTALE34 and ZmTALE36 in anthers, and ZmTALE16 and ZmTALE12 in filaments, which showed higher expression levels, indicating their involvement in maize reproduction. Only ZmTALE27 in embryos and ZmTALE6 in endosperms exhibited high expression, indicating their active roles in seed formation, while most ZmTALE genes appear to have little to no effect on seed formation, with some potentially having a negative impact. ZmTALE6, ZmTALE15, and ZmTALE20 were highly expressed in seeds 24 days post-pollination, suggesting their positive contribution to seed development and maturation. Conversely, ZmTALE3, ZmTALE21, and ZmTALE23 showed low expression in embryos, endosperms, and throughout the seed cycle, possibly indicating a detrimental effect on seed germination and growth. In stems, both pollinated and unpollinated, most ZmTALE genes exhibited high expression levels, indicating their active involvement in stem growth and development, maintenance of plant structure, and nutrient transportation, thus underscoring the TALE gene family’s role in plant morphogenesis. The expression of ZmTALE9 and ZmTALE12 in stem apices and meristematic tissues suggests that these genes influence maize meristematic activity, affecting morphogenesis and the transition between vegetative and reproductive growth phases.

3.8. Analysis of ZmTALE Gene Expression under Drought Stress and qPCR Validation

The gene expression response to drought stress can reveal a gene’s potential beneficial or detrimental role in stress adaptation. In this study, to assess whether maize ZmTALE family genes respond to drought stress, expression profiles of ZmTALE genes in maize roots during severe drought conditions at 6 h and 24 h were extracted from previously published RNA-seq data (Table S5). Analysis of these transcriptomic data revealed that, under drought stress, 8 ZmTALE genes exhibited increased expression levels, 9 showed decreased expression, and 15 displayed variable trends in expression at the two time points. Specifically, ZmTALE4, 5, 19, and 27 experienced an increase in expression at 6 h followed by a decrease at 24 h, whereas ZmTALE18 and ZmTALE30 showed the opposite pattern, with an initial decrease and subsequent increase in expression levels (Figure 6).
Based on the post-drought gene expression profiles of the ZmTALE genes in maize, eight genes were randomly selected for qRT-PCR analysis at 0, 6, 12, and 24 h of drought stress, with primers detailed in Table S6. This approach was used to study the gene expression patterns of these selected genes under drought stress (Figure 7). The expression levels of ZmTALE8, ZmTALE28, and ZmTALE36 exhibited a marked upregulation 12 h after the onset of drought stress, displaying significant differences compared to the control conditions. In contrast, ZmTALE37 displayed a decreasing trend at 12 h but remained upregulated compared to the control group. ZmTALE1 and ZmTALE31 showed a decrease in expression level 6 h into the stress, while ZmTALE3 and ZmTALE24 started to decrease significantly at 6 h, with ZmTALE24 exhibiting an upregulation trend at 12 h, but overall, they followed a decreasing pattern. When compared with transcriptome data, the expression patterns of the selected genes were consistent. Overall, certain ZmTALE genes in maize respond to drought, and the different trends observed may indicate varying degrees of drought stress resistance.

4. Discussion

4.1. The Functional Domains and Evolutionary Dynamics of the ZmTALE Family

In this paper, we delved into the unique structural domains found within the ZmTALE gene family and their implications for the family’s evolutionary trajectory. The Homeobox_KN domain, found across all ZmTALE family members, is crucial for DNA binding and is located at the C-terminal end of the protein. In contrast, the ELK domain, primarily associated with nuclear localization and transcriptional repression, alongside the KNOX1 and KNOX2 domains, defines the molecular identity of the KNOX subfamily members. The Bell subfamily members are distinguished by the presence of the POX domain [25,26].
Our intraspecific collinearity analysis uncovered 13 collinear gene pairs, delineating the segmental duplications that have played a pivotal role in the expansion of the ZmTALE gene family within maize. These duplications were found predominantly among the Knox and Bell subfamilies, emphasizing the differential evolutionary paths within the family. The observed Ka/Ks ratios below 0.5 for these gene pairs indicate a history of purifying selection, underscoring the selective pressures that have shaped the current composition of the ZmTALE gene family. This pattern of gene duplication and subsequent evolutionary refinement is a widespread mechanism contributing to the diversification of gene families in flowering plants [17,27]. These duplicated genes show similar features in gene structure, such as the ZmTALE14-ZmTALE17 gene pair, which exhibits structurally similar lengths and has conserved structural domains and motifs of the same order. Other gene pairs follow the same pattern, further validating the evolutionary relationship among ZmTALE genes in maize.

4.2. The TALE Gene Family as Transcription Factors in Plant Development

The TALE gene family, serving as transcription factors, plays a pivotal role in plant development. Hay’s identification of the initial KNOTTED1-like homologous chromosome in maize signified a significant breakthrough [28]. Subsequently, Bolduc et al. revealed that KNOTTED1 regulates the maintenance of maize meristematic tissues by influencing the synthesis of growth hormones [29]. This finding underscores the expression of KNOX in meristematic tissues and stems across monocotyledonous plants like maize and Arabidopsis thaliana, underscoring its pivotal role in plant development.
The KNOX subfamily of TALE in maize has been found to critically influence plant morphology; aberrant expression of KNOX genes can lead to leaves exhibiting a “knotted” appearance due to constriction [30]. In Lilium brownii var. viridulum Baker, the LtKNOX1 gene impacts leaf lateral growth, resulting in leaves that display varying degrees of wrinkles and curls [31]. Beyond structural development, the TALE family also regulates the development of reproductive organs in plants. Bai et al. demonstrated that modulating the expression of PmKNAT2/6-a in Arabidopsis thaliana (L.) can adjust the number of carpels [32]. Additionally, the Arabidopsis AS1 gene is involved in the development of sepals and petals by modulating the expression of KNAT1, showcasing the TALE family’s diverse regulatory roles in plant morphogenesis and reproductive development [33]. In poplars, PagKNAT2/6b’s interaction with GA20ox1 curtails internode length, manifesting in a shorter stature [34]. This phenomenon, observed alongside maize’s tissue-specific expression analysis, underscores the ZmTALE genes’ pivotal role in stem growth. Nearly half of these genes are predominantly expressed in stem nodes, highlighting their significance in stem development.

4.3. The Role of TALE Gene Family in Response to Abiotic Stress

The TALE gene family’s responsiveness to abiotic stress is evidenced in various plants. In Camellia japonica L., the cloning and subsequent transcriptome analysis of 11 KNOX genes illustrated their substantial impact on drought and salinity tolerance [35]. Research on Dendrobium huoshanense’s 19 KNOX genes revealed their responsiveness to hormonal treatments and adverse conditions, including ABA, MeJA, SA, and drought [36]. Poplar’s PagKNat2/6b might mediate drought responses by influencing the GA pathway gene PagGA20ox1 [34]. In soybean, the TALE gene family’s promoters harbor cis-elements that react to stress, indicating potential changes in GmTALE expression in response to salt and drought [11]. In cotton, the upregulation of various TALE genes under abiotic stresses suggests their role in stress adaptation [37]. The ZmTALE1, ZmTALE37, and ZmTALE38 genes in maize are associated with the homologous gene KNAT7 in Arabidopsis thaliana. It has been reported that this gene can regulate lignin synthesis in Arabidopsis, thereby affecting the formation of the vascular tissue [38]. Researchers Yan and Zhang have indicated that lignin synthesis plays a significant role in plants’ resistance to drought [39,40]. Additionally, the ZmTALE24 gene, reported to be homologous to KNAT1 in Arabidopsis, interacts with DELLA (negative elements of the gibberellin signaling pathway) to regulate gibberellin function, thus influencing vascular tissue differentiation [41]. It has been demonstrated that the degree of vascular tissue differentiation affects plants’ tolerance to drought [42,43]. Therefore, it is hypothesized that ZmTALE genes may influence maize’s response to drought by modulating the biosynthesis of lignin or the formation of the wood component. This regulatory mechanism may involve the expression modulation of ZmTALE genes under drought stress conditions. Interestingly, during qRT-PCR experiments conducted on ZmTALE1, ZmTALE37, and ZmTALE38 genes, it was observed that their expression levels changed under drought treatment. This finding suggests that these genes may play crucial roles in maize’s response to drought stress, potentially by regulating the biosynthesis of lignin or the formation of the wood component to adapt to drought conditions. This result provides new clues for further research into the molecular mechanisms of ZmTALE genes in maize drought adaptation. These findings highlight the TALE gene family’s crucial response to environmental challenges, such as drought, underscoring the value in exploring the ZmTALE family’s contribution to drought resilience in maize. Our results indicate that the ZmTALE gene family’s expression in maize shifts under drought conditions, showcasing their specific functions during development and under stress scenarios.

5. Conclusions

In this study, we successfully identified 40 ZmTALE genes within the maize genome and conducted a comprehensive analysis of them. Our detailed investigation into gene structures and sequences revealed that the KNOX I and KNOX II domains are primarily distributed in the KNOX subfamily, while the POX domain is unique to the Bel1-Like subfamily. Additionally, we observed the distribution of several other domains across these two subfamilies, demonstrating the structural domain diversity within this gene family. These ZmTALE genes are unevenly distributed across nine maize chromosomes, as well as on Scaf_110 and Scaf_186. RNA-seq analysis suggested that these genes might be involved in maize’s response to drought stress. Subsequent RNA-Seq and qRT-PCR experiments confirmed the significant role of ZmTALE genes in maize’s adaptation to drought stress. Therefore, our research provides a solid foundation for the functional study of the ZmTALE gene family in response to drought stress and lays the theoretical groundwork for further exploring their potential application in enhancing drought resistance in maize.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14061267/s1, Table S1: Gene ID of ZmTALE gene in maize; Table S2: ZmTALE gene classification; Table S3: Type collinearity gene pairs of ZmTALE genes; Table S4: RNA-Seq data of ZmTALE genes under drought; Table S5: Maize ZmTALE genes in different tissues RNA-Seq data; Table S6: qRT-PCR primer sequences.

Author Contributions

R.Z. and Y.Y. designed the experiments and methods; C.Z. and J.G. performed the experiments and data analysis; Z.Y., J.H. and H.X. assisted with the experiments; B.Q., Q.W., R.Z. and Y.Y. participated in the discussion for the experimental direction; R.Z. and Q.W. supervised and guided the experiments; B.Q. and Q.W. drafted the manuscript; R.Z., Y.Y., Q.W. and B.Q. proofread the manuscript; R.Z. and Y.Y. reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

Jilin Agricultural Science and Technology Innovation Project (CXGC2023RCB006); National Natural Science Foundation of China (Key Program) (U23A20186); National Natural Science Foundation of China (No. 32171928).

Data Availability Statement

Data are contained within the article.

Acknowledgments

We thank our contributors for their dedication and compliance through the many stages of this research as well as the editors and anonymous reviewers whose comments helped to greatly improve this paper.

Conflicts of Interest

The authors declare no conflicts of interest.

References

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Agronomy 14 01267 g001
Figure 1. Chromosomal localization of the maize ZmTALE genes. Chromosome numbers are positioned on the left, with the scale on the left measured in megabases (Mb). An estimated genetic interval of 350 kb was set to accurately depict gene distribution. The color gradient from red to blue across the chromosomes represents gene density from high to low, where red signifies areas of higher gene density and blue indicates areas of lower gene density. Unmarked regions on the chromosomes represent genetic areas lacking gene distribution data.
Figure 1. Chromosomal localization of the maize ZmTALE genes. Chromosome numbers are positioned on the left, with the scale on the left measured in megabases (Mb). An estimated genetic interval of 350 kb was set to accurately depict gene distribution. The color gradient from red to blue across the chromosomes represents gene density from high to low, where red signifies areas of higher gene density and blue indicates areas of lower gene density. Unmarked regions on the chromosomes represent genetic areas lacking gene distribution data.
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Figure 2. Phylogenetic tree of maize and Arabidopsis, in which ZmTALE genes are categorized into four main classes: KNOX I, KNOX II, KNOX III, and BEL1-Like. Within this phylogenetic tree, AtTALE genes from Arabidopsis are specifically marked with a pentagram for easy identification.
Figure 2. Phylogenetic tree of maize and Arabidopsis, in which ZmTALE genes are categorized into four main classes: KNOX I, KNOX II, KNOX III, and BEL1-Like. Within this phylogenetic tree, AtTALE genes from Arabidopsis are specifically marked with a pentagram for easy identification.
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Agronomy 14 01267 g003
Figure 3. The structure, conserved domains, and motif patterns of maize ZmTALE genes. In part (a), the structure of ZmTALE genes is shown, where blue boxes represent the untranslated regions (UTRs) at 5′ and 3′ ends; yellow boxes indicate coding sequences (CDS); and black lines denote introns, with numbers (0, 1, 2) indicating the phase of introns. Different conserved domains are marked with boxes of various colors. Part (b) depicts the motif patterns of ZmTALE members. Additionally, the lengths of related gene structures and motif components can be estimated using the corresponding scale at the bottom of the panel.
Figure 3. The structure, conserved domains, and motif patterns of maize ZmTALE genes. In part (a), the structure of ZmTALE genes is shown, where blue boxes represent the untranslated regions (UTRs) at 5′ and 3′ ends; yellow boxes indicate coding sequences (CDS); and black lines denote introns, with numbers (0, 1, 2) indicating the phase of introns. Different conserved domains are marked with boxes of various colors. Part (b) depicts the motif patterns of ZmTALE members. Additionally, the lengths of related gene structures and motif components can be estimated using the corresponding scale at the bottom of the panel.
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Agronomy 14 01267 g004
Figure 4. Collinearity among maize ZmTALE homologous genes. In the diagram, collinear blocks across the whole genome are depicted with a grey background, and colorful curves are used to connect pairs of duplicated ZmTALE genes.
Figure 4. Collinearity among maize ZmTALE homologous genes. In the diagram, collinear blocks across the whole genome are depicted with a grey background, and colorful curves are used to connect pairs of duplicated ZmTALE genes.
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Agronomy 14 01267 g005
Figure 5. The transcriptomic expression levels of the ZmTALE gene family across various tissues, including stamens, embryos, endosperm, internodes, and leaves before and after pollination, pistil filaments, stems, and meristematic tissues, the complete root system, and whole seeds. Note: DAP, days after pollination; R1, reproductive 1; SAM, Shoot Apical Meristem; 7d, 7days after sowing.
Figure 5. The transcriptomic expression levels of the ZmTALE gene family across various tissues, including stamens, embryos, endosperm, internodes, and leaves before and after pollination, pistil filaments, stems, and meristematic tissues, the complete root system, and whole seeds. Note: DAP, days after pollination; R1, reproductive 1; SAM, Shoot Apical Meristem; 7d, 7days after sowing.
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Agronomy 14 01267 g006
Figure 6. The expression levels of maize ZmTALE gene family members under drought stress at 6 h and 24 h. Note: Severe_water_deficit represents severe water shortage treatment (−0.8 Mp water potential).
Figure 6. The expression levels of maize ZmTALE gene family members under drought stress at 6 h and 24 h. Note: Severe_water_deficit represents severe water shortage treatment (−0.8 Mp water potential).
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Agronomy 14 01267 g007
Figure 7. Quantitative RT-PCR analysis of selected representative genes in the maize ZmTALE family. Data were normalized to the Zm18SRNA gene, and vertical bars indicated the standard deviations. The values represented the mean ± standard deviation (SD) of three independent replicates. Asterisks indicate the corresponding gene significantly up- or down-regulated compared with the 0-h statuses (* p < 0.05, ** p < 0.01, t-test).
Figure 7. Quantitative RT-PCR analysis of selected representative genes in the maize ZmTALE family. Data were normalized to the Zm18SRNA gene, and vertical bars indicated the standard deviations. The values represented the mean ± standard deviation (SD) of three independent replicates. Asterisks indicate the corresponding gene significantly up- or down-regulated compared with the 0-h statuses (* p < 0.05, ** p < 0.01, t-test).
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Table 1. Gene and protein characteristics of the ZmTALE members.
Table 1. Gene and protein characteristics of the ZmTALE members.
Gene NameSequence IDLength (aa)WM (Da)pIGRAVYAliphatic IndexPredicted Location (s)
ZmTALE1Zm00001eb001720_T00131034,336.785.73−0.55575.61nucleus
ZmTALE2Zm00001eb001770_T00162066,061.116.16−0.48668.18nucleus
ZmTALE3Zm00001eb005020_T00558762,181.775.82−0.43967.31nucleus
ZmTALE4Zm00001eb013560_T00159864,715.136.69−0.2188.63nucleus
ZmTALE5Zm00001eb021970_T00161264,715.256.34−0.33869.69cytosol
ZmTALE6Zm00001eb031950_T0019510,998.394.88−0.48978.11cytosol
ZmTALE7Zm00001eb032780_T00166872,679.925.76−0.62764.64cytosol
ZmTALE8Zm00001eb051900_T00265171,815.745.68−0.68663.16cytosol
ZmTALE9Zm00001eb051910_T00237440,996.239.07−0.52384.47cytosol
ZmTALE10Zm00001eb052120_T00133236,589.865.96−0.72665.66nucleus
ZmTALE11Zm00001eb055920_T00135939,826.686.41−0.63573.43nucleus
ZmTALE12Zm00001eb055940_T00136039,643.756.03−0.5269nucleus
ZmTALE13Zm00001eb056260_T00175579,167.796.49−0.49562.07nucleus
ZmTALE14Zm00001eb058930_T00236440,276.275.91−0.64262.88nucleus
ZmTALE15Zm00001eb108700_T00111613,112.024.97−0.23191.72nucleus
ZmTALE16Zm00001eb116630_T00136240,246.688.32−0.5579.5chloroplast
ZmTALE17Zm00001eb117820_T00136039,215.026.23−0.62664.72nucleus
ZmTALE18Zm00001eb130180_T00129532,493.475.51−0.55468.51nucleus
ZmTALE19Zm00001eb147970_T00158763,158.837.29−0.44168.07nucleus
ZmTALE20Zm00001eb181490_T00113615,591.794.91−0.20796.76nucleus
ZmTALE21Zm00001eb202140_T00167169,914.656.06−0.41362.43nucleus
ZmTALE22Zm00001eb206760_T00131434,111.336.02−0.51471.34nucleus
ZmTALE23Zm00001eb217350_T00263970,848.355.46−0.7163.87nucleus
ZmTALE24Zm00001eb217470_T00116318,005.314.59−0.32577.98mitochondrion
ZmTALE25Zm00001eb217480_T00121424,066.877.77−0.76267.57nucleus
ZmTALE26Zm00001eb234270_T00130032,669.765.89−0.54470.73nucleus
ZmTALE27Zm00001eb239680_T00253956,452.116.73−0.25168.78nucleus
ZmTALE28Zm00001eb264910_T00129832,662.695.32−0.57965.91nucleus
ZmTALE29Zm00001eb268690_T00149854,229.076.68−0.38173.78nucleus
ZmTALE30Zm00001eb289480_T00157661,910.338.29−0.4568.87nucleus
ZmTALE31Zm00001eb299420_T00135138,800.646.4−0.67764.7nucleus
ZmTALE32Zm00001eb322410_T00115016,4696.29−0.038104.07nucleus
ZmTALE33Zm00001eb347710_T00159264,138.129.24−0.44970.12nucleus
ZmTALE34Zm00001eb354670_T00116718,305.625.48−0.42381.8nucleus
ZmTALE35Zm00001eb354880_T00232735,593.025.27−0.51267.25nucleus
ZmTALE36Zm00001eb384240_T00249152,469.657.19−0.31766.86nucleus
ZmTALE37Zm00001eb386830_T00131634,522.645.69−0.56369.05nucleus
ZmTALE38Zm00001eb403720_T00131834,768.185.64−0.45880.13nucleus
ZmTALE39Zm00001eb437470_T0019310,577.179.23−0.60582.9nucleus
ZmTALE40Zm00001eb438600_T0019310,547.089.23−0.63382.9cytosol
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Qian, B.; Wang, Q.; Zhang, C.; Guo, J.; Yu, Z.; Han, J.; Xia, H.; Zhao, R.; Yin, Y. Exploring the Roles of TALE Gene Family in Maize Drought Stress Responses. Agronomy 2024, 14, 1267. https://doi.org/10.3390/agronomy14061267

AMA Style

Qian B, Wang Q, Zhang C, Guo J, Yu Z, Han J, Xia H, Zhao R, Yin Y. Exploring the Roles of TALE Gene Family in Maize Drought Stress Responses. Agronomy. 2024; 14(6):1267. https://doi.org/10.3390/agronomy14061267

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Qian, Buxuan, Qi Wang, Chuang Zhang, Jia Guo, Zhijia Yu, Jiarui Han, Hanchao Xia, Rengui Zhao, and Yuejia Yin. 2024. "Exploring the Roles of TALE Gene Family in Maize Drought Stress Responses" Agronomy 14, no. 6: 1267. https://doi.org/10.3390/agronomy14061267

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