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Article

Genome-Wide Identification and Analysis of ZF-HD Gene Family in Moso Bamboo (Phyllostachys edulis)

by
Feiyi Huang
1,
Jiaxin Wang
1 and
Chao Tang
2,*
1
Co-Innovation Center for Sustainable Forestry in Southern China, Bamboo Research Institute, College of Life Sciences, Nanjing Forestry University, Nanjing 210037, China
2
State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Centre of Pear Engineering Technology Research, Nanjing Agricultural University, Nanjing 210095, China
*
Author to whom correspondence should be addressed.
Plants 2023, 12(23), 4064; https://doi.org/10.3390/plants12234064
Submission received: 19 July 2023 / Revised: 5 October 2023 / Accepted: 23 October 2023 / Published: 3 December 2023
(This article belongs to the Special Issue Molecular Mechanisms Associated with Plant Tolerance upon Abiotic Stress)
Browse Figures
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Abstract

:
Zinc finger-homeodomain (ZF-HD) proteins play essential roles in plant growth, development and stress responses. However, knowledge of the expression and evolutionary history of ZF-HD genes in moso bamboo remains limited. In this study, a total of 24 ZF-HD genes were found unevenly distributed on 12 chromosomes in moso bamboo (Phyllostachys edulis). Phylogenetic analysis indicated that PeZF-HDs were divided into two subfamilies: ZHD and MIF. The ZHD subfamily genes were further classified into seven groups according to their orthologous relationships among the rice and Arabidopsis ZF-HD gene family. The gene structures and conserved motifs of PeZF-HDs were analyzed. Whole-genome duplication (WGD) or segmental duplication promoted the evolution and expansion of the moso bamboo ZF-HD gene family. Ka/Ks ratios suggested that the twenty-four duplication pairs had undergone purifying selection. Promoter analysis showed that most PeZF-HDs contained cis-elements associated with stress responses and hormones. Expression analysis demonstrated that many PeZF-HDs were responsive to abiotic stress treatment. Overall, this work investigated PeZF-HD genes in moso bamboo using bioinformatic approaches. The evolutionary research on gene structure, motif distribution and cis-regulatory elements indicated that PeZF-HDs play distinct roles in biological processes, which provides a theoretical basis for exploring the physiological functions of ZF-HDs and selecting candidate stress-related genes in moso bamboo.

1. Introduction

Plants often face various abiotic stresses during their life cycle, including extreme temperatures, drought and salinity, which seriously limit plant growth, development, quality and yield [1]. The transcription factor is a key kind of regulatory protein which can bind to the promoters of downstream genes and regulate their expression to adapt to multiple stresses [2]. As plant-specific transcription factors, zinc finger-homeodomain (ZF-HD) proteins have aroused much interest as they play vital regulatory roles in plant growth and development, as well as various stress responses [3].
The ZF-HD protein contains the conserved ZF-HD_dimer domain (PF04770) which consists of two highly conserved domains: the N-terminal C2H2-type zinc finger (ZF) and the C-terminal homeodomain (HD) [4]. The ZF domain can not only bind DNA but enhance the protein–DNA interactions controlled by the HD domain to either enhance or repress transcription [5]. As a DNA-binding domain, the HD has approximately 60 conserved amino acids, which fold into a three-helix structure and specifically connect to DNA [6]. HD-containing proteins are also involved in protein–protein interactions and other regulatory functions. Based on the size, location and structure of the HD domain and its association with other domains, HD-containing proteins can be divided into six distinct families: finger-like domain-associated HD (PHD finger), WUSCHEL-related homeobox (WOX), knotted-related homeobox (KNOX), zinc finger motif-associated HD (ZF-HD), leucine zipper-associated HD (HD-Zip) and bell-type HD [7]. The zinc finger structure contains a single zinc ion surrounded by two pairs of conserved cysteine and/or histidine residues [8]. According to the number, spacing pattern and nature of zinc-binding residues, zinc finger structures are classified into different types, such as C2H2 and C3H [9]. ZF-HD proteins can be divided into ZF-HD and mini zinc finger (MIF) groups based on phylogeny. MIF groups only contain the ZF domain without the HD domain, and are involved in integrating signals from GA, auxin, abscisic acid (ABA) and brassinosteroid [10]. However, the origins of and evolutionary relationship between these two groups remains unclear.
ZF-HD proteins were first discovered in the C4 plant Flaveria [5]. Subsequently, ZF-HD genes were reported in many plant species, such as Arabidopsis, rice, maize and tomato [11,12,13,14]. There has been increasing evidence suggesting that ZF-HD genes play important roles in responding to adverse stresses, except for plant growth and development [12]. Multiple ZF-HDs in Arabidopsis are involved in stress responses to adversity, and similar findings have also been reported in wheat and tomato [15,16,17]. AtZF-HD1 can bind to the promoter of early response to dehydration stress 1 (ERD1) and its expression is inducible by drought, salinity and ABA. An overexpression of ZF-HD1 and NAC enhances drought resistance in Arabidopsis [15]. A silencing of SlZF-HD13 decreases the salt and drought tolerance of tomato [17]. In rice, four ZF-HDs can bind to a DREB1B promoter and activate its expression under drought and cold stress [12]. Most BraZF-HDs are induced by abiotic stress, indicating their important roles in controlling stress response [18]. Except for in the model plant, the identification and functions of ZF-HDs have also been broadly elucidated. There have been, respectively, 49, 50, 22, and 32 ZF-HD genes identified in four cotton genomes, in which gene duplication drove the expansion of the ZF-HD gene family during the divergence of the Gossypium species [19]. Twenty FtZF-HD genes have been identified in Tartary buckwheat (Fagopyrum tataricum), which have been further divided into five subfamilies [20]. In quinoa, 23 CqZF-HDs were detected in its genome, and CqZF-HD14 was able to promote its resistance to drought by regulating the expressions of CqNAC79 and CqHIPP34 [21]. Although ZF-HD genes have been widely studied in many plant species, reports on ZF-HD genes in moso bamboo (Phyllostachys edulis) are limited.
Moso bamboo belongs to the Bambusoideae subfamily of the Poaceae family and is an important non-timber forest product. It is the most widespread bamboo species in China and has the highest economic, ecological and ornamental value [22]. Due to its propensity for fast growth, it may contribute to water and soil conservation and climate regulation [23]. Disadvantageous environmental and climatic conditions restrict the growth and development of moso bamboo, leading to severe yield losses. Recently, the genome of moso bamboo has been published, providing the foundation for a genome-wide analysis of ZF-HD genes in moso bamboo [24]. Herein, 24 putative PeZF-HD genes were identified and a comprehensive analysis was performed, including analyses of physicochemical properties, phylogenetic relationships, gene structure, conserved motifs, chromosomal localization, cis-elements, expression profiling and evolutionary analysis. These results will improve the understanding of the PeZF-HD gene family and provide the key candidate genes related to abiotic stress in moso bamboo.

2. Results

2.1. Identification of ZF-HD Genes in Moso Bamboo

P. edulis ZF-HD genes were screened by BLASTP and HMM. After excluding the redundant sequences, SMART was performed to confirm the presence of ZF-HD_dimer domains (Table S3). A total of 24 ZF-HD proteins were identified as PeZF-HD genes, and were named PeZF-HD1–PeZF-HD24. The characteristics of these PeZF-HDs are shown in Table 1, including the length of CDS and protein, molecular weight, theoretical isoelectric point, exon number, chromosome location and subcellular localization. The length of CDS of PeZF-HD genes varied from 252 bp to 1212 bp. The protein sequence lengths ranged from 83 to 403 amino acids, the molecular weights spanned 8.59 to 43.36 kDa, and the isoelectric points had a range of 5.90 to 10.30. The number of exons in PeZF-HD genes ranged from one to three. The predicted subcellular localization results indicated that all PeZF-HD proteins were located in the nucleus.

2.2. Phylogenetic Analysis of the Moso Bamboo ZF-HD Gene Family

To study the evolutionary relationships of PeZF-HDs, a phylogenetic tree consisting of the ZF-HD protein sequences from moso bamboo, rice and Arabidopsis was constructed using the Maximum Likelihood (ML) method (Figure 1). The phylogenetic distribution revealed that the PeZF-HD family can be divided into two major groups: MIF and ZHD. ZHD included 43 genes and could be subdivided into seven subgroups: ZHD I, ZHD II, ZHD III, ZHD IV, ZHD V, ZHD VI and ZHD VII. The quantitative distribution of each group of ZF-HD proteins in moso bamboo, rice and Arabidopsis were counted (Table S4). Compared to MIF, ZHD had more members in moso bamboo, rice and Arabidopsis. The number of ZHD V genes was the highest, with four PeZF-HD, two OsZF-HD and five AtZF-HD genes. Phylogenetic analysis of ZF-HDs in three species showed that PeZF-HDs shared more sequence similarity with OsZF-HDs than with AtZF-HDs (Figure 1).

2.3. Conserved Motifs and Gene Structure Analysis of the Moso Bamboo ZF-HD Gene Family

To investigate the structural diversity of the PeZF-HD genes, a phylogenetic tree using only the full-length PeZF-HD protein sequences was constructed. Phylogenetic analysis showed that the PeZF-HDs could be categorized into six classes, which was consistent with the phylogenetic tree data among moso bamboo, rice and Arabidopsis (Figure 2A). MEME was used to determine differences in the PeZF-HD proteins. Eight conserved motifs were identified and named motifs 1–8 (Figure 2B). Motif 1 was the largest motif and was composed of 60 amino acids. Motif 2 and Motif 3, which were the components of the ZF-HD_dimer domain, were the most common motifs. Motif 2 was present in all PeZF-HDs, whereas Motif 3 was absent in PeZF-HD23. Motif 5 was present in ZHD IV and ZHD V. Motifs 7 and 8 were found exclusively in ZHD V, whereas Motif 4 was detected specifically in MIF. PeZF-HDs within the same class showed similar motif distributions, suggesting that they have functional similarities. Furthermore, the motif distribution in MIF differed greatly from that in the other classes, as it had only two to three motifs (motifs 2, 3 and 4) and the shortest sequence length. These motif distribution differences were probably results of the functional diversity of PeZF-HDs.
The exon–intron organizations were analyzed with an online GSDS tool. As shown in Figure 2C, half of the PeZF-HDs were intronless and the remaining half had one intron. Most PeZF-HDs in the same class had similar intron–exon structures. For example, the PeZF-HDs in ZHD V (except for PeZF-HD23) all contained no introns. However, the intron–exon structure was not always conserved in most sister gene pairs. For instance, PeZF-HD5/-7 and PeZF-HD1/-3 had different numbers of introns and exons. Moreover, all PeZF-HDs were less than 2 kb in length, except for PeZF-HD17 (4.4 kb).

2.4. Chromosome Distribution and Gene Duplication of the PeZF-HD Genes

The 24 PeZF-HDs were unevenly distributed across the 12 chromosome scaffolds based on their location in the moso bamboo genome (Figure 3). Chromosomes 3 and 13 contained the largest number of PeZF-HD members (four and four genes, respectively), followed by chromosomes 18 and 22 (three and three genes, respectively). Both chromosomes 11 and 12 contained two genes, while chromosomes 2, 9, 16, 17, 23 and 24 possessed only one gene, and no ZF-HDs were present on the twelve remaining moso bamboo chromosomes. Eighteen PeZF-HDs were located on the positive-strand chromosomes, while the remaining six genes were positioned on the negative-strand chromosomes. To further investigate the mechanism of the PeZF-HD gene family expansion, the potential duplication events of PeZF-HDs were identified with the MCScanX program. All PeZF-HDs appeared to have arisen from WGD or segmental duplications, except for PeZF-HD19, which underwent dispersed duplication (Table S5). No tandem duplication event was found in PeZF-HDs.
To estimate the selection constraints of the duplicated PeZF-HD genes, the Ka, Ks replacement rate and Ka/Ks ratios of the twenty-four duplication pairs were calculated and listed in Table S6. The Ka/Ks ratios of these paralogous pairs ranged from 0.106 to 0.679, with an average value of 0.375, suggesting that these genes have undergone strong purifying selection during evolution. The Ks values of the PeZF-HD gene pairs varied from 0.099 to 0.639, indicating that a large-scale PeZF-HD gene duplication event occurred as early as 7.65–49.14 million years ago (MYA). The divergence for most PeZF-HD gene pairs (16 of 24) was about 16.51 to 49.14 MYA, which differs from the moso bamboo whole-genome duplication 7–12 MYA, suggesting that the PeZF-HD gene underwent other ancient whole-genome duplication events earlier.

2.5. Analysis of Cis-Regulatory Elements in PeZF-HD Promoters

To explore the potential functions of PeZF-HDs, the cis-regulatory elements at the promoter regions were investigated. Besides basic elements, cis-elements responsive to light, development, environmental stress and hormones were found in PeZF-HD promoters (Figure 4 and Table S1). A light-responsive element, with the largest proportion in PeZF-HD promoters, was represented by as many as 22 types. Each PeZF-HD promoter contained between 3 and 10 types. The elements related to development were also analyzed, such as the CAT-box, CCGTCC-box, RY-element, O2-site and GCN4 motif. With regard to environmental stress-related elements, we mainly investigated the elements related to low temperature stress (LTR), drought induction (MBS), salicylic acid response (TCA-element and SARE), and defense and stress response (TC-rich repeats). Interestingly, all PeZF-HD promoters contained the MYB element. Numerous elements in the PeZF-HD promoters were related to the response to hormones, like ABA (ABRE), MeJA (TGACG-motif and CGTCA-motif), auxin (AuxRR-core, TGA-box and TGA-element) and gibberellic acid (P-box, GAREmotif and TATC-box). Among them, the ABRE was the most abundant element in the PeZF-HD promoters, as it was found in 22 promoters. These results indicate that PeZF-HDs might be associated with moso bamboo development and have different roles in response to different stresses and hormone signals.

2.6. Expression Profiles of PeZF-HD Genes against Different Abiotic Stresses

The analysis of potential cis-acting elements indicated that PeZF-HDs may play roles in plant responses to multiple environmental stresses. Based on the published transcriptome data, twelve PeZF-HDs with significantly different expressions were screened. Their expression profiles under cold, salt and drought stresses were determined by qPCR analysis (Figure 5). For moso bamboo seedlings treated with cold stress, the expression of PeZF-HD2, 4 and 20 displayed significant up-regulation, while rapid down-regulation was observed for PeZF-HD5 and 22. Under salt stress, PeZF-HD14 was repressed, whereas PeZF-HD4, 10 and 13 were induced. In the drought stress, the expression of PeZF-HD5 and 14 was down-regulated and PeZF-HD4, 10, 20 and 22 were up-regulated. PeZF-HD4 was significantly up-regulated under cold, salt and drought stresses. The expression of PeZF-HD14 was reduced and PeZF-HD10 was induced in both drought and salt stresses, while that of PeZF-HD5 was down-regulated and PeZF-HD20 was up-regulated in both cold and drought stresses. Interestingly, some PeZF-HDs exhibited inverse gene expression profiles in response to cold, salt and drought treatments. For instance, PeZF-HD22 was reduced under cold treatment, but was induced under salt and drought treatment. Moreover, the expression of PeZF-HD22 first decreased and then increased under cold, salt or drought treatments. The plant hormone ABA acts in plant stress signal response and plant growth. Thus, the expression profiles of the twelve PeZF-HDs under ABA treatment were also analyzed. Most of the PeZF-HDs signals were dramatically up-regulated in response to ABA. Eight of twelve PeZF-HDs (PeZF-HD1, 2, 4, 10, 13, 20, 21 and 23) were up-regulated to varying degrees with this treatment. We concluded the potentially functional ZF-HD genes of different species in response to various environmental stresses (Table S7), and the expressions of most PeZF-HDs showed similar responses to various environmental stresses in different species. However, the diverse PeZF-HDs may differ in their modes of regulation in moso bamboo under abiotic stress.

3. Discussion

Plants often face adverse environmental conditions during their lifetime, such as drought, high salinity and cold, which affect physiological and biochemical processes and thus inhibit plant growth and development. To this end, plants have evolved a sophisticated stress resistance system regulated by a series of genes. To date, ZF-HDs have attracted increasing attention in applied and plant basic sciences. ZF-HD family genes are only existent in plants and play crucial roles in plant development and abiotic stress response [3]. The structural characteristics and functions of the ZF-HD gene family have been studied in various plants, such as Arabidopsis, rice, maize, tomato and Chinese cabbage [11,12,13,14,18]. However, ZF-HD genes have not been studied in moso bamboo.
Based on the moso bamboo genome, 24 ZF-HD genes (18 ZHD genes and 6 MIF genes) were identified and their physical and chemical properties, conserved motifs, gene evolution and expression were analyzed in this study. The amino acid length of ZF-HDs in moso bamboo ranged from 83 to 403, which was similar to that in rice (105–417). The number of PeZF-HDs was more than that of rice and Arabidopsis, similar to that of maize and tomato, and less than that of Chinese cabbage [11,12,13,14,18]. The genome size of moso bamboo (2021 Mb) is larger than that of Arabidopsis (164 Mb), rice (441 Mb), tomato (950 Mb) and Chinese cabbage (283.8 Mb), and comparable to that of maize (2300 Mb) [25,26,27,28,29]. These results indicate that the number of ZF-HDs has no relationship to the plant’s genome size, but may be related to a gene duplication event (Table S5).
PeZF-HDs were classified into eight groups based on sequence homology and classification related to rice and Arabidopsis, different from the seven subfamilies in alfalfa and cucumber [30,31]. Phylogenetic analysis showed that all PeZF-HD subgroups had at least one homolog of rice ZF-HDs (Figure 1), indicating that the PeZF-HDs shared more sequence similarity with OsZF-HDs, and the subgroups of ZF-HDs were usually conserved in monocotyledonous plants. The groups of PeZF-HDs lacked the ZHD III and ZHD VI groups according to classification in relation to rice and Arabidopsis. Rice and Arabidopsis ZF-HDs were found in ZHD VI, but only Arabidopsis ZF-HDs were found in ZHD III, suggesting the protein divergence between monocots and dicots. The number of each group in moso bamboo was different compared to rice and Arabidopsis. ZF-HDs in plants with different gene numbers in different groups may be under different evolutionary constraints. Furthermore, MIF proteins of moso bamboo, rice and Arabidopsis form a phylogenetically distinct clade with ZHD proteins, indicating that the structural divergence between MIF and ZHD genes may be derived from ZHDs after losing the HD domain or may originate from MIFs after gaining the HD domain [4].
Conserved motifs and structural analysis showed that PeZF-HDs in the same class were similar in structure (Figure 2), suggesting that PeZF-HD members may be functionally conserved during their evolution. Motifs 2 and 3 were the essential components of the ZF-HD_dimer domain and existed in all 24 PeZF-HDs, implying that these two motifs were crucial for PeZF-HDs functions. The intron–exon analysis exhibited that half of PeZF-HDs lacked introns, and the remaining twelve PeZF-HDs had one intron, which reflected intron gain and was almost consistent with the ZF-HDs in tomato [13]; yet, most plant ZF-HDs are intronless [11,12,14,18]. Precise and complete intron gains and losses stimulate the production of new genes, based on previous reports [32]. The variable intron–exon structures of ZF-HDs in moso bamboo compared with that in other plants suggested that there existed structural divergence among ZF-HDs in moso bamboo. Moreover, the similar exon–intron organization in different subfamilies suggests that these genes were highly conserved during evolution. Thus, different motifs and exon–intron organizations may provide the structural basis for the diverse functions of PeZF-HDs. These results, combined with phylogenetic analysis, confirmed the reliability of group classification and the similar biological functions of PeZF-HDs within the same group.
Gene duplication patterns may reveal the generational types of genes and evolutionary ways of gene functions [33]. Almost all PeZF-HDs (except for PeZF-HD19) were duplicated through WGD or segmental duplication events, suggesting that WGD or segmental duplication played a key role in the expansion of PeZF-HDs, which was similar to the ZF-HDs in other plants, like tomato and Chinese cabbage [13,18]. The Ka/Ks values of paralogous genes were high at 0.106-0.679 (the average value was 0.375), implying purifying selection and a powerful selection constraint in PeZF-HDs (Table S6). Intra-genomic collinearity analysis of PeZF-HDs was performed and 24 pairs of duplicated genes were found in the moso bamboo genome (Figure 3). Most duplication pairs had conserved motifs and gene structures, and only a few had a certain degree of differentiation (Figure 2). For example, PeZF-HD1 was intronless, while its corresponding PeZF-HD3 had one intron, which could be due to the gaining of a single intron in the gene structure during evolution. Most divergence times of the PeZF-HD gene pairs occurred from 16.51 to 49.14 MYA, which differs from the recent whole-genome duplication time of moso bamboo (7-12 MYA) [20], suggesting that the effects of other earlier ancient whole-genome duplication events also influenced the expansion of PeZF-HD genes.
The different cis-elements on promoters likely led to functional differentiation in PeZF-HDs. Elements related to stress responses were found in PeZF-HD promoters, including MYB, MBS, LTR, TCA-element, TC-rich repeats and ABRE (Table S1), which are directly related to ABA, drought, cold and salt stress responses. ZF-HD genes were reported to be involved in various abiotic stresses and ABA treatment, such as salt and drought stress [12,17,19,34]. Moreover, ZF-HD genes in alfalfa also showed similarly decreased expression levels under alkaline stress [31]. Previous studies investigated the expression profiles of ZF-HD genes under multiple stress conditions with transcriptome analysis and qPCR [11,19,31]. In this study, the qPCR results showed that PeZF-HDs 5, 4 and 6 were differentially expressed under cold, salt and PEG stresses, respectively, which also verified the results of the cis-elements analysis. Most differentially expressed PeZF-HDs were also significantly changed under ABA treatment (Figure 5). Particularly, overlapping responses of PeZF-HDs to multiple stresses were found, like PeZF-HD10, which was induced under drought and salt stresses, helping the potential hub genes in moso bamboo to acclimate to stressful conditions. The overexpression of AtZHD1 improved drought tolerance in Arabidopsis [15] and the overexpression of CqZF-HD14 enhanced the defense system of quinoa under drought [21]. PeZF-HD4, the homologous gene to AtZF-HD1, was up-regulated under cold, salt, PEG and ABA treatments. PeZF-HD5, another homologous gene to AtZF-HD1, was up-regulated under salt treatment. AtZHD4 was induced under cold, salt and drought treatments [35]. The expression of AtZHD4 homolog PeZF-HD2 also increased under cold, salt and drought treatments. These results showed that PeZF-HDs may play important roles in response to various abiotic stresses, most of which may be mediated by ABA signaling. The above results provide an information base for selecting candidate genes and promote further functional investigations of biotic stress resistance in moso bamboo.

4. Materials and Methods

4.1. Plant Material and Treatments

The moso bamboo (Phyllostachys edulis) was selected for this experiment as it has completed whole-genome sequencing. The germinated seeds were planted in pots with medium (soil and vermiculite, 1:1) in a growth room under a controlled environment (16 h light at 23 °C/8 h dark at 18 °C). Two-month-old seedlings were treated with 20% PEG6000, 100 µM ABA and 250 mM NaCl, respectively. For the low temperature treatment, the seedlings were transferred to 4 °C conditions. The leaf samples were collected along a continuous time course (0, 1, 2, 3, 4, 8 h) with three biological replicates and then stored at −80 °C. Total RNA was extracted by the RNAsimple Total RNA Kit (Tiangen, Beijing, China) and residual genomic DNA was removed with DNase I (Qiagen, Valencia, CA, USA) following the manufacturer’s instructions.

4.2. Identification of ZF-HD Genes in Moso Bamboo

The P. edulis genome sequence was downloaded from the Bamboo Genome Database (http://202.127.18.221/bamboo/index.php, accessed on 8 April 2023). The ZF-HD gene sequences of Oryza and Arabidopsis were obtained from the rice genome annotation project and the Arabidopsis information resource based on published studies, respectively [4,11]. Members of the PeZF-HD genes were identified by BLASTP searches and Hidden Markov Model (HMM) searches. Protein sequences of Oryza and Arabidopsis ZF-HDs were used as queries to make BLASTP searches (E value < 1 × 10−10). The annotation file of ZF-HD_dimer domain (PF04770) was applied to build the HMM profile against the P. edulis protein dataset (E value < 1 × 10−10). The ZF-HD proteins were further identified by InterProScan (https://www.ebi.ac.uk/interpro/, accessed on 8 April 2023). A total of 24 PeZF-HD genes were identified in the moso bamboo genome and redundant sequences were removed.

4.3. Sequence Analysis

The molecular weight, length and isoelectric point of PeZF-HD proteins were analyzed by the ExPASy website (https://web.expasy.org, accessed on 20 April 2023) (Table 1). The CDS and genomic sequences of PeZF-HD were aligned to analyze the exon–intron structures using the GSDS online program [36]. The protein sequences were analyzed by the MEME program (http:/meme.nbcr.net/meme/intro.html, accessed on 20 April 2023) with the following parameters: the maximum number of motifs was 8, and the width of the optimum motif was 6–300. The subcellular location of the putative PeZF-HD proteins was predicted by Plant-mPLoc (http://www.csbio.sjtu.edu.cn/bioinf/plant-multi/, accessed on 20 April 2023).

4.4. Phylogenetic Analysis and Classification

The ZF-HD protein sequences of rice and Arabidopsis were obtained from the TIGR-Rice Genome Annotation Project and Arabidopsis Information resource, respectively [37,38]. The full-length amino acid sequences were aligned using Clustal X according to our previous report [39]. The phylogenetic tree was built using MEGA 7.0 software with the Maximum Likelihood (ML) algorithm and 1000 bootstrap replicates.

4.5. Analysis of Cis-Element in the Promoter Regions

To predict cis-regulatory elements in promoters of PeZF-HD genes, 2000 bp upstream sequences of the translational start codon were detected by PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 10 May 2023). The heat map was made using TBtools by counting the cis-regulatory elements on each promoter (Table S1) [40].

4.6. Chromosome Localization and Gene Duplication

The structural and positional information of PeZF-HDs on the chromosomes of moso bamboo was downloaded from the moso bamboo genome database [24]. The positions of PeZF-HDs on the moso bamboo chromosomes were drawn using the MapGene2Chromosome2 web tool (http://mg2c.iask.in/, accessed on 19 May 2023) [41]. The syntenic relationships of the ZF-HDs in moso bamboo, rice and Arabidopsis were analyzed using MCScanX with default parameters [42]. The results of the chromosomal location and synteny relationships were visualized by Circos software (http://mkweb.bcgsc.ca/circos) [43]. The duplication events of the PeZF-HDs were analyzed using MCScanX following the default parameters.

4.7. Calculation of Ka/Ks Ratios

The non-synonymous (Ka) and synonymous (Ks) replacement rates and Ka/Ks values of the duplicated ZF-HD gene pairs were calculated using KaKs_Calculator software v2.0 [44]. Evolutionary divergence times of the moso bamboo ZF-HD gene family were calculated by the bamboo-specific divergence time formula (T = Ks/2λ, λ = 6.5 × 10−9). The selection pressure of the duplicate gene pairs was determined by the Ka/Ks ratio [45].

4.8. Quantitative Real-Time PCR Expression Analysis

Total RNA extraction, cDNA synthesis and qPCR reaction were performed according to our protocol [39]. To confirm the specificity of the qPCR reactions, a melting curve was implemented. The PeNTB gene was used as an internal standard [46]. Data were calculated by the 2−ΔΔCT method [47]. The heat map was made by TBtools with a normalized row scale [40]. The expression results were analyzed by three independent biological replicates. Primers are shown in Table S2. The published transcriptome data of moso bamboo under PEG, NaCl and ABA treatments were obtained from the Gene Expression Omnibus database with the accession number GSE169067 (http://www.ncbi.nlm.nih.gov/geo, accessed on 10 April 2023).

5. Conclusions

In this study, genome-wide detection and analyses of the PeZF-HD gene family were conducted in moso bamboo. The twenty-four PeZF-HDs were classified into two main groups and eight subgroups based on the grouping principles of the rice and Arabidopsis ZF-HD family, which was further supported by their similar motif compositions and exon–intron structures. WGD or segmental duplications were indicated to have been the major driving force for the expansion of PeZF-HDs. Multiple PeZF-HD expressions were stimulated by various types of abiotic stress. Our results provide a valuable basis for the functional study of ZF-HD genes and facilitate the identification of candidate genes in moso bamboo stress response networks, which may shed a light on moso bamboo cultivation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants12234064/s1, Table S1: Detailed information of ZF-HDs identified in moso bamboo genome; Table S2: Catergory information of cis-elements in PeZF-HDs promoters; Table S3: Primers used in the paper; Table S4: Identification of conserved domains in PeZF-HD proteins using the SMART tool; Table S5: Quantitative distribution of each group of ZF-HDs in moso bamboo, rice and Arabidopsis; Table S6: The mode of gene duplication in PeZF-HDs; Table S7: The KaKs ratios and estimated divergence times for duplicate gene pairs of PeZF-HDs. References [48,49] are cited in the supplementary materials.

Author Contributions

Conceptualization, methodology and software, F.H. and C.T.; Data curation, J.W.; writing—original draft preparation, F.H.; writing—review and editing, F.H., J.W. and C.T. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by grants from the National Natural Science Foundation of China (32102410) and the Natural Science Foundation of Jiangsu province (BK20210394).

Data Availability Statement

The data is contained within the manuscript and Supplementary Materials.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Plants 12 04064 g001
Figure 1. Phylogenetic analysis of ZF-HD proteins from rice, Arabidopsis and moso bamboo. The tree was built using the Maximum Likelihood (ML) method with 1000 bootstrap replicates. The branched lines of the subtrees are colored to indicate different subgroups.
Figure 1. Phylogenetic analysis of ZF-HD proteins from rice, Arabidopsis and moso bamboo. The tree was built using the Maximum Likelihood (ML) method with 1000 bootstrap replicates. The branched lines of the subtrees are colored to indicate different subgroups.
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Plants 12 04064 g002
Figure 2. Phylogenetic relationships, gene structures and conserved domains of PeZF-HDs. (A) ML phylogenetic tree of PeZF-HDs. (B) Motif distributions in PeZF-HDs. The colored boxes represent motifs 1–8. Scale bar: 100 amino acids. (C) Exon–intron distribution of PeZF-HDs. The black lines and yellow boxes represent introns and exons, respectively. Scale bar: 500 bp.
Figure 2. Phylogenetic relationships, gene structures and conserved domains of PeZF-HDs. (A) ML phylogenetic tree of PeZF-HDs. (B) Motif distributions in PeZF-HDs. The colored boxes represent motifs 1–8. Scale bar: 100 amino acids. (C) Exon–intron distribution of PeZF-HDs. The black lines and yellow boxes represent introns and exons, respectively. Scale bar: 500 bp.
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Plants 12 04064 g003
Figure 3. Chromosome distribution and syntenic relationships of PeZF-HDs. Chromosomes are shown in a circular form. The duplicate PeZF-HD gene pairs are connected by black lines.
Figure 3. Chromosome distribution and syntenic relationships of PeZF-HDs. Chromosomes are shown in a circular form. The duplicate PeZF-HD gene pairs are connected by black lines.
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Figure 4. The cis-acting elements of PeZF-HDs promoters. The closed boxes of different colors represent different kinds of cis-acting elements.
Figure 4. The cis-acting elements of PeZF-HDs promoters. The closed boxes of different colors represent different kinds of cis-acting elements.
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Plants 12 04064 g005
Figure 5. Heatmap and cluster of PeZF-HDs expressions under cold (A), Nacl (B), PEG (C) and ABA (D) treatment. The relative expression levels of PeZF-HDs under these treatments are shown by fold-change values and converted to log2 format compared to the control. The x-axis represents the days of treatment. The color scale at the right of each heatmap represents relative expression levels. The qPCR results were obtained based on three biological and three technical replicates.
Figure 5. Heatmap and cluster of PeZF-HDs expressions under cold (A), Nacl (B), PEG (C) and ABA (D) treatment. The relative expression levels of PeZF-HDs under these treatments are shown by fold-change values and converted to log2 format compared to the control. The x-axis represents the days of treatment. The color scale at the right of each heatmap represents relative expression levels. The qPCR results were obtained based on three biological and three technical replicates.
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Table 1. Detailed information of ZF-HDs identified in moso bamboo genome.
Table 1. Detailed information of ZF-HDs identified in moso bamboo genome.
Gene NameCDS (bp)Size (aa)Mass (KDa)pIDomain Exon NumberLocationPredicted Localization
PeZF-HD181627129.36 9.41 ZF-HD1chromosomes 12:13827712:13828527:+Nucleus
PeZF-HD280126628.61 9.05 ZF-HD1chromosomes 3:49715743:49719049:+Nucleus
PeZF-HD376225327.04 8.50 ZF-HD2chromosomes 11:13377647:13378939:+Nucleus
PeZF-HD467222323.46 8.78 ZF-HD2chromosomes 18:35699501:35700292:+Nucleus
PeZF-HD571723824.80 6.36 ZF-HD2chromosomes 13:57959543:57960412:+Nucleus
PeZF-HD6116438740.65 8.59 ZF-HD1chromosomes 13:15365059:15366222:-Nucleus
PeZF-HD786728829.90 6.75 ZF-HD1chromosomes 22:13492044:13492910:+Nucleus
PeZF-HD863321022.79 8.41 ZF-HD2chromosomes 3:15339955:15340674:+Nucleus
PeZF-HD980426727.82 8.49 ZF-HD1chromosomes 24:36670935:36671738:-Nucleus
PeZF-HD1068422724.51 8.99 ZF-HD2chromosomes 9:63441848:63443360:+Nucleus
PeZF-HD11120640143.36 6.58 ZF-HD1chromosomes 3:87050975:87052180:-Nucleus
PeZF-HD12121240343.21 6.35 ZF-HD1chromosomes 17:17852519:17853730:+Nucleus
PeZF-HD133009910.57 8.60 ZF-HD2chromosomes 13:2989657:2990222:-Nucleus
PeZF-HD142799210.17 6.79 ZF-HD1chromosomes 18:45423575:45424757:-Nucleus
PeZF-HD1541713815.17 10.30 ZF-HD2chromosomes 11:2971936:2974744:+Nucleus
PeZF-HD1646215316.81 9.06 ZF-HD2chromosomes 12:2567371:2568681:+Nucleus
PeZF-HD1751917218.32 8.95 ZF-HD2chromosomes 2:29976915:29981334:+Nucleus
PeZF-HD18252838.59 6.86 ZF-HD2chromosomes 22:21025823:21026158:-Nucleus
PeZF-HD1934811511.41 5.90 ZF-HD2chromosomes 16:73535364:73537228:+Nucleus
PeZF-HD20106535436.91 7.26 ZF-HD1chromosomes 3:24470226:24471290:+Nucleus
PeZF-HD21103534435.64 7.71 ZF-HD1chromosomes 22:20913172:20914206:+Nucleus
PeZF-HD22104134635.73 6.97 ZF-HD1chromosomes 13:64992849:64993889:+Nucleus
PeZF-HD2395731833.41 6.73 ZF-HD2chromosomes 18:45322937:45323998:+Nucleus
PeZF-HD2480126627.63 8.14 ZF-HD1chromosomes 23:37483279:37484079:+Nucleus
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Huang, F.; Wang, J.; Tang, C. Genome-Wide Identification and Analysis of ZF-HD Gene Family in Moso Bamboo (Phyllostachys edulis). Plants 2023, 12, 4064. https://doi.org/10.3390/plants12234064

AMA Style

Huang F, Wang J, Tang C. Genome-Wide Identification and Analysis of ZF-HD Gene Family in Moso Bamboo (Phyllostachys edulis). Plants. 2023; 12(23):4064. https://doi.org/10.3390/plants12234064

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Huang, Feiyi, Jiaxin Wang, and Chao Tang. 2023. "Genome-Wide Identification and Analysis of ZF-HD Gene Family in Moso Bamboo (Phyllostachys edulis)" Plants 12, no. 23: 4064. https://doi.org/10.3390/plants12234064

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