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Plant AT-rich protein and zinc-binding protein (PLATZ) family in Dendrobium huoshanense: identification, evolution and expression analysis

BMC Plant Biology volume 24, Article number: 1276 (2024) Cite this article

Abstract

PLATZ (plant A/T-rich protein and zinc-binding protein) transcription factors are essential for plant growth, development, and responses to abiotic stress. The regulatory role of PLATZ genes in the environmental adaptation of D. huoshanense is inadequately comprehended. The genome-wide identification of D. huoshanense elucidates the functions and regulatory processes of the gene family. Our investigation encompassed the examination of PLATZ gene structures and chromosome distribution, the construction of the phylogenetic tree with its relatives, and the analysis of the cis-acting elements and expression profiles potentially implicated in growth and stress responses. Eleven DhPLATZs were classified into three clades (I, II, and III) according to their evolutionary homology. The distribution of these genes over six chromosomes indicated that both whole genome duplication (WGD) and segmental duplication events have contributed to the expansion of this gene family. The Ka/Ks analysis revealed a pattern of purifying selection after duplication occurrences, suggesting little alterations in functional divergence. The collinearity and microsynteny results revealed that the three DhPLATZ genes shared the same conserved domains as the paralogs from D. huoshanense and D. chrysotoxum. Expression profiling and quantitative analysis demonstrated that DhPLATZ genes had unique expression patterns in response to phytohormones and cold stress. Subcellular localization indicated that three DhPLATZ genes were expressed in the nucleus, suggesting their role as transcription factors. These findings enhance our understanding of PLATZ genes’ involvement in D. huoshanense species and underscore their significance as important areas for further research.

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Introduction

Transcription factors precisely regulate gene expression by indirectly attaching to DNA regions known as cis-acting elements, located within the promoters of target genes. In the realm of plants, the zinc finger transcription factor family is quite extensive [1]. They always participate in diverse biological processes such as plant growth, transcription control, and response to stress. Different types of zinc finger proteins have been found across plant species, including CCCH, ERF, DOF, WRKY, and PHD proteins [2]. Among these proteins, the PLATZ family is noteworthy as a zinc transcription factor that was first identified as the plant AT-rich sequence and zinc-binding protein 1 in peas [3]. It contains two conserved domains: the zinc finger domain and the DNA-binding domain, which are unique yet crucial for its function as a plant-specific transcriptional regulator [4]. Zinc finger proteins play a role in controlling biological functions, attracting considerable attention lately for their involvement in plant growth, hormonal reactions, and stress alleviation [5]. One example is OsDRZ1, a member of the C2H2-type zinc finger group known for its ability to handle stresses and influence the characteristics of young rice plants [6]. Another example is OsZFP36, which enhances tolerance to water and oxidative stress in plants [7]. AtC3H17, classified as a non-tandem CCCH zinc finger protein, functions as a positive regulator governing the development of plant organs and life cycles in A. thaliana [8]. Overexpression of the OsTZF1 gene has revealed its capacity to retard seed germination, impede seedling growth, and prolong leaf senescence [9].

PLATZ family members, the zinc-dependent DNA-binding proteins found across various species, have been extensively studied [9]. In peas, PLATZ1, initially identified as a zinc-dependent DNA-binding protein, features two conserved zinc finger motifs. In the same way, a PLATZ transcription factor controls leaf size and senescence in Arabidopsis by changing the expression of GRF1 and GRF4 in the GRF/GIF pathway [10]. In maize, the FL3 semi-dominant negative mutant displays severe endosperm defects, with FL3 specifically expressed in starch endosperm cells and interacting with RPC53 and TFC1, components of the RNAPIII transcriptional machinery. A study of the maize genome shows that it has 17 PLATZ genes, with 9 and 13 ZmPLATZs that can interact with RPC53 and TFC1, respectively [11]. The maize ZmPLATZ2 protein is activated by glucose and helps make starch by attaching to the promoters for starch synthetic processes, which changes the Glu signal pathway [12]. In rice, the PLATZ gene GL6 regulates grain development through cell proliferation promotion [13]. AtPLATZ1 and AtPLATZ2 contribute to seed desiccation tolerance, with AtPLATZ1 promoting dehydration tolerance in vegetative tissues and AtPLATZ2 negatively affecting plant salt tolerance by suppressing downstream gene expression [13]. Additionally, PLATZ1 from the cotton enhances osmotic and salt insensitivity during germination and seedling establishment in transgenic Arabidopsis by mediating the ABA, GA, and ethylene pathways [14, 15]. So far, the PLATZ gene family has been recognized across various species, with 13 PLATZ genes in A. thaliana, 15 in O. sativa, 17 in Z. may, 62 in T. aestivum, 9 in Rosa hybrida, 28 in Linum usitatissimum, 17 in Malus domestica, 27 in Phyllostachys edulis, 12 in Citrullus lanatus, and 11 in Ginkgo biloba [16,17,18].

D. huoshanense, classified as a perennial epiphytic plant within the Orchidaceae family, is esteemed as a traditional Chinese medicinal plant under national safeguard [19,20,21]. The cultivation of D. huoshanense encounters problems caused by various abiotic factors, such as low temperatures, elevated salinity, cold, and drought, which may detrimentally affect its growth and hinder the production of bioactive components [22,23,24]. Furthermore, the sequencing of the entire D. huoshanense genome provides a valuable asset for thorough molecular-level studies [25]. Although PLATZ proteins have been extensively studied in species like A. thaliana and Z. mays, the identification and expression analysis of the PLATZ gene family in Dendrobium species remains scarce. Our study utilized bioinformatics techniques to identify DhPLATZ genes and performed a comprehensive genome-wide analysis of D. huoshanense. This entailed the collection and identification of PLATZ genes in D. huoshanense, their categorization into three clades, and the analysis of their gene structure, conserved motifs, and evolutionary divergence. Furthermore, we delved into the roles of these genes by examining their promoter elements, expression patterns, and connections within networks. Subsequently, we carried out an experiment to pinpoint the locations of the 11 genes in the D. huoshanense genome. Analysis of RNA-seq data revealed how gene expression changes during exposure to MeJA and cold stress. Notably, DhPLATZ1, DhPLATZ3 and DhPLATZ5 exhibited responses to stressors, indicating their functions in coping with stress. DhPLATZ3 consistently showed activity post-MeJA treatment, suggesting its role in long-term responses to this stimuli. On the other hand, DhPLATZ1 exhibited alterations in gene expression upon exposure to MeJA, suggesting underlying mechanisms at play. Subcellular localization demonstrated that DhPLATZ2, DhPLATZ4, and DhPLATZ6 were expressed in the nucleus.

Materials and methods

Retrieving PLATZ protein sequences from databases

The genome and amino acid sequences of PLATZ proteins of D. huoshanense were downloaded from the Medicinal Plants Multi-Omics Database (MPOD) (http://applegbd.ynau.edu.cn/genome). The blastp program was used to find the PLATZ genes of D. huoshanense, using the protein sequence with the PF04640 domain as a query [26]. Following this, the acquired amino acid sequences underwent verification through retrieval against the NCBI Conserved Domain Database (https://www.ncbi.nlm.nih.gov/genome/) [27].

Properties, subcellular localization and cis-acting element analysis

Two sources were used to collect data on 11 PLATZ proteins: Protparam (https://web.expasy.org/protparam/) and MPOD. The MPOD provided information about the number and location of chromosomes, as well as the gene’s direction (sense or antisense) in that specific area. It also gave information on mRNA length (CDS) and peptide size. Protparam provided information about these proteins, such as theoretical pI, molecular weight, GRAVY (grand average of hydropathy), and stability index. The WoLF PSORT database (https://wolfpsort.hgc.jp/) was used to predict the subcellular localization. The 1500-base pair upstream promoter regions were obtained from PhytozomeV3 (https://phytozome-next.jgi.doe.gov). In each case, the web tool PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) was used to make a prediction of cis-acting elements of the promoters based on 5 to 20 base pairs of upstream sequence from the transcription start site. These outputs were shown as a heat map, using TBtools for visualization [28].

Analysis of conserved motif and exon-intron composition

The MEME program, which can be found online at (http://meme.sdsc.edu/meme/website/intro.html), was used to find conserved motifs in the amino acid sequences. The CDD (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi) database is used for the analysis and identification of conserved domains or superfamilies in amino acid sequences [26]. To analyze the distribution of exons and introns, the GSDS web tool (http://gsds.cbi.pku.edu.cn/) was used to process the genomic and CDS sequences of the DhPLATZ gene family [29, 30]. The gene structure display server (v.2.0) (http://gsds.cbi.pku.edu.cn/) was chosen to be a tool for studying the gene structure, and the exon-intron patterns were discovered.

Comparative phylogenetic analysis of PLATZ proteins

The amino acid sequences of DhPLATZ proteins were aligned with those from A. thaliana, L. tulipifera, and C. kanehirae to build a phylogenetic tree [31,32,33]. The software MEGA 11 was used with the maximum likelihood method to build the tree, and bootstrapping was done with 1000 replications. The tree was visually adjusted using the iTOL program (https://itol.embl.de/), which allows users to examine and annotate the phylogenetic relationships [34].

Whole genome duplication, collinearity and selection pressure analysis

The MCScanX program was used to make a collinearity plot between three Dendrobium species in order to uncover the type of duplication of PLATZ genes and the syntenic block of interspecies. The copies of genes were detected using MCScanX with default settings [35]. The MUSCLE program was used in the process of aligning protein sequences, while the Ka/Ks ratio was determined using TBtools, which served to reveal the pace of each gene pair’s evolution. To determine the time of divergence of these genes, the following formula, which incorporated T = Ks/2λ (λ = 6.56 × 10− 9) for monocot [36].

Sequence alignment and amino acid composition of DhPLATZ proteins

All DhPLATZ sequences were first aligned using the alignment program in MEGA X. To obtain the amino acid coloring results, the alignment file was uploaded to ESPript 3.0 (https://espript.ibcp.fr/ESPript/cgi-bin/ESPript.cgi).

Protein-protein interaction

The protein interactions among PLATZ proteins were conducted by utilizing the String database (https://string-db.org). This online resource contributed to an accurate description of the complicated web of interactions among protein domains and these PLATZ proteins of D. huoshanense [5].

Expression profiles of DhPLATZ genes under cold and MeJA treatment

The raw expression data of DhPLATZ genes were obtained from the NCBI GEO database (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE217439) to analyze and investigate their expression profiles in response to cold stress. For growth conditions, the annual plants were randomly selected and cultured at a temperature of 4 °C, under a light cycle of 12 h per day, with a light intensity ranging from1500 to 2000 lx [37]. These plants were then collected and frozen in liquid nitrogen at different time points (0 and 7 days) post-treatment, with each sample having three biological replicates. The expression levels of DhPLATZ genes were determined and normalized as FPKM using transcriptome datasets available at https://bigd.big.ac.cn/gsa/browse/CRA006607. The HISAT package was used to align all the reads to the D. huoshanense genome, and StringTie was used to calculate the FPKM values for mRNA expression analysis. Additionally, Salmon was utilized to compute expression levels from RNA-seq data. For hierarchical clustering analysis, the normalized FPKM values of the unigenes were employed [38].

qRT-PCR analysis of DhPLATZ genes

D. huoshanense materials used in this study were obtained from the tissue culture room at West Anhui University. Samples were grown in MS medium at 25 ± 2 °C, with a 12/12 h light/dark cycle and 60% relative humidity in a growth chamber. The seedlings were subcultured every 45 days until their stems were 5 to 8 cm tall. The 100 µmol/L ABA solution that had been made was added to the medium, and on days 0, 2, and 4, the levels of PLATZ genes were measured. Similarly, the samples were sprayed with a 50 µmol/L MeJA solution, and samples were collected at days 0, 2, and 8. The prepared 0.1 mg/L IAA solution and 100 µmol/L salicylic acid solution were added to the culture medium, and the expression levels of the PLATZ gene were measured on days 0, 2, and 4. The plants were sprayed with the prepared 0.5 mmol/L GA solution, and samples were collected on days 0, 3, and 6, and the expressions of PLATZ genes were determined. After 4 °C low-temperature treatment, samples were collected on days 0, 1, and 4, and the expression of PLATZ genes was determined. Total RNA of the seedling leaves was extracted and reverse transcribed using the Total RNA Extractor (Trizol) extraction kit. Random Primer p(dN)6, dNTP Mix, and RNase-free ddH2O were added to an RNase-free PCR tube in an ice bath, mixed, centrifuged, and incubated at 65 °C for 5 min before being placed on ice. For reverse transcription, 5X RT Buffer, RNase Inhibitor, and Maxima Reverse Transcriptase were added. Real-time quantitative PCR analysis used the SybrGreen qPCR Master Mix method. The cDNA sample was diluted 10 times before it was used in PCR. 2X SG Fast qPCR Master Mix, forward and reverse primers, and ddH20 were then added. The 96-well plate with the added sample was placed in a fluorescent quantitative PCR instrument for reaction determination. The Actin was chosen as internal reference gene according to previous studies [38].

Subcellular localization analysis

The vector construction primarily uses homologous recombination and Golden Gate seamless cloning techniques. According to the existing target gene sequence and designed primers, the target gene was amplified using the BioRun Magic PCR Mix kit. After the PCR, the product was obtained by gel recovery, and the target gene and vector pAN580 were cut twice with BsmB1 and Esp31, following the cutting site of the restriction enzyme. After mixing, the mixture was centrifuged instantly and then kept in a water bath at 37 °C for 1 h. The pAN580 vector was connected with the three genes DhPLATZ2, DhPLATZ4, and DhPLATZ6, respectively, mixed evenly, centrifuged instantly, and connected at 37 °C for 30 h. Take the competent Escherichia coli cells and melt them on ice. Take 5–10 µL of the connection product to the competent medium, place it on ice for 30 min, water bath at 42 ℃ for 90 s, and ice bath for 5 min. Add 400 µL of LB liquid culture medium and activate it on a shaker at 37 ℃, and 180 rpm for 40–50 min. After the end, centrifuge it instantly, discard 200 µL of supernatant, blow and mix the remaining bacteria, take 50 µL to coat the Amp resistance plate, and invert it in a 37℃ constant temperature incubator for overnight culture. The leaves of Nicotiana benthamiana seedlings were cultured at about 5 °C for 15–20 d, and then 5–10 mL of enzymatic solution was added to soak the tissue. Let the enzymatic hydrolysis stand for 4 h at 24 °C, filter with a 40 μm filter, and centrifuge. After removing the supernatant, wash it twice with 10 mL of pre-cooled W5 solution and centrifuge it for 3 min. Add an appropriate amount of MMG solution to suspend it to a concentration of 2 × 105/mL, and select round and less broken protoplasts under a microscope. Take 200 µL of protoplast suspension and add 20 µL of DNA (10 µL of vector plasmid + 10 µL of marker plasmid), gently and evenly mix it with an equal volume of PEG 4000 solution, and let it stand at room temperature for 10–15 min. To dilute and terminate the reaction, 1 mL of W5 was used, centrifuged to collect the protoplasts, and the supernatant was removed. 1 mL of W5 was added to the protoplasts and washed twice, then 1 mL of W5 solution was added and incubated in the dark at 25 °C for 18–24 h. 100 µL of protoplasts were placed under a fluorescence microscope or laser confocal microscopy.

Results

Identification and physical properties of DhPLATZ genes

Genome-wide analysis was carried out to determine the DhPLATZ genes in the D. huoshanense genome. The PF04640 domain was chosen as the query, and the Blastp search was done on the D. huoshanense genome database deposited on MPOD. A total of 11 DhPLATZ proteins were identified and their sequences were explored using the Pfam, InterPro, and SMART databases to ensure the plant AT-rich protein and zinc-binding protein domains (Table 1). Additionally, the molecular weights of the DhPLATZ proteins were found to be between 20189.8 and 38554.21 kDa, with an average of 27217.74 kDa. The isoelectric point (pI) were approximately 7.62 to 10.04, with an average of 8.55. The GRAVY is in the range of -0.011 to -0.671, with an average of -0.31945. Within the 11 DhPLATZ genes analyzed, five were found on chromosome 7, with two genes each on chromosomes 3 and 6. It was also seen that one such gene exists on different chromosomes 8, 14, and 17 independently. After conducting a detailed analysis of gene orientations, it was discovered that five DhPLATZ genes were intrinsic to moving forward (F), while the remaining six were located in the reverse (R) position. Prediction of the subcellular localization showed that most PLATZ genes were predicted to be localized in the nucleus, with only DhPLATZ5 localized in the chloroplast.

Table 1 DhPLATZ genes discovered in the D. huoshanense genome
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Chromosome mapping analysis of DhPLATZ genes

Chromosome 7 hosts the majority of PLATZ genes, including DhPLATZ1, DhPLATZ2, DhPLATZ3, and DhPLATZ5. Other chromosomes also contain specific DhPLATZ genes, such as DhPLATZ10 and DhPLATZ6 on chromosome 3, DhPLATZ8 and DhPLATZ9 on chromosome 6, and DhPLATZ4 on chromosome 8. Chromosome 14 contained DhPLATZ7, and chromosome 17 bears DhPLATZ11. These findings provide insights into the chromosomal mapping of DhPLATZ genes (Fig. 1).

Fig. 1
figure 1

The chromosomal distribution of DhPLATZ genes indicates their dispersion across different chromosomes. Eleven PLATZ genes are spread on six chromosomes

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Whole-genome duplication and selection pressure analysis of DhPLATZ genes

MCScanX software was applied to do a genome-wide synteny analysis of D. huoshanense to find the exact gene duplication from which the DhPLATZ gene came. A dotplot shows the distribution and gene duplication of these DhPLATZ genes on the chromosomes (Fig. 2). The results showed that Dhu0000009245 (DhPLATZ1), Dhu000009024 (DhPLATZ2), and Dhu000008902 (DhPLATZ3), all located on chromosome 7, had emerged from WGD or segmental duplication. Dhu000018013 (DhPLATZ6) and Dhu000025488 (DhPLATZ10) are originated from tandem duplications on chromosome 3. For other DhPLATZ genes, it may be obtain through dispersed duplication or transposition. In the investigation of Ka/Ks ratios, a total of 21 duplicate pairs of DhPLATZ genes were identified in the D. huoshanense genome (Table S1). Analysis of Ka/Ks ratios revealed that DhPLATZ6_DhPLATZ10 and DhPLATZ5_DhPLATZ11 demonstrated higher Ka/Ks values (0.8401 and 0.434, respectively). Conversely, DhPLATZ1_DhPLATZ2 and DhPLATZ1_DhPLATZ3 exhibited lower values (0.066 and 0.082, respectively). The estimation of divergence time, expressed in million years ago (MYA), corroborates these findings. Pairs with lower MYA values, like DhPLATZ8_and DhPLATZ9, and DhPLATZ5_and DhPLATZ11, show more recent divergence. On the other hand, pairs with higher MYA values, like DhPLATZ1 and DhPLATZ10, and DhPLATZ9 and DhPLATZ11, show more ancient divergence from a common ancestor (Fig. 3).

Fig. 2
figure 2

Whole-genome duplication analysis of the PLATZ genes. The red boxes are WGD or segmental duplication, while the green boxes are tandem duplication

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Fig. 3
figure 3

The expression Ka/Ks represents the ratio of mutations involving synonymous substitutions (Ks) to mutations involving non-synonymous substitutions (Ka). The gene duplication over selection and evolutionary pressure to paralogous pairings of DhPLATZ genes were calculated based on Ks and Ka values

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Microsynteny analysis of DhPLATZ genes

We used colinearity to build gene-conserved blocks that showed the evolutionary relationship of PLATZ homologs among Dendrobium species (Fig. 4). The results showed that Dhu0000009245 (DhPLATZ1), Dhu000009024 (DhPLATZ2), and Dhu000008902 (DhPLATZ3) on chromosome 7 all shared colinear blocks with Dnobile13G00724.1 on the CM039730.1 fragment of D. nobile. Dhu000009245 (DhPLATZ1) also shared a colinear block with Dnobile13G01342.1 on the CM039730.1 fragment. Dhu000009024 (DhPLATZ2) and Dhu000008902 (DhPLATZ3) share colinear blocks with Maker79634 on CM034309.1 fragment of D. chrysotoxum. Dhu000009245 (DhPLATZ1) shares a colinear block with Maker66867 on CM034309.1 fragment (Table S2). Our findings demonstrated that Dendrobium PLATZ family had a common evolutionary origin. The expansion of PLATZ homolog might happen through WGD or segmental duplication.

Fig. 4
figure 4

Syntenic blocks of evolutionarily conserved PLAZT genes in D. huoshanense, D. nobile and D. chrysotoxum. The red blocks represent the orthologous genes of DhPLATZ, and the yellow lines indicate the colinearity between them

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Phylogenetic analysis of DhPLATZ proteins

PLATZ proteins from four plant species, D. huoshanense, A. thaliana, L. tulipifera, and C. kanehirae show different phylogenetic relationships (Table S3). The PLATZ proteins were categorized into three distinct groups, designated as I–III. The analysis involved a total of 56 genes, with 11 from D. huoshanense, 13 from A. thaliana, 11 from L. tullipifera, and 21 from C. kanehirae. Based on the homology between proteins, DhPLATZ10, AtPLATZ10, and AtPLATZ12 were clustered into a small branch, while DhPLATZ8 and DhPLATZ9 were clustered into a class with AtPLATZ2. To make it easier to grasp the relationships between them, each category was assigned a color: green for Clade I, blue for Clade II, and red for Clade III (Fig. 5).

Fig. 5
figure 5

The phylogenetic relationships of PLATZ genes from four plant species(D. huoshanense, A. thaliana, L. tulipifera, and C. kanehirae). The number in the branches was the branch length

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The exon-intron structure, conserved motifs and domains of DhPLATZ proteins

For gene structure analysis, the intron and exon composition of DhPLATZ was examined. It was indicated that only DhPLATZ6 and DhPLATZ7 retained complete exons, introns, and 5’ and 3’ UTRs. DhPLATZ10, DhPLATZ11, DhPLATZ8, DhPLATZ2, and DhPLATZ4 all contain only 3’UTR. The longest intron is from DhPLATZ4, followed by DhPLATZ1. While DhPLATZ5 only has one truncated exon, we speculate that DhPLATZ6 and DhPLATZ7 have complete transcriptional regulatory functions. DhPLATZ4 stood out with one exon and no introns. On the other hand, DhPLATZ10 and DhPLATZ8 showed a pattern, with six exons and five introns and five exons and four introns, respectively, showing a high level of similarity among these genes (Fig. 6A). In the domain analysis across the 11 DhPLATZ proteins, all DhPLATZs containing a conserved domain was identified as PLATZ domain. This major domain was further categorized into four subfamilies, such as Bbox2, the UBR-box superfamily, the PLATZ superfamily, and the HAD-like superfamily. Notably, Bbox2 was present in one gene (DhPLATZ3), the UBR-box superfamily was present in DhPLATZ5, and the HAD_like, PLATZ, and PLATZ superfamilies were all present in DhPLATZ10 simultaneously. This underscores a significant level of conservation of the PLATZ domain across all 11 DhPLATZ genes (Fig. 6B). Our examination of conserved motifs among the 11 DhPLATZ genes revealed that no motif was consistently conserved across the entire gene set. Motif conservation was investigated according to domain categorization. The PLATZ domain is highly conserved and has motifs (1, 3, and 4), while Bbox2 contains motifs (2, 5, 6, and 10), the UBR-box superfamily has motifs (1, 2, 3, 4, and 5), and the HAD_like superfamily contains motifs (1, 3, 9, 6, 7, and 4). The PLATZ superfamily contained only one motif (Motif 5). This observation suggests that each PLATZ gene possesses distinct functions. The fact that motifs are composed of different parts suggests that they have unique regulatory elements or functional properties that set them apart from other gene families (Fig. 6B).

Fig. 6
figure 6

Gene structure and conserved domain and motif analysis of DhPLATZ proteins. (A) The intron-exon structure is phylogenetically represented, blue color represent exons and black line show introns. (B) The domain pattern and 10 motifs of all DhPLATZ in D. huoshanense were visualized which represent the domain and motif conservation

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Sequence alignment and amino acid composition of DhPLATZ proteins

DhPLATZ contains a typical PLATZ transcription factor domain, including two zinc finger domains and a DNA-binding domain. The first zinc finger domain is located at the C-terminus, i.e., the C-X12-C-L-C-D-C-X4-L-C-X-X-C motif, and the second zinc finger domain is located at the N-terminus, i.e., the C-X-X-C-X-R-X-L-X-D/E-X-F/Y-X-X-C-S-L-G-C-K-L motif. The DNA-binding domain contains the conserved X4-Q-I-R-R-S/Y-X-Y-H motif. The other DNA-binding domain is located at the N-terminus, composed of the R-R-K-G-I/V-P-X-R-A/S-P conserved motif. There is a signal peptide of 14 short peptides at the start of the protein sequence. This may have something to do with where the PLATZ transcription factor is located in the nucleus (Fig. 7).

Fig. 7
figure 7

Multiple sequence alignment and amino acid composition of PLATZ proteins. The blue line represents the conserved domain of PLATZ transcription factors

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Protein-protein interaction of DhPLATZ proteins

For the protein-protein interaction, 5 nodes and 5 edges were identified. The average node degree was calculated as 2, with an average local clustering coefficient of 0.667. Surprisingly, the expected number of edges was zero, and the p-value for protein-protein interaction enrichment was exceptionally low at 1.89 e− 10, indicating a significant enrichment of interactions. To meet the minimum interaction score, a low confidence threshold of 0.150 was applied. Among the 11 examined DhPLATZ proteins, only four (DhPLATZ3, DhPLATZ7, DhPLATZ10, and DhPLATZ11) displayed interactions. Notably, each DhPLATZ protein of the four DhPLATZs exhibited the highest number of interactions, being associated with four other proteins, while all proteins demonstrated self-associations. DhPLATZ3 and DhPLATZ11 have 4 interactions (including themselves), while DhPLATZ7 and DhPLATZ10 have 3 interaction (Fig. 8).

Fig. 8
figure 8

The interaction of of the DhPLATZ proteins and periodic gene regulation. The black lines represent they are co-expression

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Cis-acting element analysis of DhPLATZ genes

Cis-acting elements, found in coding and non-coding genome regions, coordinate regulatory networks, modulating genes in response to stimuli and influencing stress- or tissue-specific expression patterns. These patterns are often dictated by cis-acting elements in gene promoters, which can be grouped into phytohormone responses, stress responses, and growth and development (Fig. 9). There are many patterns in promoter regions that are linked to growth and development. These patterns include the Skn-1_motif, the GCN4_motif, the MRE, the Box-4, the CAT-box, the O2-site, and the circadian elements. The DhPLATZ genes contained a wide range of cis-regulatory elements. The CAT-box motif (6%) is mainly related to meristem expression. The MRE (8%) and Box-4 (66%) motifs control zein metabolic processes and plant growth in response to light, respectively [35]. Additionally, specific elements, such as the TGA element, are implicated in auxin sensitivity, while the ABRE motif and P-box are associated with gibberellin responses and ERE for ethylene-responsive expression. The CGTCA motif and the TGACG motif, which are linked to methyl jasmonic acid (MeJA) responsiveness, stand out as the most common cis-elements. There are five phytohormone responses that have been identified: ABRE (28%), P-box (5%), TGACG motif (25%), TCA-element (17%), and CGTCA motif (25%). These are linked to responses to salicylic acid (SA), abscisic acid (ABA), ethylene, and meja. Moreover, different stress-response elements, like ARE (31%), LTR (15%), MBS (24%), and W box (24%), are linked to responses to light stress, cold stress, and drought stress. This helps us understand how the DhPLATZ gene responds to abiotic stress (Table S4).

Fig. 9
figure 9

The distribution of cis-elements within the DhPLATZ gene family. The regions of high value are represented in red and those of low value in green. Panel B illustrates the classification of cis-elements and their respective percentages

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Expression profile analysis of DhPLATZ genes under cold and MeJA treatment

To investigate their expression profiles in response to cold stress and MeJA, the transcriptome data from a public database and previous study were used to analyze the expression pattern of the DhPLATZ genes (Tables S5 and S6). Significant changes in gene expression levels appeared in response to cold stress. Notably, several DhPLATZ genes exhibited upregulation, including DhPLATZ1, DhPLATZ3, and DhPLATZ10, with substantial increases in expression levels compared to the control. DhPLATZ2, DhPLATZ8 and DhPLATZ9 showed upregulated expression under cold stress, while the remaining genes displayed responses that shed light on how control systems regulate plant responses to stress (Fig. 10A). Over different time intervals, the effect of MeJA application on the expression levels of various genes was investigated. We analyzed how DhPLATZ genes behaved after being treated with JA for durations ranging from 0.25 to 16 h [36]. Interestingly, DhPLATZ3 showed a consistent rise in expression levels during the peak at 8 h post-treatment, then gradually declined. In contrast, DhPLATZ1 initially experienced a drop in expression at 0.25 h, followed by a decrease at 1 h, and continued to decrease over time points. DhPLATZ4, DhPLATZ5, and DhPLATZ6 displayed responses with fluctuating levels of expression across time periods. On the other hand, DhPLATZ7 demonstrated alterations in expression throughout the study period. These results underscore how gene activity evolves dynamically in response to JA treatment, shedding light on the mechanisms involved in stress responses (Fig. 10B).

Fig. 10
figure 10

The expression profile of DhPLATZ genes. (A) The expression profile of DhPLATZ genes in response to a 7-day cold treatment. (B) The expression profile of DhPLATZ genes under MeJA application at different times

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RT-PCR analysis of DhPLATZ genes under phytohormones and cold stress

To clarify the expression of DhPLATZ genes in response to abiotic stress, the expression patterns of 11 DhPLATZ genes were analyzed under different hormones and cold treatments (Table S6). The expression levels of 11 PLATZ genes were analyzed by the qRT-PCR method, with actin as the internal reference gene (Table S7). The results showed that DhPLATZ5 was strongly induced by ABA, MeJA, and IAA, with the highest expression levels on the 4th, 8th, and 4th days of treatment, respectively. Similarly, DhPLATZ11 was also strongly induced by ABA, reaching a peak on the 4th day. Cold stress significantly increased the expression of DhPLATZ1, reaching its a peak on the 2nd day and then gradually decreasing. Cold treatment also induces DhPLATZ5 expression. In addition to DhPLATZ5, IAA treatment also induced the expression of DhPLATZ2, DhPLATZ3, and DhPLATZ10. SA can significantly induce the expression of DhPLATZ5, DhPLATZ8, and DhPLATZ9, among which DhPLATZ9 is most obviously activated by SA. GA treatment could slightly increase the expression of DhPLATZ2, DhPLATZ4, and DhPLATZ7 but did not reach a significant level (Fig. 11).

Fig. 11
figure 11

The expression pattern of DhPLATZ genes under different hormone and cold treatments. (A) ABA treatment; (B) MeJA treatment; (C) IAA treatment; (D) Cold treatment; (E) SA treatment; (F) GA treatment

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Subcellular localization of DhPLATZ genes

To verify the expression location of PLATZ genes in cells, we constructed a fusion protein co-expression vector with GFP and mkate genes. Three genes, DhPLATZ2, DhPLATZ4 and DhPLATZ6, were randomly selected and recombined with the green fluorescent protein (GFP) gene to construct fusion proteins, and the nuclear localization marker (mKATE) was co-localized in tobacco protoplasts. The results showed that the protoplasts containing GFP control showed green fluorescence as a whole, while the protoplasts introduced with DhPLATZ2-GFP, DhPLATZ4-GFP, and DhPLATZ6-GFP only found green fluorescence signals in the nucleus, which overlapped with the nuclear maker red fluorescent protein mKATE signal, and the chloroplast channel only had chloroplast autofluorescence (Fig. 12). These results indicate that DhPLATZ2, DhPLATZ4 and DhPLATZ6 proteins are all localized in the nucleus.

Fig. 12
figure 12

Subcellular localization of DhPLATZ2, DhPLATZ4, and DhPLATZ6 genes. Green fluorescence is GFP protein, red fluorescence is mKATE nuclear marker, and purple is chloroplast fluorescence. The scale bar is 10 μm

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Discussion

A genome-wide examination was carried out to view and identify DhPLATZ genes in the D. huoshanense genome. The physicochemical characteristics of the 11 DhPLATZ proteins were deeply studied to differentiate the members of the gene family that were specified. Our study showed that all but one of the DhPLATZ proteins were hydrophilic, which was shown by their negative GRAVY values (which are based on pH and the ability to interact with water) and charge, which could be positive or negative. Additionally, instability index analysis disclosed that only the DhPLATZ11 protein possessed characteristics reflecting stability, whereas the remaining proteins had features suggesting instability [39, 40]. DhPLATZ proteins were hydrophilic, which, together with their GRAVY value and instability index, determined their stability within the cell [41]. The results shed light on the structure-function relationships of DhPLATZ proteins and their role in physiological and stress tolerance mechanisms [42]. Studies have revealed many cis-acting elements in the promoters of DhPLATZ genes that are connected to plant hormones and stress reactions. This shows that they play a part in controlling gene expression in some situations [43]. Elements such as ABRE, P box, TGACG motif, and CGTCA motif were connected to hormone sensitivity, while stress-related elements like ARE, LTR, MBS, and W box are linked to environmental stresses. These results suggest that PLATZ transcription factors combine signals, such as plant hormones and environmental pressures, to regulate genes in response to stress and synchronize plant adaptation to stressful situations [44]. The PLATZ domain of all DhPLATZ proteins is very similar, but there are differences in the Bbox2, UBR-box, PLATZ, and HAD_like superfamilies. Motif conservation was associated with domain classification, even though no single motif was shared by all the genes. In particular, there is significant conservation between the PLATZ domain and certain motifs, indicating that the PLATZ domain is critical in stress response control. Every subfamily also has distinct motifs, which may aid in differentiating the regulatory components or functional characteristics of PLATZ genes. Thus, they play different roles in stress adaptation.

The evolutionary and exon-intron analysis of the DhPLATZ gene family shares insights into their diverse functions and genetic structure, complementing their involvement in plant stress response mechanisms [16]. By studying where DhPLATZ proteins were located within cells, it becomes evident that they exhibit distribution patterns in the nucleus, indicating a potential role in regulating gene expression. Moreover, the presence of most PLATZ proteins in the nucleus suggests involvement in the transcription of signaling-transduction genes. The identification of these proteins within cell organelles emphasizes their significance in plant biology [45]. Analyzing their structural composition reveals intriguing patterns, such as DhPLATZ4 having a single exon structure while DhPLATZ10 and DhPLATZ8 share similar exon-intron configurations. A study on the genes in plant species delved into their evolutionary paths and whether they had evolved differently or remained similar in function [46]. The distinct color codes assigned to each group make it easier to understand how they have evolved and find any connections between their functions. This indicates that PLATZ genes from the lineage might share functions and regulatory mechanisms [47]. Understanding the functions and evolutionary relationships of genes has provided a clearer view of how they contribute to plant adaptation and growth under stressful conditions. This knowledge has inspired ideas and breeding efforts focused on enhancing crop yield and resilience in different environments [48]. Based on the orthologous genes in A. thaliana, we can preliminarily infer the functions of some DhPLATZ genes. Some studies have shown that AtPLATZ11 and AtPLATZ12 are highly expressed in meristems, while AtPLATZ1, AtPLATZ3, and AtPLATZ11 are highly expressed in roots, leaves, seedlings, and stems, and AtPLATZ5 is highly expressed in seeds. AtPLATZ5 plays a role in salt stress response, and AtPLATZ1 and AtPLATZ2 can regulate seed dehydration tolerance [49]. AtPLATZ2 lowers the ability to handle salt by targeting and blocking CBL4 and CBL10 [50]. Analysis of drought resistance of overexpressed PLATZ4 and mutant strains revealed that the stomatal aperture of the PLATZ4 overexpression strain was reduced and drought resistance was significantly enhanced, while the stomatal aperture of PLATZ4-RNAi and platz4 mutants was increased and drought resistance was significantly reduced. This revealed that PLATZ4 plays a key role in plant drought resistance by regulating ABA signaling and stomatal movement [51]. Since AtPLATZ1 has a high homology with DhPLATZ7, we infer that the latter plays an important role in the drought resistance of D. huoshanense. We speculate that DhPLATZ8 and DhPLATZ9, belonging to the same subclade as AtPLATZ2, may contribute to its resistance to salt stress.

Observing gene duplication and evolutionary relationships within the gene family in D. huoshanense provides valuable insights into their evolutionary history and functional similarities [52, 53]. The presence of genes on chromosomes, especially chromosomes 3, 14, 6, 7, 8, and 17, suggests a complex chromosomal layout with potential areas prone to gene duplication events. Ka/Ks ratios show the evolutionary pressures on genes that have been copied [54]. They measure the rates of non-synonymous (Ka) to synonymous (Ks) substitutions. Higher Ka/Ks ratios in pairs like DhPLATZ6_and DhPLATZ10, as well as DhPLATZ5 and DhPLATZ11 suggested that new functions may have been obtained through selection or changes in functions after duplication [55]. Conversely, lower Ka/Ks ratios in pairs such as DhPLATZ1_DhPLATZ2 and DhPLATZ1_DhPLATZ3 suggest conservation of function or purifying selection among duplicated genes. The estimation of divergence times further supports these findings by revealing divergences from an ancestor based on MYA values [56]. The syntenic analysis uncovered both tandem duplications within the D. huoshanense genome, shedding light on mechanisms that have influenced the gene family’s evolution. Tandem duplications observed on chromosomes 3, 6, and 7 occur when DNA segments were duplicated consecutively on a chromosome, potentially contributing to the expansion of gene families with functions [57, 58]. Segmental duplications discovered on chromosomes 8, 14, and 17 involve replicating sections of the genome. This may help preserve duplicated genes with functions across chromosomes. These discoveries showcase the evolving dynamics that influence the gene family in D. huoshanense, where gene duplication events greatly impact changes of trait-related genes and germplasm resources conservation.

The protein-protein interaction study revealed significant interactions among DhPLATZ proteins, suggesting their involvement in complex regulatory networks governing gene expression [59]. The fact that only four DhPLATZ proteins (DhPLATZ3, DhPLATZ7, DhPLATZ10, and DhPLATZ11) displayed interactions implies that these interactions have specific functional roles. Each DhPLATZ protein is associated with the highest number of interactions, including self-associations, indicating potential roles in forming protein complexes or regulatory complexes involved in gene expression regulation. These interactions likely facilitate the recruitment of transcriptional co-regulators or chromatin remodeling factors, influencing the expression of stress-responsive genes regulated by PLATZ transcription factors [60]. The expression of DhPLATZ genes has been discovered to play a role in stress resistance under cold and MeJA stress, as evidenced by dynamic expression patterns that are significant for the stress adaptation mechanisms in D. huoshanense [61, 62].

PLATZ TFs play a role in helping plants adapt to JA when faced with environmental stresses. By attaching to DNA sequences in the gene promoters, they work as transcription factors and change genes that are important for adapting to different climates and protecting against JA [63]. When plants encounter stress, PLATZ genes are activated, indicating their involvement in triggering stress-related pathways, such as gene expression during challenging conditions and regulating hormones. PLATZ were exposed as the key players in plant defense mechanisms along the path of their acclimatization to severe ambient conditions [22]. In addition to the important roles of AtPLATZ1, AtPLATZ2, and AtPLATZ4 mentioned in drought and salt stress, some other PLATZ genes have also been functionally identified in Arabidopsis. AtPLATZ7 regulates root ROS accumulation through the RGF1 signaling pathway, thereby influencing meristem development [64]. Transgenic Arabidopsis plants that had ectopic expression of GhPLATZ1 showed faster seed germination and better seedling establishment in salt and mannitol stress situations. Seed germination occurred more rapidly; nevertheless, the seedling establishment of transgenic Arabidopsis was comparable to that of wild type [49]. PAC, a gibberellin production inhibitor, had no effect on GhPLATZ1 transgenic or wild-type. However, exogenous GA may help even out the differences in growth between GhPLATZ1 transgenic and wild-type Arabidopsis when exposed to salt stress. DhPLATZ1, DhPLATZ3, and DhPLATZ5 were upregulated in cold stress; hence, this suggests their relevance in cold tolerance. Importantly, DhPLATZ2 and DhPLATZ11 levels decreased, implying adaptability to cold stress. DhPLATZ3 has been a continuously induced gene during MeJA treatment, peaking at 8 h after treatment started, which may suggest involvement in MeJA long-term responses. In response to MeJA, DhPLATZ1 showed an intricate regulatory model with a decreasing tendency, followed by multiple up- and down-regulations. DhPLATZ4, DhPLATZ5, and DhPLATZ6 displayed levels of regulation that highlighted the control of genes. These findings underscore the systems of processes that responded to stress and pinpoint specific DhPLATZ genes crucial for D. huoshanense’s ability to adapt to cold and MeJA stress. The results obtained in this study may contribute to the development of crop varieties that perform effectively in challenging conditions.

Conclusion

Here, eleven DhPLATZ genes were identified in D. huoshanense. Although the 11 DhPLATZ genes were unevenly distributed on six chromosomes, whole genome duplication and colinearity analysis revealed the important role of WGD and tandem duplication in PLATZ gene evolution and expansion. The conserved evolutionary blocks showed that DhPLATZ and the orthologous genes of D. nobile and D. chrysotoxum all came from the same ancestor. Phylogenetic, conserved motif, and conserved domain analyses revealed that DhPLATZ on the same branch had similar compositions. Amino acid composition and protein-protein interaction analysis showed that they had DNA-binding domains, which may be related to their transcriptional activation properties. Expression patterns and qRT-PCR analysis of DhPLATZ1, DhPLATZ3, and DhPLATZ5 showed activation during stress, indicating their significance in cold stress and phytohormone application. DhPLATZ3 consistently showed activity under MeJA treatment, suggesting its role in prolonged responses to MeJA induction. The subcellular localization experiment confirmed that DhPLATZ2, DhPLATZ4, and DhPLATZ6 were expressed in the cell nucleus. These results show that the DhPLATZ gene family plays a big part in how plants adapt to stress. This helps us learn how to make targeted strategies that help this plant more resistant to stress.

Data availability

The datasets of this study are included in the manuscript and additional file. The genome sequence of D. huoshanense were downloaded from the NCBI database with accession code PRJNA597621. The raw sequence data of transcriptome used in this study was obtained from the GSA database of NGDC with accession code CRA006607.

Abbreviations

PLATZ:

Plant A/T-rich protein and zinc-binding protein

WGD:

Whole genome duplication

MeJA:

Methyl jasmonic acid

GFP:

Green fluorescent protein

MYA:

Million years ago

MPOD:

Medicinal Plants Multi-Omics Database

TF:

Transceiption Factor

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Acknowledgements

Not applicable.

Funding

This work was supported by National Health Commission Scientific Research Fund (SBGJ202301010) and Joint construction project of Henan Provincial Medical Science and Technology Research Program (LHGJ20190550).

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Authors and Affiliations

  1. College of Biological and Pharmaceutical Engineering, West Anhui University, Luan, 237012, China

    Fangli Gu, Renshu Huang, Naifu Chen & Cheng Song

  2. Henan Key Laboratory of Rare Diseases, Endocrinology and Metabolism Center, The First Affiliated Hospital, College of Clinical Medicine of Henan, University of Science and Technology, Luoyang, 471003, China

    Yanshuang Ren, Tingting Wang & Yingyu Zhang

  3. Department of Plant Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 201109, China

    Muhammad Aamir Manzoor

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  1. Fangli Gu
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  2. Yanshuang Ren
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  5. Renshu Huang
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  7. Cheng Song
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Contributions

Fangli Gu: Investigation, Formal analysis, Software, Writing-Original Draft, Writing - Review & Editing. Yanshuang Ren: Formal analysis, Writing-Original Draft, Software. Muhammad Aamir Manzoor: Investigation, Software, Writing-Review & Editing. Tingting Wang: Investigation, Formal analysis. Renshu Huang: Investigation, Formal analysis, Software, Writing-Original Draft. Naifu Chen: Supervision, Resources, Writing - Review & Editing. Yingyu Zhang: Investigation, Formal analysis, Funding acquisition, Writing-Review & Editing. Cheng Song: Supervision, Formal analysis, Data Curation, Resources, Writing - Review & Editing.

Corresponding authors

Correspondence to Cheng Song or Yingyu Zhang.

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The authors declared that permission to collect D. huoshanense material has been obtained and that it complies with institutional, national, and international guidelines.

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The authors declare no competing interests.

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Gu, F., Ren, Y., Manzoor, M.A. et al. Plant AT-rich protein and zinc-binding protein (PLATZ) family in Dendrobium huoshanense: identification, evolution and expression analysis. BMC Plant Biol 24, 1276 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12870-024-06009-0

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12870-024-06009-0

Keywords

BMC Plant Biology

ISSN: 1471-2229

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