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Article

The Moso Bamboo D-Type Cell Cycle Protein Family: Genome Organization, Phylogeny, and Expression Patterns

by
Hui Fang
,
Changhong Mu
,
Jutang Jiang
,
Jian Gao
and
Zhanchao Cheng
*
Key Laboratory of National Forestry and Grassland Administration/Beijing for Bamboo and Rattan Science and Technology, International Center for Bamboo and Rattan, Beijing 100102, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(2), 289; https://doi.org/10.3390/f15020289
Submission received: 22 December 2023 / Revised: 30 January 2024 / Accepted: 1 February 2024 / Published: 2 February 2024
(This article belongs to the Special Issue Ecological Functions of Bamboo Forests: Research and Application)
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Abstract

:
Cell cycle proteins and cyclin-dependent kinases (CDKs) play a vital role in the control of cell division, and their complexes form a powerful driving force in pushing cell cycle progression. D-type cyclins (CycDs) are essential for interpreting outside mitogenic signals and regulating the G1 phase. At least 19 distinct CycDs are present in the Moso bamboo (Phyllostachys edulis) genome, belonging to subgroups identified previously in other plants. Silico analysis validated the representative distinctive cyclin domains of each CycD in Moso bamboo, revealing that the genomic architectures of these genes were identical to those of their orthologs in Arabidopsis and rice. Both the phylogeny and covariance suggested that PheCycDs were structurally conserved and had undergone gene duplication. Transcriptome data analysis related to different tissues revealed that most CycDs were highly expressed in Moso bamboo shoots. The addition of growth hormone (NAA) significantly increased the transcript levels of PheCycD4;4, D5;1, D5;2, and D6;1 for a short period of time (6 h), and inhibitors (PCIB) also greatly decreased their expression. These results improved the understanding of PheCycDs in our study, notably in relation to auxin response, and offered an initial insight into the expression pattern and functional mining of the PheCycD gene family.

1. Introduction

Cell division, differentiation, and expansion are very important steps in the complex process of plant development. Cell division is essential for controlling growth and organ development. Shoot apical meristem (SAM) is an example of an organ primordium where cell proliferation predominates. Cell division and expansion continue as shoot and leaf development advances, and then cells gradually differentiate [1,2]. Cell cycle processes are related to similar proteins, enzymatic activity, and regulatory mechanisms in plant and animal cells [3].
The G1 phase, S (or DNA synthesis) phase, G2 phase, and M (or mitotic) phase are the four major stages of the cell cycle. The transitions from the S phase to the M phase are important control points during the cell cycle [4,5]. Cyclin proteins play basic roles in the regulation of these phases by activating and directing corresponding sites or particular substrates of cyclin-dependent kinases (CDKs) [6]. Different types of cyclins are found in eukaryotes, and each has a specific function. For instance, in animal cells, CycBs play a major role in M phase entry [7], whereas CycDs are essential for re-entering cell progression in reaction to extracellular signals [8], and the S phase is accelerated by CycEs [9]. CycD/CDK (D-type cyclin) complexes are stimulated by mitogenic signals, including the gene expression process, complex formation, and migration into nuclei [10]. In animal cells, CDK4 and CDK6 form complexes that bind and phosphorylate the pRB (retinoblastoma protein and the fragment sequence in CycDs) and then inactivate and release the E2F, letting cells transition from the G1 phase into the S phase [11]. The cyclin core is a conserved area of around 250 amino acids and a component of the cyclin structure, which comprises the cyclin_N and cyclin_C domains [12]. The cyclin_N domain (around 130 amino acids) contains the CDK-binding site, which is present in all known cyclins. In contrast, the cyclin_C domain is less conserved. Plant cyclins are divided into types A, B, C, D, H, and L based on how closely they resemble animal cyclins; no type E has been discovered [13,14]. Ten CycD genes have been found in the Arabidopsis genome, and they are organized into six or seven groups [1,15]. Plant cells have been discovered to have a similar cyclin/pRB (or pRB-related, pRBR) pathway [16,17], and practically, all plant CycDs feature a pRBR-binding motif made up of a consensus LxCxE sequence that is close to the amino end [18,19]. Some CycDs also include a PEST or destruction box, which is a hydrophilic region and abundant in Thr [T], Ser [S], Glu [E], and Pro [P], and is typical of proteins that undergo fast turnover [14,15]. CycDs exhibit similar functional modes in different species. AtCycD3;1 specifically is expressed highly in tissues with vigorous cell division activities such as shoot apices, root tips, and leaf primordia meristems. Overexpressing the CycD3;1 gene accelerates the transition from the G1/S phase and shortens the cell cycle [20]. The overexpression and silencing of CycD5;1 in Arabidopsis results in significant changes in the rate of DNA ploidy accumulation [21]. Transgenic rice overexpressing CycD2 accelerated its growth at the early stage of development and showed higher root length and plant height [22]. It has also been investigated how diverse signals, such as mitogenic substances like sugar and hormones like auxin and jasmonic acid, as well as several biotic and abiotic stimuli, affect the expression of plant cell cycle genes. Before entering the S phase, the CycD/CDKA complex highly phosphorylates its RBR, detaches from the E2F/DP/RBR complex, activates the transcriptional activity of the E2F/DP complex, and thus enables the cell cycle to enter the S phase and promotes the expression of related genes [23]. In this process, plant hormones such as auxin and cytokinin induce the expression of CycD, promote the synthesis of the CycD/CDKA complex, and accelerate cell cycle progression [24,25]. Exogenous cytokinin has been shown to enhance CycD3 transcript levels and induce the cell cycle [2], while auxin has been shown to stimulate cell division in Arabidopsis [26].
Bamboo is widely distributed in multiple regions of the globe, and Moso bamboo (Phyllostachys edulis) is an important timber-producing forest [27]. Moso bamboo is known for its rapid growth; it grows an average of more than 1.0 m per day during the rapid growth stage, reaching its greatest height in about 45 days [28]. The length of the culm, which is entirely dependent on the number of nodes and the length of internodes, affects the ecological and economic benefits of bamboo. The total number of bamboo shoot nodes is determined before it emerges from the soil, which remains constant once the bamboo shoots have grown aboveground. [29,30]. The fast growth of bamboo shoots can mostly be attributed to cell division and proliferation, which are controlled by several elements, such as hormones [27], proteins [31], transcriptional factors [32], and so on. The function of CycDs in bamboo is yet unknown, even though cell cycle proteins play a crucial regulatory function in cell division and cell proliferation throughout plant growth and development. In this study, the CycD gene family was discovered in Moso bamboo genomes, and a thorough analysis of its molecular characteristics, evolutionary relationship, and hormone signaling response was then carried out. In this study, these results enhanced our knowledge of PheCycDs, particularly in response to auxin, and provided a preliminary exploration of the expression pattern and functional mining of the PheCycD gene family.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

Moso bamboo seeds were obtained from Lingchuan County, Guangxi Zhuang Autonomous Region. Seeds were nurtured for three months in a climatic chamber (24 °C; 16 h/8 h light/dark cycle) to produce live seedlings, which were used for qPCR.

2.2. Identification and Characteristics of PheCycDs

The plant database Phytozome v13 (https://phytozome-next.jgi.doe.gov/, accessed on 20 July 2023) [33] was the source of 10 Arabidopsis CycDs and 14 rice CycDs in a phylogenetic tree. Genome sequences, gene annotation files, and protein sequence files of Moso bamboo were imported from the Moso bamboo whole-genome database (https://ngdc.cncb.ac.cn/gwh/ncbi_assembly/56063/show, accessed on 23 July 2023) [34]; the BioProject number was PRJNA587014. The HMM sequence profile (PF00134) of the CycD protein family was obtained from the PFAM database (https://pfam.xfam.org/, accessed on 25 July 2023) [35], and the HMM sequence profile was established by HMMER with a threshold of E-value < 1 × 10−3 (http://www.ebi.ac.uk/, accessed on 8 August 2023) [36] to validate and screen the CycD protein sequences in the Moso bamboo genome. Additionally, Blast P from the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov, accessed on 11 August 2023) was also used to assist in verifying the identity of the CycD protein sequence with thresholds of E-value < 10−5 and 50% identity.

2.3. Phylogenetic Analysis of CycDs in Moso Bamboo

The CycD genes in Arabidopsis and rice were analyzed by amino acid multiple sequence alignment with CycD proteins in Moso bamboo using ClustaIW in the MEGA7.0 software [37]. The phylogenetic evolutionary tree was constructed by applying the neighbor-joining (NJ) method in MEGA7.0, with the self-extension value set to 1000, and the rest of the parameters were set to default. The rice CycD gene family classification was used as a reference for the classification of CycD in Moso bamboo.

2.4. Analysis of Gene Structure and Motif of CycDs in Moso Bamboo

The CycD genes’ coding sequences were used to establish their gene structures. Gene structure and conserved motif analysis were performed using GSDS2.0 and MEME (the web addresses are http://gsds.cbi.pku.edu.cn (accessed on 19 August 2023) and http://meme-suite.org/tools/meme (accessed on 20 August 2023) [38,39], respectively, with parameters set to default, and TBtools [40] graphing was used for visual analysis.

2.5. Promoter Region of CycDs in Moso Bamboo: Analysis of Cis-Acting Elements

With PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 25 August 2023) [41], cis-acting elements at 2000 bp upstream of each CycD gene start codon were predicted, and the predicted results were analyzed and visualized in terms of components.

2.6. Identification of the Structural Domain of CycD Protein in Moso Bamboo

Specific structural domains of the CycD protein were resolved online using the Eukaryotic Linear Motif Database (http://elm.eu.org/, accessed on 28 August 2023) [42] and PFAM24.0 (http://pfam.sanger.ac.uk/, accessed on 28 August 2023) [40], and 19 CycD protein sequences were matched using DNAMAN (Version 6) to visualize their conserved protein structural domains, amino acid sequences, and helix structures.

2.7. Collinearity Analysis of CycDs in Moso Bamboo

MCScanX in TBtools was used to identify CycD gene replication and obtain Moso bamboo intraspecific covariance, and the data related to duplicated gene pairs were calculated with the help of the KaKs_Calculator, consisting of the non-synonymous substitution rate (Ka), the synonymous substitution rate (Ks), and their ratio (Ka/Ks). The genomic covariance information of Moso bamboo and rice was input into a Dual Synteny Plot to visualize the CycD gene covariance.

2.8. Expression Analysis of CycDs in Moso Bamboo

For gene tissue-specific and spatiotemporal expression analyses, the available transcriptome data of 26 different Moso bamboo tissues were taken from previous studies [43]. Referring to the Sequence Read Archive (SRA) database at the National Center for Biotechnology Information (NCBI) (http://www.ncbi.nlm.nih.gov/sra, accessed on 29 August 2023), the accession numbers were SRS1847048–SRS1847073. The values of fragment per kilobase million (FPKM) representing CycD expression levels were retrieved, and then, gene expression profiles were shown using the TBtools software (v2.042) to plot heat maps [44].
We constructed Moso bamboo root scRNA-seq libraries by using the Illumina NovaSeq 6000 platform, accession number GSE229126 [45]. Two copies of the biological material were produced. R package was used to t-SNE visualize the members of the PheCycD gene family in root cell clusters.

2.9. qPCR Analysis

Referring to a previous study [46], three-month-old seedlings were treated with the NAA and PCIB hormones (5μM of NAA solution was sprayed on Moso bamboo seedlings, and the PCIB hormone treatment was adopted using the same concentration and method). Leaf, stem, and root samples from Moso bamboo seedlings were collected at 0 h, 3 h, 6 h, 12 h, and 24 h; frozen in liquid nitrogen; and stored at −80 °C for later use. Total RNA was extracted from frozen samples using a plant RNA extraction kit (Mei5bio, Beijing, China). Following the relevant directions, a reverse transcription system (TaKaRa, Kyoto, Japan) was used to create first-strand cDNA. qPCR was carried out as directed using a qTOWER 2.2 system (Analytik, Jena, Germany) and SYBR Green Chemicals (Roche, Mannheim, Germany). Using PheTIP41 as an internal reference gene [47], the relative expression of the chosen genes was determined using the 2−∆∆CT technique [48]. Specific primers were constructed (Table S5) using the Primer 5.0 software (Jin Wang, Suzhou, China).

2.10. Statistical Analysis

Statistics were analyzed using the SPSS 19.0 software. For all experimental data, the mean and standard deviation (SD) were taken from three biological replications. One-way ANOVA in SPSS was used to evaluate the statistical significance of the difference between the values. Significant differences were seen for * 0.01 ≤ p ≤ 0.05 and ** p < 0.01.

3. Results

3.1. Identification and Analysis of CycD Gene Family in Moso Bamboo

With reference to the conserved sequences of CycD genes in Arabidopsis and rice, 19 CycD genes were screened and identified from the whole-genome database of Moso bamboo, belonging to the D1, D3, D4, D5, D6, and D7 subfamilies, using local BlastP homology alignment and PFAM-conserved structural domain analysis (Table 1). The CycDs of Moso bamboo were assigned names based on homology with rice CycD genes. In the PheCycD family, the amino acid sequences ranged from 277 aa (PheCycD4;6) to 372 aa (PheCycD7;1), with an average protein sequence length of 337 aa. Additionally, CycD proteins ranged from 31,348.15 Da (PheCycD4;6) to 41,603.30 Da (PheCycD7;1); the average theoretical isoelectric point was approximately 5.17, all of which were below 7. The instability coefficient of most PheCycD proteins was between 35.68 and 68.94, but only that of PheCycD4;6 was 35.68, less than 40, belonging to an unstable protein; the rest were greater than 40, which were stable proteins. The lipid solubility index indicated that PheCycD4;2 and PheCycD4;6 exhibited a lipid solubility of over 100, classifying them as hydrophobic proteins; hydrophilicity index analysis showed that all the CycDs of Moso bamboo were amphiphilic proteins (hydrophilicity index less than 0.5).
According to an analysis of the secondary structure data of the α-helix, extended chain, the β-turn angle, and irregular curl proteins, the 19 PheCycD gene family members were evenly distributed in each secondary structure without significant differences (Table S1). Among the predicted protein secondary structures, the α-helix and irregular curl occupied a larger proportion, the β-turn angle occupied the smallest proportion, and the overall structure distribution was α-helix > irregular curl > extension chain > β-turn angle, indicating that the PheCycD proteins of Moso bamboo exhibited minimal variation between each other, and their protein structures demonstrated enhanced stability.

3.2. Phylogenetic Tree Analysis of the CycD Genes

The evolutionary and kinship relationships between the CycD gene family members of Moso bamboo were clear in the evolutionary tree. For a more systematic understanding of the evolutionary relationships of the CycD gene family in Moso bamboo, the protein sequences of 43 CycD gene family members were obtained from the genome databases of Arabidopsis, rice, and Moso bamboo, and an evolutionary tree was built using MEGA7.0 (Figure 1). The results from the evolutionary tree showed that Moso bamboo was more homologous to rice in terms of kinship but had more members than rice. Cluster analysis showed that the 19 CycD genes in Moso bamboo were grouped into six subgroups, which were consistent with these in rice, and the number of CycD genes in each subgroup was significantly different. The subgroup D4, containing eight members, was the largest. D5 comprised four members, D1 had three members, and each of the remaining three groups had only one gene. The evolutionary classification of each group showed that D4 and D5 had the largest number and variety among the six subgroups, suggesting their potential for performing greater functions in development and evolution.

3.3. Structural and Protein Sequence Analysis of CycD Genes in Moso Bamboo

The evolution of this gene family is characterized by the diversity of its gene structure. In the gene structures of the 19 CycD members, the number of introns and exons differed very little (Figure 2A). Among the ten motifs, all seven PheCycDs were included, and the number of motifs had small differences in the overall distribution. Motifs 1, 2, 3, and 4 were distributed in all members, suggesting that these conserved motifs were key structures for each CycD. The similar types of cyclins exhibited comparable motifs. A MEME motif search also turned up several other unidentified motifs (Table S2). The N-terminal portions held the majority of motifs 5, 7, and 8, whereas the C-terminal portions held the majority of motifs 6, 9, and 10 (Figure 2B). At present, the function of most motifs remains unclear, but the evidence for the existence of these conserved motifs surely confirms the functional similarity among PheCycDs, which exhibited shared motifs.
In contrast to other eukaryotes, plant cyclins share the same cyclin core, including the cyclin domain LxCxE near the amino terminus and cyclin_N or cyclin_C near the carboxyl terminus; in our case, and cyclin_N was present in all cyclins and was the binding site for CDK. All members of the Moso bamboo CycDs contained cyclin_N, cyclin_C, and cyclin box; five helix structures (H1–H5) spanning cyclin_N, which were highly conserved in CycD; and five non-contiguous highly conserved residues (R, D, L, K, and E) that affected mitotic activity. Previous studies have demonstrated that animal CycD contains the binding site LxCxE of the retinoblastoma protein (RBR), and some plants have also been shown to contain RBR-binding sequences. Most of the Moso bamboo CycDs contained LxCxE motifs and showed sequence diversity, e.g., LLCAE, LYCDE, LLCGE, etc. These different LxCxE sequences might indicate subgroup-specific differences in the binding of different Moso bamboo CycDs to RBR (Figure 3). Although there were variances in the amino acid sequences, these data suggested that all segmentally duplicated cyclin genes had comparable or overlapping roles.

3.4. Analysis of CycD Promoter Element of Moso Bamboo

The type, number, and specific distribution of cis-acting elements in PheCycD promoters were closely related to gene function. With the genome and annotation files of Moso bamboo, the start codon ATG upstream 2 kb was selected as the promoter sequence of the corresponding gene, as shown in Figure 4. PlantCare, an online promoter analysis database, was used to conduct a cis-element analysis of PheCycDs, which showed that these promoters mainly contained nine types of cis-acting elements (Figure 4 and Table S3). Most of the PheCycD promoters included one or more hormone-responsive elements, such as auxin-responsive elements (16), gibberellin response elements (12), abscisic acid-responsive elements (43), and MeJA-responsive elements (42), which provided some clues for the future theoretical validation of hormone response of PheCycDs. In addition, meristem expression elements (31) were also distributed in most promoter regions, indicating that these elements may be associated with the meristem development of Moso bamboo. The stress response elements (23) in 13 PheCycD promoters were identified, indicating that these elements would respond to changes in external environmental factors and improve plant stress resistance. The number of circadian control elements (four) was relatively small with four PheCycDs, which suggested that these PheCycDs might perceive circadian rhythms and external environmental changes. Interestingly, cell cycle regulation elements were only in PheCycD4;6. In most PheCycD promoters, salicylic acid, and auxin response elements were mainly distributed at −1000 to 0 bp, while gibberellin response elements were distributed at −2000 to −1600 bp and −1000 to 0 bp. Moreover, stress response elements were concentrated at −2000 to −1000 bp. The above results show that the promoters of PheCycDs are regulated by several external signals, affecting Moso bamboo gene expression, and play a vital role in physiological processes that include hormone-induced responses, stress, and photoperiods.

3.5. Gene Duplication and Collinearity Analysis

In evolution, gene duplication provides sufficient genetic material for species evolution and is also the main way to generate new genes [49,50]. There were many types of gene duplication, such as tandem duplication, segmental duplication, and whole-genome duplication (WGD) [51]. WGD, tandem duplication, and fragment duplication are all genomic sequence duplications that allow the genetic evolution of a species to be traced (Figure 5). Gene segmental duplication occurred in 10 chromosomes, including 15 segmental duplications and 15 pairs of CycD genes, and three PheCycDs (PheCycD1;3, PheCycD4;7, and PheCycD4;8) were predicted to occupy the largest number in Chr-3. The Ka/Ks ratio, as an indicator of the molecular evolution of nucleic acids, determines whether there is selective pressure acting on the corresponding protein-coding genes. The Ka/Ks ratio of the duplicated CycD genes was less than one, indicating that the CycD gene family has undergone purifying selection (Table S4). Furthermore, segmental duplication in Moso bamboo CycDs made the number of their family members relatively higher than that of rice belonging to Poaceae. So, we speculated that tandem duplication might accelerate the process of genetic evolution in Moso bamboo.
To further investigate the evolution of the PheCycDs, collinearity analysis of CycD gene families in Moso bamboo, Ma bamboo, and rice was performed (Figure 6). The findings of interspecific linear profiles revealed distinct linear relationships between 17 Moso bamboo genes and associated genes in the Ma bamboo genome. Meanwhile, all 14 CycD family members in rice were collinearly related to 11 CycDs in Moso bamboo, which showed a close evolutionary relationship between them and those belonging to Poaceae. Compared with rice, most of the CycD genes were homologous to Ma bamboo CycD genes. Closely related species included more homologous information and evolutionarily co-associated genes and showed similarity in gene function. In Moso bamboo, other non-collinear genes might evolve new gene functions depending on already-existing gene functions. These analyses provided significant evidence of the conservation and specificity of CycD gene function, highlighting its importance in biological processes.

3.6. Expression Characteristics of PheCycDs

Tissue expression profiles can provide an important reference in verifying the function of genes, and we analyzed the transcript levels of PheCycDs according to the transcriptomic data of 26 tissues [43] of Moso bamboo (Figure 7). All genes except PheCycD4;6 were highly expressed in 3 m shoot tips (top, middle, and lower), and most genes showed high expression in shoot tips of 1.5 m, 3 m, and 6.7 m at different growth stages; only PheCycD5;3 and PheCycD4;3 were highly expressed in 0.2 m shoot tips. The rest had transcriptional preferences in other tissues; for instance, PheCycD3;1 had the highest expression in rhizome buds; PheCycD4;6, PheCycD5;1, and PheCycD5;2 were expressed at high levels in rhizome roots; and PheCycD5;4 was more inclined to be expressed in the leaf sheath. However, most CycDs were expressed at relatively low levels in roots (0.1 cm), leaves, rhizomes, and shoots at the middle and lower tips. Moso bamboo CycDs were more concentrated in the shoots of different tissues with high cell division statuses, indicating that they might play a crucial part in shoot growth and development. To further clarify the function of PheCycDs, single-cell sequencing was used to detect gene expression levels more accurately. According to the single-cell data of Moso bamboo basal roots [45], PheCycD4;1 and PheCycD4;2 are expressed in the initial cell of the root; PheCycD5;1 and PheCycD6;1 are specifically expressed in the ground tissues; and PheCycD6;2 is specifically expressed in the root cap (Figure 8). The results showed that these genes might have a significant role in Moso bamboo root development.

3.7. Expression Patterns of PheCycD Genes under Extrinsic NAA and PCIB Treatment

The results for the promoter-acting elements and the transcriptome data analysis of 19 PheCycD genes revealed that there was both growth hormone and non-biological stress corresponding to cis-acting elements in promoter regions, which might influence the transcriptional expression levels of the genes. Based on the above results and our lab’s study of the transcriptome data, we identified four representative genes (PheCycD4;4, PheCycD5;1, PheCycD5;2, and PheCycD6;1) for qPCR analysis. The exogenous growth hormone NAA and the growth hormone inhibitor PCIB were used to treat Moso bamboo seedlings. Under the treatment of NAA, these four genes displayed an increasing pattern and then experienced a downtrend relative to the expression. in five different periods (0 h, 3 h, 6 h, 12 h, and 24 h), of leaves, stems, and roots. All genes showed a peak of relative expression 6 h after NAA treatment; then, their expression went down slowly. PheCycD4;4 had about an 8-fold higher expression at 6 h in leaves than at 0 h (Figure 9C). PheCycD5;1 (Figure 9A) and PheCycD5;2 (Figure 9D) had 3-fold higher expressions at 6 h than at 0 h, while PheCycD6;1 (Figure 9B) had the lowest expression at 6 h. In culms, the relative expression of these genes was more evenly distributed, with minimal overall variation. The expression of PheCycD5;2 was highest in roots and was likewise higher at 24 h than that of the other genes. Comparing the three separate organs, it could be seen that PheCycD5;1, PheCycD5;2, and PheCycD6;1 all responded to growth hormones more quickly than PheCycD4;4.
The expression of the four representative genes was downregulated in three different organs under treatment with the growth hormone inhibitor PCIB and reached its lowest point at 6 h in these organs. The response to PCIB treatment varied between different organs. For example, PheCycD5;1 (Figure 9E) exhibited different expression patterns in leaves and stems compared with roots, while PheCycD6;1 (Figure 9F) had consistent changes; the relative expressions of PheCycD4;4 (Figure 9G) and PheCycD5;2 (Figure 9H) were similar in leaves, stems, and roots. The upregulation of CycD4;4, CycD5;1, CycD5;2, and CycD6;1 expression in PheCycDs was observed in response to growth hormone signals, indicating differential gene expression across various organs. Additionally, the precise functionalities of other members within the PheCycD family necessitate further experimental validation.

4. Discussion

4.1. CycD Gene Family and Its Structures

According to previous studies [52,53,54,55], each CycD has a unique function in the cell cycle and cell division. PheCycDs can be grouped into various subgroups based on sequence similarity, pattern of expression, and protein comparison [13,56,57,58,59]. Different types of cell cycle proteins have been shown to be present in the genomes of Oryza sativa (9) [60], Zea mays (6) [61], Populus trichocarpa (7) [62], and Arabidopsis thaliana (10) [15]. It has been inferred that D-type cyclin is more conserved among plant species. Phylogenetic studies have revealed a closer homology between Moso bamboo and rice. This indicates that the CycD gene family is mostly preserved in these two genomes. It has also been established that Moso bamboo and rice share a closer genetic link than they do to Arabidopsis.
PheCycDs exhibited significant conservation and particular motifs according to the sequence of protein alignment and structural study. Nearly all of the CycDs in Moso bamboo contained a cyclin_N domain, similar to other CycD families in plant species. This indicates that the N domain is more conserved than the C domain, which is further supported by analyses of the chromosomal distribution and nature of cyclin_D motifs.

4.2. Duplication of PheCycDs

One of the main factors influencing the development of genes and genetic systems is gene duplication [63]. Tandem duplications and segmental duplications have an impact on the substantial changes in size and distribution that most gene families experience [64]. According to research on Arabidopsis, its genome possesses several massive fragment copies that are caused by persistent polyploid events and disrupted by chromosomal rearrangements [65,66,67,68]. The majority of the duplications in Moso bamboo are found on chromosomes 3, 10, and 21 (Figure 5). Previous research has revealed that Moso bamboo has experienced numerous segment duplications after at least one cycle of whole-genome duplication [69,70,71]. The phenomenon of expansion that exists in the evolution of CycD gene family members may be linked to gene duplication [5]. Genome replication events [72], including series replication such as fragment replication [53], may be the main source of discrepancies between CycD members. These results provide insight into the evolution of the Moso bamboo genome.

4.3. Multiple Functions of CycDs in Plant Growth and Development

The changing expression of some G1-S checkpoint genes in cells might be used to control plant cell cycles [73]. One of the most crucial cell cycle checkpoints is the G1-S phase, and CycDs have been suggested as a sensor of extracellular growth conditions [74]. Arabidopsis might express B-type cyclin when CycD3;1 is overexpressed, which would promote endoreduplication and mitosis [75]. In contrast with our results, BpCycD3.1 has a higher expression level in leaves [76], while PheCycD3.1 is slightly low. In our study, almost all CycD genes were highly expressed in Moso bamboo shoot tips and showed similar patterns of expression, indicating that these CycDs might play a key role in bamboo shoot growth.
The gene expression pattern is an essential representation of gene function. In our study, most of the PheCycDs were found to be highly expressed in bamboo shoots, bud tips, 0.5 cm roots, and rhizome roots [43]. These results are broadly consistent with previous studies. For instance, the S phase of maize germination begins 12 h after imbibition, as shown by a rise in tagged nuclear DNA and an accumulation of proliferating cell nuclear antigen [77,78,79]. ZmCycD2;2, ZmCycD4;2, and ZmCycD5;3 are highly expressed in seeds and seedlings [50], and the CycD3 subgroup in birch has a higher expression in leaves, roots, and stems [64]. Low expression of CycD1;3, CycD4;4, and CycD7;1 has been found in rice roots, and they vary in the leaf growth zone [49]. Overexpression of AtCycD1 and AtCycD4 in Arabidopsis exhibits a significant delay in cell division and proliferation [80]. In tomatoes, D3 cyclin is likely involved in signal transduction, which results in cell divisions and, thus, fruit development [81]. CycDs are also expressed in the shoot apical meristem, leaf primordia, and vascular tissues of Arabidopsis [82]. We primarily deduced that CycD might promote the transition from the G1 phase to the S phase, advance the mitotic process, and accelerate cell proliferation in actively dividing tissues such as the stem tip, shoot tip, root tip, and leaf primordium, but some experimental evidence is still lacking. Some plant hormones also control cell division and expansion. The transcription of numerous cell cycle genes has been found to be significantly regulated by NAAs [83,84].

5. Conclusions

In this study, 19 CycDs were identified in Moso bamboo. The expression profiles and evolutionary relationships revealed that exhibiting consistent expression patterns across multiple growth stages might potentially serve similar functions. This protein sequence alignment and structural study revealed considerable conservation among these genes. The Moso bamboo genome has evolved through duplication and subsequent expansion. Given the expression levels of PheCycDs, they might be involved in bamboo shoot growth and development, and we can preliminarily speculate that most of them are able to respond to the auxin. The selection of potential genes for functional validation in connection to many elements of Moso bamboo’s fast-growing development would thus benefit from these data.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/f15020289/s1: Table S1: Secondary structures of the CycD gene family members of Moso bamboo. Table S2: Details of the putative motifs. Table S3: The cis-elements in the promoter of PheCycDs. Table S4: Ka/Ks values between duplicate gene pairs. Table S5: List of primers used for qPCR.

Author Contributions

Conceptualization, H.F. and Z.C.; methodology, C.M.; software, C.M. and J.J.; validation, H.F., C.M., and J.J.; formal analysis, H.F.; investigation, C.M.; resources, C.M.; data curation, H.F.; writing—original draft preparation, H.F. and C.M.; writing—review and editing, H.F.; visualization, H.F.; supervision, Z.C. and J.G.; project administration, Z.C.; funding acquisition, Z.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Fundamental Research Funds of ICBR (1632021017), the National Natural Science Foundation of China (32071849), and the National Key Research and Development Program of China (2021YFD2200505).

Data Availability Statement

All data generated or analyzed during this study are included in the article and its information files.

Conflicts of Interest

The authors declare no conflicts of interest. The funding agency was not involved in the design of the study; in the collection, analysis, or interpretation of the data; or in writing the manuscript.

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Figure 1. Phylogenetic analysis of CycD proteins in different plant species. (Phe: P. edulis; Os: Oryza sativa; At: A. thaliana). The outer and inner arcs with different colors represent different subgroups and CycD gene family members, respectively.
Figure 1. Phylogenetic analysis of CycD proteins in different plant species. (Phe: P. edulis; Os: Oryza sativa; At: A. thaliana). The outer and inner arcs with different colors represent different subgroups and CycD gene family members, respectively.
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Figure 2. UTR/CDS genomic structure and protein motif organization of CycDs in Moso bamboo. (A) Protein motif organization of PheCycDs: the evolutionary tree of the CycD family is shown on the left, and the different colored square boxes on the right indicate the species and positional information of the predicted 10 motifs in the CycD proteins of Moso bamboo. (B) CDS/UTR genomic structure of PheCycDs; gray lines represent introns.
Figure 2. UTR/CDS genomic structure and protein motif organization of CycDs in Moso bamboo. (A) Protein motif organization of PheCycDs: the evolutionary tree of the CycD family is shown on the left, and the different colored square boxes on the right indicate the species and positional information of the predicted 10 motifs in the CycD proteins of Moso bamboo. (B) CDS/UTR genomic structure of PheCycDs; gray lines represent introns.
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Figure 3. Amino acid sequence comparison diagram of CycDs. The CycD protein names and sequences are shown on the left and right, respectively. Consistent colors indicate amino acid identity; protein motifs are marked by different colored lines.
Figure 3. Amino acid sequence comparison diagram of CycDs. The CycD protein names and sequences are shown on the left and right, respectively. Consistent colors indicate amino acid identity; protein motifs are marked by different colored lines.
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Figure 4. Analysis of cis-acting and responsive elements in PheCycD promoter sequences. (A) Quantitative statistical map of cis-acting elements in the PheCycD promoter region. The color depth of the cell indicates the quantity. (B) Types (different colored blocks) and distribution of cis-acting elements of PheCycDs.
Figure 4. Analysis of cis-acting and responsive elements in PheCycD promoter sequences. (A) Quantitative statistical map of cis-acting elements in the PheCycD promoter region. The color depth of the cell indicates the quantity. (B) Types (different colored blocks) and distribution of cis-acting elements of PheCycDs.
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Figure 5. Statistical analysis of genomic segmental duplication in Moso bamboo. Outer arcs indicate the chromosome lengths of Moso bamboo chromosomes and the chromosome localization of CycD members. Column maps are represented by the central arcs. Chromosomes are shown as gene density in the inner arcs. The covariance of all the genes found in the Moso bamboo genome is shown by the gray line in the circle. Fifteen PheCycD duplication pairs are linked with different color lines.
Figure 5. Statistical analysis of genomic segmental duplication in Moso bamboo. Outer arcs indicate the chromosome lengths of Moso bamboo chromosomes and the chromosome localization of CycD members. Column maps are represented by the central arcs. Chromosomes are shown as gene density in the inner arcs. The covariance of all the genes found in the Moso bamboo genome is shown by the gray line in the circle. Fifteen PheCycD duplication pairs are linked with different color lines.
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Figure 6. Chromosome distribution and collinearity analysis of CycDs of Moso bamboo, Ma bamboo, and rice (A,B). Gray lines indicate linear relationships in both genomes, and red lines indicate CycD-associated gene pairs.
Figure 6. Chromosome distribution and collinearity analysis of CycDs of Moso bamboo, Ma bamboo, and rice (A,B). Gray lines indicate linear relationships in both genomes, and red lines indicate CycD-associated gene pairs.
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Figure 7. Expression analysis of CycDs in 26 tissues of Moso bamboo. Red and blue blocks represent high and low expression levels. The depth of the color indicates a level change.
Figure 7. Expression analysis of CycDs in 26 tissues of Moso bamboo. Red and blue blocks represent high and low expression levels. The depth of the color indicates a level change.
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Figure 8. Visualization of PheCycDs in scRNA-seq data of Moso bamboo basal roots. The t-SNE (t-distributed stochastic neighbor embedding) shows the expression levels of PheCycD4;1, PheCycD4;2, PheCycD5;1, PheCycD5;2, PheCycD6;1 and PheCycD6;2 (A–F) in single-cell date of Moso bamboo basal roots. The gray shading represents different cell clusters. The depth of the color represents the expression of the genes.
Figure 8. Visualization of PheCycDs in scRNA-seq data of Moso bamboo basal roots. The t-SNE (t-distributed stochastic neighbor embedding) shows the expression levels of PheCycD4;1, PheCycD4;2, PheCycD5;1, PheCycD5;2, PheCycD6;1 and PheCycD6;2 (A–F) in single-cell date of Moso bamboo basal roots. The gray shading represents different cell clusters. The depth of the color represents the expression of the genes.
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Figure 9. Patterns of spatiotemporal expression of PheCycD under exogenous NAA and PCIB treatment. (A–D) A 5 μM NAA treatment. (E–H) A 5 μM PCIB treatment. Different colored blocks represented different hormone treatment times, and all data were calculated and plotted using 0 h as a control. Asterisks indicate the significance level (* 0.01 ≤ p ≤ 0.05, ** p < 0.01) as determined by Fisher’s least-significant-difference test.
Figure 9. Patterns of spatiotemporal expression of PheCycD under exogenous NAA and PCIB treatment. (A–D) A 5 μM NAA treatment. (E–H) A 5 μM PCIB treatment. Different colored blocks represented different hormone treatment times, and all data were calculated and plotted using 0 h as a control. Asterisks indicate the significance level (* 0.01 ≤ p ≤ 0.05, ** p < 0.01) as determined by Fisher’s least-significant-difference test.
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Table 1. Information on members of the CycD family in Moso bamboo.
Table 1. Information on members of the CycD family in Moso bamboo.
Gene NameGene IDNumber of Amino AcidsMolecular Weight (Da)Theoretical pIInstability IndexAliphatic IndexGrand Average of Hydropathicity
PheCycD1;1PH02Gene07957.t131734,778.655.2368.9482.56−0.039
PheCycD1;2PH02Gene24350.t133336,242.854.9454.9180.96−0.072
PheCycD1;3PH02Gene27422.t131834,935.844.6956.2487.23−0.006
PheCycD3;1PH02Gene36726.t136438,402.584.7556.1590.030.084
PheCycD4;1PH02Gene01286.t133736,893.075.4966.3188.28−0.077
PheCycD4;2PH02Gene08554.t134638,378.144.9262.31102.310.093
PheCycD4;3PH02Gene10625.t134738,051.535.0551.3190.430.038
PheCycD4;4PH02Gene10755.t135038,750.444.9268.3995.140.065
PheCycD4;5PH02Gene13845.t135238,562.895.0457.2785.94−0.07
PheCycD4;6PH02Gene27933.t127731,348.154.5235.68104.550.094
PheCycD4;7PH02Gene41784.t134738,106.615.0268.2991.470.038
PheCycD4;8PH02Gene46436.t133937,490.875.3165.9690.94−0.071
PheCycD5;1PH02Gene01190.t134737,761.434.857.0181.64−0.088
PheCycD5;2PH02Gene15833.t135337,645.344.7744.3280.880.02
PheCycD5;3PH02Gene24302.t133436,464.295.8346.2683.08−0.181
PheCycD5;4PH02Gene38666.t134938,148.834.7560.5975.93−0.124
PheCycD6;1PH02Gene07025.t130632,639.46.5154.3286.670.066
PheCycD6;2PH02Gene18100.t231133,250.066.1144.4284.020.02
PheCycD7;1PH02Gene23789.t137241,603.35.5857.3586.8−0.218
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Fang, H.; Mu, C.; Jiang, J.; Gao, J.; Cheng, Z. The Moso Bamboo D-Type Cell Cycle Protein Family: Genome Organization, Phylogeny, and Expression Patterns. Forests 2024, 15, 289. https://doi.org/10.3390/f15020289

AMA Style

Fang H, Mu C, Jiang J, Gao J, Cheng Z. The Moso Bamboo D-Type Cell Cycle Protein Family: Genome Organization, Phylogeny, and Expression Patterns. Forests. 2024; 15(2):289. https://doi.org/10.3390/f15020289

Chicago/Turabian Style

Fang, Hui, Changhong Mu, Jutang Jiang, Jian Gao, and Zhanchao Cheng. 2024. "The Moso Bamboo D-Type Cell Cycle Protein Family: Genome Organization, Phylogeny, and Expression Patterns" Forests 15, no. 2: 289. https://doi.org/10.3390/f15020289

APA Style

Fang, H., Mu, C., Jiang, J., Gao, J., & Cheng, Z. (2024). The Moso Bamboo D-Type Cell Cycle Protein Family: Genome Organization, Phylogeny, and Expression Patterns. Forests, 15(2), 289. https://doi.org/10.3390/f15020289

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