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Article

Comprehensive Analysis of JAZ Family Genes Involved in Sex Differentiation in Areca catechu

by
Jin Du
†,
Changlei Ji
†,
Xinyu Wen
,
Han Li
and
Fusun Yang
*
School of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2025, 16(7), 1133; https://doi.org/10.3390/f16071133
Submission received: 12 June 2025 / Revised: 4 July 2025 / Accepted: 7 July 2025 / Published: 9 July 2025
(This article belongs to the Special Issue Tree Breeding: Genetic Diversity, Differentiation and Conservation)
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Abstract

Jasmonate ZIM-domain (JAZ) proteins play a pivotal role in mediating plant growth, development, and responses to both biotic and abiotic stresses. However, our knowledge about the JAZ family genes in Areca catechu remains limited. This study conducted a genome-wide screening and analysis of JAZ genes in A. catechu to investigate their biochemical characteristics, gene structure features, phylogenetic relationships, and expression profiles in different organs. A total of 14 JAZ genes (AcJAZs) were detected in the A. catechu genome, all containing an N-terminal TIFY domain and a C-terminal Jas domain. Phylogenetic analysis categorized these AcJAZs into five subfamilies according to their similarities in protein sequences. Quantitative real-time reverse transcription PCR (qRT-PCR) experiments demonstrated the ample expression specificity of these AcJAZ genes across different organs and flower development stages. More importantly, most AcJAZ genes are expressed significantly higher in blooming male flowers than female flowers, suggesting that they may participate in regulating the difference between male and female flowers of A. catechu. This study elucidates the genomic features and functions of JAZ genes in A. catechu, providing new insights into the mechanisms underlying the development and differentiation of unisexual flowers in A. catechu.

1. Introduction

Flowering is a vital biological process in angiosperms, involving the complex coordination and interaction of numerous genes [1]. The majority of angiosperms are hermaphroditic and possess bisexual flowers, while only 10% have unisexual flowers [2]. Development of unisexual flowers is influenced by various factors, including environmental and genetic cues, as well as plant hormones [3,4].
Areca catechu is a monoecious plant widely cultivated in tropical regions of Asia, including Southern China, India, Malaysia, and Indonesia [5,6]. A. catechu has unisexual flowers, with male and female flowers borne together on an inflorescence. The male flowers are small and numerous, distributed from the center to the tip of the inflorescence, while the female flowers are larger and fewer in number, located at the base of the inflorescence. The male-to-female flower ratio is crucial for fruit formation; thus, a comprehensive understanding of the molecular mechanisms underlying flower development and differentiation can provide valuable genetic resources for future bioengineering-based improvements in fruit yield and quality.
Previous studies have shown that the differentiation of female flowers in A. catechu is related to the synthesis and transduction of jasmonic acid (JA) [7,8]. JA serves as a crucial phytohormone regulating plant growth, developmental processes, and stress responses [9]. Jasmonate ZIM-domain (JAZ) proteins act as core repressors in the JA signal transduction pathway, whose functions have been investigated in various plant species, including Arabidopsis thaliana [10], rice (Oryza sativa) [11], tomato (Solanum lycopersicum) [12], maize (Zea mays) [13], and poplar (Populus trichocarpa) [14]. JAZ proteins exhibit a highly conserved domain architecture, featuring a 36-amino acid TIFY domain (alternatively designated as ZIM domain) at their N-terminal region, coupled with a C-terminal Jas domain (also referred to as CCT-2 domain) [15]. Both domains execute critical yet specialized functions: the TIFY domain enables the interaction between JAZ proteins and the NINJA-TPL complex to block JA signal transduction [16], whereas the Jas domain regulates the stability of JAZ proteins and their interaction with CORONATINE INSENSITIVE 1 (COI1) and MYC [17].
Despite their functional importance, our knowledge about the regulatory role of JAZ genes in the differentiation of male and female flowers of A. catechu remains limited. To address the gap, this investigation implemented a genome-wide screening of the JAZ genes in A. catechu (AcJAZ), and their chromosomal localization, gene structure, and phylogenetic relationships were characterized. Furthermore, expression profiles of these AcJAZ genes in A. catechu flowers of different sexual types and developmental stages, as well as other vegetative organs, were analyzed using quantitative real-time reverse transcription PCR (qRT-PCR) experiments. These findings will unravel the genomic features and potential biological functions of AcJAZ genes, which deepen our understanding of the molecular mechanisms underlying flower differentiation in A. catechu.

2. Materials and Methods

2.1. Identification and Characterization of JAZ Genes in A. catechu

The genome assembly of A. catechu was downloaded from the National Genomics Data Center (NGDC) (accession number PRJNA767949). The Hidden Markov Model (HMM) profiles corresponding to the TIFY (PF06200) and Jas (PF09425) domains were acquired from the Pfam database (http://pfam.xfam.org/) (accessed on 27 September 2024). Using these seed files, putative AcJAZ genes were identified with HMMER 3.0 software, employing an E-value cutoff of <1 × 10−5. The domain integrity of these identified AcJAZ genes was further validated using the SMART server (http://smart.embl-heidelberg.de/) (accessed on 30 September 2024), and the genes with incomplete domains or redundant sequences were removed. Protein properties, including amino acid length, molecular weight (MW), isoelectric point (pI), and exon structure, were explored for each AcJAZ using the ExPASy server (http://www.expasy.org/) (accessed on 9 October 2024).

2.2. Chromosomal Location, Gene Structure, and Conserved Motif Analysis of AcJAZ Genes

The physical locations and gene structures of AcJAZ genes were extracted from the annotation data of the A. catechu genome and visualized using TBtools software (v2.154). Conserved motifs in AcJAZ proteins were identified using the MEME suite (http://meme-suite.org) (accessed on 15 October 2024) with default parameter settings.

2.3. Phylogenetic Analysis of the JAZ Gene Family in A. catechu

JAZ homolog proteins from A. thaliana and O. sativa were obtained from the TAIR database (https://www.arabidopsis.org) (accessed on 18 October 2024) and the Rice Annotation Project Database (https://rice.uga.edu) (accessed on 18 October 2024), respectively. Multiple sequence alignments were performed with ClustalW under default settings, followed by phylogenetic reconstruction employing the neighbor-joining (NJ) method in MEGA7. A total of 1000 bootstrap replicates were used to assess the robustness of the tree.

2.4. Expression Profiling of AcJAZ Genes by qRT-PCR

A. catechu samples of vegetative and floral organs were collected from the trees cultivated at the Danzhou campus experimental base of Hainan University, including roots, stems, leaves, male and female flowers at full bloom, and male and female flower buds from four key developmental stages. The samples were quickly frozen in liquid nitrogen and subsequently stored at −80 °C. For each tissue, three independent biological replicates were collected to ensure the accuracy and reproducibility of the results.
Total RNA was extracted from each sample using the DP441 RNAprep Pure Plant Plus Kit (Tiangen Biotech, Beijing, China). After evaluating the RNA quantity and quality, cDNA synthesis was carried out using the PrimeScript RT reagent Kit with gDNA Eraser (Tiangen Biotech, Beijing, China). Actin of A. catechu was used as the internal reference gene, following a previous study in A. catechu by Li et al. [18]. All the qRT-PCR primers were designed using Primer Premier 5 and listed in Supplemental Table S1. qRT-PCR was performed on an ABI PRISM 7500 real-time PCR system (Applied Biosystems, Foster City, CA, USA) using ChamQ™ Universal SYBR® qPCR Master Mix (Vazyme, Nanjing, China). Reactions were prepared in a 20 μL mixture consisting of 10 μL 2 × ChamQ Universal SYBR qPCR Master Mix, 2 μL cDNA, 2 μM of each primer, and 6 μL double-distilled water. Three technical replicates were performed for each sample to ensure the reproducibility of the experiments. The relative expression levels of AcJAZ genes were quantified using the 2−ΔΔCt method.

3. Results

3.1. Identification of the AcJAZ Genes

Genome-wide screening found 14 non-redundant AcJAZ genes distributed across eight chromosomes of the A. catechu genome (Figure 1). These genes were named AcJAZ1 to AcJAZ14 according to their physical chromosome positions (Table 1). Chromosomes 3 and 5 hosted the highest number of AcJAZ genes (four genes in each chromosome). It is noteworthy that the four AcJAZ genes on chromosome 3 formed a cluster at the end of the chromosome. There was only one single AcJAZ gene in chromosomes 2, 4, 6, 7, 14, and 15, respectively.
Physicochemical analysis revealed that the length of AcJAZ proteins ranged from 158 (AcJAZ1) to 465 amino acid residues (AcJAZ8), with molecular weights varying from 17.92 kDa to 48.66 kDa. The isoelectric points (pI) of these proteins ranged from 5.54 (AcJAZ4) to 10.52 (AcJAZ11). Notably, the pI of 12 out of the 14 AcJAZ proteins exceeded 7.0, demonstrating a predominant alkaline character among these proteins.

3.2. Gene Structure and Conserved Motif Analysis

Gene structure analysis revealed that the number of exons in the AcJAZ genes ranged from 3 to 7. Both AcJAZ1 and AcJAZ13 contained 3 exons, while AcJAZ2, AcJAZ3, AcJAZ7, and AcJAZ8 had 7 exons. Notably, six AcJAZ genes (43% of the total) consisted of 5 exons. Three highly conserved motifs were identified in AcJAZ proteins (Figure 2B), where Motif 1 and 3 corresponded to the TIFY and Jas domains, respectively, that were present in all AcJAZ proteins. Motif 2 also existed in the majority of AcJAZ proteins, except AcJAZ11, which merely had Motifs 1 and 3.

3.3. Phylogenetic Analysis of AcJAZ Genes

To further investigate the phylogenetic relationships of AcJAZ genes, a phylogenetic tree was constructed for JAZ proteins from A. catechu, A. thaliana (13 AtJAZs; Supplemental Table S2), and rice (Oryza sativa; 23 OsJAZs; Supplemental Table S3). The results revealed that the 50 JAZ homolog proteins segregated into five distinct groups (Group I to Group V) (Figure 3). Both Groups I and IV contained four AcJAZ proteins, while each of the other three groups consisted of two AcJAZ proteins.

3.4. Expression Profiling of AcJAZ Genes in Different Organs

To better understand the functional roles of AcJAZ genes in A. catechu, their expression profiles in six organs, including roots, stems, leaves, fruits, blooming female flowers, and blooming male flowers, were examined using qRT-PCR. The results showed distinct expression patterns for AcJAZ genes across different tissues, indicating their various functions in the growth and development of A. catechu (Figure 4A).
Overall, all AcJAZ genes showed minimal expression in the stem of A. catechu. AcJAZ3 and AcJAZ12 exhibited the highest expression in leaves and fruits, respectively. In roots, AcJAZ1, AcJAZ12, and AcJAZ13 were more highly expressed than the others. Notably, the expression levels of all AcJAZ, except for AcJAZ2, AcJAZ4, and AcJAZ8, were significantly higher in blooming male flowers than in blooming female flowers, suggesting their key role in male flower development. Highly expressed AcJAZ genes in each organ were presented in Figure 4B.

3.5. AcJAZ Genes in Male and Female Flower Development

The expression analysis of AcJAZ genes mentioned above highlighted their putative role in newly opened male flowers. qRT-PCR experiments were conducted to analyze the transcriptional dynamics of AcJAZ genes in male and female flower buds of A. catechu across four developmental stages, assessing their expression dynamics during the differentiation of male and female flowers. The results are presented in Figure 5.
Overall, most AcJAZ genes exhibited stage-specific expression patterns, except for AcJAZ9, which had lower expression levels than the other AcJAZ genes. Ten out of the 14 AcJAZ genes, including AcJAZ1, AcJAZ4, AcJAZ6, AcJAZ7, AcJAZ8, AcJAZ10, AcJAZ11, AcJAZ12, AcJAZ13, and AcJAZ14, had the highest expression level at Stage 4 of both male and female flower buds. In contrast, AcJAZ3 showed higher expression in early flower development (Stages 1–2), followed by significant downregulation in later developmental stages (Stages 3–4) in both male and female flowers. And AcJAZ5 displayed the highest expression in female flowers at Stage 3.

4. Discussion

JA is a hormone specific to plants that plays a crucial role in plant development and survival [19]. The JA-mediated signaling pathway is highly conserved in vascular plants [9,20]. In this pathway, JAZ proteins are key regulators, linking the Jasmonoyl-L-isoleucine (JA-Ile) receptor, which is the bioactive form of JA, to changes in the activity of the MYC transcription factor. This allows them to function as a central hub in the hormone response network [21]. In this research, we conducted a comprehensive investigation into the roles of the JAZ family genes during the critical stage of flower sex differentiation in A. catechu.
A total of 14 members were identified in the JAZ family in A. catechu, a number similar to that of other plants such as A. thaliana (13), rice (18), and maize (16) [10,11,13]. However, the genome size of A. catechu (2730 Mb) is larger than that of these species; it is approximately 22 times that of A. thaliana (119.1 Mb) and seven times that of rice (374 Mb) [7,22,23]. This suggests that the variation in the number of JAZ genes between different species is not necessarily related to genome size, but may be associated with gene evolutionary history, such as gene duplication events.
The amino acid length of AcJAZ proteins varied from 158 to 465, similar to those in A. thaliana [10]. Except for AcJAZ4 and AcJAZ10, which have pI values of 5.54 and 5.93, respectively, all other AcJAZ proteins have alkaline pI values (pI > 7.0). This might be due to the relatively higher proportion of acidic amino acids, such as aspartic acid and glutamic acid, in AcJAZ4 and AcJAZ10 compared to other AcJAZ proteins. A similar phenomenon was also observed in JAZ proteins of tea trees (Camellia sinensis) and mint (Mentha canadensis) [24,25].
JAZ proteins typically contain at least one conserved TIFY domain and one Jas domain. In A. catechu, the core motif of the TIFY domains in 13 of the 14 AcJAZ proteins is TIF[F/Y]XG, while AcJAZ1 possesses a less common motif pattern (TLF[F/Y]XG) with an amino acid change from “I” to “L” at the second position of the motif. This variation in the core sequence may alter its strength of interactions with other proteins, thus affecting the regulation of the JA signaling pathway. At the C-terminus, all AcJAZ proteins contain a highly conserved Jas domain with the length of approximately 30 amino acids and a core sequence of SLX2FX2KRX2RX5PY. The Jas domain is primarily involved in interactions with COI1 and transcription factors such as MYC2, which mediate negative feedback regulation in the JA signaling pathway and influence JAZ protein localization [26].
Interestingly, certain JAZ genes, such as AtJAZ7 and AtJAZ8, contain an EAR motif (LxLxL) at their N-terminus. This motif facilitates the recruitment of the TPL-coupled inhibitory complex and reduces the JA response in the absence of NINJA [27,28]. Similarly, AcJAZ1 and AcJAZ13 from Group IV also possess an additional EAR motif at their N-terminus like AtJAZ7 and AtJAZ8, suggesting that these proteins may have similar functions (Supplementary Figure S1).
While most studies on JA have focused on its role in environmental stress responses, it also plays a crucial role in reproductive development [29]. For instance, JA is vital for male fertility in A. thaliana, where mutations in the COI1 gene, such as coi1-1, can disrupt the interaction between COI1 and JAZ proteins, leading to male sterility [30]. In maize, genes responsible for the synthesis and metabolism of JA, for example, those encoding tasselseed1 (ts1), tasselseed2 (ts2), tasselseed5 (ts5), and silkless (sk1), have also been found to be involved in sex determination [31,32,33,34]. In rice, defects in JA biosynthetic enzymes, such as OsAOC, lead to early flowering and abnormal flower morphology, including elongated sterile lemmas and bract-like organs [35]. In A. catechu, most AcJAZ genes exhibited increased expression levels along with the development of both male and female flower buds (Figure 5). More importantly, although their expressions were similar between flower buds of different sexes, most AcJAZ genes expressed significantly higher in blooming male flowers than female flowers, suggesting they may play different roles in the formation of unisexual flowers in A. catechu. These findings provide putative targets for future gene overexpression or CRISPR-based knockdown/knockout experiments to validate the detailed regulatory functions of JAZ genes in flower development and differentiation in A. catechu.

5. Conclusions

This study investigated 14 AcJAZ genes in the genome of A. catechu and characterized their features in terms of physicochemical properties, phylogenetic relationships, gene structure, and conserved motifs. Expression analysis revealed that these genes are involved in the differentiation and development of male and female flowers in A. catechu. Our findings lay the groundwork for further studies on the functional roles of JAZ genes in the formation of unisexual flowers in A. catechu, which may serve as putative targets for bioengineering improvements in A. catechu, leading to enhanced fruit yield and quality.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f16071133/s1, Figure S1: Multiple sequence alignment of the AcJAZ genes; Table S1: The detailed information of primers; Table S2: Sequences of AtJAZs; Table S3: Sequences of OsJAZs.

Author Contributions

Conceptualization, F.Y.; validation, F.Y.; formal analysis, J.D. and C.J.; resources, F.Y.; data curation, C.J. and H.L.; writing—original draft preparation, J.D. and C.J.; writing—review and editing, J.D. and X.W.; visualization, J.D. and H.L.; supervision, J.D., C.J., X.W. and H.L.; project administration, F.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Research and Development Project of Hainan Province (grant number: ZDYF2022XDNY265) and the Agriculture Research System of Hainan Province (grant number: HNARS-01-ZJ03).

Data Availability Statement

All data generated or analyzed during this study are included in this published article (and its Supplementary Material files).

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Chromosomal location of AcJAZ family genes.
Figure 1. Chromosomal location of AcJAZ family genes.
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Figure 2. Gene structure and conserved motifs analysis of AcJAZ family genes. (A) Gene structure; (B) conserved motifs analysis.
Figure 2. Gene structure and conserved motifs analysis of AcJAZ family genes. (A) Gene structure; (B) conserved motifs analysis.
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Figure 3. Comparative phylogeny of JAZ proteins in A. catechu, A. thaliana, and rice. The red dots represent JAZ proteins of A. catechu (AcJAZs), gray dots show JAZ proteins of A. thaliana (AtJAZs), and gray boxes show rice JAZ proteins (OsJAZs).
Figure 3. Comparative phylogeny of JAZ proteins in A. catechu, A. thaliana, and rice. The red dots represent JAZ proteins of A. catechu (AcJAZs), gray dots show JAZ proteins of A. thaliana (AtJAZs), and gray boxes show rice JAZ proteins (OsJAZs).
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Figure 4. Organ-specific expression profiles of AcJAZ genes. (A) qRT-PCR results of AcJAZ genes. Different letters indicate significant statistical differences (p < 0.05) in expression levels, as determined by an ordinary one-way ANOVA. (B) Schematic figure showing the AcJAZ genes in an adult Acrea plant. RT: root, ST: stem, LE: leaf, FF: blooming female flower, MF: blooming male flower, FR: fruit.
Figure 4. Organ-specific expression profiles of AcJAZ genes. (A) qRT-PCR results of AcJAZ genes. Different letters indicate significant statistical differences (p < 0.05) in expression levels, as determined by an ordinary one-way ANOVA. (B) Schematic figure showing the AcJAZ genes in an adult Acrea plant. RT: root, ST: stem, LE: leaf, FF: blooming female flower, MF: blooming male flower, FR: fruit.
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Figure 5. Roles of the AcJAZ genes in male and female flower development. FF, female flower; MF, male flower.
Figure 5. Roles of the AcJAZ genes in male and female flower development. FF, female flower; MF, male flower.
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Table 1. Molecular characteristics of AcJAZ genes in A. catechu.
Table 1. Molecular characteristics of AcJAZ genes in A. catechu.
RenameGene IDChrAA LengthMW (KDa)pI
AcJAZ1AC02G143000.1215817.92 9.33
AcJAZ2AC03G008620.1331333.66 9.98
AcJAZ3AC03G012030.1342344.45 8.99
AcJAZ4AC03G015370.1319019.95 5.54
AcJAZ5AC03G016350.1326929.25 9.05
AcJAZ6AC04G007780.1421022.86 7.93
AcJAZ7AC05G004750.1539342.99 9.30
AcJAZ8AC05G022110.1546548.66 9.55
AcJAZ9AC05G066040.1527829.78 9.19
AcJAZ10AC05G067940.1518919.63 5.93
AcJAZ11AC06G024110.1620221.72 10.52
AcJAZ12AC07G003060.1719521.33 9.77
AcJAZ13AC14G051720.11421724.78 9.05
AcJAZ14AC15G004960.11528330.90 9.13
AA length, MW, and pI: amino acid length, molecular weight, and isoelectric point of gene product.
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Du, J.; Ji, C.; Wen, X.; Li, H.; Yang, F. Comprehensive Analysis of JAZ Family Genes Involved in Sex Differentiation in Areca catechu. Forests 2025, 16, 1133. https://doi.org/10.3390/f16071133

AMA Style

Du J, Ji C, Wen X, Li H, Yang F. Comprehensive Analysis of JAZ Family Genes Involved in Sex Differentiation in Areca catechu. Forests. 2025; 16(7):1133. https://doi.org/10.3390/f16071133

Chicago/Turabian Style

Du, Jin, Changlei Ji, Xinyu Wen, Han Li, and Fusun Yang. 2025. "Comprehensive Analysis of JAZ Family Genes Involved in Sex Differentiation in Areca catechu" Forests 16, no. 7: 1133. https://doi.org/10.3390/f16071133

APA Style

Du, J., Ji, C., Wen, X., Li, H., & Yang, F. (2025). Comprehensive Analysis of JAZ Family Genes Involved in Sex Differentiation in Areca catechu. Forests, 16(7), 1133. https://doi.org/10.3390/f16071133

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