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Published: 5 October 2025

Identification of Carrot Expansin Gene Family and Its Regulation of Carrot Growth and Development

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State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Ministry of Agriculture and Rural Affairs Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
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Institute of Agricultural Information, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
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Zhengzhou Agricultural Science and Technology Research Institute, Zhengzhou 450015, China
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National Experimental Teaching Center for Animal Sciences, Nanjing Agricultural University, Nanjing 210095, China
Agronomy2025, 15(10), 2338;https://doi.org/10.3390/agronomy15102338 
(registering DOI)
This article belongs to the Special Issue Applications of Pre- and Post-Harvest Techniques in Horticultural Products—2nd Edition
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Abstract

Carrot (Daucus carota L.) is an important root vegetable crop in the Apiaceae and is widely cultivated around the world. Expansins play crucial roles in the growth and development of plants. Here, a total of 35 carrot expansins were identified from carrot. Sequence alignment and phylogenetic analysis revealed that carrot expansins could be classified into four subfamilies, each with similar exon/intron structures and motif compositions, indicating that carrot expansins were relatively conserved during evolution. Chromosomal localization and gene duplication analysis indicated that DcEXP genes were unevenly distributed across carrot nine chromosomes and had evolved predominantly under purifying selection. Measurements of key agronomic characters of carrots at different developmental stages (30, 60, and 90 days after sowing) indicated significant positive correlations among root fresh weight, aboveground fresh weight, root–shoot ratio, root length, and root diameter. The period from 30 to 60 days after sowing was identified as the primary phase of taproot enlargement. Analysis of spatiotemporal expression patterns revealed that most DcEXP genes were specifically expressed in the taproots, and only one gene, DcEXP18, was specifically expressed in leaves. During the rapid growth period of carrot taproots (30 and 60 days after sowing), the genes DcEXP2, DcEXP3, DcEXP5, DcEXP8, DcEXP11, DcEXP13, DcEXP17, DcEXP19, DcEXP20, DcEXP22, DcEXP26, DcEXP28, and DcEXP33 exhibited high expression levels, suggesting that they played potential important roles in carrot taproot enlargement. These findings will advance our knowledge of the molecular mechanisms underlying expansin regulation of carrot growth and development.

1. Introduction

Carrot (Daucus carota L.), a biennial herbaceous plant belonging to the genus Daucus in the Apiaceae family, is a cultivated variant of its wild counterpart. As a prominent member of the world’s top ten most widely grown vegetables, carrot is extensively cultivated across the globe [1,2]. The taproot of carrot, being the main edible part, is highly favored by consumers for its significant nutritional and economic value [3]. During the growth and development of carrots, the growth of the aerial parts and the underground parts is interdependent and mutually restrictive. Poor growth of the aerial parts can negatively impact the development of the taproot. Conversely, if the aerial parts grow excessively vigorous, the translocation of assimilates to the underground parts is reduced, which also affects the development and nutrient accumulation of the taproot. Only when the aerial stem and leaves grow robustly can it be conducive to the development and nutrient accumulation of the taproot, achieving a strong plant with a large root [4,5].
McQueen-Mason et al. isolated two proteins, CsEXP1 and CsEXP2, with molecular weights of 29–30 kDa from the hypocotyls of cucumber seedlings [6]. These proteins were found to possess the ability to restore the expansibility of cell walls in vitro under acidic conditions; they were consequently named expansins [6]. Expansins are widely distributed in both monocotyledonous and dicotyledonous plants. To date, various expansins have been identified in different plant species, such as maize [7,8], rice [9,10], tobacco [11], Arabidopsis thaliana [12,13], soybean [14], grape [15], and tomato [16,17,18,19]. Expansins constitute a large superfamily of genes. Based on the results of gene sequence analysis, expansins can be divided into four independent subfamilies, namely α-expansin (EXPA), β-expansin (EXPB), expansin-like A (EXLA), and expansin-like B (EXLB) [20]. Among them, the EXPA and EXPB families are the most diverse and extensively studied expansins. Research has shown that expansins are low-molecular-weight proteins composed of 250–270 amino acid residues, featuring three distinct domains: a signal peptide domain, a catalytic domain, and a binding domain. The signal peptide domain is located at the N-terminus, consisting of 20–30 amino acids. It directs the expansin protein into the endoplasmic reticulum, where it undergoes processing and modification before being transported to the plasma membrane and subsequently released into the cell wall [21,22]. Catalytic domain is composed of 120–135 amino acids and shares homology with endoglucanase GH45. Its core sequence includes the HFD (His-Phe-Asp) motif and cysteine residues (Cys, C), which are capable of weakening the hydrogen bond connections between cell wall polysaccharides [23]. The binding domain consists of 90–120 amino acids and exhibits sequence homology with Group II grass pollen allergens. It contains four conserved tryptophan residues (Trp, W) that enable it to interact with the cellulose framework, thereby exerting its function [24,25]. Expansin genes typically contain four conserved introns (A, C, B, F), whose positions within the gene are generally fixed [25,26]. The function of expansins relies on the synergistic action of these domains, which weaken the hydrogen bonds between cell wall polysaccharides, thereby promoting cell wall loosening and expansion [24,26].
Expansins are of great significance in plant growth and development, participating in nearly the whole process of plant growth and development, such as seed germination, leaf development, stem elongation, root growth, and the development of flowers and fruits [26]. Choi et al. introduced the OsEXPA4 gene into rice and observed that the length of the coleoptile and mesocotyl in sense transgenic plants was significantly increased, with a notable elevation in the expression level of the OsEXPA4. Conversely, in antisense transgenic seedlings, the opposite effects were seen [27]. Muller et al. discovered that 19 expansin genes in maize could influence leaf growth and development by regulating cell division, cell wall differentiation, and leaf expansion [28]. The soybean expansin gene GmEXPB2 has been shown to promote root cell differentiation and root elongation [29]. In carrot, previous research has characterized the phenotypes and agronomic traits at different growth and development stages [3]. Based on proteome and transcriptome data combined with carrot phenotype analysis, Wang et al. preliminarily identified the DcEXP gene family associated with carrot root development [30]. However, research on the DcEXP gene family in carrot remains relatively limited. It is currently unclear which DcEXP members participate in the critical period of carrot taproot enlargement, nor whether their expression levels correlate with yield traits such as root fresh weight and root diameter.
In this study, the expansin gene family in carrot were identified. To identify potential regulatory nodes where DcEXP genes may participate in carrot development at the phenotypic level, we first profiled five agronomic traits (root fresh weight, aboveground fresh weight, root–shoot ratio, root length, and root diameter) at 30, 60 and 90 days after sowing and performed trait correlation analyses. Subsequently, we conducted whole-family expression profiling of DcEXP genes in taproot and leave samples from this period, integrating “trait variation” with “gene expression” to provide a foundation for further research into the molecular mechanisms underlying the regulation of taproot swelling in carrots by DcEXP genes.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

The carrot cultivar ‘Kurodagosun’ (‘KRD’) was cultivated in the artificial climate chamber of the State Key Laboratory of Crop Genetics and Germplasm Enhancement and Utilization at Nanjing Agricultural University. The growth conditions were as follows: a daytime temperature of 25 °C, a nighttime temperature of 18 °C, a photoperiod of 16 h·d−1, and a light intensity of 300 μmol·m−2·s−1. The planting substrate consisted of a mixture of organic soil, vermiculite, and perlite in a volume ratio of 2:2:1. A total of 20 pots were sown, with 100 plants in total. Leaf and taproot samples were collected at 30, 60, and 90 days after sowing (DAS) from 30 well-growing plants per sample type, mixed thoroughly, and then immediately frozen in liquid nitrogen and stored at −80 °C for subsequent experiments. Three independent biological replicates were prepared for each carrot plant sample.

2.2. Extraction of Total RNA and Synthesis of cDNA

Total RNA was extracted from plant tissues using the polysaccharide polyphenol plant total RNA extraction kit (Proteinssci, Shanghai, China). The extracted RNA samples were reverse-transcribed into cDNA using the HiScript II Q RT SuperMix for qPCR (+gDNA wiper) (Vazyme, Nanjing, China). The synthesized cDNA was diluted 15-fold with sterile ddH2O and stored at −20 °C for subsequent use.

2.3. Identification of the Carrot DcEXP Gene Family

To identify the DcEXP gene family in carrot, we obtained the carrot genome data from the Phytozome database (JGI) (https://phytozome.jgi.doe.gov/pz/portal.html) (accessed on 10 January 2025). The sequences of the expansin gene family from Arabidopsis thaliana were downloaded from the TAIR database (https://www.arabidopsis.org/) [31]. An HMM (Hidden Markov Model) for the expansin family was constructed using the HMMER 3.4 software. The DcEXP proteins in the carrot genome were identified using the HMM and the Pfam online tool (http://pfam.xfam.org/), specifically by intersecting the PF01357 and PF03330 domains. Finally, redundant sequences were removed using the Blastp program to obtain the final identification results.

2.4. Multiple Sequence Alignment and Phylogenetic Tree Construction of the Carrot DcEXP Gene Family

Multiple sequence alignment of DcEXP proteins in carrot was performed using ClustalX 1.81 software and DNAMAN 6.0 software. The phylogenetic tree was constructed by the Neighbor-Joining (NJ) method in MEGA 7.0 with the parameters set for 1000 bootstrap replications [32]. Based on the phylogenetic tree topology and the classification of homologous genes in Oryza sativa and Arabidopsis thaliana, the DcEXP proteins in carrot were classified into different subfamilies.

2.5. Protein Properties and Sequence Analysis of the Carrot DcEXP Gene Family

Genomic DNA, CDS, amino acid sequences, and gene annotations were extracted from the carrot genome database. The amino acid count (aa), molecular weight (MW), isoelectric point (pI), and hydropathy (GRAVY) of DcEXP protein sequences were analyzed using the online tool Expasy (https://web.expasy.org/protparam/) (accessed on 10 January 2025). The gene structure of DcEXP genes was analyzed using the Gene Structure Display Server (GSDS) 2.0 (http://gsds.cbi.pku.edu.cn/). Conserved motifs within the DcEXP gene family were identified using the MEME Suite (https://meme-suite.org/meme/tools/meme) (accessed on 10 January 2025). The results were visualized using TBtools-II software [33].

2.6. Chromosomal Localization, Collinearity and Selection Pressure Analysis of the Carrot DcEXP Gene Family

Chromosomal localization information of the DcEXP gene family was obtained from the carrot genome database, and chromosomal localization maps were drawn using Tbtools software. Synteny analysis of the DcEXP gene family was completed in MCScanX. Non-synonymous substitution rate (Ka), synonymous substitution rate (Ks), and Ka/Ks analyses of homologous genes were performed using KaKs_calculator2.0 software and Tbtools software.

2.7. Cis-Acting Element Analysis of the Carrot DcEXP Gene Family

The genomic DNA sequences 2000 bp upstream of the start sites of the DcEXP genes were defined as promoter regions. The cis-acting elements in the promoter regions of the DcEXP genes were analyzed using the PlantCARE database (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) (accessed on 12 January 2025). The results were visualized using TBtools software.

2.8. Measurement of Agronomic Characters and Correlation Analysis

To gain further insight into how the DcEXP genes participate in and regulate carrot growth and development, we first analyzed the phenotypes and agronomic characters during key developmental stages of carrots. Agronomic characters of carrots were measured at 30, 60, and 90 days after sowing. The root fresh weight and aboveground fresh weight were measured using an electronic analytical balance. The root–shoot ratio was calculated as the ratio of the fresh weight of the taproot to that of the aerial parts. Root length was measured with a ruler, and root diameter (the diameter at the root head) was measured using a vernier caliper with automatic reading. Each of these measurements was conducted with three biological replicates. Statistical analysis, significant difference analysis, and Pearson’s correlation analysis were performed using SPSS 25.0 software, and the results were visualized with TBtools software.

2.9. Gene Expression Analysis

The expression levels of DcEXP genes in carrot at different growth stages and in various tissues were determined using Hieff qPCR SYBR Green Master Mix (Yeason, Shanghai, China). The experiments were conducted in 96-well plates using the Real-Time PCR detection system (Bio-rad, CFX96, California, USA). Carrot DcActin was used as the reference gene [34], and specific quantitative primers were designed using Primer Premier 6.0 software (Supplemental Table S1). The total reaction volume for RT-qPCR was 20 μL, which included 10 μL of SYBR Premix Ex Taq, 2 μL of cDNA template, 7.2 μL of ddH2O, and 0.4 μL of each forward and reverse primer. The thermal cycling program was as follows: initial denaturation at 95 °C for 5 min, followed by 40 cycles of denaturation at 95 °C for 10 s and annealing at 60 °C for 30 s. Fluorescence signals were continuously measured during a stepwise increase in temperature from 65 °C to 95 °C to generate melting curves. The relative expression levels of the genes were calculated using the 2−ΔΔCT method [35]. Each sample was analyzed in triplicate. Statistical analysis was performed using SPSS 25.0 software, and significant differences were determined by Duncan’s multiple range test at p < 0.05.

3. Results

3.1. Identification and Analysis of the Carrot DcEXP Gene Family

Based on the carrot genome database, a total of 35 DcEXP genes were identified. According to the nomenclature proposed by Wang et al. [30], these genes were designated as DcEXP1~DcEXP26 and DcEXP28~DcEXP36. A comparative sequence analysis of the DcEXP gene family members was conducted (Table 1). The results indicated that the 35 DcEXP genes were distributed across all 9 carrot chromosomes. The lengths of the DcEXP gene sequences varied significantly, within the range of 671~4266 bp. The amino acid sequence of DcEXP19 was the longest (293 aa), while that of DcEXP18 was the shortest (186 aa). The molecular weights of the DcEXP proteins were within the range of 20.60~31.36 kDa, and their theoretical isoelectric points (pI) were within the range of 4.89~9.92. Except for DcEXP2, DcEXP9, DcEXP10, DcEXP16, DcEXP19, DcEXP24, and DcEXP31, all other DcEXP proteins were predicted to be hydrophilic. The multiple sequence alignment results showed that the 35 DcEXP amino acid sequences share 45% identity (Figure 1).
Table 1. Information of DcEXP family members and physicochemical properties of DcEXP proteins in carrot.
Figure 1. Multiple sequence alignment of DcEXP protein amino acid sequences in carrot. ‘◆’ represent conserved cysteine (Cys, C) residues, ‘●’ represent the HFD (His-Phe-Asp) motif, and ‘▲’ represent tryptophan (Trp, W) residues.

3.2. Phylogenetic Analysis of the Carrot DcEXP Gene Family

The amino acid sequences of EXP proteins from carrot, rice, and Arabidopsis were aligned, and a phylogenetic tree was constructed using the Neighbor-Joining method (Figure 2). The results showed that the carrot, rice, and Arabidopsis EXP proteins were divided into four subfamilies: α-expansin (EXPA), β-expansin (EXPB), expansin-like A (EXLA), and expansin-like B (EXLB), with members of each subfamily forming their own distinct clade. Among them, the EXPA subfamily contained the most DcEXP proteins, with 24 members; the EXPB subfamily included 7 DcEXP proteins; only DcEXP2 (DCAR_103393) belonged to the EXLA subfamily; and the EXLB subfamily comprised three DcEXP proteins, namely DcEXP7 (DCAR_209418), DcEXP35 (DCAR_728680), and DcEXP36 (DCAR_728679).
Figure 2. Phylogenetic tree of EXP protein in carrot, rice, and Arabidopsis.

3.3. Conserved Motif and Gene Structure Analysis of the Carrot DcEXP Gene Family

Based on the phylogenetic relationships of EXP proteins in carrot and Arabidopsis thaliana, the DcEXP proteins were classified into four distinct subfamilies (Figure 3A). The conserved motifs of the DcEXP family members were analyzed using the MEME online tool, resulting in the identification of 10 conserved motifs, which were distributed among the different subfamilies as shown in Figure 3B and Supplemental Figure S1. Genes with high homology share the same motif composition. Motif 1, motif 2, and motif 9 were present only in the EXPA subfamily, while motif 10 was exclusive to the EXPB subfamily. Except for the EXPA subfamily, all other subfamilies contain motif 7. The domain analysis results (Figure 3C) indicated that the EXPA subfamily genes possessed the PLN00050 (DPBB_1 domain) and PLN00193 (Pollen_allerg_1 domain). The EXPB subfamily genes mainly contained the DPBB_EXPB_N, Expansin_C, and PLN03023 (DPBB_1 and Pollen_allerg_1 domains). Members of the EXLA and EXLB subfamilies shared the same domain composition, with a conserved PLN03023 domain. The gene structure analysis results (Figure 3D) showed that, except for DcEXP18, all EXPA subfamily genes had two introns. EXPB subfamily genes contained three introns, and EXLA and EXLB subfamily genes had the same number of introns, which was four.
Figure 3. Phylogenetics, conserved motif, conserved domain, and gene structure analysis of the DcEXP protein in carrot. (A): Phylogenetic tree; (B): Conserved motif distribution; (C): Conserved domain distribution; (D): Gene structure.

3.4. Chromosomal Localization and Collinearity Analysis of the Carrot DcEXP Gene Family

A chromosomal localization map was drawn based on genomic annotations to investigate the distribution of DcEXP genes on carrot chromosomes (Figure 4A). As shown in the figure, the 35 DcEXP genes were located on all nine chromosomes. The highest number of genes, seven, was found on chromosome 7, while the lowest number, one, was found on chromosome 9. To explore the potential relationships and possible gene duplications among DcEXP genes in carrot, a collinearity analysis was performed. As shown in Figure 4B and Supplemental Table S2, among the 35 members of the DcEXP gene family, 24 pairs of homologous gene pairs were identified as segmental duplications. The selection pressure analysis of these 24 pairs of homologous genes revealed that the Ka/Ks ratios were all less than 1, indicating that the evolution of DcEXP genes within the species was primarily driven by purifying selection.
Figure 4. Chromosomal determination and collinearity analysis of DcEXP genes in carrot. (A): Chromosomal determination; (B): Collinearity analysis. Lines represent collinear gene pairs.

3.5. Cis-Acting Elements Analysis of the Carrot DcEXP Gene Family

To explore the potential regulatory mechanisms of DcEXP genes in carrot, a cis-acting element analysis was conducted on the 2000 bp upstream sequences from the start codons of the DcEXP gene family members. The results showed that the promoter regions of DcEXP genes contained a variety of cis-acting elements, which were categorized into three classes based on their functions: elements related to plant growth and development, plant hormone response, and abiotic and biotic stress response (Figure 5). Among these, light-responsive elements (GT1-motif), abscisic acid-responsive elements (ABRE), methyl jasmonate-responsive elements (CGTCA-motif and TGACG-motif), anaerobic induction elements (ARE), and low-temperature responsive elements (LTR) were widely present in DcEXP genes. The majority of the genes had a predominance of plant growth and development-related elements in their promoter regions. DcEXP11 and DcEXP28 had the highest number of plant growth and development-related elements in their promoter regions, with 23 elements each. The promoter region of DcEXP32 did not contain any plant hormone-responsive elements. The auxin-responsive element (AuxRR-core) was only found in the promoter regions of DcEXP23 and DcEXP35.
Figure 5. Distribution of cis-elements of DcEXP gene promoters in carrot.

3.6. Agronomic Characters and Correlation Analysis of Carrot at Different Growth and Development Stages

The phenotypes of ‘Kurodagosun’ (‘KRD’) carrot plants at 30, 60, and 90 days after sowing were shown in Figure 6A. As the carrot plants grew, the aerial parts of ‘KRD’ became more lush, and the taproots gradually enlarged. The taproots showed significant enlargement between 30 and 60 days after sowing. The root fresh weight, aboveground fresh weight, root–shoot ratio, root length, and root diameter were measured at 30, 60, and 90 days after sowing (Figure 6B). The results indicated that during the growth and development of carrots, the root fresh weight, root–shoot ratio, and root diameter all increased significantly. There were no significant differences in the aboveground fresh weight and root length between 60 and 90 days after sowing.
Figure 6. Growth status and analysis of agronomic characters of carrot ‘Karodagosun’ at three growth stages. (A): The status of carrot ‘Karodagosun’ at three growth stages. The white line represent 2 cm; (B): Root fresh weight, aboveground fresh weight, root–shoot ratio, root length, and root diameter at 30, 60, 90 days after sowing of carrot ‘Karodagosun’. Error bars represent mean standard deviation (SD). Different lowercases indicate the significant difference at p < 0.05 level. (C): Correlation coefficient analysis of agronomic characters of carrot. ** indicate significant correlation at the level of p < 0.01.
To further investigate the relationships between different agronomic characters during the growth and development of carrots, a Pearson’s correlation analysis was conducted on the five agronomic characters. As shown in Figure 6C, all five agronomic characters exhibited highly significant positive correlations. The strongest correlations were found between root diameter and root–shoot ratio (0.979 **), root diameter and root fresh weight (0.970 **), and root fresh weight and root–shoot ratio (0.965 **). These results suggested that as the taproot diameter increases, the root fresh weight and root–shoot ratio also increase, indicating that a thicker taproot was associated with a greater root fresh weight and a higher root–shoot ratio.

3.7. Temporal and Spatial Expression Pattern Analysis of DcEXP Genes in Carrot

The expression levels of DcEXP genes in leaves and taproots of ‘Kurodagosun’ (‘KRD’) carrot plants at 30, 60, and 90 days after sowing were shown in Figure 7. The results indicated that DcEXP18 was specifically expressed in leaves, with the highest expression level at 60 days after sowing, which was 7.95 and 5.57 times higher than that at 30 and 90 days after sowing, respectively. The expression levels of DcEXP6, DcEXP16, DcEXP24, DcEXP25, and DcEXP29 in leaves at 30 days after sowing were significantly higher than those at other stages. The genes of DcEXP2, DcEXP3, DcEXP5, DcEXP8, DcEXP11, DcEXP13, DcEXP17, DcEXP19, DcEXP20, DcEXP22, DcEXP26, DcEXP28, and DcEXP33 were mainly expressed in taproots, with very low or undetectable expression levels in leaves at all three time points. All 35 DcEXP genes exhibited relatively low expression levels in taproots at 90 days after sowing.
Figure 7. The relative expression levels of DcEXP genes in different tissues of carrot at different growth stages. Error bars represent mean standard deviation (SD). Different lowercase letters indicate significant differences (p < 0.05) for each gene among the combinations of three growth stages (30, 60, and 90 days after sowing) and two tissues (leaf and taproot).

4. Discussion

Expansins play crucial roles in plant growth and development [24]. In recent years, with the advancement of genomics and bioinformatics, expansin gene families have been identified in multiple plant species [36]. For instance, the soybean genome contained 75 expansin family members [14], there were 52 expansin family members in tobacco [37], 88 expansin genes in maize [38], and 29 expansin genes in grape [15]. In this study, based on the carrot genome database, we identified 35 expansin genes in carrot, designated as DcEXPs. The variation in the number of expansin family members among different species may be related to genome duplication, chromosomal recombination, and translocation events. According to phylogenetic analysis, plant expansin genes can be divided into four subfamilies: α-expansin (EXPA), β-expansin (EXPB), expansin-like A (EXLA), and expansin-like B (EXLB) [20]. Previous studies have indicated that during plant evolution, the EXPA subfamily emerged first, followed by the EXPB subfamily, while the EXLA and EXLB subfamilies appeared most recently [6,9,22,24,26,39]. The EXPA subfamily first emerged before the divergence of algae and bryophytes, and its DPBB_1 domain has never been lost in land plants, consistently preserving the “acid-growth” cell-wall-loosening function [6,9]. In this study, all carrot DcEXPA members retained this domain intact and clustered with rice and Arabidopsis EXPA genes in the same clade, suggesting that DcEXPA proteins likely regulate the enlargement of parenchyma cells in the carrot taproot and thereby influence carrot growth and development. EXPB has been shown to function in plant reproduction. In Arabidopsis, AtEXPB5 was highly expressed in reproductive organs and facilitates pollen-tube elongation [40]. DcEXP33 and DcEXP19 were most closely related to AtEXPB5, suggesting that they might retain their reproductive tissue expression characteristics, which can be validated in the future through flower and root RNA-seq ratios. The EXPA subfamily has the most members, followed by the EXPB subfamily, while the EXLA and EXLB subfamilies have the fewest members. For example, in Arabidopsis thaliana, the EXPA subfamily had the highest number of genes (26), while the EXPB, EXLA, and EXLB subfamilies had 6, 3, and 1 genes, respectively [20,25]. In rice, the expansin genes were distributed among the four subfamilies as follows: EXPA (34 genes), EXPB (19 genes), EXLA (4 genes), and EXLB (1 gene) [41]. In tomato, the expansin gene family included 25 EXPA, 8 EXPB, 1 EXLA, and 4 EXLB members [37]. In this study, based on the phylogenetic tree topology and the classification of homologous genes in rice and Arabidopsis, the 35 DcEXP genes in carrot were classified into four subfamilies: EXPA, EXPB, EXLA, and EXLB, containing 24, 7, 1, and 3 genes, respectively. The classification results and the number of genes in each subfamily were consistent with the findings of previous studies, the members of the subfamily gather in groups, revealing the regular origin and evolutionary relationships between subfamilies.
The exon/intron structure is typically conserved among members of homologous gene families, and its analysis can help reveal the evolutionary history of gene families [42]. A comprehensive analysis of the exon/intron structure of expansin gene families in grape, soybean, tobacco, wheat, and cabbage [14,15,37,43,44] revealed that the typical number of introns in the four expansin subfamilies are as follows: EXPA (2 introns), EXPB (3 introns), EXLA (4 introns), and EXLB (3 or 4 introns). In this study, most EXPA subfamily genes in carrot contained 2 introns, all EXPB subfamily genes contained 3 introns, and all EXLA and EXLB subfamily genes had the same number of introns, which was 4. These results were consistent with previous studies, indicating a high degree of similarity in exon/intron structure within the same subfamily. In addition to the DPBB_1 and Pollen_allerg_1 domains, expansin gene family sequences also contain multiple conserved motifs. Previous studies have identified 10 motifs in soybean expansin genes and 11 motifs in tobacco expansin genes [14,37]. The analysis results showed that the type and number of motifs are similar within the same subfamily but differ among different subfamilies. In this study, we analyzed the conserved motifs of DcEXP family members in carrot and identified 10 conserved motifs. Genes within the same subfamily had similar motif compositions, which was consistent with previous findings, indicating that the gene structure and domain composition of expansin subfamilies are highly conserved during evolution.
Genome-wide phylogeny showed that the expansin subfamilies originated before the monocot-eudicot divergence and were repeatedly expanded by successive whole-genome duplications. Branch-specific analyses revealed that positively selected sites cluster in the catalytic HFD motif and the cellulose-binding face carrying conserved tryptophans, indicating that evolutionary fine-tuning of these domains alters their polysaccharide affinity. Consequently, duplicated genes with novel functions acquired unique expression domains, participating in diverse cell wall relaxation events [36]. This tightly links gene family diversification with the functional diversity required for complex plant morphologies. Expansins are stable and widely present in plants, and they are localized on most chromosomes of plants. However, their distribution on chromosomes is uneven [45]. Studies have shown that expansin genes in rice were distributed across 10 chromosomes. In Arabidopsis thaliana and Chinese cabbage, expansin genes were found on every chromosome [25,46]. In this study, the 35 carrot expansin genes were distributed across all nine chromosomes, indicating that the expansin gene family may have certain selective advantages during the evolution of carrots. Moreover, the differences in the chromosomal distribution patterns of expansins may be related to the genomic evolutionary history and functional requirements of different species. During the course of evolution, plants frequently undergo gene duplication events to adapt to changes in external environmental conditions. Gene duplication is one of the main drivers of genome and gene family evolution [47]. Among these, tandem duplication and segmental duplication are the primary modes of expansion in gene families [48]. After the formation of new genes, they may undergo functional divergence due to different types of selective pressures [49]. Studies have shown that tandem duplication was the main expansion mode of the expansin gene family in monocots, such as rice and wheat [40,50]. In dicots, the expansion mode of the expansin gene family was mainly through segmental duplication [14,25,41,43]. Additionally, during the study of the chromosomal localization patterns of expansin gene families, previous research has found that some genes distributed on different chromosomes had collinear relationships [14], indicating that chromosomal rearrangements may have occurred in the gene family during evolution. In this study, among the 35 members of the carrot DcEXP gene family, 24 pairs of collinear gene pairs were identified, all of which were segmental duplications. The Ka/Ks ratios were less than 1, indicating that the DcEXP gene family has evolved in a relatively conservative manner, which may be related to the similar regulatory functions of expansin genes in plant growth and development.
Expansins, key cell wall-loosening proteins, play a pivotal role in the enlargement of carrot storage roots [30]. To elucidate the relationship between the DcEXP gene family and phenotypic development, we first analyzed five core agronomic characters (root fresh weight, aboveground fresh weight, root–shoot ratio, root length, and root diameter) at three critical developmental stages: 30, 60, and 90 days after sowing. The results revealed that 30~60 days after sowing constituted the critical period for rapid taproot enlargement. All five characters exhibited highly significant positive correlations, consistent with previous reports [3,30], indicating this stage as the golden period for carrot morphological establishment and yield accumulation. Based on this phenotypic temporal pattern, we further examined the expression differences of DcEXP family members in taproots and leaves across developmental stages. This approach aims to integrate the “gene family-critical taproot enlargement period-trait correlation” framework to elucidate, at the molecular level, how DcEXP regulates rapid carrot taproot enlargement and to deliver actionable gene targets for high-yield carrot breeding. Numerous studies have shown that expansins are primarily present in growing plant tissues and organs, and their gene expression exhibits temporal and spatial specificity [24]. Lee et al. analyzed the transcriptional level of the soybean expansin gene GmEXP1 and found that GmEXP1 was specifically expressed in roots, with varying expression levels at different stages of root development, peaking in the root system at 5 days after seed germination [51]. In this study, most carrot expansin genes were specifically expressed in the taproot, with only one gene, DcEXP18, being specifically expressed in leaves. DcEXP36 was not expressed in either the taproot or leaves of carrots, suggesting that it may be expressed during the reproductive growth stage of carrots. During the taproot expansion period of carrots (30~60 days after sowing), the expression levels of genes such as DcEXP2, DcEXP3, DcEXP5, DcEXP8, DcEXP11, DcEXP13, DcEXP17, DcEXP19, DcEXP20, DcEXP22, DcEXP26, DcEXP28, and DcEXP33 were relatively high, indicating that they may play roles in taproot development. Pacifici et al. found that inhibiting the expression of the Arabidopsis EXPA1 gene resulted in impaired cell wall elongation in atexpa1 mutants, thereby affecting cell differentiation in the root apical meristem [52]. It was closely related to carrot DcEXP26, and DcEXP26 was highly expressed in taproot, speculating that DcEXP26 might play a similar role to AtEXPA1 in carrot taproot by maintaining the extensibility of root apical meristem cell walls, promoting the differentiation and expansion of thin-walled cells, and regulating the development of carrot taproot. The Arabidopsis AtEXLA2 gene was associated with lateral root formation [53] and was most closely related to the carrot DcEXP2. In this study, DcEXP2 exhibited the highest expression levels in 30 days after sowing taproots. It was hypothesized that DcEXP2 might influence storage root branching and final morphogenesis by regulating the initiation and elongation of lateral root primordia during early carrot taproot development. Moreover, all 35 DcEXP genes exhibited lower expression levels in the taproot at 90 days after sowing, demonstrating that the expression of carrot expansin genes was temporally and spatially specific and mainly involved in taproot development. Wang et al., based on proteomic and transcriptomic analyses, found that DcEXP genes were involved in regulating taproot development in carrots [30], which was consistent with the results of this study. It was inferred that DcEXP genes are key regulators of taproot enlargement in carrots and their functions can be further explored through functional validation. With the rapid development of carrot genomics, further research and verification will be carried out [54,55,56].
This study systematically identified the expansin gene family in carrot and analyzed the temporal and spatial expression patterns of these genes in conjunction with growth phenotypes. The findings provide a reference for further research and validation of the regulatory functions of DcEXP genes in carrot taproot enlargement, and lay the foundation for regulating carrot growth and improving yield and quality.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy15102338/s1, Figure S1. Predicted conserved motifs of carrot DcEXP proteins. Table S1. Nucleotide sequences of primers used for RT-qPCR. Table S2. The duplicate DcEXP gene pairs in carrot.

Author Contributions

Conceptualization, A.-S.X. and R.-R.Z.; methodology, R.-R.Z. and Y.-H.W.; investigation, R.-R.Z. and N.Z.; formal analysis, R.-R.Z., J.-P.T., J.-H.Z., X.-F.P., L.Z., X.X., Y.-J.S. and G.-F.T.; resources, A.-S.X.; writing—original draft preparation, R.-R.Z.; writing—review and editing, A.-S.X.; visualization, R.-R.Z.; supervision, A.-S.X.; project administration, A.-S.X. and R.-R.Z.; funding acquisition, A.-S.X. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Fundamental Research Funds for the Central Universities (KYLH2025002), Key Laboratory of Vegetable Genetics and Physiology of Qinghai Province Open Research Project (2020-SCSYS-01), Priority Academic Program Development of Jiangsu Higher Education Institutions Project (PAPD), and the Bioinformatics Center of Nanjing Agricultural University.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

In this section, all the other data sets supporting the conclusions of this article are included within this article.

Conflicts of Interest

The authors declare no conflicts of interest.

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