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Journal of Ginseng Research logoLink to Journal of Ginseng Research
. 2025 Sep 18;50(2):100901. doi: 10.1016/j.jgr.2025.09.002

First-year seasonal growth regulation mechanism underlying storage root thickening in perennial Panax ginseng

Jeongeui Hong a,b, Wonsil Bae a, Jung-Woo Lee b, Jang-Uk Kim b, Kyung Ho Ma b, Donghwan Shim c, Hojin Ryu a,d,⁎
PMCID: PMC12959290  PMID: 41788577

Abstract

Background

Panax ginseng (Korean ginseng) is a valuable perennial medicinal herb characterized by its unique storage roots, which develop through an annual growth cycle. Despite its significant agricultural and pharmaceutical importance, the molecular mechanisms driving the seasonal thickening of storage roots remain poorly understood.

Methods

This study utilized histological analysis and genome-wide transcriptome profiling to investigate the development of 1-year-old P. ginseng storage roots at early, middle, and late growth stages. Gene ontology (GO) enrichment and network analyses were conducted to identify key signaling pathways. Additionally, the effects of exogenous treatment with storage root development related factors and transgenic Arabidopsis plants overexpressing PgEXP4 were evaluated.

Results

The development of storage roots was characterized by the regeneration, activation and dormancy cycles of the vascular cambium. Early-stage growth was regulated by auxin, gibberellin (GA), and nitrate signaling, promoting cambium regeneration and storage parenchyma cell differentiation. Middle-stage growth involved enhanced cell division, cell wall biogenesis, and secondary growth facilitated by the GA-expansin module. Consistently, transgenic Arabidopsis overexpressing PgEXP4 showed enhanced root growth, suggesting its role in cell expansion during root development. Late-stage growth showed upregulation of jasmonic acid (JA) pathways, indicating their role in preparing for dormancy.

Conclusion

This study elucidates the first-year seasonal growth regulation mechanisms of P. ginseng storage roots, highlighting the intricate hormonal and genetic interactions across developmental stages. These findings provide insights into optimizing ginseng cultivation practices and enhancing crop yields.

Keywords: Panax ginseng, Storage root, Vascular cambium, RNA-Seq, Hormone

Graphical abstract

Image 1

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1. Introduction

Root and tuber crops with specialized storage organs—such as tubers, tuberous roots, taproots, and rhizomes—have served as important sources of human nutrition and pharmacological materials for thousands of years [1]. During their domestication, these root crops were selectively bred for their ability to store energy and beneficial compounds in their storage organs. Among them, Korean ginseng (Panax ginseng) has been widely used for millennia as a significant medicinal root crop, particularly in East Asia [[2], [3], [4]]. The roots of P. ginseng contain starch granules within storage parenchyma tissues, which also harbor numerous bioactive compounds, including ginsenosides, polysaccharides, and phytosterols [[5], [6], [7], [8]]. Because P. ginseng is a shade plant, it is primarily cultivated under semi-shade conditions. In addition, it is a perennial plant that requires a lengthy cultivation period (4–6 years) for the roots to harvest. Genetic and physiological analyses of growth and development in P. ginseng have been challenging due to its limited cultivar characteristics and limited genome information [[9], [10], [11]].

Storage organ size in root crops is an important agricultural trait that determines overall crop yield. In the root crops, the root procambium develops into a highly organized vascular cambium [1,12], and the growth and development of storage roots are driven by cell division in this tissue. Plant hormones—especially auxin and cytokinin (CK)—and various transcription factors regulate the maintenance, patterning, and formation of the vascular cambium. Auxin provides spatial information to cambium stem cells and their daughter cells via an auxin gradient [12] and likely stimulates vascular cambium formation in storage roots [13]. In sweet potato, for example, the auxin-responsive MADS-box transcription factor IbSRD1 promotes the proliferation of metaxylem and cambium cells [[14], [15], [16]]. Recent studies have shown that strigolactone (SL) signaling in the vascular cambium is sufficient to stimulate cambium activity; it also interacts strongly with auxin signaling [17]. SL is conserved across species and positively regulates cambium cell activity. CK, known to stimulate cell division, also regulates cambium activity in Arabidopsis and poplar [18,19]. In root crops such as cassava and sweet potato, cambial activity is essential for storage root expansion. Cell proliferation in the radish cambium, for instance, is associated with CK-dependent secondary growth and is positively correlated with radish yield [20]. Although the major regulatory mechanisms of cambium formation may be similar across species, the differentiation of cambium daughter cells differs significantly. Tree species primarily produce xylem fiber cells and lignified xylem vessels, whereas root crops form starch-storing xylem parenchyma cells.

Recent research on sweet potato, cassava, and potato has indicated that storage root formation is associated with significant reductions in gibberellin (GA) [1]. Decreased lignification has been observed during storage organ formation [21]. In contrast, high levels of lignification, as seen in tree species during secondary growth, appear detrimental to the development of storage organs. To accommodate an increasing circumference in storage organs, the number of cells in the root cortex grows. Sweet potato and cassava develop a protective periderm [22], and the phellogen (cork cambium) remains active throughout the season, producing suberized phellem cells and generating new cells to replace shed cells as the fleshy root surface expands. Recent studies have also shown that GA promotes root suberization and acts in a non-antagonistic manner with abscisic acid (ABA) in Arabidopsis roots [23,24]. Despite considerable research on Arabidopsis and other root crops, the genetic and physiological characteristics affecting the growth and development of ginseng roots are still largely unexplored [2,10].

A recent study on P. ginseng found that GA treatment increases storage parenchymal cell division by enhancing cambium activity, thereby facilitating root secondary growth [25]. In addition, GA promotes cell division and cell wall biogenesis in P. ginseng roots, as revealed by a genome-wide transcriptome analysis. Genes involved in nitrate assimilation are tightly linked to the GA signaling network in GA-treated P. ginseng roots [25]. Nitrate (N) is crucial for plant hormone homeostasis and is related to both auxin and CK signaling [[26], [27], [28]]. Exogenous N application stimulates the auxin receptor AFB3, which activates auxin signaling by promoting the degradation of Aux/IAA transcriptional repressors in the presence of auxin [29]. CK signaling is also linked to the expression of nitrate transporter (NRT) genes and to nitrate distribution. Moreover, N promotes root secondary growth by enhancing both the maintenance of cambial stem cell activity and the differentiation of storage parenchyma cells [30]. Many factors involved in the root growth of P. ginseng—and closely tied to agricultural productivity have thus far been investigated via genome-wide transcriptome analyses [25,30,31].

In this study, we examined the growth and development of one-year-old P. ginseng storage roots. Early in the growth process, we observed enhanced shoot development, periderm generation, and the development of storage parenchyma cells in roots. Transcriptome analysis revealed that nitrate assimilation and plant hormones are induced at the early stage, activating downstream signaling pathways. These results suggest that nitrate, auxin, CK, GA, ABA, jasmonic acid (JA), and salicylic acid (SA) collectively break vascular cambium dormancy and initiate regeneration. During the middle stage of root growth, root expansion, cambial stem cell activation, and periderm suberization were noted. Correspondingly, auxin, GA, and ABA signaling pathways were enhanced, leading to upregulation of genes involved in cell division, cell wall organization, biogenesis, and suberization. In the later stage, genes related to JA and ABA were upregulated, indicating that the interaction of these hormonal pathways may prepare P. ginseng roots for dormancy. Overall, these findings provide insights into the growth and developmental mechanisms of one-year-old P. ginseng storage roots.

2. Materials and methods

2.1. Plant materials and transgenic plants

One-year-old Panax ginseng seedlings (Yunpoong, provided by the National Institute of Horticultural and Herbal Science) were grown at 21–23 °C with a 16 h light/8 h dark cycle in ginseng cultivation soil medium. For comparison with greenhouse-grown seedlings, plants were also grown in a field at the Department of Herbal Crop Research in Eumseong, South Korea (127°45′13.14 E, 36°56′36.63 N) from March to October 2023 under a four-layer shade net. One-year-old ginseng seedlings were treated with various solutions—indole-3-acetic acid (IAA), potassium nitrate (KNO3), N-1-naphthylphthalamic acid (NPA), methyl jasmonate (MeJA), or DMSO (mock control)—by a soaking method. After shoot emergence, DMSO, 1 μM IAA, 5 mM KNO3, and 5 mM KNO3 + 10 μM NPA were applied once a week for three weeks. Four weeks after shoot emergence, DMSO and 10 μM MeJA were applied once a week for four weeks. Two weeks after transplantation, one-year-old ginseng seedlings were treated once a week for three weeks with 10 μM GA3, 100 μM paclobutrazol (PCZ), and DMSO. All exogenous treatments were subjected to at least three biological replicates. Developmental changes in storage roots under each treatment were evaluated through measurements of root diameter and histological analyses. Root diameter was measured using a digital caliper (CAS, Yangju, Korea) at the widest point of the main taproot (about 0.5 cm below the shoot-root junction). SPAD (Single-Photon Avalanche Diode, index of leaf chlorophyll content) values were measured at the center of the leaf using a SPAD-502 Plus chlorophyll meter (Konica Minolta, Tokyo, Japan). To generate transgenic plants overexpressing GUS-tagged Pg_S0898.3 (PgEXPA4) in Col-0 (Arabidopsis thaliana) background, cDNA was cloned into the pBI121 vector plasmid under the control of a 35S promoter. All transgenes were introduced into the Col-0 genome via Agrobacterium-mediated floral dipping with strain GV3101. Transgene expression was confirmed by GUS staining, for which seedlings were incubated in GUS-staining buffer (100 mM sodium dihydrogen phosphate monohydrate, 10 mM EDTA, 0.5 mM potassium ferricyanide, 0.5 mM potassium ferrocyanide, 0.1 % Triton X-100, and 1 mM X-Gluc) for 16 h at 37 °C. To examine GUS expression patterns during root growth, PgEXPA4-GUS seedlings were analyzed at 3 and 14 days old.

2.2. Histological sections and microscopy

P. ginseng roots were hand-cut and fixed in 3 % glutaraldehyde and 3 % formaldehyde in PBS (pH 7.0) at 4 °C overnight. For paraffin sectioning, root tissues were dehydrated through an ethanol series (30 %, 50 %, 60 %, 70 %, 80 %, 90 %, 95 %, and 100 % ethanol; each step 1 h, repeated twice), then embedded in paraffin (50 % ethanol + 50 % HistoClear for 3 h, 100 % HistoClear for 5 h twice, 50 % HistoClear + 50 % paraffin for 5 h, and 100 % paraffin for 4 h twice). The samples were sectioned into 10–12 μm slices and mounted onto slides. After dewaxing in HistoClear, the slides were rehydrated and counterstained with 1 % Safranin-O (Sigma, cat. S2255) and 0.8 % Astra Blue (Santa Cruz Biochem, cat. sc-214558A) for 3 min. Safranin-O preferentially stains lignified cell walls (e.g., xylem vessels) red, while Astra Blue stains cellulose-rich tissues blue, enabling the distinction of vascular and storage tissues. The slides were then rinsed and mounted with Permount mounting medium (Fisher Chem., cat. SP15-100). Samples were examined under bright-field and polarized light using a Slideview scanner (SLIDEVIEW VS200, Evident Scientific, Tokyo, Japan) and an Olympus BX53 microscope (Olympus, Tokyo, Japan). The number of cell rows generated by cambial layers was determined by drawing a straight line from the last resin duct cell layer to the inner xylem vessel cells. The lengths of developmental zones in P. ginseng storage roots, including the transition zone (TZ), elongation zone (EZ), and maturation zone (MZ), were measured from stained cross-sections using ImageJ software. For histochemical staining, propidium iodide (PI) was used to visualize cell membranes and structure. Col-0 and PgEXPA4-GUS plants were incubated in a 1 g/mL PI (Sigma, USA) solution for 1–5 min. Samples were then observed using a laser-scanning confocal microscope (Carl Zeiss, German) with a 561 nm excitation laser and a 581–652 nm band-pass filter for detecting PI fluorescence. For quantitative analysis of cell growth, the length of root cells in the maturation zone of Arabidopsis roots was measured using ImageJ software. Cell length was determined by drawing a straight longitudinal line along the differentiated epidermal or cortical cells in the maturation zone. Statistical analysis was performed using Student's t-test or one-way ANOVA followed by Tukey's multiple range test for multiple comparisons.

2.3. RNA-seq analysis

Total RNA was extracted weekly from root samples using an Easy Spin RNA Extraction Kit (iNtRON Biotechnology, Seoul, Korea) according to the manufacturer's instructions. RNA-seq libraries were prepared using the TruSeq Stranded mRNA Library Prep Kit (Illumina, Inc., San Diego, CA) from three biological replicates of total RNA. Differentially expressed genes (DEGs) were identified using methods described previously [32]. TMM-normalized TPM values for all annotated genes were calculated by first converting raw RNA-seq read counts into TPM (Transcripts Per Million) values. The TPM calculation accounts for gene length and sequencing depth, allowing for comparisons across genes within samples. Subsequently, to enable comparisons between different samples, TPM values underwent additional normalization using the Trimmed Mean of M-values (TMM) method, which corrects for differences in RNA composition and sequencing library size across samples. This two-step normalization ensured accurate, cross-sample comparability of gene expression levels. Raw RNA-seq data were deposited in the NCBI Short Read Archive (SRA) under accession number PRJNA1216732 (Table S1). To validate RNA-seq results, cDNA was synthesized with TOPscript™ RT Dry MIX (Enzynomics, Daejeon, Korea), and qRT-PCR was performed using KOD SYBR qRT MIX (TOYOBO, Osaka, Japan). Pg_S0354.5 (PgACT) served as the internal control, and all primer sequences are listed in Table S2. Gene expression levels were normalized using the Trimmed Mean of M-values (TMM) method implemented in the edgeR package.

2.4. Functional annotation

The functional annotation of DEGs was performed using the BLAST algorithm (e-value < 1E-5) against the Arabidopsis thaliana protein database. Gene Ontology (GO) term enrichment was performed with DAVID and identified using the Fisher Exact Test (P < 0.05) [33]. Gene Set Enrichment Analysis (GSEA) was carried out as described previously [34]. In the enrichment graphs, the red line represents the subset of genes contributing most to the enrichment score (ES). The ranking list metric shows the relationship between a gene and the plant phenotype: positive values (red gradient) are upregulated genes in mock-treated control samples, while negative values (blue gradient) are downregulated genes. Network analysis was performed using DEGs and visualized in Cytoscape version 3.10.0 with the GeneMANIA app version 3.5.2 [35,36]. Bar graphs were generated using Prism 6 (GraphPad, Boston, USA).

3. RESULTS

3.1. The first-year seasonal growth phenotypes of the storage root of one-year-old P. ginseng

The secondary growth of storage organs is one of the most important agricultural traits for optimizing P. ginseng yields. To investigate the growth and developmental characteristics of perennial storage roots, we first monitored the growth patterns of one-year-old P. ginseng in a greenhouse. After the shoot as established at 2 weeks after dormancy release (WAD) from dormant perennating buds, the first-year seasonal growth and development of the one-year-old ginseng plants were completed around 20 WAD under greenhouse conditions (Fig. S1). We observed that the first-year seasonal photosynthetic life cycle of ginseng shoot in the greenhouse begins when the green leaves are established (1 WAD), sustains high photosynthetic activity from 2 to 10 WAD (higher SPAD values), and progresses to leaf senescence around 16 WAD (Fig. 1A and B). Similar to the first-year seasonal shoot growth patterns, the formation of storage roots in one-year-old P. ginseng was characterized by gradual thickening of the taproot and vigorous development of lateral roots over time during the second year (Fig. 1C and Fig. S1). Specifically, secondary growth of the storage roots increased substantially between 4 and 10 WAD (Fig. 1D), suggesting that storage root formation occurs during a distinct middle stage of development. We compared these findings under greenhouse conditions with those from a cultivated field. One-year old ginseng seedlings transplanted in mid-March 2023 were sampled in May, August, and October for an assessment of shoot and underground storage root development. Field-grown ginseng exhibited leaf senescence and perennating bud formation around mid-October (Fig. 1E), whereas storage root development accelerated rapidly between May and August (Fig. 1F). These developmental features were consistent with those of greenhouse-grown P. ginseng (Fig. S1), indicating that while developmental stages are similar, the growth rate and duration were slightly acceleratec in the greenhouse compared to field conditions. These results suggest that the greenhouse system can effectively mimic the growth stages of P. ginseng seen in shaded field conditions, without exhibiting major differences.

Fig. 1.

Fig. 1

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Phenotypes of 1-year-old P. ginseng shoot and root development. (A) Phenotype of 1-year-old P. ginseng cultivar, Yunpoong, shoots at 2, 6, and 16 weeks after dormancy release (WAD). Scale bar = 5 cm. (B) Measurement of SPAD value 1-year-old P. ginseng leaves (n = 36). (C) Phenotype of 1-year-old P. ginseng roots at 2 and 16 WAD. Scale bar = 1 cm. (D) Measurement of root diameter of Fig. 1A (n = 10). (E) Phenotype of 1-year-old P. ginseng cultivar from May, August, and November at field. (F) Measurement of root diameter of Fig. 1E (n = 15). Dots represent individual values. Different lowercase letters indicate statistically significant differences (p < 0.05; one-way analysis of variance [ANOVA]), followed by Tukey's multiple range test.

To further characterize the first-year seasonal growth pattern of ginseng storage root, we conducted histological analyses of paraffin-embedded root sections from 0 to 16 WAD using safranin–astra blue staining. Storage root formation was initiated by the regeneration of vascular cambium cells (CZ) by 2 WAD (Fig. 2A). At this stage, the development of xylem vessels (XV) with secondary cell walls, along with storage parenchyma cells containing starch granules, was observed. These tissues were confirmed to be differentiated from reactivated meristematic cambium cells at 2 WAD. As early development proceeded, the number of cambium cells and vascular-conducting tissues (phloem [PH] and XV) gradually increased (Fig. 2A). By 4 WAD, storage parenchyma cells containing starch granules dominated the storage roots, and by 16 WAD, most tissues had differentiated from vascular cambium stem cells into storage parenchyma cells (Fig. 2B). Next, we examined vascular cambium cell activity during storage root development (Fig. 2C). High levels of cambium activity persisted until 4 WAD (nearly 70 % of cells consisted of three or more cambium layers), then slightly decreased at 6 and 8 WAD. Sustained cambium activity promoted storage-parenchyma cell differentiation in the cambium zone (CZ). However, from 10 WAD to 16 WAD, the frequency of meristematic cell division in the CZ declined (Fig. 2B and C), indicating the onset of cambium cell dormancy at later developmental stages. A similar pattern was observed in one-year-old field-grown ginseng (Fig. S2). In May, cambium stem cells were highly active, leading to abundant differentiation of starch granule–containing storage parenchyma cells and a few vascular-conduction cells by August; however, the pace of storage root development dropped in October as cambium activity decreased (Fig. S2). Taken together, these data suggest that the first-year seasonal cycle of P. ginseng storage root thickening is regulated by vascular cambium homeostasis, marked by alternating phases of meristematic regeneration and dormancy.

Fig. 2.

Fig. 2

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Developmental patterns of 1-year-old P. ginseng storage roots. (A, B) Representative images of stained root cross-section of P. ginseng plants from 0 to 16 WAD, visualized using polarized light microscopy after staining with Safranin-O and Astra Blue. XV: xylem vessel, CZ: cambial cell layer zone, PH, phloem cells, RD: resin duct cells. Scale bar = (A) 100 μm, (B) 200 μm. (C) The numbers of cambial stem cells in the cambial cell layer zone (CZ) (n = 60).

3.2. Transcriptome analysis of first-year seasonal secondary growth patterns in P. ginseng storage roots

Based on the histological data, three critical developmental stages were identified for the first-year seasonal secondary growth of ginseng storage roots: early cambium regeneration, rapid mid-stage growth, and a late stage of stable growth/cambium dormancy. To further examine the underlying mechanisms in these stages of perennial P. ginseng root development, we performed time-course transcriptome analyses on ginseng roots sampled at 2 WAD (early), 8 WAD (middle), and 12 WAD (late) (Fig. S3 and Table S3). DEGs (fold change [FC] ≥ 2, false discovery rate [FDR] q-value <0.05) were identified for the 2, 8, and 12 WAD samples (Fig. S3). Specifically, we identified 2807 genes up-regulated and 3277 genes down-regulated in 8 WAD roots compared to 2 WAD roots, 393 genes up-regulated and 1011 genes down-regulated in 12 WAD roots compared to 8 WAD roots, and 2078 genes up-regulated and 3378 genes down-regulated in 12 WAD roots compared to 2 WAD roots (Fig. S3A). Cluster analysis of functional categories revealed stage-specific clusters (CL2: 2 WAD, CL3: 8 WAD, CL4: 12 WAD; Fig. S3B). These analyses identified developmentally specific functional terms (CL1), including “response to stimulus” in early-stage roots, “cell division and terpene biosynthesis” in mid-stage roots, and “cell wall modification and organization” in late-stage roots (Fig. S3C). In CL2 (early stage), stress- and growth-related hormones and developmental processes were significantly up-regulated, while genes related to cell division and carbohydrate and cell wall metabolism were down-regulated (Fig. S4A and Table S3). In CL3 (middle stage), secondary growth–related pathways (strigolactone, cell wall organogenesis, and suberin biosynthesis) and terpenoid synthetic processes were highly up-regulated (Fig. S4B and Table S3). By contrast, the late stage (CL4) showed up-regulation of JA responses and predominantly down-regulation of growth-related pathways (Fig. S4C and Table S3). The expression patterns of selected DEGs in these four clusters were confirmed by qRT-PCR (R = 0.93, Fig. S5 and Table S2). The expression patterns of representative genes were well-correlated between RNA-seq (TPM) and qRT-PCR results, as demonstrated by linear regression analysis (Fig. S5E). These findings indicate that distinct signaling and metabolic pathways regulate each stage of first-year seasonal storage root growth in P. ginseng.

3.3. Functional annotation of storage-root developmental processes in the early and middle stages of P. ginseng

Combining the histological and GO enrichment analyses of the DEGs highlighted global changes in growth and developmental processes in one-year-old P. ginseng roots during early, middle, and late stages. To identify the key signaling pathways that promote early cambium regeneration and accelerate mid-stage secondary growth, we conducted a GSEA for each developmental stage.

GSEA identified 13 and 22 significantly enriched gene sets (FDR <0.05) in the 2 WAD and 8 WAD samples, respectively (Fig. 3A and Table S4). Specifically, 2 WAD roots were enriched in “nitrate transmembrane transport” (normalized enrichment score [NES]: 1.96), “nitrate assimilation” (1.89), “response to salicylic acid” (1.77), “jasmonic acid mediated signaling pathway” (1.66), “auxin homeostasis” (1.64), and “abscisic acid–activated signaling pathway” (1.42) (Fig. 3A and B, and Figs. S5–8). In contrast, 8 WAD roots were enriched in “plant-type cell wall organization or biogenesis” (−1.78), “cell division” (−1.69), “xylem and phloem pattern formation” (−1.63), “positive regulation of auxin mediated signaling pathway” (−1.49), and “gibberellin biosynthetic process” (−1.29), compared to those at 2 WAD (Fig. 3A and C, and Figs. S6–9).

Fig. 3.

Fig. 3

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Gene set enrichment analysis (GSEA) comparing early and middle stage of storage root development. (A) Results of GSEA analysis showing enriched gene sets (false discovery rate [FDR] q-value <0.05). A positive normalized enrichment score (NES) value indicates enrichment in 2 WAD (red line), a negative NES indicates enrichment in 8 WAD (blue line). (B) Enrichment plots comparing 2 WAD and 8 WAD for auxin homeostasis (GO:0010252) and nitrate assimilation (GO:0042128). (C) Enrichment plots for plant-type cell wall organization or biogenesis (GO:0071669) and gibberellin biosynthetic process (GO:0009686). In enrichment plot, the red line represents the leading-edge subset that made the largest contribution to the enrichment score (ES) (false discovery rate [FDR] < 0.05).

Our previous work demonstrated that nitrate supplementation enhances cambium activity in P. ginseng storage roots [30], and the interplay of auxin and nitrate signaling is essential for cambium development [27,30,37]. Based on these observations, we hypothesized that elevated nitrate uptake and assimilation, along with enhanced auxin homeostasis, would be key cues for cambium regeneration and activation during ginseng storage root development. To test this hypothesis, we treated two-week-old ginseng roots with indole-3-acetic acid (IAA) and KNO3 weekly for three weeks. We found that both auxin and nitrate treatments increased the population of undifferentiated stem cells in the interfascicular cambium (IC, between storage parenchyma cells) and in the vascular cambium (between xylem and phloem) compared to mock-treated controls (Fig. 4). However, treatment with N-1-naphthylphthalamic acid (NPA), an auxin transporter inhibitor, eliminated the nitrate-induced proliferation of cambium cells (KNO3 + NPA, Fig. 4). These results indicate that nitrate-driven auxin accumulation [38] in the storage roots promotes cambium regeneration for ginseng storage root development. Gene network analyses further revealed that stage-specific signaling in the early and middle stages integrates hormonal regulation (auxin, CK, GA, ethylene, JA, ABA, and SA) with cell division, photosynthesis, vascular development, and nitrate assimilation (Fig. S10).

Fig. 4.

Fig. 4

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Auxin and nitrate treatment promote cambium regeneration. (A) Representative storage root image of stained cross-sections of P. ginseng treated with a mock control (Con), 1 μM IAA (indole-3-acetic acid), 5 mM KNO3, or 5 mM KNO3 + 10 μM NPA (N-1-naphthylphthalamic acid) once a week for 3 weeks using polarized light microscopy. Ph: Phloem, XV: Xylem vessel. Scale bar = 100 μm. (B, C) The numbers of cambial stem cells in the IC (Interfascicular cambium) (D, E) The numbers of cambial stem cells from in XV and PH. Error bars represent standard error. Dots represent individual values (n = 45; p < 0.05; one-way ANOVA, followed by Tukey's multiple range test).

3.4. Identification of expansin-mediated facilitation of storage root development

Comparative analyses of the 8 WAD and 12 WAD samples showed 23 and 1 significantly enriched gene sets (FDR <0.05) in the middle and late stages, respectively (Fig. S11A and Table S5). The gene sets enriched at 8 WAD were primarily related to secondary growth, including “suberin biosynthetic process” (NES: 2.04), “terpenoid biosynthetic process” (1.98), “plant-type secondary cell wall biogenesis” (1.88), “strigolactone biosynthetic process” (1.62), and “cell division” (1.51). Many of these were leading-edge subset genes (Figs. S11A, 11B, and Fig. S12). Conversely, only “jasmonic acid (JA) mediated signaling pathway” (−1.24) was significantly enriched in late-stage samples (Fig. S11A and 11C).

We next focused on the cell wall modification terms that were strongly enriched in the middle stage (Fig. 3C, Fig. S11 and S12). Numerous expansin (EXP) genes were identified in the leading-edge subset, such as Pg_S7147.5 (EXPB2), Pg_S3554.24 (EXPB3), and Pg_S1423.8 (EXPA4) (Fig. 5A, Fig. S11B and 12B). Detailed histological analysis of ginseng storage parenchyma development showed three distinct zones derived from cambium cells: a transition zone (TZ), where cell division and differentiation begin; an elongation zone (EZ), where cell expansion occurs; and a maturation zone (MZ), where growth concludes (Fig. 5B). Cell expansion in the EZ was particularly active during the middle and late stages (Fig. 5C and D). Previous work has shown that gibberellin (GA) application promotes ginseng storage root growth [25,39], and the heightened expression of GA synthesis factors in the middle stage (Fig. 3C) suggests a positive effect on secondary growth. Indeed, GA treatment enhanced storage-cell expansion, whereas PCZ, a GA-synthesis inhibitor, reduced this process (Fig. 5E). To investigate the functional role of PgEXPs in storage root development, we employed a heterologous transgenic Arabidopsis model system. For candidate PgEXP gene selection, we first examined expression patterns during the course of storage root development. Among the tested PgEXP genes, only Pg_S0898.3 and Pg_S1423.8 (PgEXPA4s) maintained consistently high expression levels at 8, and 10 WAD, corresponding to the middle developmental stage (Fig. S13). In contrast, the expression of other PgEXP genes either declined (PgEXPB3 and PgEXPA1) by 10 WAD or remained unchanged (Pg_S0605.6) compared to 6 and 8 WAD. These results imply that several key EXPs, such as Pg_S0898.3 and Pg_S1423.8 would play a more persistent role in facilitating cell expansion during storage root thickening. Based on these results, we performed a functional analysis by introducing a representative Pg_S0898.3 (PgEXPA4) into Arabidopsis roots. GUS staining confirmed that PgEXPA4 exhibited strong expression in the roots (Fig. S14A). Also, we confirmed that overexpressing PgEXPA4 in Col-0 promoted both root and cell growth (Fig. 5F and Fig. S14B and C). These findings collectively indicate that middle-stage storage root growth is facilitated by a GA–EXP module that mediates storage-parenchyma cell expansion.

Fig. 5.

Fig. 5

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GA and expansin positively regulate storage root development. (A) Enrichment plots and heat map of DEGs in the leading-edge subset genes contained plant-type cell wall modification (GO:0009827). Red line indicated leading-edge subset genes and the expression heat maps were presented (right). Heatmap shows the expression patterns of P. ginseng genes involved in cell wall modification. Arabidopsis gene name in parentheses represent putative orthologs of the corresponding P. ginseng genes, based on BLASTP similarity. (B) Representative section images of stained storage root cross-section of P. ginseng at 6 WAD using polarized light microscopy. Scale bar = 200 μm. CZ: cambial cell layer zone (green area), TZ: transition zone (red area), EZ: elongation zone (purple area), MZ: maturation zone (yellow area). (C, D) Quantification cell length in the elongation zone of storage roots of greenhouse-grown (C) and field-grown ginseng (D) presented in Fig. 2 and Fig. S2, respectively. (E) Quantification cell length in the elongation zone of GA- and PCZ-treated ginseng storage roots. Dots represent individual values (n = 60; p < 0.05; one-way ANOVA). (F) Measurement of root length of 35S:PgEXPA4-GUS lines presented in Fig. S13B. Dots represent individual values (n = 14; p < 0.05; one-way ANOVA, followed by Tukey's multiple range test).

3.5. JA regulates storage root development in late-stage P. ginseng

Gene network analyses indicated that stress- and dormancy-related hormones (JA, ABA, and SA) are linked to cell division and cell wall development during the middle and late stages (Fig. S15). These data suggest that late-stage JA and stress signaling responses are closely associated with finalizing cambium dormancy and storage root development. To evaluate this idea, we examined how exogenous JA affects cambium-mediated storage root formation in P. ginseng. Treating ginseng at 4 WAD (when cambium activity was high) with JA for 2–4 weeks markedly suppressed cambium cell proliferation (Fig. 6A). JA-treated ginseng displayed a reduced number and frequency of cambium cells (Fig. 6B and C), which impaired storage-parenchyma cell differentiation and ultimately diminished storage root growth (Fig. S16). Overall, these findings highlight the key signaling pathways orchestrating the first-year seasonal growth patterns of P. ginseng (Fig. S17). Early-stage P. ginseng storage root development involves auxin and gibberellin signaling triggered by nitrate uptake and assimilation, leading to cambium activation. Subsequently, GA up-regulates vascular cambium activity and EXPAs gene expression, driving the differentiation and expansion of storage-parenchyma cells. During the late stage, heightened JA signaling appears to finalize storage root development for the first-year seasonal growth cycle and prepare the plant for winter dormancy.

Fig. 6.

Fig. 6

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JA treatment represses the cambial stem cell activity. (A) Representative images of stained cross-sections of P. ginseng plants treated with a mock control (Con) or 10 μM MeJA once a week for 3 weeks using polarized light microscopy. Scale bar = 100 μm. VC: Vascular cambium, IC: Interfascicular cambium. (B, C) The numbers and frequency of cambial stem cells in the IC. Error bars represent standard error. Dots represent individual values (n = 90). The significance of the difference was analyzed by student t-test method (∗p < 0.05, ∗∗p < 0.01).

4. Discussion

Perennial plants often produce underground storage organs (such as rhizomes, bulbs, and tubers) to store carbohydrates. Above-ground tissues (leaves and stems) supply photosynthetic products necessary for growth and maintenance. These stored carbohydrates in underground organs are vital for survival and growth in subsequent years, offering protection against extreme environmental disturbances. Storage organs also serve multiple functions, including nutrient storage, recovery from damage, and support for asexual reproduction. P. ginseng is a domesticated medicinal herb valued for its pharmacological compounds stored in its roots. Recent advances in histological and molecular studies have greatly improved our understanding of how plant storage organs develop [12,25,30,31]. Despite this progress, the mechanisms by which secondary growth in Panax ginseng storage roots is integrated into broader plant signaling networks remain underexplored. In this study, we combined histological, transcriptomic, and physiological analyses to uncover the regulatory mechanisms underlying storage root thickening in P. ginseng. Through detailed examination of cambial activity and stage-specific hormonal signaling, we provide new insights into the coordinated control of storage root development. To our knowledge, this represents the first comprehensive study to dissect the first-year seasonal cycle of storage root growth in P. ginseng.

The secondary growth of these storage organs is critical for achieving high crop yields. Storage root and tuber development typically includes induction, growth, and enlargement phases [1]. For P. ginseng, the initial year establishes the storage roots, which then undergo annual phases of expansion and further development [40]. Our histological analysis revealed that the secondary growth of ginseng storage roots follows three stages: early dormancy release (regeneration), rapid mid-stage enlargement, and a late stage of renewed dormancy (Fig. 2 and S2). These developmental phases were observed under both in vivo and in vitro conditions, albeit with differences in timing and final growth potential (Fig. 2 and S1-2). Collectively, our work underscores distinct annual growth phases that govern secondary growth in P. ginseng, offering insights into histological developments across these stages.

Plant hormones and environmental factors significantly influence cambium stem-cell activity, thereby modulating secondary growth in P. ginseng storage roots [25,30,41]. Our combined histological and RNA-seq analyses confirm that each growth stage is characterized by complex hormonal regulation and environmental cues. Notably, nitrate and auxin are crucial in promoting secondary growth by sustaining cambial stem-cell activity [30]. Our GSEA and RNA-seq findings indicate that cambium regeneration at 2 WAD is associated with auxin homeostasis and nitrate assimilation (Fig. 3 and S6). Nitrate influences auxin transport and signaling activity, shaping root development [41,42]. Consistent with these observations, exogenously applied auxin or nitrate to ginseng seedlings boosted meristematic activity in cambial cells, whereas the auxin-transport inhibitor NPA negated the nitrate effect (Fig. 4). Hence, nitrate-mediated regulation of auxin homeostasis likely contributes to cambium regeneration.

Nitrate has also been shown to reduce DELLA proteins by elevating GA levels via the induction of GA-metabolism genes [43]. Our previous work demonstrated the importance of GA in ginseng's secondary root growth, specifically in promoting storage parenchyma cell development [25]. Consistent with this, we observed that exogenous GA increased parenchyma cell length in storage roots, whereas PCZ (GA-biosynthesis inhibitor) reduced this process (Fig. 5). Transcriptomic analyses showed an up-regulation of GA biosynthesis–related terms in the middle stage of P. ginseng roots (Fig. 3, Fig. 5). Previous studies suggest that GA application to roots significantly enhances both plant growth and ginsenoside accumulation in ginseng [39], in agreement with our GO analysis showing higher terpenoid biosynthetic process (Fig. 3A) which may be driven by elevated GA synthesis in the middle stage. In contrast, our data suggest that JA inhibits the secondary growth of P. ginseng roots by promoting dormancy in cambial stem cells (Fig. 6 and S16). GO and GSEA analyses revealed that JA-mediated signaling was significantly enriched at 12 WAD. Studies have reported that JA can influence dormancy release and cambium activity [37,44,45], but our results show that JA reduces cambium stem-cell proliferation in ginseng roots, thereby slowing secondary growth (Fig. 6 and S16). Further investigations are needed to clarify the molecular mechanisms by which JA represses cambial stem-cell function in ginseng roots.

Understanding the first-year seasonal growth patterns of ginseng storage roots and their hormonal regulation is crucial for improving our knowledge of P. ginseng growth and development. However, our study could not provide sufficient evidence to determine whether the annual growth regulation in Panax ginseng, a perennial species, mirrors the first-year seasonal growth pattern. Moreover, many questions remain about how downstream pathways interact with upstream hormonal signaling to orchestrate storage root development. Nevertheless, our findings offer a solid foundation for advancing the understanding of storage root development in P. ginseng. Overall, our findings suggest that clarifying first-year seasonal storage root growth in P. ginseng will not only boost root-crop productivity but also serve as a valuable foundation for future research.

Author contributions

J.H and H.R designed the experiments. J.H, W.B and D.S. were contributed to RNA extraction and sequencing analysis. J.H, W.B., J.W.L, K.H.M and J.U.K carried out P. ginseng growth experiments and histological sectioning analysis. J.H., D.S. and H.R. analyzed bioinformatic analysis and qRT-PCR validation. J.H, W.B and H.R wrote the manuscript.

Declaration of competing interest

The authors declare no conflict of interest.

Acknowledgments

This work was supported by the National Research Foundation (NRF-2021R1I1A3050947, H.R.).

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.jgr.2025.09.002.

Appendix A. Supplementary data

The following are the Supplementary data to this article.

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