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. 2025 Jun 13;14(12):1821.
doi: 10.3390/plants14121821.

A Non-Specific Phytohormone Regulatory Network in Saccharina japonica Coordinates Growth and Environmental Adaptation

Jiexin Cui  1   2 , Jinli Zhu  1   2 , Yinru Dai  1   2 , Jincheng Yuan  1   2 , Wen Lin  3 , Tao Liu  1   2
Affiliations

A Non-Specific Phytohormone Regulatory Network in Saccharina japonica Coordinates Growth and Environmental Adaptation

Jiexin Cui et al. Plants (Basel). .

Abstract

Saccharina japonica (S. japonica) is a large-scale intertidal aquatic plant that exhibits characteristics such as rhizoid, holdfast, and blade differentiation. It demonstrates remarkable environmental adaptability. However, compared with higher plants, details about its phytohormone content, distribution, synthesis, and accumulation remain poorly understood. In this study, the phytohormone contents distribution and expression patterns of synthetic genes in different parts of S. japonica, including the rhizoid, petiole, basis, middle, and tip, were analyzed in detail by combining targeted metabolomics and transcriptomics analyses. A total of 20 phytohormones were detected in S. japonica, including auxin, abscisic acid (ABA), cytokinin (CTK), ethylene (ETH), gibberellin (GA), jasmonate acid (JA), and salicylic acid (SA), with significant site-differentiated accumulation. ABA and JA were significantly enriched in the tips (28.01 ng·g-1 FW and 170.67 ng·g-1 FW, respectively), whereas SA accumulated specifically only in the rhizoid. We also identified 12 phytohormones, such as gibberellin A1, methyl jasmonate, and trans-zeatin for the first time in S. japonica. Transcriptomic profiling revealed the tissue-specific expression of phytohormone biosynthesis genes, such as CYP735A (CTK synthesis), in the rhizoids and LOX/NCED (JA/ABA synthesis) in the tips. Key pathways, such as carotenoid biosynthesis and cysteine methionine metabolism, were found to be differentially enriched across tissues, aligning with hormone accumulation patterns. Additionally, an enrichment analysis of differentially expressed genes between various parts indicated that different parts of S. japonica performed distinct functions even though it does not have organ differentiation. This study is the first to uncover the distribution characteristics of phytohormones and their synthetic differences in different parts of S. japonica and elucidates how S. japonica achieves functional specialization through non-specific phytohormone regulation despite lacking organ differentiation, which provides an important theoretical basis for research on the developmental biology of macroalgae and their mechanisms of response to adversity.

Keywords: Saccharina japonica; abiotic stress; metabolomics; phytohormones; tissue-specific adaptation; transcriptomics.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
Different parts of S. japonica. (A) Rhizoid. (B) Petiole. (C) Basis. (D) Middle. (E) Tip.
Figure 2
Figure 2
Overview of integrated metabolic data detected in S. japonica. (A) Pearson correlation of integrated metabolic data. (B) Principal component analysis of integrated metabolic data.
Figure 3
Figure 3
Presence of phytohormones in different parts of S. japonica. ABA: abscisic acid. tZT: trans-zeatin. TZR: trans-zeatin-riboside. 2IP: N6-(delta2-isopentenyl) adenine. IPA: N6-(delta2-isopentenyl) adenosine. DHZ: dihydrozeatin. DHZR: dihydrozeatin riboside. GA1: gibberellin A1. GA3: gibberellic A3. GA4: gibberellin A4. GA7: gibberellin A7. MeJA: methyl jasmonate. H2JA: dihydrojasmonic acid. JA: jasmonic acid. JA-lie: jasmonic acid-isoleucine. ACC: aminocyclopropane carboxylic acid. BR: brassinolide. SA: salicylic acid. IAA: indole-3-acetic acid. IBA: 3-indolebutyric acid. ICA: 3-indolecarboxylic acid. IPA: 3-indolepropionic acid. IAN: 3-indoleacetonitrile. IAM: 3-indoleacetamide. The colors indicate the presence of phytohormones as follows: red (detected in the rhizoid, petiole, basis, middle, and tip), yellow (partially detected in five parts), and black (undetectable).
Figure 4
Figure 4
Comparison of the content of major phytohormones in different parts of S. japonica. (A) Indole-3-acetie acid. (B) Abscisic acid. (C) Cytokinins. (D) Gibberellin. (E) Aminocyclopropane carboxylic acid. (F) Jasmonic acid. According to Duncan’s multiple range test, different letters indicate significant differences between the means of different parts (p < 0.05).
Figure 5
Figure 5
Overview of transcriptomic data detected in S. japonica. (A) Pearson correlation of transcriptomic data. (B) Principal component analysis of transcriptomic data.
Figure 6
Figure 6
Analysis of DEGs. (A) The sample correlation heat map in the R, P, B, M, and T of S. japonica. (B) Venn diagram of DEGs from different parts of S. japonica. The numbers in the figure represent the number of DEGs. (C) Number of DEGs from R vs. P, R vs. B, R vs. M, R vs. T, P vs. B, P vs. M, P vs. T, B vs. M, B vs. T, and M vs. T. The numbers in the figure represent the number of DEGs.
Figure 7
Figure 7
GO annotation classification maps of DEGs from comparison between different parts in S. japonica. (A) R vs. P. (B) R vs. B. (C) R vs. M. (D) R vs. T. (E) P vs. B. (F) P vs. M. (G) P vs. T. (H) B vs. M. (I) B vs. T. (J) M vs. T. CC: cellular component; MF: molecular function; BP: biological regulation.
Figure 8
Figure 8
KEGG pathway enrichment analysis of DEGs from comparison between different parts in S. japonica. (A) R vs. P. (B) R vs. B. (C) R vs. M. (D) R vs. T. (E) P vs. B. (F) P vs. M. (G) P vs. T. (H) M vs. T. (I) B vs. M. (J) B vs. T.
Figure 9
Figure 9
Expression of genes related to mainly phytohormone biosynthesis pathway in S. japonica. (A) CTK biosynthesis. (B) Eth biosynthesis. (C) JA biosynthesis. (D) ABA biosynthesis.
Figure 10
Figure 10
Expression comparison of RT-qPCR and transcriptional analysis of six genes in R, P, B, M, and T from S. japonica. The broken line represented gene expression data obtained from a transcriptome sequencing analysis, while the column depicted the gene expression date from RT-qPCR.
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