# Temporal Transcriptomic and Metabolomic Reprogramming Unveils a Two-Phase Salt Tolerance Mechanism in Apocynum venetum

**Authors:** Syeda Wajeeha Gillani, Meng Wang, Lu Wang, Xueli Lu, Yu Bai, Yiru Song, Chen Meng, Xi Jia, Yiqiang Li, Chengsheng Zhang, Zongchang Xu

PMC · DOI: 10.3390/ijms27041917 · International Journal of Molecular Sciences · 2026-02-17

## TL;DR

This study reveals how Apocynum venetum adapts to salt stress through two distinct phases involving gene and metabolite changes.

## Contribution

The paper identifies a two-phase salt tolerance mechanism in A. venetum using integrated transcriptomic and metabolomic analyses.

## Key findings

- Early salt stress activates hormone and MAPK signaling pathways and accumulates specific metabolites like ferulic acid.
- Late salt stress involves metabolic adaptation with increased flavonoids and enriched pathways like phenylpropanoid biosynthesis.
- Hub genes like AOC, CPK, and CYP90C1 coordinate early and late stress responses, including antioxidant and calcium signaling.

## Abstract

Soil salinization poses a major constraint to global agriculture. Apocynum venetum, a salt-tolerant halophyte, provides an effective model for investigating salt-adaptive strategies; however, the temporal dynamics of its tolerance-associated genes and metabolites remain unclear. In this study, integrated transcriptomics, metabolomics (UHPLC-MS), physiological assays, and weighted gene co-expression network analysis (WGCNA) were conducted to characterize early (7-day) and late (18-day) responses to 200 mM NaCl stress. NaCl stress significantly reduced chlorophyll content while increasing Na+ accumulation, MDA levels, antioxidant enzyme activities (SOD and CAT), and total flavonoid content. Early responses (NaCl7) were marked by accumulation of ferulic acid, rhamnetin, and 3,4-dihydrocoumarin, with activation of plant hormone (ABA, auxin, zeatin) and MAPK signaling pathways. Late responses (NaCl18) exhibited increased accumulation of scopoletin, formononetin, and caffeyl-alcohol, with enrichment of phenylpropanoid biosynthesis, glutathione metabolism, and photosynthesis-related pathways. WGCNA identified early-response hub genes, including AOC, MAPKKK17/18, CYP98A, and CCoAOMT, coordinating stress signaling and antioxidant metabolism. Late stress responses involved genes like CPK, GST, CYCD3, and ARF, modulating calcium signaling and ROS detoxification. Genes shared across phases included CYP90C1, HD-ZIP, HSP20, and PP2C, regulating protein stabilization and stress signaling. These findings reveal a two-phase salt tolerance strategy in A. venetum, integrating early signaling and late metabolic adaptation.

## Linked entities

- **Genes:** AOC (allene oxide cyclase) [NCBI Gene 544306], MAPKKK17 (mitogen-activated protein kinase kinase kinase 17) [NCBI Gene 817812], MAPKKK18 (mitogen-activated protein kinase kinase kinase 18) [NCBI Gene 839324], CCoAOMT (caffeoyl-CoA O-methyltransferase) [NCBI Gene 100134898], PIK3C2A (phosphatidylinositol-4-phosphate 3-kinase catalytic subunit type 2 alpha) [NCBI Gene 5286], SLCO6A1 (solute carrier organic anion transporter family member 6A1) [NCBI Gene 133482], cycD3 (cyclin D3.1) [NCBI Gene 543748], CDKN2A (cyclin dependent kinase inhibitor 2A) [NCBI Gene 1029], ROT3 (Cytochrome P450 superfamily protein) [NCBI Gene 829790], LOC107863056 (homeobox-leucine zipper protein ATHB-12-like) [NCBI Gene 107863056], HSPB6 (heat shock protein family B (small) member 6) [NCBI Gene 126393], PP2C (putative protein phosphatase) [NCBI Gene 5069542]
- **Chemicals:** NaCl (PubChem CID 5234), ferulic acid (PubChem CID 445858), rhamnetin (PubChem CID 5281691), 3,4-dihydrocoumarin (PubChem CID 660), scopoletin (PubChem CID 5280460), formononetin (PubChem CID 5280378), caffeyl-alcohol (PubChem CID 5282096)
- **Species:** Apocynum venetum (taxon 377125)

## Full-text entities

- **Genes:** CAT (catalase) [NCBI Gene 847], KRT18 (keratin 18) [NCBI Gene 3875] {aka CK-18, CYK18, K18}, RRM1 (ribonucleotide reductase catalytic subunit M1) [NCBI Gene 6240] {aka PEOB6, R1, RIR1, RR1}, SOD1 (superoxide dismutase 1) [NCBI Gene 6647] {aka ALS, ALS1, HEL-S-44, IPOA, SOD, STAHP}, SNAP91 (synaptosome associated protein 91) [NCBI Gene 9892] {aka AP180, CALM}, GALM (galactose mutarotase) [NCBI Gene 130589] {aka BLOCK25, GALAC4, GLAT, HEL-S-63p, IBD1}, PAM (peptidylglycine alpha-amidating monooxygenase) [NCBI Gene 5066] {aka PAL, PAM-1, PHM}, DHX16 (DEAH-box helicase 16) [NCBI Gene 8449] {aka DBP2, DDX16, NMOAS, PRO2014, PRP8, PRPF2}, CCND3 (cyclin D3) [NCBI Gene 896], P4HA1 (prolyl 4-hydroxylase subunit alpha 1) [NCBI Gene 5033] {aka P4HA}, SUPT4H1 (SPT4 homolog, DSIF elongation factor subunit) [NCBI Gene 6827] {aka SPT4, SPT4H, SUPT4H, Supt4a}, PIK3C2A (phosphatidylinositol-4-phosphate 3-kinase catalytic subunit type 2 alpha) [NCBI Gene 5286] {aka CPK, OCSKD, PI3-K-C2(ALPHA), PI3-K-C2A, PI3K-C2-alpha, PI3K-C2alpha}, PHGDH (phosphoglycerate dehydrogenase) [NCBI Gene 26227] {aka 3-PGDH, 3PGDH, HEL-S-113, NLS, NLS1, PDG}, CLPB (ClpB family mitochondrial disaggregase) [NCBI Gene 81570] {aka ANKCLB, ANKCLP, HSP78, MEGCANN, MGCA7, MGCA7A}, KRT7 (keratin 7) [NCBI Gene 3855] {aka CK7, K2C7, K7, SCL}, MCU (mitochondrial calcium uniporter) [NCBI Gene 90550] {aka C10orf42, CCDC109A, HsMCU}, HCAR3 (hydroxycarboxylic acid receptor 3) [NCBI Gene 8843] {aka GPR109B, HCA3, HM74, PUMAG, Puma-g}, G6PD (glucose-6-phosphate dehydrogenase) [NCBI Gene 2539] {aka CNSHA1, G6PD1}, HSP90AA1 (heat shock protein 90 alpha family class A member 1) [NCBI Gene 3320] {aka EL52, HEL-S-65p, HSP86, HSP89A, HSP90A, HSP90N}, ANXA13 (annexin A13) [NCBI Gene 312] {aka ANX13, ISA}, MGRN1 (mahogunin ring finger 1) [NCBI Gene 23295] {aka RNF156}, GSTK1 (glutathione S-transferase kappa 1) [NCBI Gene 373156] {aka GST, GST 13-13, GST13, GST13-13, GSTK1-1, hGSTK1}, CALM1 (calmodulin 1) [NCBI Gene 801] {aka CALML2, CAM2, CAM3, CAMB, CAMC, CAMI}, IDH1 (isocitrate dehydrogenase (NADP(+)) 1) [NCBI Gene 3417] {aka HEL-216, HEL-S-26, IDCD, IDH, IDP, IDPC}, PAOX (polyamine oxidase) [NCBI Gene 196743] {aka PAO}, GSS (glutathione synthetase) [NCBI Gene 2937] {aka CNSHA6, GSHS, HEL-S-64p, HEL-S-88n}, NFYA (nuclear transcription factor Y subunit alpha) [NCBI Gene 4800] {aka CBF-A, CBF-B, HAP2, NF-YA}, UBC (ubiquitin C) [NCBI Gene 7316] {aka HMG20}, HSPB6 (heat shock protein family B (small) member 6) [NCBI Gene 126393] {aka HEL55, Hsp20, PPP1R91}, GGCT (gamma-glutamylcyclotransferase) [NCBI Gene 79017] {aka C7orf24, CRF21, GCTG, GGC}, XYLT2 (xylosyltransferase 2) [NCBI Gene 64132] {aka PXYLT2, SOS, XT-II, XT2, xylT-II}, TCN1 (transcobalamin 1) [NCBI Gene 6947] {aka HC, TC-1, TC1, TCI}
- **Diseases:** ion toxicity (MESH:D064420), injury to (MESH:D014947)
- **Chemicals:** pantothenol (MESH:C007288), amino acid (MESH:D000596), MDA (MESH:D015104), nitrogen (MESH:D009584), EDTA (MESH:D004492), Cl- (MESH:D002713), Chlorophyll (MESH:D002734), TCA (MESH:D014238), rutin (MESH:D012431), arginine (MESH:D001120), MDA (MESH:D008315), carbohydrate (MESH:D002241), CK0 (-), H2O2 (MESH:D006861), NaCl (MESH:D012965), methanol (MESH:D000432), hypotaurine (MESH:C003949), pinoresinol (MESH:C103298), ABA (MESH:D000040), vermiculite (MESH:C003760), K+ (MESH:D011188), phosphate (MESH:D010710), Salt (MESH:D012492), rhamnetin (MESH:C063423), zeatin (MESH:D015026), Na+ (MESH:D012964), brassinosteroid (MESH:D060406), lysine (MESH:D008239), 3,4-dihydrocoumarin (MESH:C026308), 5-oxoproline (MESH:D011761), HClO4 (MESH:C576518), IAA (MESH:C030737), membrane lipid (MESH:D008563), caffeic acid (MESH:C040048), citrulline (MESH:D002956), L-Tryptophan (MESH:D014364), flavonoid (MESH:D005419), nitric oxide (MESH:D009569), HNO3 (MESH:D017942), indole (MESH:C030374), jasmonate (MESH:C011006), ethanol (MESH:D000431), calcium (MESH:D002118), Poly(A) (MESH:D011061), L-Cysteinyl glycine (MESH:C028505), ROS (MESH:D017382), auxin (MESH:D007210), scopoletin (MESH:D012603), polyphenol (MESH:D059808), water (MESH:D014867), lignin (MESH:D008031), polyamine (MESH:D011073), taurine (MESH:D013654), Glutathione (MESH:D005978), formononetin (MESH:C007768), ferulic acid (MESH:C004999), lipid (MESH:D008055), alkali (MESH:D000468), apigenin (MESH:D047310), (+) catechin (MESH:D002392)
- **Species:** Apocynum venetum (species) [taxon 377125], Homo sapiens (human, species) [taxon 9606]
- **Cell lines:** S2 — Drosophila melanogaster (Fruit fly), Spontaneously immortalized cell line (CVCL_Z232)

## Full text

_Full body text omitted from this summary view._ Fetch the complete paper as Markdown: https://tomesphere.com/paper/PMC12940728/full.md

## Figures

7 figures with captions in the complete paper: https://tomesphere.com/paper/PMC12940728/full.md

## References

99 references — full list in the complete paper: https://tomesphere.com/paper/PMC12940728/full.md

---
Source: https://tomesphere.com/paper/PMC12940728