# Integrated Multi-Omics Analysis Revealed the Synergistic Regulatory Mechanisms of Salt Tolerance in Soybean (Kefeng 1)

**Authors:** Yuan Yuan, Lihua Zhu, Biting Cao, Jiaqi You, Haijian Zhi, Kai Li, Weihong Gu, Hongjuan Yang, Chaohan Li

PMC · DOI: 10.3390/plants15040555 · 2026-02-10

## TL;DR

This study identifies key genes and mechanisms in soybean that help it tolerate salt stress, offering insights for breeding salt-tolerant crops.

## Contribution

The study reveals novel synergistic regulatory mechanisms and candidate genes for salt tolerance in soybean roots.

## Key findings

- Kefeng 1 maintains Na+/K+ ion homeostasis via CHX15 and CAX3 up-regulation and CNGC13 down-regulation.
- Salt tolerance in Kefeng 1 involves PIN3-mediated auxin homeostasis and enhanced antioxidant systems.
- Glyma.09G117900 (PIN3) and Glyma.19G244200 (AKR1) are identified as hub genes critical for salt tolerance.

## Abstract

Soil salinisation has become one of the major abiotic stresses limiting crop growth in the world. To enhance soybean productivity on saline lands, understanding its salt-stress response and underlying mechanisms is necessary. In this study, the salt-tolerant soybean Kefeng 1 and the salt-sensitive soybean Qihuang 1 were used to elucidate the synergistic regulatory networks underlying soybean salt tolerance. After 12 days of 150 mM NaCl treatment, both varieties were subjected to phenotypic evaluation, physiological measurements, and integrated transcriptomic and metabolomic analysis. The results showed that the salt tolerance in Kefeng 1 primarily originated from its root. Under salt stress, Kefeng 1 maintained Na+/K+ ion homeostasis by up-regulating Cation/H+ Exchanger 15 (CHX15) and Cation Exchanger 3 (CAX3), and down-regulating Cyclic Nucleotide-Gated Channel 13 (CNGC13). Furthermore, Kefeng 1 stabilised auxin (IAA) homeostasis by inhibiting IAA biosynthesis and regulating concentrations through PIN-FORMED 3 (PIN3)-mediated efflux. It also scavenged reactive oxygen species (ROS) by employing enhanced enzymatic antioxidant systems, specifically aldo-keto reductase 1 (AKR1), glutathione S-transferase (GST), and catalase (CAT), alongside non-enzymatic antioxidants like the isoflavone genistein. Gene–metabolite correlation network analysis identified Glyma.09G117900 (PIN3) and Glyma.19G244200 (AKR1) as two hub genes. These two genes were specifically up-regulated in Kefeng 1 root under NaCl stress, and the proteins they encoded played important roles in salt tolerance in Kefeng 1 root as described above. Accordingly, these two genes were identified as candidate genes for salt tolerance in Kefeng 1. This study offered a theoretical framework and genetic resources for developing salt-tolerant soybean cultivars.

## Linked entities

- **Genes:** CHX15 (cation/hydrogen exchanger 15) [NCBI Gene 815847], CAX3 (cation exchanger 3) [NCBI Gene 824349], CNGC13 (cyclic nucleotide-gated channel 13) [NCBI Gene 826427], PIN3 (Auxin efflux carrier family protein) [NCBI Gene 843432], AKR1 (palmitoyltransferase AKR1) [NCBI Gene 851857]
- **Chemicals:** NaCl (PubChem CID 5234), IAA (PubChem CID 802), genistein (PubChem CID 5280961)
- **Species:** Glycine max (taxon 3847)

## Full-text entities

- **Genes:** CDPK1 (calcium-dependent protein kinase 1) [NCBI Gene 838470] {aka ATCDPK1, AtCPK10, CALCIUM-DEPENDENT PROTEIN KINASE, CPK10, F6A14.1, F6A14_1}, Chalcone synthase [NCBI Gene 100170701], TT5 (Chalcone-flavanone isomerase family protein) [NCBI Gene 824678] {aka A11, AtCHI, CFI, CHALCONE FLAVANONE ISOMERASE, CHI, TRANSPARENT TESTA 5}, MPK1 (mitogen-activated protein kinase 1) [NCBI Gene 837559] {aka ATMPK1, F14N23.9, F14N23_9, MITOGEN-ACTIVATED PROTEIN KINASE, mitogen-activated protein kinase 1}, ARF [NCBI Gene 547532], YUC1 (Flavin-binding monooxygenase family protein) [NCBI Gene 829389] {aka L23H3.20, L23H3_20, YUC, YUCCA, YUCCA 1}, HKT1 (high-affinity K+ transporter 1) [NCBI Gene 826623] {aka ATHKT1, HKT1;1, T9A4.5, high-affinity K+ transporter 1}, CHI1A (chalcone--flavonone isomerase 1A) [NCBI Gene 547602] {aka CHI, CHI1}, SOS3 (Calcium-binding EF-hand family protein) [NCBI Gene 832494] {aka ATSOS3, CALCINEURIN B-LIKE PROTEIN 4, CBL4, MOP9.19, MOP9_19, SALT OVERLY SENSITIVE 3}, TT4 (Chalcone and stilbene synthase family protein) [NCBI Gene 831241] {aka ATCHS, CHALCONE SYNTHASE, CHALCONE/STILBENE SYNTHASE, CHS, MAC12.28, MAC12_28}, beta-glucosidase [NCBI Gene 547491], SKP1 (S phase kinase-associated protein 1) [NCBI Gene 843928] {aka ARABIDOPSIS SKP1 HOMOLOGUE 1, ASK1, ATSKP1, S phase kinase-associated protein 1, SKP1A, T4O12.17}, AKR1 [NCBI Gene 100301897], CNGC13 (cyclic nucleotide-gated channel 13) [NCBI Gene 826427] {aka ATCNGC13, CYCLIC NUCLEOTIDE-GATED CHANNEL 13, F3I3.1, F3I3_1, cyclic nucleotide-gated channel 13}, TSB2 (tryptophan synthase beta-subunit 2) [NCBI Gene 828815] {aka T24A18.20, T24A18_20, TRYPTOPHAN SYNTHASE BETA-SUBUNIT, tryptophan synthase beta-subunit 2}, CHX15 (cation/hydrogen exchanger 15) [NCBI Gene 815847] {aka ATCHX15, CATION/H+ EXCHANGER 15, T10F5.16, T10F5_16, cation/hydrogen exchanger 15}, CAX3 (cation exchanger 3) [NCBI Gene 824349] {aka ATCAX3, ATHCX1, CALCIUM/PROTON EXCHANGER CAX1-LIKE PROTEIN, CAX1-LIKE, cation exchanger 3}, 4CL3 (4-coumarate:CoA ligase 3) [NCBI Gene 842814] {aka 4-COUMARATE:COA LIGASE, 4-coumarate:CoA ligase 3, F16G16.6, F16G16_6}, TIR1 (F-box/RNI-like superfamily protein) [NCBI Gene 825473] {aka AtTIR1, TRANSPORT INHIBITOR RESPONSE 1}, peroxidase [NCBI Gene 547504], GH3 [NCBI Gene 100811309], SOS1 (sodium proton exchanger, putative (NHX7) (SOS1)) [NCBI Gene 814729] {aka ARABIDOPSIS NA+/H+ ANTIPORTER 7, ARABIDOPSIS SALT OVERLY SENSITIVE 1, ATNHX7, ATSOS1, F14H20.5, F14H20_5}, GST [NCBI Gene 547580], CUL1 (cullin 1) [NCBI Gene 825648] {aka ATCUL1, AUXIN RESISTANT 6, AXR6, T10P11.26, T10P11_26, cullin 1}, MATE (aluminum-activated citrate transporter) [NCBI Gene 100170750], TAA1 (uncharacterized protein) [NCBI Gene 843393] {aka CKRC1, F24J13.13, F24J13_13, SAV3, SHADE AVOIDANCE 3, WEAK ETHYLENE INSENSITIVE 8}, SOS2 (Protein kinase superfamily protein) [NCBI Gene 833502] {aka ATSOS2, CBL-INTERACTING PROTEIN KINASE 24, CIPK24, K21B8.3, K21B8_3, SALT OVERLY SENSITIVE 2}, CAT [NCBI Gene 100037447]
- **Diseases:** SOS (MESH:D013651), injury to (MESH:D014947), cytotoxicity (MESH:D064420), DAMs (MESH:D012734), Ion homeostasis disorder (MESH:D009358), metabolic disorders (MESH:D008659)
- **Chemicals:** betaine (MESH:D001622), zeatin (MESH:D015026), aminoacyl-tRNA (MESH:D012346), polytetrafluoroethylene (MESH:D011138), SA (MESH:D020156), Na+ (MESH:D012964), flavone (MESH:C043562), K+ (MESH:D011188), Salt (MESH:D012492), sugars (MESH:D000073893), NaCl (MESH:D012965), malonylgenistin (MESH:C521200), methanol (MESH:D000432), (S) (MESH:D013455), proline (MESH:D011392), (+)-abscisic acid (MESH:D000040), cutin (MESH:C000521), Ca2+ (-), metal (MESH:D008670), H2O2 (MESH:D006861), daidzein (MESH:C004742), glycitein (MESH:C086566), naringenin chalcone (MESH:C027329), oil (MESH:D009821), homoglutathione (MESH:C402172), serine (MESH:D012694), wax (MESH:D014885), ketones (MESH:D007659), acetonitrile (MESH:C032159), Amino-acid (MESH:D000596), Isoflavone (MESH:D007529), nitrogen (MESH:D009584), glycosphingolipid (MESH:D006028), NADPH (MESH:D009249), ethylene (MESH:C036216), naringenin (MESH:C005273), alpha-tocopherol (MESH:D024502), nucleosides (MESH:D009705), genistein (MESH:D019833), TRIzol (MESH:C411644), nitrogen compounds (MESH:D017672), isoliquiritigenin (MESH:C040920), OH (MESH:C031356), lipid (MESH:D008055), suberin (MESH:C065875), CK (MESH:D003583), GSH (MESH:D005978), phloridzin (MESH:D010695), carotenoids (MESH:D002338), water (MESH:D014867), benzene (MESH:D001554), aldehydes (MESH:D000447), glycosides (MESH:D006027), ROS (MESH:D017382), Auxin (MESH:D007210), diterpenoid (MESH:D004224), flavonoid (MESH:D005419), indole (MESH:C030374), HNO3 (MESH:D017942), polyketides (MESH:D061065)
- **Species:** Arabidopsis thaliana (mouse-ear cress, species) [taxon 3702], Glycine max (soybean, species) [taxon 3847], Homo sapiens (human, species) [taxon 9606], Populus euphratica (Euphrates poplar, species) [taxon 75702]
- **Cell lines:** Kefeng 1 — Mus musculus (Mouse), Hybridoma (CVCL_C7RB)

## Figures

8 figures with captions in the complete paper: https://tomesphere.com/paper/PMC12944372/full.md

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Source: https://tomesphere.com/paper/PMC12944372