. 2023 Feb 11;24(4):3638.

doi: 10.3390/ijms24043638.

Transcriptome and Metabolome Analysis Reveals Salt-Tolerance Pathways in the Leaves and Roots of ZM-4 (Malus zumi) in the Early Stages of Salt Stress

Dajiang Wang^{1

2}, Kun Wang², Simiao Sun², Peng Yan³, Xiang Lu^{1

2}, Zhao Liu^{1

2}, Qingshan Li^{1

2}, Lianwen Li², Yuan Gao², Jihong Liu^{1

4}

Affiliations

¹ Xinjiang Production and Construction Corps Key Laboratory of Special Fruits and Vegetables Cultivation Physiology and Germplasm Resources Utilization, Agricultural College, Shihezi University, Shihezi 832003, China.
² National Repository of Apple Germplasm Resources, Research Institute of Pomology, Chinese Academy of Agricultural Sciences (CAAS), Key Laboratory of Horticulture Crops Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs of the People's Republic of China, Xingcheng 125100, China.
³ Institute of Horticulture Crops, Xinjiang Academy of Agricultural Sciences, No. 403 Nanchang Road, Urumqi 830091, China.
⁴ Key Laboratory of Horticultural Plant Biology (MOE), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, China.

PMID: 36835052
PMCID: PMC9960305
DOI: 10.3390/ijms24043638

Transcriptome and Metabolome Analysis Reveals Salt-Tolerance Pathways in the Leaves and Roots of ZM-4 (Malus zumi) in the Early Stages of Salt Stress

Dajiang Wang et al. Int J Mol Sci. 2023.

. 2023 Feb 11;24(4):3638.

doi: 10.3390/ijms24043638.

Authors

Dajiang Wang^{1

2}, Kun Wang², Simiao Sun², Peng Yan³, Xiang Lu^{1

2}, Zhao Liu^{1

2}, Qingshan Li^{1

2}, Lianwen Li², Yuan Gao², Jihong Liu^{1

4}

Affiliations

¹ Xinjiang Production and Construction Corps Key Laboratory of Special Fruits and Vegetables Cultivation Physiology and Germplasm Resources Utilization, Agricultural College, Shihezi University, Shihezi 832003, China.
² National Repository of Apple Germplasm Resources, Research Institute of Pomology, Chinese Academy of Agricultural Sciences (CAAS), Key Laboratory of Horticulture Crops Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs of the People's Republic of China, Xingcheng 125100, China.
³ Institute of Horticulture Crops, Xinjiang Academy of Agricultural Sciences, No. 403 Nanchang Road, Urumqi 830091, China.
⁴ Key Laboratory of Horticultural Plant Biology (MOE), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, China.

PMID: 36835052
PMCID: PMC9960305
DOI: 10.3390/ijms24043638

Abstract

The breeding of salt-tolerant rootstock relies heavily on the availability of salt-tolerant Malus germplasm resources. The first step in developing salt-tolerant resources is to learn their molecular and metabolic underpinnings. Hydroponic seedlings of both ZM-4 (salt-tolerant resource) and M9T337 (salt-sensitive rootstock) were treated with a solution of 75 mM salinity. ZM-4's fresh weight increased, then decreased, and then increased again after being treated with NaCl, whereas M9T337's fresh weight continued to decrease. The results of transcriptome and metabolome after 0 h (CK) and 24 h of NaCl treatment showed that the leaves of ZM-4 had a higher content of flavonoids (phloretinm, naringenin-7-O-glucoside, kaempferol-3-O-galactoside, epiafzelechin, etc.) and the genes (CHI, CYP, FLS, LAR, and ANR) related to the flavonoid synthesis pathway showed up-regulation, suggesting a high antioxidant capacity. In addition to the high polyphenol content (L-phenylalanine, 5-O-p-coumaroyl quinic acid) and the high related gene expression (4CLL9 and SAT), the roots of ZM-4 exhibited a high osmotic adjustment ability. Under normal growing conditions, the roots of ZM-4 contained a higher content of some amino acids (L-proline, tran-4-hydroxy-L-prolin, L-glutamine, etc.) and sugars (D-fructose 6-phosphate, D-glucose 6-phosphate, etc.), and the genes (GLT1, BAM7, INV1, etc.) related to these two pathways were highly expressed. Furthermore, some amino acids (S-(methyl) glutathione, N-methyl-trans-4-hydroxy-L-proline, etc.) and sugars (D-sucrose, maltotriose, etc.) increased and genes (ALD1, BCAT1, AMY1.1, etc.) related to the pathways showed up-regulation under salt stress. This research provided theoretical support for the application of breeding salt-tolerant rootstocks by elucidating the molecular and metabolic mechanisms of salt tolerance during the early stages of salt treatment for ZM-4.

Keywords: Malus; integrated analysis; molecular mechanism; salt tolerance.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

**Figure 1**
Fresh weight of ZM-4 and M9T337 and differential-expression genes (DEGs) in different combinations under salt stress. (a) Fresh weight of ZM-4 and M9T337 after NaCl treatment. (b) The number of DEGs in different combinations.

**Figure 2**
The top 20 GO terms for DEGs in three combinations. (a) The top 20 GO terms for DEGs in M-CKL vs. M-TL. (b) The top 20 GO terms for DEGs in Z-CKL vs. Z-TL. (c) The top 20 GO terms for DEGs in M-TL vs. Z-TL. (d) The top 20 GO terms for DEGs in M-CKR vs. M-TR. (e) The top 20 GO terms for DEGs in Z-CKR vs. Z-TR. (f) The top 20 GO terms for DEGs in M-TR vs. Z-TR.

**Figure 3**
The top 20 KEGG pathways for DEGs in three combinations. (a) The top 20 KEGG pathways for DEGs in M-CKL vs. M-TL. (b) The top 20 KEGG pathways for DEGs in Z-CKL vs. Z-TL. (c) The top 20 KEGG pathways for DEGs in M-TL vs. Z-TL. (d) The top 20 KEGG pathways for DEGs in M-CKR vs. M-TR. (e) The top 20 KEGG pathways for DEGs in Z-CKR vs. Z-TR. (f) The top 20 KEGG pathways for DEGs in M-TR vs. Z-TR.

**Figure 4**
Venn diagrams of DEGs in leaves and roots among different combinations. (a) The Venn diagram of DEGs in leaves among different combinations. (b) The Venn diagram of DEGs in roots among different combinations.

**Figure 5**
PCA of metabolites in leaves and roots in ZM-4 and M9T337 under salt stress. (a) PCA of metabolites in leaves in ZM-4 and M9T337 under salt stress. (b) PCA of metabolites in roots in ZM-4 and M9T337 under salt stress.

**Figure 6**
The number of DAMs in leaves and roots of different combinations. (a) The number of DAMs in leaves of different combinations. (b) The number of DAMs in roots of different combinations.

**Figure 7**
The top 15 DAMs based on the values of VIP in different combinations. (a) The top 15 DAMs based on the values of VIP in leaves of M-CKL vs. M-TL. (b) The top 15 DAMs based on the values of VIP in leaves of Z-CKL vs. Z-TL. (c) The top 15 DAMs based on the values of VIP in leaves of M-TL vs. Z-TL. (d) The top 15 DAMs based on the values of VIP in roots of M-CKR vs. M-TR. (e) The top 15 DAMs based on the values of VIP in roots of Z-CKR vs. Z-TR. (f) The top 15 DAMs based on the values of VIP in roots of M-TR vs. Z-TR.

**Figure 8**
Venn diagrams of DAMs in leaves and roots among different combinations. (a) The Venn diagram of DAMs in leaves among different combinations. (b) The Venn diagram of DAMs in roots among different combinations.

**Figure 9**
The top 25 joint-loading elements of genes and metabolites in different combinations. (a) The top 25 joint-loading elements of genes and metabolites of leaves in M-CKL vs. M-TL. (b) The top 25 joint-loading elements of genes and metabolites of leaves in Z-CKL vs. Z-TL. (c) The top 25 joint-loading elements of genes and metabolites of leaves in M-TL vs. Z-TL. (d) The top 25 joint-loading elements of genes and metabolites of roots in M-CKR vs. M-TR. (e) The top 25 joint-loading elements of genes and metabolites of roots in Z-CKR vs. Z-TR. (f) The top 25 joint-loading elements of genes and metabolites of roots in M-TR vs. Z-TR.

**Figure 10**
The main salt-tolerance genes and metabolites in phenylpropanoid biosynthesis pathway (PAL, phenylalanine ammonia-lyase; C4′H, cinnamate-4′-hydroxylase; CYP, cytochrome P450; PGT, phydroxybenzoate geranyltransferases; CHS, chalcone synthase; CHI, chalcone isomerase; F3′H, flavonoid-3′-hydroxylase; F3H, flavonoid-3-hydroxylase; LDOX, leucoanthocyanidin dioxygenase; FLS, flavonol synthase; F3′5′H, flavonoid-3′,5′-hydroxylase; LAR, leucoanthocyantin reductase; ANR, anthocyanidin synthase).

**Figure 11**
The possible paths of salt stress tolerance in the roots of ZM-4. (Ellipsis indicates the presence of other substances or genes that are not listed).

See this image and copyright information in PMC

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Transcriptome and Metabolome Analysis Reveals Salt-Tolerance Pathways in the Leaves and Roots of ZM-4 (Malus zumi) in the Early Stages of Salt Stress

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Transcriptome and Metabolome Analysis Reveals Salt-Tolerance Pathways in the Leaves and Roots of ZM-4 (Malus zumi) in the Early Stages of Salt Stress

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Abstract

Conflict of interest statement

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