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Cited by 17Plant Stress Responses and ToleranceWheat and Barley Genetics and PathologyGenetic Mapping and Diversity in Plants and Animals

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Integrated GWAS and transcriptomic analysis reveal the candidate salt-responding genes regulating Na(+)/K(+) balance in barley (Hordeum vulgare L.)

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Xu, Tingting, Meng, Shan, Zhu, Xiaopin, Di, Jiachun, Zhu, Yin, Yang, Xin, Yan, Wei·2023·Frontiers in Plant Science
DOI 10.3389/fpls.2022.1004477PMC PMC9910287
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Abstract

Salt stress is one of the main abiotic stresses affecting crop yield and quality. Barley has strong salt tolerance, however, the underlying genetic basis is not fully clear, especially in the seedling stage. This study examined the ionic changes in barley core germplasms under the control and salt conditions. Genome-wide association study (GWAS) analysis revealed 54 significant SNPs from a pool of 25,342 SNPs distributed in 7 chromosomes (Chr) of the Illumina Barley 50K SNP array. These SNPs are associated with ion homeostasis traits, sodium (Na+) and potassium (K+) content, and Na+/K+ ratio representing five genomic regions on Chr 2, 4, 5, 6, and 7 in the leaves of worldwide barley accessions. And there are 3 SNP peaks located on the Chr 4, 6, and 7, which could be the “hot spots” regions for mining and identifying candidate genes for salt tolerance. Furthermore, 616 unique candidate genes were screened surrounding the significant SNPs, which are associated with transport proteins, protein kinases, binding proteins, and other proteins of unknown function. Meanwhile, transcriptomic analysis (RNA-Seq) was carried out to compare the salt-tolerant (CM72) and salt-sensitive (Gairdner) genotypes subjected to salt stress. And there was a greater accumulation of differentially expressed genes(DEGs) in Gairdner compared to CM72, mainly enriched in metabolic pathway, biosynthesis of secondary metabolites, photosynthesis, signal transduction,emphasizing the different transcriptional response in both genotypes following salt exposure. Combined GWAS and RNA-Seq analysis revealed 5 promising salt-responding genes (PGK2, BASS3, SINAT2, AQP, and SYT3) from the hot spot regions, which were verified between the salt-tolerant and salt-sensitive varieties by qRT-PCR. In all, these results provide candidate SNPs and genes responsible for salinity responding in barley, and a new idea for studying such genetic basis in similar crops.

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Figure 1 Phenotypic analysis of barley accessions under control (CK: 0 mM) and salt treatment (300 mM NaCl) conditions after 3 weeks. Seedlings growth performance of (A) salt-tolerant and (B) salt-sensitive varieties of barley. Bars, 10 cm. (C) Raincloud plots for Na+ content, K+ content, and Na+/K+ ratio traits under contrasting growth conditions. **p < 0.01 (D) Frequency distribution of Na+, K+content, and Na+/K+ ratio under contrasting growth conditions and relative value of Na+, K+, Na+/K+ ratio. CK: 0 mM NaCl, Salt: 300 mM NaCl.
Figure 1 Phenotypic analysis of barley accessions under control (CK: 0 mM) and salt treatment (300 mM NaCl) conditions after 3 weeks. Seedlings growth performance of (A) salt-tolerant and (B) salt-sensitive varieties of barley. Bars, 10 cm. (C) Raincloud plots for Na+ content, K+ content, and Na+/K+ ratio traits under contrasting growth conditions. **p < 0.01 (D) Frequency distribution of Na+, K+content, and Na+/K+ ratio under contrasting growth conditions and relative value of Na+, K+, Na+/K+ ratio. CK: 0 mM NaCl, Salt: 300 mM NaCl.CC BY · PubMed Central
Figure 2 Population structure analysis of barley accessions. (A) Genome-wide SNP density in the entire association mapping panel. (B) Geographical distribution of barley accessions. (C) Population structure analysis revealed that barley accessions belong to four subgroups (K = 4). (D) Principal component analysis showing the four subpopulations. (E) A neighboring joining tree shows the four different subpopulations. (F) Genome-wide average LD decay distance in the barley genome.
Figure 2 Population structure analysis of barley accessions. (A) Genome-wide SNP density in the entire association mapping panel. (B) Geographical distribution of barley accessions. (C) Population structure analysis revealed that barley accessions belong to four subgroups (K = 4). (D) Principal component analysis showing the four subpopulations. (E) A neighboring joining tree shows the four different subpopulations. (F) Genome-wide average LD decay distance in the barley genome.CC BY · PubMed Central
Figure 3 GWAS analysis for the ion-related traits under different conditions. (A) Manhattan plot for CK-Na+, CK-K+, and CK-Na+/K+, respectively. (B) Manhattan plot for Salt-Na+, Salt-K+, and Salt-Na+/K+, respectively. (C) Manhattan plot for R-Na+, R-K+, and R-Na+/K+, respectively.
Figure 3 GWAS analysis for the ion-related traits under different conditions. (A) Manhattan plot for CK-Na+, CK-K+, and CK-Na+/K+, respectively. (B) Manhattan plot for Salt-Na+, Salt-K+, and Salt-Na+/K+, respectively. (C) Manhattan plot for R-Na+, R-K+, and R-Na+/K+, respectively.CC BY · PubMed Central
Figure 4 Analysis of the SNP peak and the candidate genes on chromosome 4. (A) Manhattan plots for Chr 4. The black line represents the significance threshold (P < 10-4.40) and a red line indicates the position of the strong SNP peak. (B) LD based on pairwise r 2 values between the SNPs estimated on Chr 4. The black inverted triangles indicate 8 significantly associated SNPs that were repeatedly detected. The green five-pointed star indicates the strongest SNP with the highest threshold. (C) Haplotypes were found among the barley accessions using the 8 SNPs. (D) Phenotypic differences of Salt-Na+, Salt-Na+/K+, R-Na+, and R-Na+/K+ between the two haplotypes.
Figure 4 Analysis of the SNP peak and the candidate genes on chromosome 4. (A) Manhattan plots for Chr 4. The black line represents the significance threshold (P < 10-4.40) and a red line indicates the position of the strong SNP peak. (B) LD based on pairwise r 2 values between the SNPs estimated on Chr 4. The black inverted triangles indicate 8 significantly associated SNPs that were repeatedly detected. The green five-pointed star indicates the strongest SNP with the highest threshold. (C) Haplotypes were found among the barley accessions using the 8 SNPs. (D) Phenotypic differences of Salt-Na+, Salt-Na+/K+, R-Na+, and R-Na+/K+ between the two haplotypes.CC BY · PubMed Central
Figure 5 Analysis of the SNP peak on chromosome 6. (A) Manhattan plots for Chr 6. The black line represents the significance threshold (P < 10-4.40) and a red line indicates the position of the strongest SNP peak. (B) LD based on pairwise r 2 values between the SNPs estimated on Chr 6. The black inverted triangles show 10 significantly associated SNPs. The green five-pointed star indicates the strongest SNP with the highest threshold. (C) Haplotypes were observed in the barley accessions using the 10 SNPs. (D) Phenotypic differences of R-Na+ between the two haplotypes.
Figure 5 Analysis of the SNP peak on chromosome 6. (A) Manhattan plots for Chr 6. The black line represents the significance threshold (P < 10-4.40) and a red line indicates the position of the strongest SNP peak. (B) LD based on pairwise r 2 values between the SNPs estimated on Chr 6. The black inverted triangles show 10 significantly associated SNPs. The green five-pointed star indicates the strongest SNP with the highest threshold. (C) Haplotypes were observed in the barley accessions using the 10 SNPs. (D) Phenotypic differences of R-Na+ between the two haplotypes.CC BY · PubMed Central
Figure 6 Analysis of the SNP peak on chromosome 7. (A) Manhattan plots for Chr 7. The black line represents the significance threshold (P < 10-4.40) and a red line indicates the position of the strongest SNP peak. (B) LD based on pairwise r 2 values between the SNPs estimated on Chr 7. The black inverted triangles show 8 significantly associated SNPs that were detected repeatedly. The green five-pointed star indicates the strongest SNP with the highest threshold. (C) Haplotypes were observed in the barley accessions using the 8 SNPs. (D) Phenotypic differences of Salt-Na+ and Salt-Na+/K+ between the two haplotypes.
Figure 6 Analysis of the SNP peak on chromosome 7. (A) Manhattan plots for Chr 7. The black line represents the significance threshold (P < 10-4.40) and a red line indicates the position of the strongest SNP peak. (B) LD based on pairwise r 2 values between the SNPs estimated on Chr 7. The black inverted triangles show 8 significantly associated SNPs that were detected repeatedly. The green five-pointed star indicates the strongest SNP with the highest threshold. (C) Haplotypes were observed in the barley accessions using the 8 SNPs. (D) Phenotypic differences of Salt-Na+ and Salt-Na+/K+ between the two haplotypes.CC BY · PubMed Central
Figure 7 Transcriptome analysis in CM72 and Gairdner under salt conditions. (A) Venn diagram showing the number of transcripts detected as up and down-regulated (P < 0.01) in CM72 and Gairdner under salt conditions. (B) Heat maps showing differentially expressed transcripts in CM72 under control and salt conditions. (C) Heat maps showing differentially expressed transcripts in Gairdner under control and salt conditions. (D) The Gene Ontology (GO) enrichment analysis in CM72 under salt conditions. (E) The Gene Ontology (GO) enrichment analysis in Gairdner under salt conditions. (F) The top 20 significantly KEGG enrichment pathways in CM72 under salt conditions. (G) The top 20 significantly KEGG enrichment pathways in Gairdner under salt conditions.
Figure 7 Transcriptome analysis in CM72 and Gairdner under salt conditions. (A) Venn diagram showing the number of transcripts detected as up and down-regulated (P < 0.01) in CM72 and Gairdner under salt conditions. (B) Heat maps showing differentially expressed transcripts in CM72 under control and salt conditions. (C) Heat maps showing differentially expressed transcripts in Gairdner under control and salt conditions. (D) The Gene Ontology (GO) enrichment analysis in CM72 under salt conditions. (E) The Gene Ontology (GO) enrichment analysis in Gairdner under salt conditions. (F) The top 20 significantly KEGG enrichment pathways in CM72 under salt conditions. (G) The top 20 significantly KEGG enrichment pathways in Gairdner under salt conditions.CC BY · PubMed Central
Figure 8 Expression pattern of candidate genes in the peak regions of Chr4, Chr6 and Chr7. (A) Heat map showing the expression levels of 59 candidate genes in Chr4 among two barley cultivars. (B) Heat map showing the expression levels of 59 candidate genes in Chr6 among two barley cultivars. (C) Heat map showing the expression levels of 17 candidate genes in Chr6 among two barley cultivars. The barley leaf samples were collected at 0, 3, 12, and 48 h under salt stress.
Figure 8 Expression pattern of candidate genes in the peak regions of Chr4, Chr6 and Chr7. (A) Heat map showing the expression levels of 59 candidate genes in Chr4 among two barley cultivars. (B) Heat map showing the expression levels of 59 candidate genes in Chr6 among two barley cultivars. (C) Heat map showing the expression levels of 17 candidate genes in Chr6 among two barley cultivars. The barley leaf samples were collected at 0, 3, 12, and 48 h under salt stress.CC BY · PubMed Central
Figure 9 Expression pattern validation of five selected genes (HORVU4Hr1G088190 (PGK2), HORVU6Hr1G016070 (BASS3), HORVU6Hr1G016120 (SINAT2), HORVU6Hr1G064140 (AQP), and HORVU7Hr1G101310 (SYT3)), which were also detected by RNA-Seq, in CM72 and Gairdner leaves by qRT-PCR. The samples were collected at 0, 3, 12, and 48 h under salt stress.
Figure 9 Expression pattern validation of five selected genes (HORVU4Hr1G088190 (PGK2), HORVU6Hr1G016070 (BASS3), HORVU6Hr1G016120 (SINAT2), HORVU6Hr1G064140 (AQP), and HORVU7Hr1G101310 (SYT3)), which were also detected by RNA-Seq, in CM72 and Gairdner leaves by qRT-PCR. The samples were collected at 0, 3, 12, and 48 h under salt stress.CC BY · PubMed Central
Figure 10 Relative expression of 5 candidate genes by RT-PCR in six salt-sensitive and six salt-tolerant varieties. HORVU4Hr1G088190 (PGK2). HORVU6Hr1G016070 (BASS3). HORVU6Hr1G016120 (SINAT2). HORVU6Hr1G064140 (AQP). HORVU7Hr1G101310 (SYT3). Six salt-sensitive varieties, S1, Shan 3; S2, AKHELOL 1; S3, Boyer; S4, Rainbow; S5, Birka; S6, Gairdner; six salt-tolerant varieties; T1, PALLIDUM 043; T2, KIMALUNG; T3, Zhu Damai 5; T4, GURZAN; T5, Kunlun 14; T6, CM72.
Figure 10 Relative expression of 5 candidate genes by RT-PCR in six salt-sensitive and six salt-tolerant varieties. HORVU4Hr1G088190 (PGK2). HORVU6Hr1G016070 (BASS3). HORVU6Hr1G016120 (SINAT2). HORVU6Hr1G064140 (AQP). HORVU7Hr1G101310 (SYT3). Six salt-sensitive varieties, S1, Shan 3; S2, AKHELOL 1; S3, Boyer; S4, Rainbow; S5, Birka; S6, Gairdner; six salt-tolerant varieties; T1, PALLIDUM 043; T2, KIMALUNG; T3, Zhu Damai 5; T4, GURZAN; T5, Kunlun 14; T6, CM72.CC BY · PubMed Central

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Metadata

Authors
Xu, T., Meng, S., Zhu, X., Di, J., Zhu, Y., Yang, X., & Yan, W.
Affiliations
Jiangsu Academy of Agricultural Sciences (CN)
Corresponding author
Yan, Wei
ORCID
Venue
Frontiers in Plant Science
Publisher
Frontiers Media SA
Published
2023-01-20
Volume
13
Pages
1004477-1004477
ISSN
1664-462X (ISSN-L)
DOI
10.3389/fpls.2022.1004477
PMC
PMC9910287
OpenAlex
W4317538198
Cited by
17
References
1
Citations by year
2026: 6 · 2025: 6 · 2024: 3 · 2023: 2
FWCI
2.68
Type
journal article
Language
en
Update notices
corrigendum (2023-11-29)
Open access
Licence
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Jiangsu Agricultural Science and Technology Innovation Fund
  • National Natural Science Foundation of China
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Wheat and Barley Genetics and Pathology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
Keywords
barley, salt stress, salt tolerance, Na+/K+ balance, ion homeostasis, candidate genes, seedling stage, differentially expressed genes, transcriptome, aquaporins

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CoChat. (2026). Citation check: Integrated GWAS and transcriptomic analysis reveal the candidate salt-responding genes regulating Na(+)/K(+) balance in barley (Hordeum vulgare L.). https://app.cochat.ai/papers/10.3389/fpls.2022.1004477
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Xu, T., Meng, S., Zhu, X., Di, J., Zhu, Y., Yang, X., & Yan, W. (2023). Integrated GWAS and transcriptomic analysis reveal the candidate salt-responding genes regulating Na(+)/K(+) balance in barley (Hordeum vulgare L.). Frontiers in Plant Science. https://doi.org/10.3389/fpls.2022.1004477