RNA-Seq and Comparative Transcriptomic Analyses of Asian Soybean Rust Resistant and Susceptible Soybean Genotypes Provide Insights into Identifying Disease Resistance Genes
Abstract
:1. Introduction
2. Results
2.1. The Phenotypic Response of Soybean Accessions to P. pachyrhizi
2.2. Analysis of RNA-Seq Data
2.3. Validation of Selected Differentially Expressed Genes (DEGs) Using qRT-PCR
2.4. Comparative Analysis of Tianlong1 and SX6907 Transcriptomes
2.5. Gene Ontology (GO)-Based Analysis of the DEGs
2.6. KEGG Pathway Analysis of the DEGs
2.7. Identification of Transcription Factors
2.8. Co-Expression Network Analysis of Soybean Resistance to P. pachyrhizi
3. Discussion
3.1. Ca2+ Signaling Pathway
3.2. MAPK Signaling Pathway
3.3. NLR Genes
3.4. Flavonoid Biosynthesis and Disease Resistance
4. Materials and Methods
4.1. Plant Genotypes, Inoculations, and Experimental Conditions
4.2. Observation by Laser Confocal Microscopy
4.3. RNA Extraction
4.4. Library Preparation and Illumina Hiseq Sequencing
4.5. Reads Quality Control and Mapping
4.6. Differential Expression Analysis and Functional Enrichment
4.7. WGCNA Construct
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Group | Sample Name | Clean Reads (M) | Clean Bases (G) | Mapped Reads (%) | Uniquely Mapped (%) | No. of Mapped Genes |
---|---|---|---|---|---|---|
1 | R-0 hpi (Rep 1) | 39.0659 | 5.8599 | 93.15 | 89.68 | 39,658 |
R-0 hpi (Rep 2) | 40.9507 | 6.1426 | 92.38 | 90.30 | 39,736 | |
R-0 hpi (Rep 3) | 39.2121 | 5.8818 | 92.11 | 89.14 | 38,620 | |
2 | R-6 hpi (Rep 1) | 40.6590 | 5.9497 | 90.14 | 87.11 | 37,646 |
R-6 hpi (Rep 2) | 37.8276 | 5.6741 | 70.75 | 69.25 | 37,054 | |
R-6 hpi (Rep 3) | 39.6647 | 6.0988 | 91.19 | 88.99 | 37,396 | |
3 | R-24 hpi (Rep 1) | 38.8942 | 5.7379 | 92.74 | 90.35 | 38,848 |
R-24 hpi (Rep 2) | 40.3832 | 6.0575 | 92.91 | 90.82 | 38,635 | |
R-24 hpi (Rep 3) | 38.2529 | 5.8341 | 78.34 | 76.65 | 38,307 | |
4 | R-10 dpi (Rep 1) | 41.4718 | 5.7205 | 80.99 | 79.11 | 38,309 |
R-10 dpi (Rep 2) | 40.0860 | 6.0129 | 82.90 | 80.90 | 37,731 | |
R-10 dpi (Rep 3) | 40.0860 | 6.2208 | 92.61 | 90.39 | 38,463 | |
5 | S-0 hpi (Rep 1) | 45.1133 | 6.7670 | 91.74 | 88.53 | 37,033 |
S-0 hpi (Rep 2) | 43.1935 | 6.4790 | 91.68 | 89.38 | 38,407 | |
S-0 hpi (Rep 3) | 41.1932 | 6.1790 | 91.16 | 87.72 | 35,172 | |
6 | S-6 hpi (Rep 1) | 42.2855 | 6.2377 | 91.19 | 88.56 | 37,847 |
S-6 hpi (Rep 2) | 43.3958 | 6.5094 | 91.02 | 88.53 | 40,092 | |
S-6 hpi (Rep 3) | 41.5849 | 6.3428 | 90.30 | 88.08 | 38,527 | |
7 | S-24 hpi (Rep 1) | 47.2346 | 6.6490 | 92.85 | 90.16 | 39,249 |
S-24 hpi (Rep 2) | 37.8453 | 5.6768 | 92.56 | 89.60 | 31,962 | |
S-24 hpi (Rep 3) | 44.3266 | 7.0852 | 91.56 | 89.30 | 38,696 | |
8 | S-10 dpi (Rep 1) | 38.9951 | 6.4775 | 86.10 | 83.94 | 37,657 |
S-10 dpi (Rep 2) | 39.0004 | 5.8501 | 73.21 | 56.29 | 35,421 | |
S-10 dpi (Rep 3) | 43.1835 | 5.8493 | 80.69 | 78.55 | 40,234 |
Gene ID | Description | Point-in-Time | |
---|---|---|---|
Glyma.18G087400, Glyma.03G087800, Glyma.03G047000, Glyma.03G054100, Glyma.14G205000, Glyma.18G082800, Glyma.14G199400, Glyma.18G088500, Glyma.07G063600, Glyma.09G208900, Glyma.07G063700, Glyma.01G046900, Glyma.06G259400, Glyma.16G214800, Glyma.16G215000 | LRR and NB-ARC domain-containing disease-resistant proteins | 6 hpi; 24 hpi; 10 dpi | upregulated |
Glyma.17G214600; Glyma.17G214700 | Rust resistance kinase Lr10 isoform | 6 hpi; 24 hpi; 10 dpi | upregulated |
Glyma.16G214000, Glyma.16G210600, Glyma.03G047700, Glyma.13G190000, Glyma.16G214500, Glyma.13G187900, Glyma.15G233200, Glyma.18G280300, Glyma.06G259800, Glyma.18G281500, Glyma.18G086400, Glyma.13G190400, Glyma.16G085400, Glyma.18G086900, Glyma.18G086600, Glyma.03G088000, Glyma.03G088100 | LRR and NB-ARC domain-containing disease-resistant proteins | 6 hpi; 24 hpi; 10 dpi | downregulated |
Glyma.12G233000, Glyma.18G198800, Glyma.18G268000, Glyma.16G185100, Glyma.09G107600, Glyma.13G188800, Glyma.06G226700 | LRR receptor protein kinase | 6 hpi; 24 hpi; 10 dpi | downregulated |
Glyma.13G033500, Glyma.13G033400 | Rust resistance kinase lr10-related protein | 6 hpi; 24 hpi; 10 dpi | downregulated |
Glyma.05G127400, Glyma.04G220200 | Programmed cell death protein | 6 hpi; 24 hpi; 10 dpi | downregulated |
Glyma.16G211500, Glyma.15G187300 | TMV resistance protein N isoform | 6 hpi; 24 hpi; 10 dpi | downregulated |
GO Term (Biological Process) | Cluster Frequency | p-Value |
---|---|---|
0 hpi | ||
defense response | 58 out of 392 genes, 14.8% | 2.96 × 10−21 |
response to stress | 72 out of 392 genes, 18.4% | 2.18 ×10−7 |
response to stimulus | 100 out of 392 genes, 25.5% | 1.2 ×10−3 |
6 hpi | ||
defense response | 106 out of 1202 genes, 8.8% | 8.55 × 10−21 |
photosynthesis, light harvesting in photosystem I | 17 out of 1202 genes, 1.4% | 3.97 × 10−12 |
photosynthesis, light harvesting | 19 out of 1202 genes, 1.6% | 3.80 × 10−10 |
protein-chromophore linkage | 19 out of 1202 genes, 1.6% | 6.04 × 10−9 |
secondary metabolic process | 55 out of 1202 genes, 4.6% | 1.85 × 10−7 |
response to stress | 163 out of 1202 genes, 13.6% | 1.41 × 10−6 |
photosynthesis, light reaction | 20 out of 1202 genes, 1.7% | 7.40 × 10−6 |
response to stimulus | 270 out of 1202 genes, 22.5% | 1.05 × 10−5 |
flavonoid metabolic process | 34 out of 1202 genes, 2.8% | 4.57 × 10−5 |
flavonoid biosynthetic process | 33 out of 1202 genes, 2.7% | 1.12 × 10−3 |
24 hpi | ||
defense response | 47 out of 320 genes, 14.7% | 7.71 × 10−17 |
response to stress | 66 out of 320 genes, 20.6% | 6.07 × 10−9 |
response to stimulus | 86 out of 320 genes, 26.9% | 5.62 × 10−3 |
10 dpi | ||
defense response | 172 out of 2179 genes, 7.9% | 7.67 × 10−30 |
secondary metabolic process | 108 out of 2179 genes, 5.0% | 1.40 × 10−19 |
multi-organism process | 66 out of 2179 genes, 3.0% | 2.21 × 10−12 |
protein phosphorylation | 307 out of 2179 genes, 14.1% | 4.79 × 10−12 |
secondary metabolite biosynthetic process | 75 out of 2179 genes, 3.4% | 5.15 × 10−12 |
oxidation-reduction process | 374 out of 2179 genes, 17.2% | 4.85 × 10−11 |
cell recognition | 42 out of 2179 genes, 1.9% | 3.47 × 10−10 |
pollen–pistil interaction | 42 out of 2179 genes, 1.9% | 3.47 × 10−10 |
recognition of pollen | 42 out of 2179 genes, 1.9% | 3.47 × 10−10 |
response to biotic stimulus | 42 out of 2179 genes, 1.9% | 1.10 × 10−9 |
Pathways | 6 hpi | 24 hpi | 10 dpi |
---|---|---|---|
Plant–pathogen interaction | 115 | 45 | 78 |
Plant hormone signal transduction | 53 | 10 | 21 |
Flavonoid biosynthesis | 29 | 5 | 14 |
Phenylpropanoid biosynthesis | 47 | 11 | 21 |
Galactose metabolism | 11 | 4 | 8 |
Photosynthesis-antenna proteins | 19 | 0 | 2 |
Ubiquitin-mediated proteolysis | 15 | 3 | 7 |
ABC transporters | 23 | 2 | 7 |
Brassinosteroid biosynthesis | 1 | 1 | 2 |
Proteasome | 2 | 0 | 2 |
Phenylalanine metabolism | 9 | 1 | 21 |
Protein processing in endoplasmic reticulum | 48 | 12 | 17 |
Flavone and flavonol biosynthesis | 7 | 1 | 5 |
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Hao, Q.; Yang, H.; Chen, S.; Qu, Y.; Zhang, C.; Chen, L.; Cao, D.; Yuan, S.; Guo, W.; Yang, Z.; et al. RNA-Seq and Comparative Transcriptomic Analyses of Asian Soybean Rust Resistant and Susceptible Soybean Genotypes Provide Insights into Identifying Disease Resistance Genes. Int. J. Mol. Sci. 2023, 24, 13450. https://doi.org/10.3390/ijms241713450
Hao Q, Yang H, Chen S, Qu Y, Zhang C, Chen L, Cao D, Yuan S, Guo W, Yang Z, et al. RNA-Seq and Comparative Transcriptomic Analyses of Asian Soybean Rust Resistant and Susceptible Soybean Genotypes Provide Insights into Identifying Disease Resistance Genes. International Journal of Molecular Sciences. 2023; 24(17):13450. https://doi.org/10.3390/ijms241713450
Chicago/Turabian StyleHao, Qingnan, Hongli Yang, Shuilian Chen, Yanhui Qu, Chanjuan Zhang, Limiao Chen, Dong Cao, Songli Yuan, Wei Guo, Zhonglu Yang, and et al. 2023. "RNA-Seq and Comparative Transcriptomic Analyses of Asian Soybean Rust Resistant and Susceptible Soybean Genotypes Provide Insights into Identifying Disease Resistance Genes" International Journal of Molecular Sciences 24, no. 17: 13450. https://doi.org/10.3390/ijms241713450