Comparative Transcriptome Analysis of High- and Low-Growth Genotypes of Eucalyptus urophylla in Response to Long-Term Nitrogen Deficiency
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Nutrient Treatments
2.2. Determination of Growth Characteristics
2.3. RNA Isolation, Sequencing, and Assembly
2.4. Normalization of Gene Expression Levels and Identification of DEGs
2.4.1. Functional Annotation and GO and KEGG Classification
2.4.2. Validation of the Expression Level
3. Results
3.1. Effect of Different Nutrient Treatments on Tree Growth Characteristics
3.2. An RNA Sequencing Approach for the Assembly, Quantification, Identification, and Clustering of DEGs in Response to Nutrient Treatments
3.3. Functional Enrichment of the DEGs of Different Genotypes in Response to Nutrient Treatments
3.4. DEGs Involved in Plant Hormone Signal Transduction
3.5. Transcription Factors (TFs) Responding to Nutrient Deficiency
3.6. Validation of RNA Sequencing Results via Quantitative Real-Time Polymerase Chain Reaction (qRT-PCR)
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Sample | ID | No. of Raw Reads (107) | No. of Clean Reads (107) | No. of Clean Basepairs (106) | No. of Mapped Reads (107) | Uniquely Mapped (107) | Mapped Percentage (%) |
---|---|---|---|---|---|---|---|
ZQUA44 | T1_1 | 9.49 | 9.18 | 13.55 | 5.13 | 5.00 | 54.48 |
ZQUA44 | T1_2 | 9.06 | 8.78 | 13.11 | 4.77 | 4.63 | 52.76 |
ZQUA44 | T1_3 | 9.73 | 9.49 | 14.24 | 4.09 | 3.94 | 41.53 |
ZQUA44 | T2_1 | 9.60 | 9.28 | 13.67 | 4.91 | 4.79 | 51.58 |
ZQUA44 | T2_2 | 9.35 | 9.08 | 13.57 | 3.79 | 3.62 | 39.82 |
ZQUA44 | T2_3 | 10.47 | 10.11 | 15.17 | 5.46 | 5.32 | 52.66 |
ZQUA44 | CK_1 | 10.28 | 9.89 | 14.85 | 5.72 | 5.57 | 56.27 |
ZQUA44 | CK_2 | 9.18 | 8.84 | 13.07 | 4.51 | 4.33 | 48.91 |
ZQUA44 | CK_3 | 8.81 | 8.58 | 12.82 | 3.63 | 3.50 | 40.75 |
ZQUB15 | T1_1 | 9.83 | 9.51 | 14.05 | 4.09 | 3.93 | 41.35 |
ZQUB15 | T1_2 | 9.70 | 9.34 | 13.95 | 4.70 | 4.56 | 48.81 |
ZQUB15 | T1_3 | 8.42 | 8.15 | 12.21 | 3.37 | 3.26 | 40.01 |
ZQUB15 | T2_1 | 9.58 | 9.22 | 13.59 | 4.99 | 4.87 | 52.75 |
ZQUB15 | T2_2 | 8.76 | 8.52 | 12.73 | 3.36 | 3.24 | 37.98 |
ZQUB15 | T2_3 | 10.58 | 10.30 | 15.37 | 4.30 | 4.15 | 40.34 |
ZQUB15 | CK_1 | 8.47 | 8.22 | 12.27 | 3.21 | 3.07 | 37.37 |
ZQUB15 | CK_2 | 8.97 | 8.68 | 12.96 | 4.29 | 4.19 | 48.24 |
ZQUB15 | CK_3 | 11.11 | 10.72 | 16.04 | 5.11 | 4.99 | 46.64 |
Groups of DEGs | GO Term | Description | Number of Enriched DEGs | p-Value | FDR |
---|---|---|---|---|---|
G1 | GO:0016701 | oxidoreductase activity, acting on single donors with incorporation of molecular oxygen | 5 | 4.00 × 10−6 | 0.001 |
G1 | GO:0003824 | catalytic activity | 80 | 0.0003 | 0.039 |
G1 | GO:0016757 | transferase activity, transferring glycosyl groups | 11 | 0.00045 | 0.039 |
G1 | GO:0016563 | transcription activator activity | 6 | 0.00074 | 0.048 |
G2 | GO:0016491 | oxidoreductase activity | 7 | 1.90 × 10−5 | 0.0001 |
G2 | GO:0003824 | catalytic activity | 13 | 0.0015 | 0.0042 |
G3 | GO:0003824 | catalytic activity | 66 | 7.00 × 10−12 | 1.20 × 10−9 |
G3 | GO:0016787 | hydrolase activity | 27 | 1.10 × 10−5 | 0.00094 |
G3 | GO:0016491 | oxidoreductase activity | 16 | 1.80 × 10−5 | 0.0011 |
G3 | GO:0004091 | carboxylesterase activity | 8 | 3.40 × 10−5 | 0.0015 |
AT | GO:0003824 | catalytic activity | 96 | 8.50 × 10−8 | 2.40 × 10−5 |
AT | GO:0016491 | oxidoreductase activity | 25 | 4.90 × 10−6 | 0.00069 |
AT | GO:0005215 | transporter activity | 22 | 0.00014 | 0.013 |
AT | GO:0046527 | glucosyltransferase activity | 6 | 0.00024 | 0.017 |
AT | GO:0022892 | substrate- transporter activity | 17 | 0.00035 | 0.018 |
AT | GO:0016706 | oxidoreductase activity, acting on paired donors, with incorporation or reduction of molecular oxygen, 2-oxoglutarate as one donor, and incorporation of one atom each of oxygen into both donors | 5 | 0.00037 | 0.018 |
AT | GO:0022857 | transmembrane transporter activity | 17 | 0.0007 | 0.028 |
AT | GO:0016705 | oxidoreductase activity, acting on paired donors, with incorporation or reduction of molecular oxygen | 6 | 0.0016 | 0.047 |
AT | GO:0022891 | substrate- transmembrane transporter activity | 14 | 0.0017 | 0.047 |
AT | GO:0016758 | transferase activity, transferring hexosyl groups | 8 | 0.0014 | 0.047 |
BT | GO:0003824 | catalytic activity | 84 | 2.00 × 10−8 | 4.00 × 10−6 |
BT | GO:0016491 | oxidoreductase activity | 22 | 5.90 × 10−6 | 0.0006 |
BT | GO:0008194 | UDP-glycosyltransferase activity | 8 | 2.10 × 10−5 | 0.0014 |
BT | GO:0016758 | transferase activity, transferring hexosyl groups | 9 | 7.20 × 10−5 | 0.0037 |
BT | GO:0016757 | transferase activity, transferring glycosyl groups | 10 | 0.00052 | 0.021 |
BT | GO:0046527 | glucosyltransferase activity | 5 | 0.00074 | 0.025 |
BT | GO:0016209 | antioxidant activity | 5 | 0.0011 | 0.033 |
BT | GO:0016765 | transferase activity, transferring alkyl or aryl (other than methyl) groups | 5 | 0.0014 | 0.036 |
Groups | KEGG Pathway | ID | DEGs Number | p-Value | Q-Value |
---|---|---|---|---|---|
G1 | Ascorbate and aldarate metabolism | ath00053 | 4 | 0.0002 | 0.0085 |
G1 | Arginine and proline metabolism | ath00330 | 3 | 0.0024 | 0.0547 |
G1 | Tyrosine metabolism | ath00350 | 2 | 0.0164 | 0.2424 |
G1 | Galactose metabolism | ath00052 | 2 | 0.0260 | 0.2424 |
G1 | Alanine, aspartate and glutamate metabolism | ath00250 | 2 | 0.0298 | 0.2424 |
G1 | Limonene and pinene degradation | ath00903 | 1 | 0.0346 | 0.2424 |
G1 | Monoterpenoid biosynthesis | ath00902 | 1 | 0.0377 | 0.2424 |
G1 | Metabolic pathways | ath01100 | 17 | 0.0439 | 0.2471 |
G2 | Phenylpropanoid biosynthesis | ath00940 | 2 | 0.0040 | 0.0202 |
G2 | Sulfur metabolism | ath00920 | 1 | 0.0249 | 0.0623 |
G3 | Phenylalanine, tyrosine and tryptophan biosynthesis | ath00400 | 2 | 0.0111 | 0.1867 |
G3 | Stilbenoid, diarylheptanoid and gingerol biosynthesis | ath00945 | 1 | 0.0243 | 0.1867 |
G3 | Metabolic pathways | ath01100 | 12 | 0.02515 | 0.1867 |
G3 | Glutathione metabolism | ath00480 | 2 | 0.0325 | 0.1867 |
AS | Galactose metabolism | ath00052 | 3 | 0.0030 | 0.0938 |
AS | Plant hormone signal transduction | ath04075 | 6 | 0.0063 | 0.0938 |
AS | Protein processing in endoplasmic reticulum | ath04141 | 5 | 0.0072 | 0.0938 |
AS | Metabolic pathways | ath01100 | 21 | 0.0112 | 0.1088 |
AS | Nitrogen metabolism | ath00910 | 2 | 0.0288 | 0.1991 |
AS | Cysteine and methionine metabolism | ath00270 | 3 | 0.0306 | 0.1991 |
AS | Glycerolipid metabolism | ath00561 | 2 | 0.0414 | 0.2308 |
BS | Cutin, suberine and wax biosynthesis | ath00073 | 2 | 0.0076 | 0.1249 |
BS | Zeatin biosynthesis | ath00908 | 2 | 0.0109 | 0.1249 |
Gene ID | AT1 (FPKM) | AT2 (FPKM) | ACK (FPKM) | BT1 (FPKM) | BT2 (FPKM) | BCK (FPKM) | Uniprot | Symbol | Subcluster |
---|---|---|---|---|---|---|---|---|---|
Eucgr.A01486 | 0.64 | 0.87 | 6.35 | 4.08 | 2.92 | 4.94 | Q5SN75 | P2C08 | sub4 |
Eucgr.A02858 | 0.24 | 0.30 | 9.65 | 10.76 | 1.75 | 3.41 | Q9FLI3 | P2C75 | sub4 |
Eucgr.C03732 | 21.00 | 24.44 | 76.28 | 46.38 | 23.80 | 40.61 | P49597 | P2C56 | sub1 |
Eucgr.F00253 | 0.55 | 0.51 | 0.00 | 0.70 | 0.00 | 0.00 | Q9FX08 | P2C12 | sub6 |
Eucgr.H04087 | 16.26 | 226.00 | 35.9 | 19.74 | 15.81 | 14.61 | Q3EAF9 | P2C49 | sub1 |
Eucgr.J02003 | 8.73 | 181.00 | 83.02 | 56.76 | 26.57 | 60.24 | Q9ZW21 | P2C24 | sub4 |
Eucgr.C03337 | 1222.61 | 1033.70 | 638.04 | 37.29 | 57.41 | 105.58 | Q9ZRA4 | AB19A | sub3 |
Eucgr.C03536 | 1079.85 | 930.58 | 667.89 | 227.95 | 439.95 | 6177.00 | Q9ZRA4 | AB19A | sub3 |
Eucgr.D00606 | 58.97 | 124.94 | 334.92 | 267.52 | 238.79 | 182.00 | Q05349 | 12KD | sub4 |
Eucgr.I01276 | 3.24 | 3.83 | 1.87 | 7.70 | 10.80 | 26.74 | Q6NMM0 | SAU61 | sub4 |
Eucgr.F03208 | 38.00 | 1.29 | 0.67 | 2.78 | 0.74 | 0.95 | Q9SQ80 | G2OX1 | sub6 |
Eucgr.F04125 | 22.90 | 32.45 | 8.65 | 10.03 | 4.30 | 3.94 | P46687 | GASA3 | sub3 |
Eucgr.K02472 | 20.46 | 20.90 | 18.74 | 117.00 | 41.92 | 58.02 | Q6NMQ7 | GASA6 | sub5 |
Eucgr.F00192 | 13.57 | 17.63 | 27.34 | 38.65 | 23.74 | 14.97 | Q8LC30 | RAP21 | sub1 |
Eucgr.F02317 | 1.08 | 0.47 | 1.55 | 58.00 | 1.66 | 0.87 | O22174 | ERF08 | sub1 |
Eucgr.F02691 | 0.04 | 0.36 | 23.00 | 34.00 | 0.00 | 0.19 | Q70II3 | EF110 | sub1 |
Eucgr.H01659 | 0.02 | 0.05 | 0.53 | 1.38 | 0.00 | 0.00 | Q9SZ06 | EF109 | sub1 |
Eucgr.K00128 | 19.27 | 9.67 | 16.3 | 75.95 | 18.5 | 13.04 | Q9LY05 | EF106 | sub1 |
Eucgr.F04203 | 0.13 | 0.20 | 8.69 | 4.30 | 0.27 | 0.15 | Q9FGF8 | ABR1 | sub4 |
Eucgr.G01970 | 0.15 | 0.37 | 3.51 | 6.09 | 1.74 | 0.32 | Q9LYU3 | EF113 | sub4 |
Eucgr.H03965 | 5.20 | 12.24 | 20.35 | 18.47 | 21.78 | 6.23 | P42736 | RAP23 | sub4 |
Eucgr.C04221 | 30.5 | 24.82 | 14.00 | 22.97 | 11.44 | 29.80 | Q9XI33 | WIN1 | sub6 |
Eucgr.F02319 | 7.73 | 5.56 | 7.53 | 12.26 | 6.01 | 2.54 | Q8LC30 | RAP21 | sub6 |
Eucgr.I00422 | 12.92 | 11.51 | 3.99 | 14.41 | 20.31 | 13.61 | O65665 | ERF60 | sub6 |
Eucgr.K00126 | 69.17 | 62.26 | 47.43 | 89.37 | 59.17 | 42.78 | Q8VY90 | EF105 | sub6 |
Eucgr.A01146 | 18.41 | 11.39 | 6.04 | 13.68 | 12.62 | 5.29 | Q8L8B8 | LOG3 | sub6 |
Eucgr.B02321 | 5.67 | 7.47 | 35.5 | 11.99 | 13.25 | 6.79 | O81077 | ABAH2 | sub1 |
Eucgr.C01524 | 7.03 | 4.49 | 2.78 | 23.39 | 14.27 | 12.84 | Q9SKK0 | EBF1 | sub1 |
Eucgr.C03157 | 33.47 | 38.36 | 13.15 | 25.79 | 30.28 | 12.39 | Q9FUJ1 | CKX7 | sub6 |
Eucgr.E01149 | 13.82 | 13.43 | 23.66 | 19.39 | 9.18 | 6.47 | Q949P1 | ABAH1 | sub1 |
Eucgr.G01437 | 0.04 | 0.29 | 1.74 | 6.04 | 1.81 | 1.43 | Q9LJK2 | ABAH4 | sub1 |
Eucgr.G03093 | 3.61 | 1.72 | 1.54 | 3.81 | 0.47 | 0.53 | Q8S8E3 | PYL6 | sub6 |
Eucgr.I01127 | 15.24 | 21.06 | 9.75 | 27.58 | 26.97 | 8.78 | Q8W3P8 | AOG | sub1 |
Eucgr.I01201 | 0.14 | 0.61 | 0.11 | 0.42 | 3.41 | 3.39 | Q6RYA0 | SABP2 | sub4 |
Eucgr.J00169 | 6.76 | 4.55 | 2.08 | 5.09 | 1.23 | 0.54 | O80920 | PYL4 | sub6 |
Eucgr.K02472 | 20.46 | 20.9 | 18.74 | 11.17 | 41.92 | 58.02 | Q6NMQ7 | GASA6 | sub5 |
Eucgr.B03374 | 1.38 | 2.09 | 4.49 | 1.70 | 1.41 | 0.96 | Q9ZWS9 | ARR3 | sub1 |
Eucgr.B02620 | 11.64 | 26.09 | 57.13 | 113.34 | 90.20 | 95.91 | Q39182 | DEF02 | sub2 |
Eucgr.H05052 | 223.79 | 163.36 | 302.39 | 893.65 | 3003.64 | 3268.99 | Q07502 | DEF | sub4 |
Transcription Factors | G1 | G2 | G3 | AS | BS |
---|---|---|---|---|---|
C2H2 | 1 | 1 | |||
CPP | 1 | ||||
ERF | 7 | 1 | 2 | ||
MYB | 4 | 3 | 1 | 2 | |
NAC | 6 | 1 | 1 | ||
RAV | 1 | ||||
WRKY | 2 | 5 | |||
B3 | 3 | ||||
bHLH | 3 | 1 | 1 | ||
bZIP | 2 | ||||
C3H | 3 | 2 | |||
Dof | 2 | ||||
G2-like | 3 | ||||
HD-ZIP | 1 | 1 | |||
HSF | 1 | 1 | 2 | ||
MYB_related | 1 | 3 | 2 | ||
NF-YA | 1 | ||||
TCP | 1 | ||||
MIKC_MADS | 1 | ||||
LBD | 1 | ||||
SBP | 1 |
Groups of DEGs | Gene ID | Gene Names | T1 | T2 | CK | log2FPKM (T1/CK) | p Value | log2FPKM (T2/CK) | p Value |
---|---|---|---|---|---|---|---|---|---|
AT | Eucgr.H00996 | WRKY23 | 1.57 | 4.82 | 8.19 | −2.38 | 0.00 | −0.76 | 0.18 |
AT | Eucgr.B03520 | WRKY75 | 6.93 | 9.67 | 24.10 | −1.80 | 0.00 | −1.32 | 0.03 |
BT | Eucgr.B04010 | WRKY26 | 15.39 | 8.77 | 4.79 | 1.68 | 0.00 | 0.87 | 0.07 |
BT | Eucgr.K02940 | WRKY33 | 8.01 | 5.62 | 2.84 | 1.50 | 0.00 | 0.99 | 0.06 |
BT | Eucgr.C00675 | WRKY50 | 26.21 | 17.53 | 7.47 | 1.81 | 0.00 | 1.23 | 0.02 |
BT | Eucgr.E04011 | WRKY6 | 4.21 | 2.48 | 1.07 | 1.98 | 0.00 | 1.22 | 0.08 |
BT | Eucgr.I01633 | WRKY75 | 1.72 | 4.70 | 0.54 | 1.66 | 0.16 | 3.11 | 0.01 |
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Yang, X.; Xu, F.; Pan, W.; Zhang, W.; Liao, H.; Zhu, B.; Xu, B.; Chen, X.; Yang, H. Comparative Transcriptome Analysis of High- and Low-Growth Genotypes of Eucalyptus urophylla in Response to Long-Term Nitrogen Deficiency. Genes 2024, 15, 60. https://doi.org/10.3390/genes15010060
Yang X, Xu F, Pan W, Zhang W, Liao H, Zhu B, Xu B, Chen X, Yang H. Comparative Transcriptome Analysis of High- and Low-Growth Genotypes of Eucalyptus urophylla in Response to Long-Term Nitrogen Deficiency. Genes. 2024; 15(1):60. https://doi.org/10.3390/genes15010060
Chicago/Turabian StyleYang, Xiaohui, Fang Xu, Wen Pan, Weihua Zhang, Huanqin Liao, Baozhu Zhu, Bin Xu, Xinyu Chen, and Huixiao Yang. 2024. "Comparative Transcriptome Analysis of High- and Low-Growth Genotypes of Eucalyptus urophylla in Response to Long-Term Nitrogen Deficiency" Genes 15, no. 1: 60. https://doi.org/10.3390/genes15010060
APA StyleYang, X., Xu, F., Pan, W., Zhang, W., Liao, H., Zhu, B., Xu, B., Chen, X., & Yang, H. (2024). Comparative Transcriptome Analysis of High- and Low-Growth Genotypes of Eucalyptus urophylla in Response to Long-Term Nitrogen Deficiency. Genes, 15(1), 60. https://doi.org/10.3390/genes15010060