Integrated Transcriptomic and Metabolomic Analysis Reveal the Underlying Mechanism of Anthocyanin Biosynthesis in Toona sinensis Leaves
Abstract
:1. Introduction
2. Results
2.1. Morphological Observation and Anthocyanin Content of Leaves in Toona sinensis
2.2. Metabolome Analysis of Anthocyanin in Five Toona Clones
2.3. Transcriptome Analysis of Five Toona sinensis Clones
2.4. Analysis of Anthocyanidin Biosynthetic Pathway Genes and Anthocyanin Derivates in JFC, BSH, and LFC
2.5. Correlation Analysis of Differentially Expressed Transcripts and Anthocyanin Compounds to Identify Key TFs and Plant Hormones Genes
2.6. Expression Profiles of TFs and Plant Hormone Genes Related to Anthocyanin Biosynthesis
2.7. Expression Analysis of Genes through qRT-PCR
3. Discussion
4. Materials and Methods
4.1. Plant Materials
4.2. Sample Preparation and Extraction
4.3. UPLC Conditions
4.4. ESI-MS/MS Conditions
4.5. Identification of Differentially Accumulated Metabolites
4.6. RNA Sequencing
4.7. Transcript Profiles and Annotation
4.8. Correlation Analysis of Transcriptome and Metabolome
4.9. Verification of RNA-Seq Data by qRT-PCR
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Gene ID | Log2FC_gene (JFC: LFC) | Gene Name | AGI | Gene Annotation | Compounds | Log2FC_meta (JFC: LFC) | Coefficient | p Value |
---|---|---|---|---|---|---|---|---|
Maker00012886 | 1.5011 | ERF4 | At5g44210 | AP2 domain | Cyanidin-3-O-galactoside | 7.9568 | 0.8479 | 6.52 × 10−5 |
Cyanidin-3-O-sambubioside | 5.4217 | 0.8049 | 0.0002953 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.8034 | 0.000309044 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8327 | 0.000116859 | |||||
Delphinidin-3-O-glucoside | 9.025 | 0.8197 | 0.00018361 | |||||
Maker00009687 | 2.2469 | CLE1 | At2g22850 | bZIP transcription factor | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.8066 | 0.000279669 |
Cyanidin-3-O-galactoside | 7.9568 | 0.8819 | 1.37 × 10−5 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.8696 | 2.54 × 10−5 | |||||
Maker00020104 | 2.8632 | bZIP46_1 | At1g68640 | bZIP transcription factor | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.8042 | 0.000301857 |
Cyanidin-3-O-rutinoside | 7.2774 | 0.8418 | 8.30 × 10−5 | |||||
Cyanidin-3-O-galactoside | 7.9568 | 0.8692 | 2.59 × 10−5 | |||||
Cyanidin-3-O-sambubioside | 5.4217 | 0.8169 | 0.000201339 | |||||
Cyanidin-3-O-glucoside | 5.7951 | 0.8047 | 0.000296932 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.8256 | 0.000149917 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8462 | 6.98 × 10−5 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8548 | 4.91 × 10−5 | |||||
Maker00026824 | 4.2921 | bZIP43 | At2g22850 | bZIP transcription factor | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.844 | 7.62 × 10−5 |
Cyanidin-3-O-rutinoside | 7.2774 | 0.8201 | 0.00018127 | |||||
Cyanidin-3-O-galactoside | 7.9568 | 0.8575 | 4.39 × 10−5 | |||||
Cyanidin-3-O-sambubioside | 5.4217 | 0.8221 | 0.000169159 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8355 | 0.000105219 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8607 | 3.81 × 10−5 | |||||
Maker00032838 | 1.3156 | bZIP46_2 | At1g68640 | bZIP transcription factor | Cyanidin-3-O-galactoside | 7.9568 | 0.8368 | 0.00010049 |
Cyanidin-3-O-arabinoside | 9.025 | 0.8284 | 0.000136002 | |||||
novel.8684 | 2.8522 | POLX | At3g45520 | bZIP transcription factor | Pelargonidin-3-O-(6-O-p-coumaroyl)-glucoside | 4.1336 | 0.8159 | 0.000208096 |
Maker00014746 | 2.4849 | CPC | At2g46410 | Myb-like DNA-binding domain | Cyanidin-3-O-(6-O-malonyl-beta-D-glucoside) | 9.025 | 0.801 | 0.000332643 |
Cyanidin-3-O-rutinoside | 7.2774 | 0.8151 | 0.000213466 | |||||
Cyanidin-3-O-galactoside | 7.9568 | 0.8915 | 8.09 × 10−6 | |||||
Cyanidin-3-O-sambubioside | 5.4217 | 0.811 | 0.000243476 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.9149 | 1.78 × 10−6 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8358 | 0.000104028 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8778 | 1.69 × 10−5 | |||||
Delphinidin-3-O-glucoside | 9.025 | 0.8114 | 0.000240963 | |||||
Delphinidin-3-O-5-O-(6-O-coumaroyl)-diglucoside | 1.0838 | 0.8249 | 0.000153878 | |||||
Maker00016969 | 1.3602 | MYB30 | At4g09460 | Myb-like DNA-binding domain | Cyanidin-3-O-galactoside | 7.9568 | 0.8189 | 0.000188654 |
Maker00023867 | 1.6363 | MYB17 | At3g61250 | Myb-like DNA-binding domain | Cyanidin-3-O-galactoside | 7.9568 | 0.8493 | 6.17 × 10−5 |
Cyanidin-3-O-arabinoside | 9.025 | 0.8159 | 0.000207999 | |||||
Maker00029632 | 4.4878 | SOC1 | At2g45660 | MADS-box transcription factor | Cyanidin-3-O-galactoside | 7.9568 | 0.9012 | 4.53 × 10−6 |
Cyanidin-3-O-arabinoside | 9.025 | 0.9525 | 4.40 × 10−8 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8064 | 0.000281454 | |||||
Delphinidin-3-O-5-O-(6-O-coumaroyl)-diglucoside | 1.0838 | 0.8166 | 0.000203571 | |||||
novel.3727 | 4.9012 | AGL9 | At1g24260 | MADS-box transcription factor | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.8712 | 2.35 × 10−5 |
Cyanidin-3-O-(6-O-malonyl-beta-D-glucoside) | 9.025 | 0.8 | 0.000341781 | |||||
Cyanidin-3-O-rutinoside | 7.2774 | 0.8165 | 0.000204 | |||||
Cyanidin-3-O-galactoside | 7.9568 | 0.9652 | 5.96 × 10−9 | |||||
Cyanidin-3-O-sambubioside | 5.4217 | 0.8078 | 0.000269708 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.9734 | 1.07 × 10−9 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8416 | 8.35 × 10−5 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8968 | 5.93 × 10−6 | |||||
Delphinidin-3-O-glucoside | 9.025 | 0.8552 | 4.83 × 10−5 | |||||
Delphinidin-3-O-5-O-(6-O-coumaroyl)-diglucoside | 1.0838 | 0.8735 | 2.10 × 10−5 | |||||
Petunidin-3-O-rutinoside | 9.025 | 0.8018 | 0.000324031 | |||||
Maker00006536 | 1.8404 | WRKY48 | At5g49520 | WRKY DNA-binding protein 48 | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.832 | 0.000119819 |
Cyanidin-3-O-galactoside | 7.9568 | 0.8644 | 3.22 × 10−5 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.8435 | 7.77 × 10−5 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8093 | 0.000257445 | |||||
novel.6183 | 3.5074 | MIK2 | At4g08850 | Leucine-rich repeat receptor-like protein kinase | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.8304 | 0.000126884 |
Cyanidin-3-O-galactoside | 7.9568 | 0.9136 | 1.95 × 10−6 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.9219 | 1.03 × 10−6 | |||||
Delphinidin-3-O-5-O-(6-O-coumaroyl)-diglucoside | 1.0838 | 0.8338 | 0.000112199 | |||||
Maker00021798 | 1.1527 | bHLH162 | At4g20970 | Helix-loop-helix DNA-binding domain | Cyanidin-3-O-galactoside | 7.9568 | 0.8684 | 2.68 × 10−5 |
Cyanidin-3-O-arabinoside | 9.025 | 0.8782 | 1.66 × 10−5 | |||||
Maker00003242 | 2.1058 | JAG | At1g13400 | C2H2 and C2HC zinc fingers superfamily protein | Cyanidin-3-O-galactoside | 7.9568 | 0.8668 | 2.90 × 10−5 |
Cyanidin-3-O-arabinoside | 9.025 | 0.8657 | 3.04 × 10−5 | |||||
Maker00011793 | 1.1426 | GRAS20 | At3g54220 | GRAS domain family | Cyanidin-3-O-(6-O-malonyl-beta-D-glucoside) | 9.025 | 0.8327 | 0.000116807 |
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8072 | 0.000275174 | |||||
novel.4188 | 1.6057 | HSP72 | At1g56410 | heat shock protein 70 family protein | Cyanidin-3-O-(6-O-malonyl-beta-D-glucoside) | 9.025 | 0.8302 | 0.000127565 |
Cyanidin-3-O-galactoside | 7.9568 | 0.9167 | 1.55 × 10−6 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.9144 | 1.84 × 10−6 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.807 | 0.00027619 | |||||
Delphinidin-3-O-glucoside | 9.025 | 0.8147 | 0.000216435 | |||||
novel.4220 | 4.8378 | LBD21 | At3g11090 | Lateral organ boundaries domain | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.8909 | 8.38 × 10−6 |
Cyanidin-3-O-rutinoside | 7.2774 | 0.8734 | 2.11 × 10−5 | |||||
Cyanidin-3-O-galactoside | 7.9568 | 0.8584 | 4.21 × 10−5 | |||||
Cyanidin-3-O-sambubioside | 5.4217 | 0.8307 | 0.00012547 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.8884 | 9.68 × 10−6 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8797 | 1.54 × 10−5 | |||||
Cyanidin-3-O-xyloside | 5.2648 | 0.8999 | 4.89 × 10−6 | |||||
Delphinidin-3-O-5-O-(6-O-coumaroyl)-diglucoside | 1.0838 | 0.9109 | 2.36 × 10−6 | |||||
Petunidin-3-O-rutinoside | 9.025 | 0.8911 | 8.31 × 10−6 | |||||
Maker00033233 | 1.0573 | STY46 | At4g35780 | Protein tyrosine kinase | Cyanidin-3-O-(6-O-malonyl-beta-D-glucoside) | 9.025 | 0.8235 | 0.000161377 |
Cyanidin-3-O-galactoside | 7.9568 | 0.8026 | 0.00031603 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.8017 | 0.000324943 | |||||
Maker00000350 | 1.9217 | ARR9 | At3g57040 | Response regulator receiver domain | Cyanidin-3-O-rutinoside-5-O-glucoside | 9.025 | 0.8952 | 6.53 × 10−6 |
Cyanidin-3-O-rutinoside | 7.2774 | 0.8032 | 0.000310451 | |||||
Cyanidin-3-O-galactoside | 7.9568 | 0.842 | 8.23 × 10−5 | |||||
Cyanidin-3-O-arabinoside | 9.025 | 0.8663 | 2.95 × 10−5 | |||||
Cyanidin-3,5-O-diglucoside | 2.6736 | 0.833 | 0.000115529 | |||||
Maker00026791 | 1.2059 | SPL1 | At3g57920 | SBP domain | Cyanidin-3-O-arabinoside | 9.025 | 0.8222 | 0.000168825 |
Maker00008503 | 1.3275 | IAA27 | At4g29080 | AUX/IAA family | Cyanidin-3-O-glucoside | 5.7951 | 0.8337 | 0.000112681 |
Maker00022256 | 1.0026 | ARG7 | At1g75590 | Auxin responsive protein | Cyanidin-3-O-arabinoside | 9.025 | 0.8388 | 9.31 × 10−5 |
Primer Name | Primer Sequence F (5′-3′) | Primer Sequence R (5′-3′) |
---|---|---|
RT-bHLH162 (Maker00021798) | CAGGTTAATGGGAATCGAAAAG | CCAACCCAGTTACCAAAACAAT |
RT-CPC (Maker00014746) | AAACTCGTTGGAGACAGGTG | GCAAACCCTTCTCCATGTTT |
RT-bZIP43 (Maker00026824) | TCGGAGACTATGATCGGAAATC | ACTTGAAACGACAGGTTTTGGT |
RT-SOC1 (Maker00029632) | CAATTGAAGCACGAAATAGCAA | TGTACCGTTTAGAGGGAAGGAA |
RT-4CL-1 (Maker00007314) | AGGTTTGAGGCTTCGCAGTA | GTCCCCAGTGACAACAATCC |
RT-CHS-1 (Maker00012884) | TGCAATTCTTGACCAAGTCG | GATGAACAAAACGCATGCAC |
RT-CHS-2 (Maker00020412) | TGGTGCAATTGATGGACACT | TGCTTCGACCAAGCTTTTCT |
RT-CHI-2 (Maker00012191) | GGGTGTTGGAAGAAAATCCA | GGTCGACTCCATCACCCTTA |
RT-DFR (Maker00011618) | CCATTCCTGGCTTCAAGTGT | AAGCAATTGACCCCATTCTG |
RT-ANS (Maker00000819) | GCTTTCAGGCAACTGGTCAT | TGCTCGGGAATATTTCTGCT |
RT-UFGT-1 (Maker00029333) | GTGGTCGAGACTGGGAGAAG | AGGACCTGCAGTCCAAAGTG |
RT-UFGT-2 (novel.8170) | GTGACAAAACCCTGGAAGGA | CAATTTTGGGAAAGCTGCAT |
RT-Actin | TGATTGGGATGGAAGCAGCA | GAACATGGTTGAACCGCCAC |
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© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
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Xu, J.; Fan, Y.; Han, X.; Pan, H.; Dai, J.; Wei, Y.; Zhuo, R.; Liu, J. Integrated Transcriptomic and Metabolomic Analysis Reveal the Underlying Mechanism of Anthocyanin Biosynthesis in Toona sinensis Leaves. Int. J. Mol. Sci. 2023, 24, 15459. https://doi.org/10.3390/ijms242015459
Xu J, Fan Y, Han X, Pan H, Dai J, Wei Y, Zhuo R, Liu J. Integrated Transcriptomic and Metabolomic Analysis Reveal the Underlying Mechanism of Anthocyanin Biosynthesis in Toona sinensis Leaves. International Journal of Molecular Sciences. 2023; 24(20):15459. https://doi.org/10.3390/ijms242015459
Chicago/Turabian StyleXu, Jing, Yanru Fan, Xiaojiao Han, Huanhuan Pan, Jianhua Dai, Yi Wei, Renying Zhuo, and Jun Liu. 2023. "Integrated Transcriptomic and Metabolomic Analysis Reveal the Underlying Mechanism of Anthocyanin Biosynthesis in Toona sinensis Leaves" International Journal of Molecular Sciences 24, no. 20: 15459. https://doi.org/10.3390/ijms242015459