Adaptive Responses of Citrus grandis Leaves to Copper Toxicity Revealed by RNA-Seq and Physiology
Abstract
:1. Introduction
2. Results
2.1. Seedling Growth and Cu Level in Roots, Stems and Leaves
2.2. Gas Exchange, Pigments, RWC, PCs and MTs in Leaves
2.3. RNA-Seq and De Novo Assembly
2.4. Functional Annotation and Cu-Toxicity-Responsive Genes
2.5. qRT-PCR Analysis
2.6. Hormones in Leaves
3. Discussion
3.1. Increased Immobilization of Cu in Roots, and Cu Homeostasis and Detoxification in Leaves
3.2. Cu-Toxic Effects on Cell Wall Metabolism in Leaves
3.3. Cu-Toxic Effects on Pigment Metabolism, Photosynthesis, and Carbon, Carbohydrate and Energy Metabolisms in Leaves
3.4. Cu-Toxic Effects on Thermal Dissipation, ROS Scavenging and Cell Redox Homeostasis in Leaves
3.5. Cu-Toxic Effects on Calcium Signaling and MAPK Signaling in Leaves
3.6. Cu-Toxic Effects on Biosynthesis and Signaling of Phytohormones in Leaves
4. Materials and Methods
4.1. Plant Culture and Cu Treatments
4.2. Cu Concentration in Leaves, Stems and Roots
4.3. Gas Exchange, Pigments, RWC, PCs and MTs in Leaves
4.4. Leaf RNA Extraction and RNA-Seq
4.5. RNA-Seq Analysis
4.6. qRT-PCR Validation
4.7. Extraction and Measurements of Hormones in Leaves
4.8. Statistical Analysis
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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Accession No. | KEGG | Swiss-Prot | Log2(FC) |
---|---|---|---|
Cu ion transmembrane transporter activity (GO:0005375) | |||
Cg4g018610 | Solute carrier family 31 (copper transporter), member 1 | Copper transporter 5; AtCOPT5 | −1.317 |
Cg8g023350 | Solute carrier family 31 (copper transporter), member 1 | Copper transporter 1; AtCOPT1 | −3.606 |
Cg8g023360 | Solute carrier family 31 (copper transporter), member 1 | Copper transporter 1; AtCOPT1 | −1.076 |
Cg8g023380 | Solute carrier family 31 (copper transporter), member 1 | Copper transporter 1; AtCOPT1 | −8.212 |
Cg6g005770 | Solute carrier family 31 (copper transporter), member 1 | Copper transporter 1; AtCOPT1 | 3.407 |
Yellow Stripe-Like (YSL) family | |||
Cg5g018670 | Fanconi-associated nuclease 1 [EC:3.1.21.- 3.1.4.1] | Metal-nicotianamine transporter YSL3; Protein YELLOW STRIPE LIKE 3; AtYSL3 | −1.609 |
Cg5g020560 | Fanconi-associated nuclease 1 [EC:3.1.21.- 3.1.4.1] | Probable metal-nicotianamine transporter YSL5; Protein YELLOW STRIPE LIKE 5; AtYSL5 | −1.066 |
Cu ion binding (GO:0005507) and/or Cu proteins | |||
Cg1g028930 | l-ascorbate oxidase [EC:1.10.3.3] | l-ascorbate oxidase | −3.067 |
Cg2g001710 | Enoyl-[acyl-carrier protein] reductase I [EC:1.3.1.9 1.3.1.10] | Enoyl-[acyl-carrier-protein] reductase [NADH], chloroplastic | 1.679 |
Cg2g018560 | Iron transport multicopper oxidase | l-ascorbate oxidase homolog | 1.069 |
Cg3g024840 | Iron transport multicopper oxidase | l-ascorbate oxidase homolog | 1.455 |
Cg3g024680 | Plastocyanin | Plastocyanin, chloroplastic | −1.448 |
Cg5g007370 | Glutamate dehydrogenase (NAD(P)+) [EC:1.4.1.3] | Glutamate dehydrogenase 2 | 1.745 |
Cg5g009340 | Copper chaperone for superoxide dismutase | Copper chaperone for superoxide dismutase, chloroplastic/cytosolic; AtCCS | 1.588 |
Cg7g012360 | Glutathione S-transferase [EC:2.5.1.18] | Glutathione S-transferase F9 | −1.318 |
Cg8g018870 | Superoxide dismutase, Cu-Zn family [EC:1.15.1.1] | Superoxide dismutase [Cu-Zn], chloroplastic | 1.344 |
Cg9g013180 | Cytochrome c oxidase subunit 3 | Cytochrome c oxidase subunit 3 | −1.324 |
CgUng010240 | Cytochrome c oxidase subunit 2 | Uncharacterized mitochondrial protein AtMg00530 | −1.581 |
Cu chaperones | |||
Cg5g009340 | Copper chaperone for superoxide dismutase | Copper chaperone for superoxide dismutase, chloroplastic/cytosolic; AtCCS | 1.588 |
Others | |||
Cg3g000750 | Cd2+/Zn2+-exporting ATPase [EC:3.6.3.3 3.6.3.5] | Cadmium/zinc-transporting ATPase HMA2 | −1.403 |
Cg4g006740 | Solute carrier family 39 (zinc transporter), member 1/2/3 | Zinc transporter 4, chloroplastic; ZRT/IRT-like protein 4 | −1.718 |
Cg8g022750 | Solute carrier family 39 (zinc transporter), member 1/2/3 | Zinc transporter 1; ZRT/IRT-like protein 1; OsZIP1 | −2.937 |
Cg5g041700 | Ferric-chelate reductase [EC:1.16.1.7] | Ferric reduction oxidase 2; AtFRO2; EC = 1.16.1.7; Ferric-chelate reductase 2 | 3.591 |
Cg1g023140 | Ferric-chelate reductase [EC:1.16.1.7] | (RefSeq) ferric reduction oxidase 7, chloroplastic-like (A) | NAC domain-containing protein 104 {ECO:0000305} | 3.271 |
Cg2g021360 | Ferric-chelate reductase [EC:1.16.1.7] | (RefSeq) ferric reduction oxidase 7, chloroplastic-like (A) | NAC domain-containing protein 72 | 2.012 |
Cg5g010410 | Ferric-chelate reductase [EC:1.16.1.7] | (RefSeq) ferric reduction oxidase 7, chloroplastic-like (A) | NAC domain-containing protein 100 {ECO:0000303|PubMed:15029955} | 1.441 |
Cg6g025130 | Ferric-chelate reductase [EC:1.16.1.7] | (RefSeq) ferric reduction oxidase 7, chloroplastic-like (A) | NAC domain-containing protein 100 {ECO:0000303|PubMed:15029955} | 1.777 |
Cg8g013730 | Ferric-chelate reductase [EC:1.16.1.7] | (RefSeq) ferric reduction oxidase 7, chloroplastic-like (A) | NAC domain-containing protein 90 | −1.805 |
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Wu, F.; Huang, H.; Peng, M.; Lai, Y.; Ren, Q.; Zhang, J.; Huang, Z.; Yang, L.; Rensing, C.; Chen, L. Adaptive Responses of Citrus grandis Leaves to Copper Toxicity Revealed by RNA-Seq and Physiology. Int. J. Mol. Sci. 2021, 22, 12023. https://doi.org/10.3390/ijms222112023
Wu F, Huang H, Peng M, Lai Y, Ren Q, Zhang J, Huang Z, Yang L, Rensing C, Chen L. Adaptive Responses of Citrus grandis Leaves to Copper Toxicity Revealed by RNA-Seq and Physiology. International Journal of Molecular Sciences. 2021; 22(21):12023. https://doi.org/10.3390/ijms222112023
Chicago/Turabian StyleWu, Fenglin, Huiyu Huang, Mingyi Peng, Yinhua Lai, Qianqian Ren, Jiang Zhang, Zengrong Huang, Lintong Yang, Christopher Rensing, and Lisong Chen. 2021. "Adaptive Responses of Citrus grandis Leaves to Copper Toxicity Revealed by RNA-Seq and Physiology" International Journal of Molecular Sciences 22, no. 21: 12023. https://doi.org/10.3390/ijms222112023