Full-Length Transcriptome Maps of Reef-Building Coral Illuminate the Molecular Basis of Calcification, Symbiosis, and Circadian Genes
Abstract
:1. Introduction
2. Results
2.1. Full-Length-Enriched Transcriptome Sequencing and Data Processing
2.2. Gene-Function Annotation and Structure Analysis
2.3. Gene Expression Profile Analysis
2.4. Expression Analysis of the Biomineralization-Related Gene Group
2.5. Genes Expressed by Symbiodiniaceae (Intracellular Symbionts of Coral) Are Mainly Involved in Energy and Nutrient Production
2.6. Phylogenetic Analysis of the Key Circadian Clock Gene Regulation Network
3. Discussion
3.1. Coral Biomineralization and Skeleton Density
3.2. Evolutionary Origins of the per Gene
4. Materials and Methods
4.1. Ethics
4.2. Sample Collection
4.3. Coral Culture System
4.4. Total RNA Extraction
4.5. Total RNA Quality Testing
4.6. Illumina cDNA Library Construction and Sequencing
4.7. PacBio cDNA Library Construction and Sequencing
4.8. Data Filtering and Processing
4.9. Coral and Symbiodiniaceae Sequences Separation
4.10. Correction and De-Redundancy
4.11. Gene-Function Annotation
4.12. Gene Structure Analysis
4.13. Gene Expression Quantification
4.14. Gene Differential Expression Analysis
4.15. Phylogenetic Analysis
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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NO. | BioProject | Data Volume, Gb | Data Volume, Mbytes | Library Strategy | Platform | Model |
---|---|---|---|---|---|---|
P. damicornis | ||||||
1 | PRJNA227785 | 27 | 17,496 | RNA-Seq | Illumina | Genome Analyzer IIx |
2 | PRJNA299443 | 24 | 10,069 | RNA-Seq | Illumina | HiSeq 4000 |
3 | PRJNA327142 | 10 | 3750 | RNA-Seq | Illumina | HiSeq 4000 |
4 | PRJNA433950 | 60 | 23,545 | RNA-Seq | Illumina | HiSeq X Ten |
5 | PRJNA435620 | 67 | 26,334 | RNA-Seq | Illumina | HiSeq X Ten |
6 | PRJNA306839 | 18 | 8574 | RNA-Seq | Illumina | MiSeq |
7 | PRJEB26650 | 45 | 21,254 | RNA-Seq | Illumina | HiSeq 2500 |
8 | PRJNA544778 | 1348 | 0.41T | RNA-Seq | PacBio Illumina | SequelII HiSeq X Ten |
9 | PRJNA545379 | 67 | 27,278 | RNA-Seq | Illumina | HiSeq 2000 |
10 | PRJNA611041 | 258 | 90,416 | RNA-Seq | Illumina | HiSeq 1500 |
P. verrucosa | ||||||
1 | PRJNA552592 | 15 | 7782 | RNA-Seq | Illumina | HiSeq 2500 |
2 | PRJNA551401 | 108 | 47,540 | RNA-Seq WGS | Illumina | HiSeq4000 HiSeq2500 |
3 | PRJNA544778 | 1348 | 0.41T | RNA-Seq | PacBio Illumina | SequelII HiSeq X Ten |
A. muricata | ||||||
1 | PRJNA544778 | 1348 | 0.41T | RNA-Seq | PacBio Illumina | SequelII HiSeq X Ten |
2 | PRJDB8519 | 1785 | 1.09T | WGS | Illumina | HiSeq 2500 |
3 | PRJDB5633 | 110 | 63,481 | WGS | Illumina | HiSeq 2500 |
M. foliosa | ||||||
1 | PRJNA544778 | 1348 | 0.41T | RNA-Seq | PacBio Illumina | SequelII HiSeq X Ten |
Sample Name | P. damicornis | P. verrucosa | A. muricata | M. foliosa |
---|---|---|---|---|
Polymerase reads (Gb) | 25.34 | 27.8 | 22.32 | 21.44 |
Subreads (Gb) | 24.43 | 26.52 | 21.36 | 20.24 |
CCS 1 (Number) | 334,111 | 292,565 | 341,490 | 305,153 |
FLNC 2 (Number) | 245,504 | 249,577 | 273,822 | 238,498 |
Polished consensus (Number) | 20,994 | 24,860 | 31,571 | 26,455 |
Transcripts (Number) | 20,609 | 24,174 | 31,242 | 25,460 |
Unigenes (Number) | 14,167 | 12,822 | 13,800 | 10,905 |
Mean length (bp) | 2668 | 2092 | 1918 | 1472 |
Minimum length (bp) | 51 | 107 | 183 | 69 |
Maximum length (bp) | 9888 | 7861 | 6991 | 5942 |
N50 3 (bp) | 2954 | 2313 | 2126 | 1678 |
N90 3 (bp) | 1793 | 1346 | 1230 | 905 |
Rank | Species | Gene Number 1 | Percentage 2 |
---|---|---|---|
P. damicornis | |||
1 | Acropora digitifera | 8310 | 62.66% |
2 | Exaiptasia pallida | 2313 | 17.44% |
3 | Nematostella vectensis | 1632 | 12.31% |
4 | Branchiostoma belcheri | 145 | 1.09% |
5 | Stylophora pistillata | 80 | 0.60% |
P. verrucosa | |||
1 | Acropora digitifera | 7144 | 62.27% |
2 | Exaiptasia pallida | 1928 | 16.80% |
3 | Nematostella vectensis | 1475 | 12.86% |
4 | Branchiostoma belcheri | 86 | 0.75% |
5 | Stylophora pistillata | 54 | 0.47% |
A. muricata | |||
1 | Acropora digitifera | 9814 | 78.14% |
2 | Exaiptasia pallida | 1098 | 8.74% |
3 | Nematostella vectensis | 1034 | 8.23% |
4 | Acropora millepora | 110 | 0.88% |
5 | Branchiostoma belcheri | 33 | 0.26% |
M. foliosa | |||
1 | Acropora digitifera | 5902 | 69.44% |
2 | Exaiptasia pallida | 1034 | 12.16% |
3 | Nematostella vectensis | 951 | 11.19% |
4 | Acropora millepora | 78 | 0.92% |
5 | Branchiostoma belcheri | 48 | 0.56% |
Class | Protein Name | P. damicornis | P. verrucosa | A. muricata | M. foliosa | |
---|---|---|---|---|---|---|
Calcium ATPase | Plasma membrane calcium-transporting ATPase 1 | 0.00 | 0.00 | 5081.58 | 0.00 | |
Plasma membrane calcium-transporting ATPase 2 | 1716.33 | 0.00 | 0.00 | 1171.67 | ||
Plasma membrane calcium-transporting ATPase 3 | 0.00 | 835.00 | 1049.33 | 528.33 | ||
Plasma membrane calcium-transporting ATPase 4 | 1596.00 | 1549.33 | 0.00 | 0.00 | ||
Plasma membrane calcium ATPase | 4570.67 | 2626.67 | 0.00 | 0.00 | ||
Calcium-transporting ATPase type 2C member 1 | 0.00 | 0.00 | 1466.92 | 0.00 | ||
Bicarbonate Transporter | Solute carrier 4 (SLC4) | 5580.66 | 8157.00 | 6321.27 | 5829.46 | |
Solute carrier 26 (SLC26) | 2160.45 | 9072.61 | 850.67 | 1447.00 | ||
Alpha Carbonic Anhydrase | Carbonic anhydrase 1 | 757.33 | 71.33 | 0.00 | 0.00 | |
Carbonic anhydrase 2 | 22,775.35 | 32,853.41 | 31,611.00 | 66,451.10 | ||
Carbonic anhydrase 3 | 508.33 | 0.00 | 0.00 | 0.00 | ||
Carbonic anhydrase 12 | 0.00 | 0.00 | 2580.00 | 6691.27 | ||
Acidic Proteins | Skeletal aspartic acid-rich protein 1 (SAARP1) | 6423.17 | 11,894.42 | 12,233.75 | 3600.29 | |
Skeletal aspartic acid-rich protein 2 (SAARP2) | 0.00 | 341.41 | 1424.33 | 0.00 | ||
Acidic skeletal organic matrix protein (Acidic SOMP) | 1831.00 | 1191.00 | 6063.00 | 4909.22 | ||
Secreted acidic protein 1 (SAP1) | 0.00 | 0.00 | 0.00 | 5512.38 | ||
Secreted acidic protein 2 (SAP2) | 0.00 | 0.00 | 14,584.00 | 8046.54 | ||
Aspartic and glutamic acid-rich protein | 0.00 | 0.00 | 23,130.97 | 13,798.33 | ||
Unique Uncharacterized Proteins | Uncharacterized skeletal organic matrix protein | Uncharacterized skeletal organic matrix protein-1 (USOMP-1) | 0.00 | 0.00 | 598.72 | 0.00 |
Uncharacterized skeletal organic matrix protein-2 (USOMP-2) | 232.00 | 133.33 | 1202.33 | 4982.33 | ||
Uncharacterized skeletal organic matrix protein-3 (USOMP-3) | 2138.94 | 0.00 | 1768.33 | 4098.34 | ||
Uncharacterized skeletal organic matrix protein-4 (USOMP-4) | 0.00 | 0.00 | 21,585.00 | 0.00 | ||
Uncharacterized skeletal organic matrix protein-5 (USOMP-5) | 7592.00 | 18,666.81 | 7931.45 | 2664.33 | ||
Uncharacterized skeletal organic matrix protein-6 (USOMP-6) | 0.00 | 0.00 | 131,300.52 | 80,894.89 | ||
Uncharacterized skeletal organic matrix protein-7 (USOMP-7) | 819.49 | 206.00 | 2158.33 | 4538.67 | ||
Uncharacterized skeletal organic matrix protein-8 (USOMP-8) | 0.00 | 4156.33 | 0.00 | 0.00 | ||
Galaxin | Galaxin | 7224.57 | 862.92 | 6324.67 | 19,549.24 | |
Galaxin2 | 0.00 | 0.00 | 5482.00 | 9479.72 | ||
Collagen alpha-6(VI) | Collagen alpha-6 (VI) chain | 0.00 | 284.67 | 3649.33 | 1082.93 |
Lineage | Key Circadian Clock Genes | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
cry1 | cry2 | Clock | Npas2 | cyc | Arntl (Bmal1) | Arntl2 (Bmal2) | per1 | per2 | per3 | tim | |
Mammalia | Y | Y | Y | Y | - | Y | Y | Y | Y | Y | Y |
Actinopterygii | Y | Y | Y | Y | - | Y | Y | Y | Y | Y | Y |
Ascidiacea | - | - | - | - | - | Y | - | - | - | - | Y |
Cephalochordata | Y | - | - | Y | - | Y | - | Y | - | - | Y |
Echinoidea | Y | Y | Y | - | - | Y | - | - | - | - | Y |
Enteropneusta | - | - | Y | - | - | Y | - | - | - | - | Y |
Nematoda | - | - | - | - | - | Y | - | - | - | - | Y |
Insecta | Y | - | Y | - | Y | - | - | Y | - | - | Y |
Bivalvia | Y | - | Y | - | Y | - | - | Y | - | - | Y |
Platyhelminthes | - | - | - | - | - | Y | - | - | - | - | Y |
Anthozoa | Y | Y | Y | Y | Y | Y | - | - | - | - | Y |
Hydrozoa | Y | - | - | - | - | Y | - | - | - | - | Y |
Cubozoa | - | - | - | Y | - | Y | - | - | - | - | Y |
Scyphozoa | Y | - | - | - | - | Y | - | - | - | - | Y |
Porifera | - | Y | Y | - | Y | - | - | - | - | - | Y |
Ctenophora | Y | - | Y | - | - | Y | - | - | - | - | Y |
Ciliophora | - | - | - | - | - | - | - | - | - | - | Y |
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Han, T.; Liao, X.; Zhu, Y.; Liu, Y.; Lu, N.; Li, Y.; Guo, Z.; Chen, J.-Y.; He, C.; Lu, Z. Full-Length Transcriptome Maps of Reef-Building Coral Illuminate the Molecular Basis of Calcification, Symbiosis, and Circadian Genes. Int. J. Mol. Sci. 2022, 23, 11135. https://doi.org/10.3390/ijms231911135
Han T, Liao X, Zhu Y, Liu Y, Lu N, Li Y, Guo Z, Chen J-Y, He C, Lu Z. Full-Length Transcriptome Maps of Reef-Building Coral Illuminate the Molecular Basis of Calcification, Symbiosis, and Circadian Genes. International Journal of Molecular Sciences. 2022; 23(19):11135. https://doi.org/10.3390/ijms231911135
Chicago/Turabian StyleHan, Tingyu, Xin Liao, Yunchi Zhu, Yunqing Liu, Na Lu, Yixin Li, Zhuojun Guo, J.-Y. Chen, Chunpeng He, and Zuhong Lu. 2022. "Full-Length Transcriptome Maps of Reef-Building Coral Illuminate the Molecular Basis of Calcification, Symbiosis, and Circadian Genes" International Journal of Molecular Sciences 23, no. 19: 11135. https://doi.org/10.3390/ijms231911135