Transcriptomic Responses of a Lightly Calcified Echinoderm to Experimental Seawater Acidification and Warming during Early Development
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Experimental Seawater Manipulation
2.2. Artificial Fertilization and Animal Culture
2.3. Sample Collection
2.4. RNA Extraction, Library Construction, and Transcriptomic Sequencing
2.5. Sequence Assembly
2.6. Identification of Differentially Expressed Genes (DEGs)
2.7. Quantitative PCR
2.8. Statistical Analysis
3. Results
3.1. Seawater Carbonate Chemistry
3.2. Effect of Seawater Acidification and Warming on Early Development
3.3. Transcriptomic Responses to OA and OW
3.3.1. Summary of Statistics and Overview of RNA-Seq
3.3.2. Distinct Transcriptomic Patterns during Early Development
3.3.3. DEG Analysis
3.3.4. GO and KEGG Classification
3.3.5. Validation of DEG Analyses
4. Discussion
4.1. Transcriptomic Responses to OA and OW across Early Stages
4.1.1. Molecular Mechanisms Underpinning Sea Cucumber’s Resilience to OA
4.1.2. Warming Influenced Embryos and Larvae at the Molecular Level
4.1.3. Molecular Response to Dual Stresses of OA and OW
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Caldeira, K.; Wickett, M.E. Oceanography: Anthropogenic carbon and ocean pH. Nature 2003, 425, 365. [Google Scholar] [CrossRef]
- IPCC. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. In Climate Change 2021: The Physical Science Basis; Cambridge University Press: Cambridge, MA, USA, 2021. [Google Scholar]
- Bongaarts, J. Intergovernmental panel on climate change special report on global warming of 1.5 °C Switzerland: IPCC, 2018. Popul. Dev. Rev. 2019, 45, 251–252. [Google Scholar] [CrossRef]
- Jones, E.M.; Chierici, M.; Fransson, A.; Assmann, K.M.; Renner, A.H.; Lødemel, H.H. Inorganic carbon and nutrient dynamics in the marginal ice zone of the Barents Sea: Seasonality and implications for ocean acidification. Prog. Oceanogr. 2023, 219, 103131. [Google Scholar] [CrossRef]
- Gao, K.; Beardall, J.; Häder, D.P.; Hall-Spencer, J.M.; Gao, G.; Hutchins, D.A. Effects of ocean acidification on marine photosynthetic organisms under the concurrent influences of warming, UV radiation, and deoxygenation. Front. Mar. Sci. 2019, 6, 322. [Google Scholar] [CrossRef]
- Arroyo, M.C.; Fassbender, A.J.; Carter, B.R.; Edwards, C.A.; Fiechter, J.; Norgaard, A.; Feely, R.A. Dissimilar sensitivities of ocean acidification metrics to anthropogenic carbon accumulation in the Central North Pacific Ocean and California Current Large Marine Ecosystem. Geophys. Res. Lett. 2022, 49, e2022GL097835. [Google Scholar] [CrossRef]
- Leung, J.Y.; Zhang, S.; Connell, S.D. Is ocean acidification really a threat to marine calcifiers? A systematic review and meta-analysis of 980+ studies spanning two decades. Small 2022, 18, 2107407. [Google Scholar] [CrossRef]
- De Wit, P.; Durland, E.; Ventura, A.; Langdon, C.J. Gene expression correlated with delay in shell formation in larval Pacific oysters (Crassostrea gigas) exposed to experimental ocean acidification provides insights into shell formation mechanisms. BMC Genom. 2018, 19, 160. [Google Scholar] [CrossRef] [PubMed]
- Manríquez, P.H.; González, C.P.; Brokordt, K.; Pereira, L.; Torres, R.; Lattuca, M.E.; Domenici, P. Ocean warming and acidification pose synergistic limits to the thermal niche of an economically important echinoderm. Sci. Total Environ. 2019, 693, 133469. [Google Scholar] [CrossRef]
- Uthicke, S.; Pecorino, D.; Albright, R.; Negri, A.P.; Cantin, N.; Liddy, M.; Symon, D.; Pamela, K.; Maria, B.; Lamare, M. Impacts of ocean acidification on early life-history stages and settlement of the coral-eating sea star Acanthaster planci. PLoS ONE 2013, 8, e82938. [Google Scholar] [CrossRef]
- Musa, S.M.; Ripley, D.M.; Moritz, T.; Shiels, H.A. Ocean warming and hypoxia affect embryonic growth, fitness and survival of small-spotted catsharks, Scyliorhinus canicula. J. Fish Biol. 2020, 97, 257–264. [Google Scholar] [CrossRef]
- Shi, D.; Zhao, C.; Chen, Y.; Ding, J.; Zhang, L.; Chang, Y. Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius. Sci. Rep. 2020, 10, 7931. [Google Scholar] [CrossRef]
- Devens, H.R.; Davidson, P.L.; Deaker, D.J.; Smith, K.E.; Wray, G.A.; Byrne, M. Ocean acidification induces distinct transcriptomic responses across life history stages of the sea urchin Heliocidaris erythrogramma. Mol. Ecol. 2020, 29, 4618–4636. [Google Scholar] [CrossRef] [PubMed]
- Runcie, D.E.; Dorey, N.; Garfield, D.A.; Stumpp, M.; Dupont, S.; Wray, G.A. Genomic characterization of the evolutionary potential of the sea urchin Strongylocentrotus droebachiensis facing ocean acidification. Genome Biol. Evol. 2016, 8, 3672–3684. [Google Scholar] [CrossRef]
- Lang, B.J.; Donelson, J.M.; Bairos-Novak, K.R.; Wheeler, C.R.; Caballes, C.F.; Uthicke, S.; Pratchett, M.S. Impacts of ocean warming on echinoderms: A meta-analysis. Ecol. Evol. 2023, 13, e10307. [Google Scholar] [CrossRef] [PubMed]
- Pereira, T.M.; Gnocchi, K.G.; Merçon, J.; Mendes, B.; Lopes, B.M.; Passos, L.S.; Gomes, A.R.C. The success of the fertilization and early larval development of the tropical sea urchin Echinometra lucunter (Echinodermata: Echinoidea) is affected by the pH decrease and temperature increase. Mar. Environ. Res. 2020, 161, 105106. [Google Scholar] [CrossRef]
- Arribas, L.P.; Alfaya, J.E.; Palomo, M.G.; Giulianelli, S.; Vilela, R.A.N.; Bigatti, G. Ocean warming lead to heat shock protein expression and decrease in the feeding rate of the Patagonian sea star Anasterias minuta. J. Exp. Mar. Biol. Ecol. 2022, 546, 151661. [Google Scholar] [CrossRef]
- Vergara-Amado, J.; Silva, A.X.; Manzi, C.; Nespolo, R.F.; Cárdenas, L. Differential expression of stress candidate genes for thermal tolerance in the sea urchin Loxechinus albus. J. Therm. Biol. 2017, 68, 104–109. [Google Scholar] [CrossRef]
- Devergne, J.; Loizeau, V.; Lebigre, C.; Bado-Nilles, A.; Collet, S.; Mouchel, O.; Servili, A. Impacts of long-term exposure to ocean acidification and warming on three-spined stickleback (Gasterosteus aculeatus) growth and reproduction. Fishes 2023, 8, 523. [Google Scholar] [CrossRef]
- Baag, S.; Mandal, S. Combined effects of ocean warming and acidification on marine fish and shellfish: A molecule to ecosystem perspective. Sci. Total Environ. 2022, 802, 149807. [Google Scholar] [CrossRef]
- Villalobos, C.; Love, B.A.; Olson, M.B. Ocean acidification and ocean warming effects on Pacific Herring (Clupea pallasi) early life stages. Front. Mar. Sci. 2020, 7, 597899. [Google Scholar] [CrossRef]
- Dahlke, F.; Lucassen, M.; Bickmeyer, U.; Wohlrab, S.; Puvanendran, V.; Mortensen, A.; Chierici, M.; Pörtner, H.-O.; Storch, D. Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation. J. Exp. Biol. 2020, 223, jeb212589. [Google Scholar] [CrossRef]
- Lenz, B.; Fogarty, N.D.; Figueiredo, J. Effects of ocean warming and acidification on fertilization success and early larval development in the green sea urchin Lytechinus variegatus. Mar. Pollut. Bull. 2019, 141, 70–78. [Google Scholar] [CrossRef] [PubMed]
- Khalil, M.; Doo, S.S.; Stuhr, M.; Westphal, H. Long-term physiological responses to combined ocean acidification and warming show energetic trade-offs in an asterinid starfish. Coral Reefs 2023, 42, 845–858. [Google Scholar] [CrossRef]
- Hu, M.Y.; Stumpp, M. Surviving in an acidifying ocean: Acid-base physiology and energetics of the sea urchin larva. Physiology 2023, 38, 242–252. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Hamel, J.-F.; Mercier, A. The Sea Cucumber Apostichopus japonicus: History, Biology and Aquaculture; Academic Press: Cambridge, MA, USA, 2015; p. 437. [Google Scholar]
- Su, F.; Liu, S.; Xing, L.; Huo, D.; Yang, H.; Sun, L. Understanding gene regulation during the development of the sea cucumber Apostichopus japonicus using comparative transcriptomics. Front. Mar. Sci. 2023, 10, 1087339. [Google Scholar] [CrossRef]
- Yuan, X.; Shao, S.; Dupont, S.; Meng, L.; Liu, Y.; Wang, L. Impact of CO2-driven acidification on the development of the sea cucumber Apostichopus japonicus (selenka) (echinodermata: Holothuroidea). Mar. Pollut. Bull. 2015, 95, 195–199. [Google Scholar] [CrossRef]
- Yuan, X.; Shao, S.; Yang, X.; Yang, D.; Xu, Q.; Zong, H.; Shinlin, L. Bioenergetic trade-offs in the sea cucumber Apostichopus japonicus (echinodermata: Holothuroidea) in response to CO2-driven ocean acidification. Environ. Sci. Pollut. Res. 2016, 23, 8453–8461. [Google Scholar] [CrossRef]
- Machado, A.M.; Fernández-Boo, S.; Nande, M.; Pinto, R.; Costas, B.; Castro, L.F.C. The male and female gonad transcriptome of the edible sea urchin, Paracentrotus lividus: Identification of sex-related and lipid biosynthesis genes. Aquac. Rep. 2022, 22, 100936. [Google Scholar] [CrossRef]
- Shi, L.; Qian, Y.; Shen, Q.; He, Y.; Jia, Y.; Wang, F. The developmental toxicity and transcriptome analyses of zebrafish (Danio rerio) embryos exposed to carbon nanoparticles. Ecotoxicol. Environ. Saf. 2022, 234, 113417. [Google Scholar] [CrossRef]
- Yang, A.; Zhou, Z.; Pan, Y.; Jiang, J.; Dong, Y.; Guan, X.; Chen, Z. RNA sequencing analysis to capture the transcriptome landscape during skin ulceration syndrome progression in sea cucumber Apostichopus japonicus. BMC Genom. 2016, 17, 459. [Google Scholar] [CrossRef]
- Su, F.; Sun, L.; Li, X.; Cui, W.; Yang, H. Characterization and Expression Analysis of Regeneration-Associated Protein (Aj-Orpin) during Intestinal Regeneration in the Sea Cucumber Apostichopus japonicus. Mar. Drugs 2022, 20, 568. [Google Scholar] [CrossRef]
- Yang, Q.; Zhang, X.; Lu, Z.; Huang, R.; Tran, N.T.; Wu, J.; Lin, Q. Transcriptome and metabolome analyses of sea cucumbers Apostichopus japonicus in Southern China during the summer aestivation period. J. Ocean Univ. China 2021, 20, 198–212. [Google Scholar] [CrossRef]
- Li, C.; Fang, H.; Xu, D. Effect of seasonal high temperature on the immune response in Apostichopus japonicus by transcriptome analysis. Fish Shellfish Immunol. 2019, 92, 765–771. [Google Scholar] [CrossRef]
- Yuan, X.; Xie, X. Chapter 30. Sea cucumbers under ocean acidification and warming. In The World of Sea Cucumbers; Mercier, A., Hamel, J.-F., Suhrbier, A., Pearce, C., Eds.; Academic Press: Cambridge, MA, USA, 2023. [Google Scholar] [CrossRef]
- Lewis, E.; Wallace, D.W.R. Program Developed for CO2 System Calculations; ORNL/CDIAC-105; Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy: Oak Ridge, TN, USA, 1998.
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Regev, A. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef]
- Li, B.; Dewey, C.N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011, 12, 323. [Google Scholar] [CrossRef]
- Stumpp, M.; Hu, M.Y.; Melzner, F.; Gutowska, M.A.; Dorey, N.; Himmerkus, N.; Holtmann, W.C.; Dupont, S.T.; Thorndyke, M.C.; Bleich, M. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc. Natl. Acad. Sci. USA 2012, 109, 18192–18197. [Google Scholar] [CrossRef]
- Byrne, M. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean. Oceanogr. Mar. Biol. 2011, 49, 1–42. [Google Scholar]
- Wolfe, K.; Dworjanyn, S.A.; Byrne, M. Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma). Glob. Chang. Biol. 2013, 19, 2698–2707. [Google Scholar] [CrossRef]
- Qiu, T.; Zhang, T.; Hamel, J.-F.; Mercier, A. Chapter 8. Development, settlement, and post-settlement growth. In The Sea Cucumber Apostichopus japonicus; History, Biology and Aquaculture; Yang, H., Hamel, J.-F., Mercier, A., Eds.; Academic Press: Cambridge, MA, USA, 2015; pp. 111–132. [Google Scholar]
- Heuer, R.M.; Grosell, M. Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 2014, 307, 1061–1084. [Google Scholar] [CrossRef]
- Hammond, L.M.; Hofmann, G.E. Early developmental gene regulation in Strongylocentrotus purpuratus embryos in response to elevated CO2 seawater conditions. J. Exp. Biol. 2012, 215, 2445–2454. [Google Scholar] [CrossRef]
- Tomanek, L.; Zuzow, M.J.; Ivanina, A.V.; Beniash, E.; Sokolova, I.M. Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: Evidence for oxidative stress. J. Exp. Biol. 2011, 214, 1836–1844. [Google Scholar] [CrossRef] [PubMed]
- Klanian, M.G.; Preciat, M.T. Effect of pH on temperature controlled degradation of reactive oxygen species, heat shock protein expression, and mucosal immunity in the sea cucumber Isostichopus badionotus. PLoS ONE 2017, 12, e0175812. [Google Scholar] [CrossRef] [PubMed]
- Salamanca-Díaz, D.A.; Ritschard, E.A.; Schmidbaur, H.; Wanninger, A. Comparative single-cell transcriptomics reveals novel genes involved in bivalve embryonic shell formation and questions ontogenetic homology of molluscan shell types. Front. Cell Dev. Biol. 2022, 10, 883755. [Google Scholar] [CrossRef]
- Shashikant, T.; Khor, J.M.; Ettensohn, C.A. From genome to anatomy: The architecture and evolution of the skeletogenic gene regulatory network of sea urchins and other echinoderms. Genesis 2018, 56, e23253. [Google Scholar] [CrossRef]
- Zhang, X.; Sun, L.; Yuan, J.; Sun, Y.; Gao, Y.; Zhang, L.; Li, S.; Dai, H.; Hamel, J.-F.; Liu, C.; et al. The sea cucumber genome provides insights into morphological evolution and visceral regeneration. PLoS Biol. 2017, 15, e2003790. [Google Scholar] [CrossRef]
- Evans, T.G.; Chan, F.; Menge, B.A.; Hofmann, G.E. Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment. Mol. Ecol. 2013, 22, 1609–1625. [Google Scholar] [CrossRef]
- Yuan, X.C.; Huang, H.; Zhou, W.H.; Guo, Y.J.; Yuan, T.; Liu, S. Gene expression pro-files of two coral species with varied resistance to ocean acidification. Mar. Biotechnol. 2019, 21, 151–160. [Google Scholar] [CrossRef]
- Le Roy, N.; Jackson, D.J.; Marie, B.; Ramos-Silva, P.; Marin, F. Carbonic anhydrase and metazoan biocalcification: A focus on molluscs. Key Eng. Mater. 2016, 672, 151–157. [Google Scholar] [CrossRef]
- Fitzer, S.C.; Phoenix, V.R.; Cusack, M.; Kamenos, N.A. Ocean acidification impacts mussel control on biomineralisation. Sci. Rep. 2014, 4, 6218. [Google Scholar] [CrossRef]
- Li, J.; Zhou, Y.; Qin, Y.; Wei, J.; Shigong, P.; Ma, H.; Li, Y.; Yuan, X.; Zhao, L.; Yan, H.; et al. Assessment of the juvenile vulnerability of symbiont-bearing giant clams to ocean acidification. Sci. Total Environ. 2022, 812, 152265. [Google Scholar] [CrossRef]
- Wang, X.D.; Wang, M.Q.; Jia, Z.H.; Qiu, L.M.; Wang, L.L.; Zhang, A.G.; Song, L. A carbonic anhydrase serves as an important acid-base regulator in pacific oyster Crassostrea gigas exposed to elevated CO2: Implication for physiological responses of mollusk to ocean acidification. Mar. Biotechnol. 2017, 19, 22–35. [Google Scholar] [CrossRef]
- Gao, J.; Liu, J.; Yang, Y.; Liang, J.; Xie, J.; Li, S.; Zheng, G.; Xie, L.; Zhang, R. Identification and expression characterization of three Wnt signaling genes in pearl oyster (Pinctada fucata). Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2016, 196, 92–101. [Google Scholar] [CrossRef] [PubMed]
- Weiss, I.M.; Stefan, K.; Karlheinz, M.; Monika, F. Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc Haliotis laevigata. Biochem. Biophys. Res. Commun. 2000, 267, 17–21. [Google Scholar] [CrossRef] [PubMed]
- Yamazaki, A.; Yamakawa, S.; Morino, Y.; Sasakura, Y.; Wada, H. Gene regulation of adult skeletogenesis in starfish and modifications during gene network co-option. Sci. Rep. 2021, 11, 20111. [Google Scholar] [CrossRef] [PubMed]
- Whittaker, C.A.; Richard, O.H. Distribution and evolution of von Willebrand/integrin A domains: Widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 2002, 13, 3369–3387. [Google Scholar] [CrossRef]
- Sillanpää, J.K.; Cardoso, J.C.D.R.; Félix, R.C.; Anjos, L.; Power, D.M.; Sundell, K. Dilution of seawater affects the Ca2+ transport in the outer mantle epithelium of Crassostrea gigas. Front. Physiol. 2020, 11, 1. [Google Scholar] [CrossRef] [PubMed]
- Röttinger, E.; Dahlin, P.; Martindale, M.Q. A framework for the establishment of a cnidarian gene regulatory network for “endomesoderm” specification: The inputs of b-catenin/TCF signaling. PLoS Genet. 2012, 8, e1003164. [Google Scholar] [CrossRef]
- Willert, K.; Nusse, R. Wnt proteins. Cold Spring Harb. Perspect. Biol. 2012, 4, a007864. [Google Scholar] [CrossRef]
- Xu, D.; Zhou, S.; Sun, L. RNA-seq based transcriptional analysis reveals dynamic genes expression profiles and immune-associated regulation under heat stress in Apostichopus japonicus. Fish Shellfish Immunol. 2018, 78, 169–176. [Google Scholar] [CrossRef]
- Li, C.; Zhao, W.; Qin, C.; Yu, G.; Chen, J. Comparative transcriptome analysis reveals changes in gene expression in sea cucumber (Holothuria leucospilota) in response to acute temperature stress. Comp. Biochem. Physiol. Part D Genom. Proteom. 2021, 7, 100883. [Google Scholar] [CrossRef]
- Tumminello, R.A.; Fuller-Espie, S. Heat stress induces ROS production and histone phosphorylation in celomocytes of Eisenia hortensis. Invertebr. Surviv. J. 2013, 10, 50–57. [Google Scholar]
- Niemisto, M.; Fields, D.M.; Clark, K.F.; Waller, J.D.; Wahle, R.A. American lobster postlarvae alter gene regulation in response to ocean warming and acidification. Ecol. Evol. 2021, 11, 806–819. [Google Scholar] [CrossRef] [PubMed]
- Huth, T.J.; Place, S.P. RNA-seq reveals a diminished acclimation response to the combined effects of ocean acidification and elevated seawater temperature in Pagothenia borchgrevinki. Mar. Genom. 2016, 87–97. [Google Scholar] [CrossRef] [PubMed]
- Vargas, S.; Zimmer, T.; Conci, N.; Lehmann, M.; Wrheide, G. Transcriptional response of the calcification and stress response toolkits in an octocoral under heat and pH stress. Mol. Ecol. 2021, 31, 798–810. [Google Scholar] [CrossRef]
- Woo, S.; Yum, S. Transcriptional response of the azooxanthellate octocoral Scleronephthya gracillimum to seawater acidifcation and thermal stress. Comp. Biochem. Physiol. Part D Genom. Proteom. 2022, 42, 100978. [Google Scholar]
Treatments | Measured | Calculated | |||||
---|---|---|---|---|---|---|---|
Salinity | Temperature (°C) | pH | TA (mol/kg−1SW) | pCO2 (µatm) | Ωca | Ωar | |
CON | 36.4 ± 0.2 | 19.1 ± 0.3 | 8.08 ± 0.07 | 2657 ± 54 | 602 ± 12 | 4.26 ± 0.64 | 2.77 ± 0.42 |
OA | 36.4 ± 0.2 | 19.0 ± 0.4 | 7.74 ± 0.11 | 2667 ± 53 | 1471 ± 393 | 2.17 ± 0.46 | 1.41 ± 0.30 |
OW | 36.4 ± 0.2 | 22.3 ± 0.3 | 8.12 ± 0.04 | 2573 ± 131 | 519 ± 65 | 4.86 ± 0.50 | 3.18 ± 0.32 |
OAW | 36.4 ± 0.2 | 22.1 ± 0.2 | 7.72 ± 0.06 | 2619 ± 33 | 1507 ± 233 | 2.23 ± 0.30 | 1.41 ± 0.20 |
Treatments | OA vs. CON | OW vs. CON | OAW vs. CON | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Developmental Stage | Blastula | Gastrula | Auricularia | Doliolaria | Blastula | Gastrula | Auricularia | Doliolaria | Blastula | Gastrula | Auricularia | Doliolaria |
NR Description | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) | log2(FC) |
Development and regulation of cell cycle | ||||||||||||
cyclin B | −2.24 ↓ | - | - | −3.99 ↓ | −5.98 ↓ | - | - | - | - | - | - | - |
cell division cycle protein 20 | 1.70 ↑ | - | - | −1.65 ↓ | −6.36 ↓ | - | - | - | 2.02 ↑ | −0.41 ↓ | - | - |
cyclin A | - | - | - | - | −4.51 ↓ | - | - | - | −1.03 ↓ | - | - | - |
cyclin E | −1.10 ↓ | - | - | −5.49 ↓ | −5.13 ↓ | - | - | - | - | - | - | - |
putative cyclin-G1 | −1.35 ↓ | 1.04 ↑ | - | - | −4.31 ↓ | - | - | - | −1.13 ↓ | - | - | - |
putative cyclin-J | −1.43 ↓ | - | - | - | −5.24 ↓ | - | - | - | −1.51 ↓ | - | - | - |
Wnt16 | - | - | - | - | 5.45 ↑ | - | - | - | - | - | - | - |
Wnt6 | 1.35 ↑ | - | - | −6.13 ↓ | 2.42 ↑ | 0.85 ↑ | - | - | 1.12 ↑ | 1.75 ↑ | - | - |
Wnt4 | - | - | - | −6.13 ↓ | 5.46 ↑ | - | - | - | - | 2.86 ↑ | 1.99 ↑ | - |
Wnt3 | - | 1.20 ↑ | - | −2.63 ↓ | 0.87 ↑ | - | - | 1.76 ↑ | - | - | - | |
Immune response and antioxidant defense | ||||||||||||
heat shock protein 26 | - | - | −3.77 ↓ | 1.32 ↑ | 5.48 ↑ | 4.54 ↑ | 5.02 ↑ | 1.65 ↑ | - | −1.21 ↓ | −1.78 ↓ | - |
heat shock protein 70 | - | - | - | 3.87 ↑ | 3.07 ↑ | 3.46 ↑ | 8.51 ↑ | 5.32 ↑ | 5.73 ↑ | 6.31 ↑ | - | 6.94 ↑ |
heat shock protein 90 | - | - | - | 6.52 ↑ | 2.57 ↑ | 1.49 ↑ | - | 4.32 ↑ | 1.05 ↑ | 1.13 ↑ | 5.43 ↑ | 9.95 ↑ |
superoxide dismutase | - | 1.33 ↑ | - | 8.48 ↑ | 6.23 ↑ | - | - | 6.98 ↑ | - | 1.25 ↑ | - | 7.00 ↑ |
glutathione S-transferase | 1.48 ↑ | 1.21 ↑ | - | - | 8.19 ↑ | 1.18 ↑ | −1.24 ↓ | 6.86 ↑ | 1.64 ↑ | 1.51 ↑ | −1.45 ↓ | 8.89 ↑ |
scavenger receptor cysteine-rich domain superfamily protein | 1.99 ↑ | 1.70 ↑ | - | - | 7.58 ↑ | - | 1.65 ↑ | - | 1.18 ↑ | 1.16 ↑ | - | - |
glutathione peroxidase | 2.09 ↑ | - | - | 7.40 ↑ | 4.89 ↑ | 1.42 ↑ | - | 7.14 ↑ | 7.39 ↑ | 3.31 ↑ | - | - |
fucolectin | - | - | - | 1.00 ↑ | 12.26 ↑ | - | - | - | - | - | - | - |
putative IgGFc-binding protein | - | - | - | −1.93 ↓ | 5.18 ↑ | - | - | - | 3.06 ↑ | 3.59 ↑ | - | - |
cathepsin | 4.70 ↑ | 1.07 ↑ | - | 8.64 ↑ | 9.76 ↑ | 1.00 ↑ | −1.58 ↓ | 8.27 ↑ | 1.83 ↑ | 1.13 ↑ | −1.34 ↓ | 7.48 ↑ |
complement component 3-2 | 2.54 ↑ | - | - | −2.08 ↓ | 2.44 ↑ | - | - | - | 2.48 ↑ | 1.79 ↑ | - | - |
complement factor B | - | - | - | −2.05 ↓ | 4.13 ↑ | - | - | - | - | 1.52 ↑ | - | - |
putative complement factor H | - | - | - | 5.85 ↑ | 8.24 ↑ | - | - | - | - | - | - | - |
Lectin 1 | - | - | - | −3.77 ↓ | −1.22 ↓ | - | 4.51 ↑ | - | - | - | 3.76 ↑ | - |
TNF receptor-associated factor 2 | - | - | - | - | −5.61 ↓ | - | - | - | - | - | - | - |
TNF receptor-associated factor 6 | −3.04 ↓ | - | - | −2.82 ↓ | −9.35 ↓ | - | - | - | −2.09 ↓ | 1.23 ↑ | - | - |
LPS-induced TNF-alpha factor | - | 1.05 ↑ | - | 1.08 ↑ | 7.57 ↑ | - | - | - | - | 1.07 ↑ | - | - |
Biomineralization and Osteoblast | ||||||||||||
putative transcription factor SOX-4 | - | - | - | - | −2.74 ↓ | - | - | - | 1.60 ↑ | - | - | - |
ets1..2 transcription factor | 1.56 ↑ | - | - | −2.01 ↓ | −2.79 ↓ | - | - | - | 1.94 ↑ | - | - | - |
fox-1 homolog 1-like isoform X9 | - | 1.66 ↑ | - | −5.14 ↓ | - | - | - | - | - | - | - | - |
alx1 | - | 1.35 ↑ | - | −7.15 ↓ | −4.86 ↓ | - | - | - | - | - | - | - |
transcription factor SOX-21 | 1.635 ↑ | 1.34 ↑ | - | −4.54 ↓ | −1.57 ↓ | - | - | - | - | - | - | - |
T-box transcription factor | - | - | - | −2.05 ↓ | 6.37 ↑ | - | - | - | 1.35 ↑ | 3.55 ↑ | - | - |
fibroblast growth factor receptor | −1.77 ↓ | 1.43 ↑ | - | −2.66 ↓ | −5.19 ↓ | 1.53 ↑ | - | - | 1.90 ↑ | 4.39 ↑ | - | - |
TGFB-induced factor homeobox 1 | 1.70 ↑ | - | - | −3.88 ↓ | −1.94 ↓ | - | - | - | 2.09 ↑ | - | - | - |
vascular endothelial growth factor receptor 2-like isoform X4 | - | - | - | −6.14 ↓ | - | - | - | - | - | - | - | - |
putative vascular endothelial growth factor receptor 1 | −1.56 ↓ | 1.49 ↑ | - | −1.65 ↓ | −5.23 ↓ | 1.13 ↑ | - | - | −1.16 ↓ | 1.52 ↑ | - | - |
GSK-3-binding protein | - | - | - | −5.04 ↓ | - | - | - | - | - | - | - | - |
putative C-type lectin domain family 19 member A | - | - | - | −6.02 ↓ | 10.13 ↑ | - | −2.11 ↓ | - | - | 5.69 ↑ | - | - |
C-type lectin domain-containing protein | - | - | - | −4.76 ↓ | - | - | - | - | - | - | - | - |
cyclophilin | 5.84 ↑ | - | - | 7.91 ↑ | - | - | - | 6.60 ↑ | - | - | - | 8.57 ↑ |
3 alpha procollagen precursor | - | - | - | −2.06 ↓ | 2.01 ↑ | 1.45 ↑ | - | - | - | 2.83 ↑ | - | - |
carbonic anhydrase 14 | - | - | - | −4.73 ↓ | 3.31 ↑ | - | −1.50 ↓ | - | - | 1.32 ↑ | - | - |
carbonic anhydrase 3 | - | - | - | −2.27 ↓ | 6.4815 ↑ | - | - | - | - | 2.13 ↑ | - | - |
carbonic anhydrase 2 | −1.76 ↓ | - | - | −3.54 ↓ | 4.6567 ↑ | - | - | - | −1.26 ↓ | 1.92 ↑ | - | −8.86 ↓ |
alpha-carbonic anhydrase | - | - | - | −5.19 ↓ | - | - | - | - | - | - | - | - |
beta-carbonic anhydrase | - | - | - | −3.33 ↓ | - | - | - | - | - | - | - | - |
protocadherin fat 1-like isoform X5 | - | 1.76 ↑ | - | −2.38 ↓ | −2.58 ↓ | 1.09 ↑ | - | - | 2.47 ↑ | 1.41 ↑ | - | - |
DE-cadherin | - | - | - | −4.19 ↓ | - | - | - | - | - | - | - | - |
serine threonine-protein ki-se mTOR | - | 1.24 ↑ | - | −5.90 ↓ | −1.23 ↓ | - | - | - | - | 1.54 ↑ | - | - |
vacuolar protein sorting-associated protein 13C | - | - | - | −2.75 ↓ | −2.98 ↓ | - | - | - | −1.64 ↓ | 4.56 ↑ | - | - |
perlucin 5 | - | - | - | −3.23 ↓ | - | - | - | - | - | - | - | - |
Transport of calcium ions and maintenance of ion homeostasis | ||||||||||||
VWFA and cache domain-containing protein 1-like | - | 1.70 ↑ | - | −4.76 ↓ | −2.24 ↓ | 1.46 ↑ | - | - | 2.24 ↑ | 1.82 ↑ | - | - |
sodium/potassium/calcium exchanger 3 isoform X1 | −2.31 ↓ | - | - | −6.38 ↓ | −1.62 ↓ | - | 1.84 ↑ | - | −1.69 ↓ | 2.57 ↑ | - | - |
probable sodium/potassium/calcium exchanger CG1090 | - | - | - | −6.57 ↓ | - | - | - | - | - | - | - | - |
proton channel | - | 1.37 ↑ | - | −7.57 ↓ | −4.56 ↓ | 1.47 ↑ | - | - | - | 2.78 ↑ | - | - |
H+Cl− exchange transporter 7 | - | 1.54 ↑ | - | −5.04 ↓ | −3.62 ↓ | - | - | - | - | 2.45 ↑ | - | - |
chloride channel protein | −1.62 ↓ | 1.2076 ↑ | - | −3.49 ↓ | −2.96 ↓ | 1.10 ↑ | - | - | −1.38 ↓ | 1.74 ↑ | - | - |
caveolin | - | - | - | 1.43 ↑ | 7.51 ↑ | - | - | - | −1.63 ↓ | 4.12 ↑ | - | - |
organic cation transporter | 2.42 ↑ | - | - | −4.86 ↓ | 10.53 ↑ | 1.51 ↑ | 1.51 ↑ | - | 2.35 ↑ | 1.89 ↑ | - | - |
calmodulin | 5.38 ↑ | - | - | 11.45 ↑ | −1.93 ↓ | 4.11 ↑ | 4.11 ↑ | 5.64 ↑ | - | 5.77 ↑ | 6.73 ↑ | −3.82 ↓ |
pct-1 | - | - | - | - | 2.75 ↑ | - | - | - | - | - | - | - |
transmembrane protein 120A | - | - | - | - | −3.04 ↓ | - | - | - | - | - | - | - |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 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/).
Share and Cite
Zhao, Y.; Song, M.; Yu, Z.; Pang, L.; Zhang, L.; Karakassis, I.; Dimitriou, P.D.; Yuan, X. Transcriptomic Responses of a Lightly Calcified Echinoderm to Experimental Seawater Acidification and Warming during Early Development. Biology 2023, 12, 1520. https://doi.org/10.3390/biology12121520
Zhao Y, Song M, Yu Z, Pang L, Zhang L, Karakassis I, Dimitriou PD, Yuan X. Transcriptomic Responses of a Lightly Calcified Echinoderm to Experimental Seawater Acidification and Warming during Early Development. Biology. 2023; 12(12):1520. https://doi.org/10.3390/biology12121520
Chicago/Turabian StyleZhao, Ye, Mingshan Song, Zhenglin Yu, Lei Pang, Libin Zhang, Ioannis Karakassis, Panagiotis D. Dimitriou, and Xiutang Yuan. 2023. "Transcriptomic Responses of a Lightly Calcified Echinoderm to Experimental Seawater Acidification and Warming during Early Development" Biology 12, no. 12: 1520. https://doi.org/10.3390/biology12121520