Substantial gene expression shifts during larval transitions in the pearl oyster Pinctada margaritifera.
Pinctada margaritifera
RNA-seq
biomineralization
environmental sensing
immune system
larval development
Journal
Journal of experimental zoology. Part B, Molecular and developmental evolution
ISSN: 1552-5015
Titre abrégé: J Exp Zool B Mol Dev Evol
Pays: United States
ID NLM: 101168228
Informations de publication
Date de publication:
06 Feb 2024
06 Feb 2024
Historique:
revised:
05
01
2024
received:
18
07
2023
accepted:
17
01
2024
medline:
6
2
2024
pubmed:
6
2
2024
entrez:
6
2
2024
Statut:
aheadofprint
Résumé
Early development stages in marine bivalve are critical periods where larvae transition from pelagic free-life to sessile mature individuals. The successive metamorphosis requires the expression of key genes, the functions of which might be under high selective pressure, hence understanding larval development represents key knowledge for both fundamental and applied research. Phenotypic larvae development is well known, but the underlying molecular mechanisms such as associated gene expression dynamic and molecular cross-talks remains poorly described for several nonmodel species, such as P. margaritifera. We designed a whole transcriptome RNA-sequencing analysis to describe such gene expression dynamics following four larval developmental stages: d-shape, Veliger, Umbo and Eye-spot. Larval gene expression and annotated functions drastically diverge. Metabolic function (gene expression related to lipid, amino acid and carbohydrate use) is highly upregulated in the first development stages, with increasing demand from d-shape to umbo. Morphogenesis and larval transition are partly ordered by Thyroid hormones and Wnt signaling. While larvae shells show some similar characteristic to adult shells, the cause of initialization of biomineralization differ from the one found in adults. The present study provides a global overview of Pinctada margaritifera larval stages transitioning through gene expression dynamics, molecular mechanisms and ontogeny of biomineralization, immune system, and sensory perception processes.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Ifremer and the government of French Polynesia
Informations de copyright
© 2024 The Authors. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution published by Wiley Periodicals LLC.
Références
Alagarswami, K., Dharmaraj, S., Chellam, A., & Velayudhan, T. S. (1989). Larval and juvenile rearing of black-lip pearl oyster, Pinctada margaritifera (Linnaeus). Aquaculture, 76, 43-56.
Anders, S., Pyl, P. T., & Huber, W. (2015). HTSeq-a python framework to work with high-throughput sequencing data. Bioinformatics, 31, 166-169.
Balseiro, P., Moreira, R., Chamorro, R., Figueras, A., & Novoa, B. (2013). Immune responses during the larval stages of Mytilus galloprovincialis: Metamorphosis alters immunocompetence, body shape and behavior. Fish & Shellfish Immunology, 35, 438-447.
Bishop, C. D., Huggett, M. J., Heyland, A., Hodin, J., & Brandhorst, B. P. (2006). Interspecific variation in metamorphic competence in marine invertebrates: the significance for comparative investigations into the timing of metamorphosis. Integrative and Comparative Biology, 46, 662-682.
Blank, S., Arnoldi, M., Khoshnavaz, S., Treccani, L., Kuntz, M., Mann, K., Grathwohl, G., & Fritz, M. (2003). The nacre protein perlucin nucleates growth of calcium carbonate crystals. Journal of Microscopy, 212, 280-291.
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics, 30, 2114-2120.
Byrne, M. (2011). impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean. Oceanography and Marine Biology, 49, 1-42.
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P., & Huerta-Cepas, J. (2021). eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Molecular Biology and Evolution, 38, 5825-5829.
Chang, T.-H., Hsieh, F.-L., Zebisch, M., Harlos, K., Elegheert, J., & Jones, E. Y. (2015). Structure and functional properties of Norrin mimic Wnt for signalling with Frizzled4, Lrp5/6, and proteoglycan. eLife, 4, e06554.
Conzelmann, M., Williams, E. A., Tunaru, S., Randel, N., Shahidi, R., Asadulina, A., Berger, J., Offermanns, S., & Jékely, G. (2013). Conserved MIP receptor-ligand pair regulates Platynereis larval settlement. Proceedings of the National Academy of Sciences, 110, 8224-8229.
Croll, R. P., Jackson, D. L., & Voronezhskaya, E. E. (1997). Catecholamine-containing cells in larval and postlarval bivalve molluscs. The Biological Bulletin, 193, 116-124.
Dixon, G. B., Davies, S. W., Aglyamova, G. V., Meyer, E., Bay, L. K., & Matz, M. V. (2015). Genomic determinants of coral heat tolerance across latitudes. Science, 348, 1460-1462.
Dubert, J., Barja, J. L., & Romalde, J. L. (2017). New insights into pathogenic Vibrios affecting bivalves in hatcheries: present and future prospects. Frontiers in Microbiology, 8, 762.
Eales, J. G. (1997). Iodine metabolism and thyroid-related functions in organisms lacking thyroid follicles: are thyroid hormones also vitamins? Experimental Biology and Medicine, 214, 302-317.
Hadfield, M., Meleshkevitch, E., & Boudko, D. (2000). The apical sensory organ of a gastropod veliger is a receptor for settlement cues. The Biological Bulletin, 198, 67-76.
Heyland, A., & Moroz, L. L. (2005). Cross-kingdom hormonal signaling: an insight from thyroid hormone functions in marine larvae. Journal of Experimental Biology, 208, 4355-4361.
Heyland, A., Reitzel, A. M., & Hodin, J. (2004). Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea). Evolution & Development, 6, 382-392.
Huang, W., Xu, F., Qu, T., Zhang, R., Li, L., Que, H., & Zhang, G. (2015). Identification of thyroid hormones and functional characterization of thyroid hormone receptor in the Pacific oyster Crassostrea gigas provide insight into evolution of the thyroid hormone system. PLoS One, 10), e0144991.
Huerta-Cepas, J., Szklarczyk, D., Heller, D., Hernández-Plaza, A., Forslund, S. K., Cook, H., Mende, D. R., Letunic, I., Rattei, T., Jensen, L. J., von Mering, C., & Bork, P. (2019). eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47, D309-D314.
Joyce, A., & Vogeler, S. (2018). Molluscan bivalve settlement and metamorphosis: Neuroendocrine inducers and morphogenetic responses. Aquaculture, 487, 64-82.
Labarta, U., Fernández-Reiriz, M. J., & Pérez-Camacho, A. (1999). Dynamics of fatty acids in the larval development, metamorphosis and post-metamorphosis of Ostrea edulis (L.). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 123, 249-254.
Langfelder, P., & Horvath, S. (2008). WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.
Le Luyer, J., Auffret, P., Quillien, V., Leclerc, N., Reisser, C., Vidal-Dupiol, J., & Ky, C.-L. (2019). Whole transcriptome sequencing and biomineralization gene architecture associated with cultured pearl quality traits in the pearl oyster, Pinctada margaritifera. BMC Genomics, 20, 111.
Li, H., Bai, L., Dong, X., Qi, X., Liu, H., & Yu, D. (2020). SEM observation of early shell formation and expression of biomineralization-related genes during larval development in the pearl oyster Pinctada fucata. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 33, 100650.
Li, H., Zhang, B., Huang, G., Liu, B., Fan, S., Zhang, D., & Yu, D. (2016). Differential gene expression during larval metamorphic development in the pearl oyster, Pinctada fucata, based on transcriptome analysis. International Journal of Genomics, 2016, 1-15.
Liu, J., Yang, D., Liu, S., Li, S., Xu, G., Zheng, G., Xie, L., & Zhang, R. (2015). Microarray: A global analysis of biomineralization-related gene expression profiles during larval development in the pearl oyster, Pinctada fucata. BMC Genomics, 16, 325.
Liu, Z., Zhang, Y., Zhou, Z., Zong, Y., Zheng, Y., Liu, C., Kong, N., Gao, Q., Wang, L., & Song, L. (2020). Metabolomic and transcriptomic profiling reveals the alteration of energy metabolism in oyster larvae during initial shell formation and under experimental ocean acidification. Scientific Reports, 10, 6111.
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq. 2. Genome Biology, 15, 550.
Mao Che, L., Golubic, S., Le Campion-Alsumard, T., & Payri, C. (2001). Developmental aspects of biomineralisation in the Polynesian pearl oyster Pinctada margaritifera var. cumingii. Oceanologica Acta, 24, 37-49.
Marshall, R., McKinley, S., & Pearce, C. M. (2010). Effects of nutrition on larval growth and survival in bivalves. Reviews in Aquaculture, 2, 33-55.
Miyazaki, Y., Nishida, T., Aoki, H., & Samata, T. (2010). Expression of genes responsible for biomineralization of Pinctada fucata during development. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 155, 241-248.
Nascimento-Schulze, J. C., Bean, T. P., Houston, R. D., Santos, E. M., Sanders, M. B., Lewis, C., & Ellis, R. P. (2021). Optimizing hatchery practices for genetic improvement of marine bivalves. Reviews in Aquaculture, 13, 2289-2304.
Plough, L. V. (2018). Fine-scale temporal analysis of genotype-dependent mortality at settlement in the pacific oyster Crassostrea gigas. Journal of Experimental Marine Biology and Ecology, 501, 90-98.
Plough, L. V., & Hedgecock, D. (2011). Quantitative trait locus analysis of stage-specific inbreeding depression in the Pacific oyster Crassostrea gigas. Genetics, 189, 1473-1486.
Rojas, I., Cárcamo, C., Stambuk, F., Mercado, L., Rojas, R., Schmitt, P., & Brokordt, K. (2021a). Expression of immune-related genes during early development of the scallop Argopecten purpuratus after Vibrio splendidus challenge. Aquaculture, 533, 736132.
Rojas, I., Rivera-Ingraham, G. A., Cárcamo, C. B., Jeno, K., de la Fuente-Ortega, E., Schmitt, P., & Brokordt, K. (2021b). Metabolic cost of the immune response during early ontogeny of the scallop Argopecten purpuratus. Frontiers in Physiology, 12, 718467.
Sangare, N., Lo-Yat, A., Moullac, G. L., Pecquerie, L., Thomas, Y., Lefebvre, S., Gendre, R. L., Beliaeff, B., & Andréfouët, S. (2020). Impact of environmental variability on Pinctada margaritifera life-history traits: A full life cycle deb modeling approach. Ecological Modelling, 423, 109006.
Simionato, E., Kerner, P., Dray, N., Le Gouar, M., Ledent, V., Arendt, D., & Vervoort, M. (2008). atonal- and achaete-scute-related genes in the annelid Platynereis dumerilii: insights into the evolution of neural basic-Helix-Loop-Helix genes. BMC Evolutionary Biology, 8, 170.
Wang, L., Song, X., & Song, L. (2018). The oyster immunity. Developmental and Comparative Immunology, 80, 99-118.
Wang, Z., Wang, B., Chen, G., Jian, J., Lu, Y., Xu, Y., & Wu, Z. (2016). Transcriptome analysis of the pearl oyster (Pinctada fucata) hemocytes in response to Vibrio alginolyticus infection. Gene, 575, 421-428.
Wu, T. D., Reeder, J., Lawrence, M., Becker, G., & Brauer, M. J. (2016). GMAP and GSNAP for genomic sequence alignment: enhancements to speed, accuracy, and functionality. Methods in Molecular Biology, 1418, 283-334.
Yurchenko, O. V., Skiteva, O. I., Voronezhskaya, E. E., & Dyachuk, V. A. (2018). Nervous system development in the Pacific oyster, Crassostrea gigas (Mollusca: Bivalvia). Frontiers in Zoology, 15, 10.
Zhao, R., Takeuchi, T., Luo, Y.-J., Ishikawa, A., Kobayashi, T., Koyanagi, R., Villar-Briones, A., Yamada, L., Sawada, H., Iwanaga, S., Nagai, K., Satoh, N., & Endo, K. (2018). Dual gene repertoires for larval and adult shells reveal molecules essential for molluscan shell formation. Molecular Biology and Evolution, 35(11), 2751-2761.
Zheng, Z., Hao, R., Xiong, X., Jiao, Y., Deng, Y., & Du, X. (2019). Developmental characteristics of pearl oyster Pinctada fucata martensii: Insight into key molecular events related to shell formation, settlement and metamorphosis. BMC Genomics, 20, 122.