Transition to Piscivory Seen Through Brain Transcriptomics in a Juvenile Percid Fish: Complex Interplay of Differential Gene Transcription, Alternative Splicing, and ncRNA Activity
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
This work has received funding from the Czech National Agency of Agricultural Research, project QK22020134 Innovative fisheries management of a large reservoir, from the programme Water for Life of the Strategy AV21 of Czech Academy of Sciences, from ELIXIR Staff Exchange (CZ-USB-2023-SEP-46) and from ELIXIR CZ Research Infrastructure (ID LM2018131, MEYS CR).
PubMed
39629900
PubMed Central
PMC11788885
DOI
10.1002/jez.2886
Knihovny.cz E-zdroje
- Klíčová slova
- (Sander (Stizostedion) lucioperca), brain transcriptome, cannibalism, developmental plasticity, heterochrony, snoRNA,
- MeSH
- alternativní sestřih * MeSH
- genetická transkripce MeSH
- mozek * metabolismus MeSH
- nekódující RNA * genetika metabolismus MeSH
- okounovití * genetika fyziologie MeSH
- regulace genové exprese fyziologie MeSH
- transkriptom * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- nekódující RNA * MeSH
Pikeperch (Sander Lucioperca) belongs to main predatory fish species in freshwater bodies throughout Europe playing the key role by reducing planktivorous fish abundance. Two size classes of the young-of-the-year (YOY) pikeperch are known in Europe and North America. Our long-term fish survey elucidates late-summer size distribution of YOY pikeperch in the Lipno Reservoir (Czechia) and recognizes two distinct subcohorts: smaller pelagic planktivores heavily outnumber larger demersal piscivores. To explore molecular mechanisms accompanying the switch from planktivory to piscivory, we compared brain transcriptomes of both subcohorts and identified 148 differentially transcribed genes. The pathway enrichment analyses identified the piscivorous phase to be associated with genes involved in collagen and extracellular matrix generation with numerous Gene Ontology (GO), while the planktivorous phase was associated with genes for non-muscle-myosins (NMM) with less GO terms. Transcripts further upregulated in planktivores from the periphery of the NMM network were Pmchl, Pomcl, and Pyyb, all involved also in appetite control and producing (an)orexigenic neuropeptides. Noncoding RNAs were upregulated in transcriptomes of planktivores including three transcripts of snoRNA U85. Thirty genes mostly functionally unrelated to those differentially transcribed were alternatively spliced between the subcohorts. Our results indicate planktivores as potentially driven by voracity to initiate the switch to piscivory, while piscivores undergo a dynamic brain development. We propose a spatiotemporal spreading of juvenile development over a longer period and larger spatial scales through developmental plasticity as an adaptation to exploiting all types of resources and decreasing the intraspecific competition.
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Institute of Computer Science Czech Academy of Sciences Prague Czech Republic
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Aalto, S. K. , and (Buck) Newsome G. E.. 1990. “Additional Evidence Supporting Demic Behaviour of a Yellow Perch (Perca Flavescens) Population.” Canadian Journal of Fisheries and Aquatic Sciences 47, no. 10: 1959–1962.
Akdel, M. , Pires D. E. V., Pardo E. P., et al. 2022. “A Structural Biology Community Assessment of AlphaFold2 Applications.” Nature Structural & Molecular Biology 29: 1056–1067. 10.1038/s41594-022-00849-w. PubMed DOI PMC
Anders, S. , Reyes A., and Huber W.. 2012. “Detecting Differential Usage of Exons from RNA‐Seq Data.” Genome Research 22, no. 10: 2008–2017. 10.1101/gr.133744.111. PubMed DOI PMC
Antolin‐Fontes, B. , Li K., Ables J. L., et al. 2020. “The Habenular G‐Protein‐Coupled Receptor 151 Regulates Synaptic Plasticity and Nicotine Intake.” Proceedings of the National Academy of Sciences 117, no. 10: 5502–5509. 10.1073/pnas.1916132117. PubMed DOI PMC
Baralle, F. E. , and Giudice J.. 2017. “Alternative Splicing as a Regulator of Development and Tissue Identity.” Nature Reviews Molecular Cell Biology 18: 437–451. 10.1038/nrm.2017.27. PubMed DOI PMC
Barua, B. , Nagy A., Sellers J. R., and Hitchcock‐DeGregori S. E.. 2014. “Regulation of Nonmuscle Myosin II By Tropomyosin.” Biochemistry 53, no. 24: 4015–4024. 10.1021/bi500162z. PubMed DOI PMC
Bastin, B. R. , and Schneider S. Q.. 2019. “Taxon‐Specific Expansion and Loss of Tektins Inform Metazoan Ciliary Diversity.” BMC Evolutionary Biology 19, no. 1: 40. 10.1186/s12862-019-1360-0. PubMed DOI PMC
Berman, J. R. , Skariah G., Maro G. S., Mignot E., and Mourrain P.. 2009. “Characterization of Two Melanin‐Concentrating Hormone Genes in Zebrafish Reveals Evolutionary and Physiological Links with the Mammalian MCH System.” Journal of Comparative Neurology 517, no. 5: 695–710. 10.1002/cne.22171. PubMed DOI PMC
Bertucci, J. I. , Blanco A. M., Sundarrajan L., Rajeswari J. J., Velasco C., and Unniappan S.. 2019. “Nutrient Regulation of Endocrine Factors Influencing Feeding and Growth in Fish.” Frontiers in Endocrinology 10: 83. 10.3389/fendo.2019.00083. PubMed DOI PMC
Bolger, A. M. , Lohse M., and Usadel B.. 2014. “Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.” Bioinformatics 30, no. 15: 2114–2120. 10.1093/bioinformatics/btu170. PubMed DOI PMC
Broms, J. , Antolin‐Fontes B., Tingström A., and Ibañez‐Tallon I.. 2015. “Conserved Expression of the GPR151 Receptor in Habenular Axonal Projections of Vertebrates.” Journal of Comparative Neurology 523: 359–380. 10.1002/cne.23664. PubMed DOI PMC
Buijse, A. D. , and Houthuijzen R. P.. 1992. “Piscivory, Growth, and Size‐Selective Mortality of Age 0 Pikeperch (Stizostedion Lucioperca).” Canadian Journal of Fisheries and Aquatic Sciences 49: 894–902.
Bush, S. J. , Chen L., Tovar‐Corona J. M., and Urrutia A. O.. 2017. “Alternative Splicing and the Evolution of Phenotypic Novelty.” Philosophical Transactions of the Royal Society, B: Biological Sciences 372, no. 1713: 20150474. 10.1098/rstb.2015.0474. PubMed DOI PMC
Carruthers, M. , Edgley D. E., Saxon A. D., et al. 2022. “Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes.” Molecular Biology and Evolution 39, no. 11: msac251. 10.1093/molbev/msac251. PubMed DOI PMC
Chen, Y. , Pandit N. P., Fu J., Li D., and Li J.. 2014. “Identification, Characterization and Feeding Response of Peptide YYb (PYYb) Gene in Grass Carp (Ctenopharyngodon Idellus).” Fish Physiology and Biochemistry 40, no. 1: 45–55. 10.1007/s10695-013-9822-6. PubMed DOI
Colchen, T. , Gisbert E., Krauss D., Ledoré Y., Pasquet A., and Fontaine P.. 2020. “Improving Pikeperch Larviculture by Combining Environmental, Feeding and Populational Factors.” Aquaculture Reports 17: 100337. 10.1016/j.aqrep.2020.100337. DOI
Concetti, C. , Peleg‐Raibstein D., and Burdakov D.. 2024. “Hypothalamic MCH Neurons: From Feeding to Cognitive Control.” Function (Oxford, England) 5, no. 1: zqad059. 10.1093/function/zqad059. PubMed DOI PMC
Cunningham, F. , Allen J. E., Allen J., et al. 2022. “Ensembl 2022.” Nucleic Acids Research 50, no. 1: D988–D995. 10.1093/nar/gkab1049. PubMed DOI PMC
D'Arcy, B. R. , Lennox A. L., Manso Musso C., et al. 2023. “Non‐Muscle Myosins Control Radial Glial Basal Endfeet to Mediate Interneuron Organization.” PLoS Biology 21, no. 2: e3001926. 10.1371/journal.pbio.3001926. PubMed DOI PMC
Das, S. , Mallick D., Sarkar S., Billington N., Sellers J. R., and Jana S. S.. 2023. “A Brain Specific Alternatively Spliced Isoform of Nonmuscle Myosin Iia Lacks Its Mechano‐Enzymatic Activities.” Journal of Biological Chemistry 299, no. 9: 105143. 10.1016/j.jbc.2023.105143. PubMed DOI PMC
Delgado, M. J. , Cerdá‐Reverter J. M., Soengas J. L.. 2017. “Hypothalamic Integration of Metabolic, Endocrine, and Circadian Signals in Fish: Involvement in the Control of Food Intake.” Frontiers in Neuroscience 11. 10.3389/fnins.2017.00354. PubMed DOI PMC
Densen, W. L. T. 1985. “Feeding Behaviour of Major 0 + Fish Species in a Shallow, Eutrophic Lake (Tjeukemeer, The Netherlands).” Journal of Applied Ichthyology 1: 49–70. 10.1111/j.1439-0426.1985.tb00412.x. DOI
van Densen, W. L. T. , Ligtvoet W., and Roozen R. W. M.. 1996. “Intra‐Cohort Variation in the Individual Size of Juvenile Pikeperch, Stizostedion Lucioperca, and Perch, Perca Fluviatilis, in Relation to the Size Spectrum of Their Food Items.” Annales Zoologici Fennici 33: 495–506.
Diniz, G. B. , and Bittencourt J. C.. 2019. “The Melanin‐Concentrating Hormone (MCH) System: A Tale of Two Peptides.” Frontiers in Neuroscience 13: 1280. 10.3389/fnins.2019.01280. PubMed DOI PMC
Dityatev, A. , and Rusakov D. A.. 2011. “Molecular Signals of Plasticity at the Tetrapartite Synapse.” Current Opinion in Neurobiology 21, no. 2: 353–359. 10.1016/j.conb.2010.12.006. PubMed DOI PMC
Dobin, A. , Davis C. A., Schlesinger F., et al. 2013. “STAR: Ultrafast Universal Rna‐Seq Aligner.” Bioinformatics 29, no. 1: 15–21. 10.1093/bioinformatics/bts635. PubMed DOI PMC
Dörner, H. , Wagner A., and Benndorf J.. 1999. “Predation By Piscivorous Fish on Age‐0 Fish: Spatial and Temporal Variability in a Biomanipulated Lake (Bautzen Reservoir, Germany).” Hydrobiologia 408/409: 39–46.
Fazeli, W. , Bamborschke D., Moawia A., et al. 2022. “The Phenotypic Spectrum of PCDH12 Associated Disorders—Five New Cases and Review of the Literature.” European Journal of Paediatric Neurology 36: 7–13. 10.1016/j.ejpn.2021.10.011. PubMed DOI PMC
Frankiewicz, P. , Dabrowski K., and Zalewski M.. 1996. “Mechanism of Establishing Bimodality in a Size Distribution of Age‐0 Pikeperch, Stizostedion Lucioperca (L.) in Sulejów Reservoir, Central Poland.” Annales Zoologici Fennici 33: 321–327.
Franz, G. P. , Lewerentz L., and Grunow B.. 2021. “Observations of Growth Changes During the Embryonic‐Larval‐Transition of Pikeperch (Sander Lucioperca) Under Near‐Natural Conditions.” Journal of Fish Biology 99: 425–436. 10.1111/jfb.14734. PubMed DOI
Franz, G. P. , Tönißen K., Rebl A., Lutze P., and Grunow B.. 2022. “The Expression of Myogenic Gene Markers During the Embryo‐Larval‐Transition in Pikeperch (Sander Lucioperca).” Aquaculture Research 53: 4767–4781. 10.1111/are.15969. DOI
Gelegen, C. , Chandarana K., Choudhury A. I., et al. 2012. “Regulation of Hindbrain Pyy Expression by Acute Food Deprivation, Prolonged Caloric Restriction, and Weight Loss Surgery in Mice.” American Journal of Physiology‐Endocrinology and Metabolism 303, no. 5: E659–E668. 10.1152/ajpendo.00033.2012. PubMed DOI PMC
Gillespie, M. , Jassal B., Stephan R., et al. 2022. “The Reactome Pathway Knowledgebase 2022.” Nucleic Acids Research 50: D687–D692. 10.1093/nar/gkab1028. PubMed DOI PMC
Ginter, K. , Kangur K., Kangur A., Kangur P., and Haldna M.. 2012. “Shifts in Prey Selection and Growth of Juvenile Pikeperch (Sander Lucioperca) Over Half a Century in a Changing Lake Võrtsjärv.” Open Journal of Applied Sciences 02: 168–176.
Gutzman, J. H. , Sahu S. U., and Kwas C.. 2015. “Non‐Muscle Myosin Iia and IIB Differentially Regulate Cell Shape Changes during Zebrafish Brain Morphogenesis.” Developmental Biology 397, no. 1: 103–115. 10.1016/j.ydbio.2014.10.017. PubMed DOI
Harno, E. , Gali Ramamoorthy T., Coll A. P., and White A.. 2018. “POMC: The Physiological Power of Hormone Processing.” Physiological Reviews 98, no. 4: 2381–2430. 10.1152/physrev.00024.2017. PubMed DOI PMC
Healy, T. M. , and Schulte P. M.. 2019. “Patterns of Alternative Splicing in Response to Cold Acclimation in Fish.” Journal of Experimental Biology 222, no. 5: jeb193516. 10.1242/jeb.193516. PubMed DOI
Hsieh, T. B. , and Jin J. P.. 2023. “Evolution and Function of Calponin and Transgelin.” Frontiers in Cell and Developmental Biology 11: 1206147. 10.3389/fcell.2023.1206147. PubMed DOI PMC
Hubert, T. , Grimal S., Carroll P., and Fichard‐Carroll A.. 2009. “Collagens in the Developing and Diseased Nervous System.” Cellular and Molecular Life Sciences 66: 1223–1238. PubMed PMC
Huss, M. , Byström P., Strand Å., Eriksson L., Persson L.. 2008. “Influence of Growth History on the Accumulation of Energy Reserves and Winter Mortality in Young Fish.” Canadian Journal of Fisheries and Aquatic Sciences 65, no. 10: 2149–2156. 10.1139/F08-115. DOI
Huss, M. , Van Kooten T., and Persson L.. 2010. “Intra‐Cohort Cannibalism and Size Bimodality: A Balance Between Hatching Synchrony and Resource Feedback.” Oikos 119: 2000–2011. 10.1111/j.1600-0706.2010.18454.x. DOI
Itoh, Y. , Sahni V., Shnider S. J., McKee H., and Macklis J. D.. 2023. “Inter‐Axonal Molecular Crosstalk Via Lumican Proteoglycan Sculpts Murine Cervical Corticospinal Innervation By Distinct Subpopulations.” Cell Reports 42, no. 3: 112182. 10.1016/j.celrep.2023.112182. PubMed DOI PMC
Jacobs, A. , Carruthers M., Yurchenko A., et al. 2020. “Parallelism in Eco‐Morphology and Gene Expression Despite Variable Evolutionary and Genomic Backgrounds in a Holarctic Fish.” PLoS Genetics 16, no. 4: e1008658. 10.1371/journal.pgen.1008658. PubMed DOI PMC
Jacobs, A. , and Elmer K. R.. 2021. “Alternative Splicing and Gene Expression Play Contrasting Roles in the Parallel Phenotypic Evolution of a Salmonid Fish.” Molecular Ecology 30, no. 20: 4955–4969. 10.1111/mec.15817. PubMed DOI PMC
Jeukens, J. , Bittner D., Knudsen R., and Bernatchez L.. 2008. “Candidate Genes and Adaptive Radiation: Insights From Transcriptional Adaptation to the Limnetic Niche Among Coregonine Fishes (Coregonus Spp., Salmonidae).” Molecular Biology and Evolution 26, no. 1: 155–166. 10.1093/molbev/msn235. PubMed DOI
Johnson, M. , Zaretskaya I., Raytselis Y., Merezhuk Y., McGinnis S., and Madden T. L.. 2008. “NCBI Blast: A Better Web Interface.” Nucleic Acids Research 36, no. Web Server issue: W5–W9. 10.1093/nar/gkn201. PubMed DOI PMC
Jůza, T. , Blabolil P., Čech M., et al. 2023. “Distribution Patterns, Annual Density Changes, Growth and Mortality of Pikeperch [Sander Lucioperca (L. 1758)] Fry Following Oligotrophication of a Reservoir.” Ecology of Freshwater Fish 32, no. 4: 724–734. 10.1111/eff.12718. DOI
Jůza, T. , Vašek M., Kratochvíl M., et al. 2014. “Chaos and Stability of Age‐0 Fish Assemblages in a Temperate Deep Reservoir: Unpredictable Success and Stable Habitat Use.” Hydrobiologia 724, no. 1: 217–234. 10.1007/s10750-013-1735-y. DOI
Kanehisa, M. , Furumichi M., Tanabe M., Sato Y., and Morishima K.. 2017. “KEGG: New Perspectives on Genomes, Pathways, Diseases and Drugs.” Nucleic Acids Research 45, no. D1: D353–D361. 10.1093/nar/gkw1092. PubMed DOI PMC
Kawauchi, H. 2006. “Functions of Melanin‐Concentrating Hormone in Fish.” Journal of Experimental Zoology. Part A, Comparative Experimental Biology 305, no. 9: 751–760. 10.1002/jez.a.310. PubMed DOI
Kawauchi, H. , and Baker B. I.. 2004. “Melanin‐Concentrating Hormone Signaling Systems in Fish.” Peptides 25, no. 10: 1577–1584. 10.1016/j.peptides.2004.03.025. PubMed DOI
Kováč, V. 2002. “Synchrony and Heterochrony in Ontogeny (of Fish).” Journal of Theoretical Biology 217: 499–507. 10.1006/yjtbi.3043. PubMed DOI
Kratochvíl, M. , Čech M., Vašek M., et al. 2010. “Diel Vertical Migrations of Age 0+ Percids in a Shallow, Well‐Mixed Reservoir.” Journal of Limnology 69, no. 2: 305–310.
Krolová, M. , Čížková H., and Hejzlar J.. 2012. “Depth Limit of Littoral Vegetation in a Storage Reservoir: A Case Study of Lipno Reservoir (Czech Republic).” Limnologica 42: 165–174.
Kubečka, J. , Balk H., and Blabolil P., et al. 2022. Methodology of monitoring fish communities in reservoirs and lakes. Institute of Hydrobiology, Institute of Hydrobiology, České Budějovice, Biology Centre CAS.
Kubečka, J. , and Švátora M.. 1993. “Abundance Estimates of Perch Fry (Perca Fluviatilis) Complicated by Grouped Behaviour.” Ecology of Freshwater Fish 2: 84–90. 10.1111/j.1600-0633.1993.tb00087.x. DOI
Kubra, K. , Gaddu G. K., Liongue C., et al. 2022. “Phylogenetic and Expression Analysis of Fos Transcription Factors in Zebrafish.” International Journal of Molecular Sciences 23, no. 17: 10098. 10.3390/ijms231710098. PubMed DOI PMC
Kuleshov, M. V. , Jones M. R., Rouillard A. D., et al. 2016. “Enrichr: A Comprehensive Gene Set Enrichment Analysis Web Server 2016 Update.” Nucleic Acids Research 44, no. W1: W90–W97. 10.1093/nar/gkw377. PubMed DOI PMC
Lafuente, E. , and Beldade P.. 2019. “Genomics of Developmental Plasticity in Animals.” Frontiers in Genetics 10: 720. 10.3389/fgene.2019.00720. PubMed DOI PMC
Lampert, W. , Lampert K. P., and Larssona P.. 2010. “Coexisting Overwintering Strategies in Daphnia Pulex: A Test of Genetic Differences and Growth Responses.” Limnology and Oceanography 55, no. 5: 1893–1900. 10.4319/lo.2010.55.5.1893. DOI
Lappalainen, J. , Dörner H., and Wysujack K.. 2003. “Reproduction Biology of Pikeperch (Sander Lucioperca (L.))—A Review.” Ecology of Freshwater Fish 12: 95–106.
Lappalainen, J. , Erm V., Kjellman J., and Lehtonen H.. 2000. “Size‐Dependent Winter Mortality of Age‐0 Pikeperch (Stizostedion Lucioperca) in Pärnu Bay, the Baltic Sea.” Canadian Journal of Fisheries and Aquatic Sciences 57: 451–458.
Lehner, B. , Crombie C., Tischler J., Fortunato A., and Fraser A. G.. 2006. “Systematic Mapping of Genetic Interactions in Caenorhabditis Elegans Identifies Common Modifiers of Diverse Signaling Pathways.” Nature Genetics 38, no. 8: 896–903. 10.1038/ng1844. PubMed DOI
Liao, Y. , Smyth G. K., and Shi W.. 2019. “The R Package Rsubread Is Easier, Faster, Cheaper and Better for Alignment and Quantification of RNA Sequencing Reads.” Nucleic Acids Research 47, no. 8: e47. 10.1093/nar/gkz114. PubMed DOI PMC
Liu, E. , Zhao X., Li C., et al. 2022. “Effects of Acute Heat Stress on Liver Damage, Apoptosis and Inflammation of Pikeperch (Sander Lucioperca).” Journal of Thermal Biology 106: 103251. 10.1016/j.jtherbio.2022.103251. PubMed DOI
Liu, X. , Xia J., Pang H., and Yue G.. 2017. “Who Eats Whom, When and Why? Juvenile Cannibalism in Fish Asian Seabass.” Aquaculture and Fisheries 2, no. 1: 1–9. 10.1016/j.aaf.2016.12.001. DOI
Lorenz, R. , Bernhart S. H., Höner Zu Siederdissen C., et al. 2011. “ViennaRNA Package 2.0.” Algorithms for Molecular Biology 6: 26. 10.1186/1748-7188-6-26. PubMed DOI PMC
Love, M. I. , Huber W., and Anders S.. 2014. “Moderated Estimation of Fold Change and Dispersion for RNA‐Seq Data With Deseq. 2.” Genome Biology 15: 550. 10.1186/s13059-014-0550-8. PubMed DOI PMC
De Luca, C. , Colangelo A. M., Alberghina L., and Papa M.. 2018. “Neuro‐Immune Hemostasis: Homeostasis and Diseases in the Central Nervous System.” Frontiers in Cellular Neuroscience 12: 459. 10.3389/fncel.2018.00459. PubMed DOI PMC
De Luca, C. , Virtuoso A., Maggio N., and Papa M.. 2017. “Neuro‐Coagulopathy: Blood Coagulation Factors in Central Nervous System Diseases.” International Journal of Molecular Sciences 18: 2128. 10.3390/ijms18102128. PubMed DOI PMC
Lund, I. , and Steenfeldt S. J.. 2011. “The Effect of Dietary Long-Chain Essential Fatty Acids on Growth and Stress Tolerance in Pikeperch Larvae (Sander lucioperca).” Aquaculture Nutrition 17: 191–199.
Madelaine, R. , Ngo K. J., Skariah G., and Mourrain P.. 2020. “Genetic Deciphering of the Antagonistic Activities of the Melanin‐Concentrating Hormone and Melanocortin Pathways in Skin Pigmentation.” PLoS Genetics 16, no. 12: e1009244. 10.1371/journal.pgen.1009244. PubMed DOI PMC
Mann, M. , Wright P. R., and Backofen R.. 2017. “IntaRNA 2.0: Enhanced and Customizable Prediction of RNA‐RNA Interactions.” Nucleic Acids Research 45, no. W1: W435–W439. 10.1093/nar/gkx279. PubMed DOI PMC
Matěna, J. , Kubečka J., and Peterka J.. 1999. “Quantitative Study of Zander Larvae in the Lipno Reservoir in 1995–1997.” Bulletin VÚRH Vodňany 35: 75–84.
Mazin, P. V. , Khaitovich P., Cardoso‐Moreira M., and Kaessmann H.. 2021. “Alternative Splicing during Mammalian Organ Development.” Nature Genetics 53: 925–934. 10.1038/s41588-021-00851-w. PubMed DOI PMC
Merico, D. , Isserlin R., Stueker O., Emili A., and Bader G. D.. 2010. “Enrichment Map: A Network‐Based Method for Gene‐Set Enrichment Visualization and Interpretation.” PLoS One 5, no. 11: e13984. 10.1371/journal.pone.0013984. PubMed DOI PMC
Mittelbach, G. G. , and Persson L.. 1998. “The Ontogeny of Piscivory and its Ecological Consequences.” Canadian Journal of Fisheries and Aquatic Sciences 55, no. 6: 1454–1465. 10.1139/f98-041. DOI
Muszbek, L. , Bereczky Z., Bagoly Z., Komáromi I., and Katona É.. 2011. “Factor XIII: A Coagulation Factor With Multiple Plasmatic and Cellular Functions.” Physiological Reviews 91: 931–972. 10.1152/physrev.00016.2010. PubMed DOI
Nguinkal, J. , Verleih M., de Los Ríos‐Pérez L., et al. 2021. “Comprehensive Characterization of Multitissue Expression Landscape, Co‐Expression Networks and Positive Selection in Pikeperch.” Cells 10, no. 9: 2289. 10.3390/cells10092289. PubMed DOI PMC
Nguinkal, J. A. , Brunner R. M., Verleih M., et al. 2019. “The First Highly Contiguous Genome Assembly of Pikeperch (Sander Lucioperca), an Emerging Aquaculture Species in Europe.” Genes 10, no. 9: 708. 10.3390/genes10090708. PubMed DOI PMC
Persaud, S. J. , and Bewick G. A.. 2014. “Peptide YY: More Than Just an Appetite Regulator.” Diabetologia 57: 1762–1769. 10.1007/s00125-014-3292-y. PubMed DOI
Policar, T. , Schaefer F. J., Panana E., et al. 2019. “Recent Progress in European Percid Fish Culture Production Technology‐Tackling Bottlenecks.” Aquaculture International 27: 1151–1174.
Porro, C. , Pennella A., Panaro M. A., and Trotta T.. 2021. “Functional Role of Non‐Muscle Myosin II in Microglia: An Updated Review.” International Journal of Molecular Sciences 22, no. 13: 6687. 10.3390/ijms22136687. PubMed DOI PMC
Rosati, D. , Palmieri M., Brunelli G., et al. 2024. “Differential Gene Expression Analysis Pipelines and Bioinformatic Tools for the Identification of Specific Biomarkers: A Review.” Computational and Structural Biotechnology Journal 23: 1154–1168. 10.1016/j.csbj.2024.02.018. PubMed DOI PMC
Rout, A. K. , Wu X., Starich M. R., Strub M. P., Hammer J. A., and Tjandra N.. 2018. “The Structure of Melanoregulin Reveals a Role for Cholesterol Recognition in the Protein's Ability to Promote Dynein Function.” Structure 26, no. 10: 1373–1383.e4. 10.1016/j.str.2018.07.009. PubMed DOI PMC
Roy, A. , Lin Y. N., Agno J. E., DeMayo F. J., and Matzuk M. M.. 2009. “Tektin 3 Is Required for Progressive Sperm Motility in Mice.” Molecular Reproduction and Development 76, no. 5: 453–459. 10.1002/mrd.20957. PubMed DOI PMC
Rønnestad, I. , Gomes A. S., Murashita K., Angotzi R., Jönsson E., and Volkoff H.. 2017. “Appetite‐Controlling Endocrine Systems in Teleosts.” Frontiers in Endocrinology 8: 73. 10.3389/fendo.2017.00073. PubMed DOI PMC
Salisbury, S. J. , Delgado M. L., and Dalziel A. C.. 2021. “Alternative Splicing: An Overlooked Mechanism Contributing to Local Adaptation?” Molecular Ecology 30, no. 20: 4951–4954. 10.1111/mec.16177. PubMed DOI
Salisbury, S. J. , and Ruzzante D. E.. 2022. “Genetic Causes and Consequences of Sympatric Morph Divergence in Salmonidae: A Search for Mechanisms.” Annual Review of Animal Biosciences 10: 81–106. 10.1146/annurev-animal-051021-080709. PubMed DOI
Sánchez‐Hernández, J. 2020. “Drivers of Piscivory in a Globally Distributed Aquatic Predator (Brown Trout): A Meta‐Analysis.” Scientific Reports 10: 11258. 10.1038/s41598-020-68207-8. PubMed DOI PMC
Saulamo, K. , Lappalainen J., and Lehtonen H.. 2005. “Biological Characteristics of Pikeperch, Sander Lucioperca, During Spawning Migration in a Baltic Bay.” Fisheries Management and Ecology 12: 131–136.
Schäfer, N. , Kaya Y., Rebl H., et al. 2021. “Insights into Early Ontogenesis: Characterization of Stress and Development Key Genes of Pikeperch (Sander Lucioperca) in Vivo and in Vitro.” Fish Physiology and Biochemistry 47, no. 2: 515–532. 10.1007/s10695-021-00929-6. PubMed DOI PMC
Schneider, K. , Adams C. E., and Elmer K. R.. 2019. “Parallel Selection on Ecologically Relevant Gene Functions in the Transcriptomes of Highly Diversifying Salmonids.” BMC Genomics 20, no. 1: 1010. 10.1186/s12864-019-6361-2. PubMed DOI PMC
Senzui, A. , and Fukada H.. 2023. “Gene Expression of Appetite‐Related Hormones: Responses to Fasting in Different Brain Regions of Yellowtail Seriola Quinqueradiata .” Fisheries Science 89: 159–170. 10.1007/s12562-022-01654-6. DOI
Shannon, P. , Markiel A., Ozier O., et al. 2003. “Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks.” Genome Research 13, no. 11: 2498–2504. 10.1101/gr.1239303. PubMed DOI PMC
Singh, P. , Börger C., More H., and Sturmbauer C.. 2017. “The Role of Alternative Splicing and Differential Gene Expression in Cichlid Adaptive Radiation.” Genome Biology and Evolution 9, no. 10: 2764–2781. 10.1093/gbe/evx204. PubMed DOI PMC
Soengas, J. L. 2021. “Integration of Nutrient Sensing in Fish Hypothalamus.” Frontiers in Neuroscience 15: 653928. 10.3389/fnins.2021.653928. PubMed DOI PMC
Steward, R. A. , de Jong M. A., Oostra V., and Wheat C. W.. 2022. “Alternative Splicing in Seasonal Plasticity and the Potential for Adaptation to Environmental Change.” Nature Communications 13: 755. 10.1038/s41467-022-28306-8. PubMed DOI PMC
Subramanian, K. S. , Lauer L. T., Hayes A. M. R., et al. 2023. “Hypothalamic Melanin‐Concentrating Hormone Neurons Integrate Food‐Motivated Appetitive and Consummatory Processes in Rats.” Nature Communications 14, no. 1: 1755. 10.1038/s41467-023-37344-9. PubMed DOI PMC
Sweeney, B. A. , Petrov A. I., Burkov B., et al. 2019. “Rnacentral: A Hub of Information for Non‐Coding RNA Sequences.” Nucleic Acids Research 47, no. D1: D221–D229. 10.1093/nar/gky1034. PubMed DOI PMC
Szczepkowski, M. , Zakęś Z., Szczepkowska B., and Piotrowska I.. 2011. “Effect of Size Sorting on the Survival, Growth and Cannibalism in Pikeperch (Sander Lucioperca L.) Larvae During Intensive Culture in Ras.” Czech Journal of Animal Science 56: 483–489.
Szklarczyk, D. , Kirsch R., Koutrouli M., et al. 2023. “The String Database in 2023: Protein–Protein Association Networks and Functional Enrichment Analyses for any Sequenced Genome of Interest.” Nucleic Acids Research 51, no. D1: D638–D646. 10.1093/nar/gkac1000. PubMed DOI PMC
Takahashi, A. , Tsuchiya K., Yamanome T., et al. 2004. “Possible Involvement of Melanin‐Concentrating Hormone in Food Intake in a Teleost Fish, Barfin Flounder.” Peptides 25, no. 10: 1613–1622. 10.1016/j.peptides.2004.02.022. PubMed DOI
Takiguchi, H. , Murayama E., Kaneko T., Kurio H., Toshimori K., and Iida H.. 2011. “Characterization and Subcellular Localization of Tektin 3 in Rat Spermatozoa.” Molecular Reproduction and Development 78, no. 8: 611–620. 10.1002/mrd.21352. PubMed DOI
Tatusov, R. L. , Galperin M. Y., Natale D. A., Koonin E. V.. 2000. “The Cog Database: A Tool for Genome‐Scale Analysis of Protein Functions and Evolution.” Nucleic Acids Research 28, no. 1: 33–36. 10.1093/nar/28.1.33. PubMed DOI PMC
Tesfaye, M. , Jůza T., Šmejkal M., et al. 2024. “The Impact of Climatic Conditions and Food Availability on Bimodality Size Structure and Density of Yoy Pikeperch (Sander Lucioperca).” Hydrobiologia 851: 3665–3681. 10.1007/s10750-024-05527-0. DOI
Tesfaye, M. , Souza A. T., Soukalová K., et al. 2023. “Somatic Growth of Pikeperch (Stizostedion Lucioperca) in Relation to Variation in Temperature and Eutrophication in a Central Europe Lake.” Fisheries Research 267: 106824. 10.1016/J.FISHRES.2023.106824. DOI
Thomas, P. D. , Hill D. P., Mi H., et al. 2019. “Gene Ontology Causal Activity Modeling (GO‐CAM) Moves Beyond go Annotations to Structured Descriptions of Biological Functions and Systems.” Nature Genetics 51, no. 10: 1429–1433. 10.1038/s41588-019-0500-1. PubMed DOI PMC
Tönißen, K. , Franz G. P., Rebl A., Lutze P., and Grunow B.. 2024. “Does Size Matter? Small and Large Larvae of Pikeperch (Sander Lucioperca) in a Comparative Gene Expression Analysis.” Fishes 9, no. 1: 33. 10.3390/fishes9010033. DOI
Topal, A. , Özdemir S., Arslan H., and Çomaklı S.. 2021. “How Does Elevated Water Temperature Affect Fish Brain? (A Neurophysiological and Experimental Study: Assessment of Brain Derived Neurotrophic Factor, cFOS, Apoptotic Genes, Heat Shock Genes, ER‐Stress Genes and Oxidative Stress Genes).” Fish & Shellfish Immunology 115: 198–204. 10.1016/j.fsi.2021.05.002. PubMed DOI
Traunmüller, L. , Schulz J., Ortiz R., et al. 2023. “A Cell‐Type‐Specific Alternative Splicing Regulator Shapes Synapse Properties in a Trans‐Synaptic Manner.” Cell Reports 42, no. 3: 112173. 10.1016/j.celrep.2023.112173. PubMed DOI PMC
Uphoff, C. S. , Schoenebeck C. W., Koupal K. D., Pope K. L., and Wyatt Hoback W.. 2019. “Age‐0 Walleye Sander Vitreus Display Length‐Dependent Diet Shift to Piscivory.” Journal of Freshwater Ecology 34, no. 1: 27–36. 10.1080/02705060.2018.1529637. DOI
Vašek, M. , Prchalová M., Říha M., et al. 2016. “Fish Community Response to the Longitudinal Environmental Gradient in Czech Deep‐Valley Reservoirs: Implications for Ecological Monitoring and Management.” Ecological Indicators 63: 219–230. 10.1016/J.ECOLIND.2015.11.061. DOI
Verleih, M. , Visnovska T., Nguinkal J. A., Rebl A., Goldammer T., and Andreassen R.. 2023. “The Discovery and Characterization of Conserved and Novel miRNAs in the Different Developmental Stages and Organs of Pikeperch (Sander Lucioperca).” International Journal of Molecular Sciences 25, no. 1: 189. 10.3390/ijms25010189. PubMed DOI PMC
Vilizzi, L. , and Kováč V., 2013. “Alternative Ontogenies and Developmental Plasticity: Implications for Ecological and Evolutionary Studies on Species Complexes.” Fish and Fisheries 15, no. 3: 523–531. 10.1111/faf.12048. DOI
Volkoff, H. 2016. “The Neuroendocrine Regulation of Food Intake in Fish: A Review of Current Knowledge.” Frontiers in Neuroscience 10: 540. 10.3389/fnins.2016.00540. PubMed DOI PMC
Volkoff, H. 2019. “Fish as Models for Understanding the Vertebrate Endocrine Regulation of Feeding and Weight.” Molecular and Cellular Endocrinology 497: 110437. 10.1016/j.mce.2019.04.017. PubMed DOI
Wang, Y. , Li C., Pan C., Liu E., Zhao X., and Ling Q.. 2019. “Alterations to Transcriptomic Profile, Histopathology, and Oxidative Stress in Liver of Pikeperch (Sander Lucioperca) Under Heat Stress.” Fish & Shellfish Immunology 95: 659–669. 10.1016/j.fsi.2019.11.014. PubMed DOI
Wellband, K. W. , and Heath D. D.. 2017. “Plasticity in Gene Transcription Explains the Differential Performance of Two Invasive Fish Species.” Evolutionary Applications 10: 563–576. 10.1111/eva.12463. PubMed DOI PMC
Wright, C. J. , Smith C. W. J., and Jiggins C. D.. 2022. “Alternative Splicing as a Source of Phenotypic Diversity.” Nature Reviews Genetics 23: 697–710. 10.1038/s41576-022-00514-4. PubMed DOI
Wu, Q. , and Jia Z.. 2021. “Wiring the Brain by Clustered Protocadherin Neural Codes.” Neuroscience Bulletin 37, no. 1: 117–131. 10.1007/s12264-020-00578-4. PubMed DOI PMC
Wysujack, K. , Kasprzak P., Laude U., and Mehner T.. 2002. “Management of a Pikeperch Stock in a Long‐Term Biomanipulated Stratified Lake: Efficient Predation vs. Low Recruitment.” Hydrobiologia 479: 169–180.
Xu, J. , Hou F., Wang D., Li J., and Yang G.. 2019. “Characterization and Expression of Melanin‐Concentrating Hormone (MCH) in Common Carp (Cyprinus Carpio) During Fasting and Reproductive Cycle.” Fish Physiology and Biochemistry 45, no. 2: 805–817. 10.1007/s10695-018-0586-x. PubMed DOI
Yang, S. , Yang K., Liu C., et al. 2015. “To What Extent is Cannibalism Genetically Controlled in Fish? A Case Study in Juvenile Hybrid Catfish Silurus Meridionalis–Asotus and the Progenitors.” Aquaculture 437: 208–214. 10.1016/j.aquaculture.2014.12.005. DOI
Yeh, L. K. , Liu C. Y., Kao W. W. Y., et al. 2010. “Knockdown of Zebrafish Lumican Gene (Zlum) Causes Scleral Thinning and Increased Size of Scleral Coats.” Journal of Biological Chemistry 285, no. 36: 28141–28155. 10.1074/jbc.M109.043679. PubMed DOI PMC
Čech, M. , Kratochvíl M., Kubečka J., Draštík V., and Matěna J.. 2005. “Diel Vertical Migrations of Bathypelagic Perch Fry.” Journal of Fish Biology 66: 685–702. 10.1111/j.0022-1112.2005.00630.x. DOI
Šmejkal, M. , Ricard D., Prchalová M., et al. 2015. “Biomass and Abundance Biases in European Standard Gillnet Sampling.” PLoS One 10: 0122437. 10.1371/journal.pone.0122437. PubMed DOI PMC
Żarski, D. , Le Cam A., Nynca J., et al. 2020. “Domestication Modulates the Expression of Genes Involved in Neurogenesis in High‐Quality Eggs of Sander Lucioperca .” Molecular Reproduction and Development 87: 934–951. 10.1002/mrd.23414. PubMed DOI