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Proteomic and gene expression differences between post-diapause and subitaneous offspring phenotypes in the cyclic parthenogen Daphnia pulex

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Abstract

In temperate waters, post-diapause and subitaneous offspring in Daphnia vary in life history traits and metabolic rates, and presumably are adapted to the seasonal environments in which they dwell. These offspring types result from different developmental programs of the same genetic background, representing the phenomenon of phenotypic plasticity. We aimed to explore the molecular mechanism of this phenotypic plasticity in Daphnia pulex from an intermittent population by applying a high-throughput proteomic analysis and expression analysis of several genes. The study revealed 176 proteins that were differentially expressed among offspring phenotypes. Post-diapause and subitaneous females clearly differed in their upregulated protein profiles and gene expression levels. There were more upregulated proteins with oxidoreductase and binding activity in post-diapause offspring, whereas more upregulated proteins with transporter and transferase activity were seen in subitaneous offspring. In contrast to subitaneous phenotype, over 1.5-fold more of the proteins that were upregulated in post-diapause phenotype are involved in metabolism and biosynthesis. Expression levels of several selected genes linked to cellular metabolism were also higher in post-diapause females. The greatest difference, 5-fold upregulation in post-diapause compared to subitaneous offspring, was recorded for the target of rapamycin-like (TOR) protein. Expression of ribosomal proteins in this offspring phenotype was also increased. These upregulations suggest that the TOR signaling pathway is involved and may be responsible for the regulation of the developmental program underlying post-diapause and subitaneous offspring phenotypes in Daphnia. Gene regulatory patterns observed in post-diapause and subitaneous offspring were in agreement with the expectations based on previously observed organismal traits of these Daphnia offspring types.

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References

  • Andre, C. & D. Cota, 2012. Coupling nutrient sensing to metabolic homoeostasis: the role of the mammalian target of rapamycin complex 1 pathway. Proceedings of the Nutrition Society 71: 502–510.

    Article  CAS  PubMed  Google Scholar 

  • Arbačiauskas, K., 1998. Life-history traits of exephippial and parthenogenetically derived daphnids: indicators of different life-history strategies. Archiv für Hydrobiologie Special Issues Advances in Limnology 52: 339–358.

    Google Scholar 

  • Arbačiauskas, K., 2001. Life-history variation related to the first adult instar in daphnids derived from diapausing and subitaneous eggs. Hydrobiologia 442: 157–164.

    Article  Google Scholar 

  • Arbačiauskas, K., 2004a. Life-history characteristics and fitness in descendents of parthenogenetic and ex-ephippio females of Daphnia magna. Hydrobiologia 526: 211–218.

    Article  Google Scholar 

  • Arbačiauskas, K., 2004b. Seasonal phenotypes of Daphnia: post-diapause and directly developing offspring. Journal of Limnology 63(Suppl. 1): 7–15.

    Article  Google Scholar 

  • Arbačiauskas, K., 2007. Does timing of emergence within a season affect the evolution of post-diapause traits? Post-diapause and directly developing phenotypes of Daphnia. In Alekseev, A., B. De Stasio & J. J. Gilbert (eds.), Diapause in Aquatic Invertebrates. Theory and Human Use, Vol. 84. Springer, Netherlands: 167–175.

    Chapter  Google Scholar 

  • Arbačiauskas, K. & Z. R. Gasiūnaitė, 1996. Growth and fecundity of Daphnia after diapause and their impact on the development of a population. Hydrobiologia 320: 209–222.

    Article  Google Scholar 

  • Arbačiauskas, K. & W. Lampert, 2003. Seasonal adaptation of ex-ephippio and parthenogenetic offspring of Daphnia magna: differences in life-history and physiology. Functional Ecology 17: 431–437.

    Article  Google Scholar 

  • Asselman, J., D. I. De Coninck, S. Glaholt, J. Colbourne, C. Janssen, J. Shaw & K. De Schamphelaere, 2012. Identification of pathways, gene networks and paralogous gene families in Daphnia pulex responding to exposure to the toxic cyanobacterium Microcystis aeruginosa. Environmental Science Technology 46: 8448–8457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates, D., M. Maechler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1): 1–48.

    Article  Google Scholar 

  • Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 57: 289–300.

    Google Scholar 

  • Byrne, B. M., M. Gruber & G. Ab, 1989. The evolution of egg yolk proteins. Progress in Biophysics and Molecular Biology 53: 33–69.

    Article  CAS  PubMed  Google Scholar 

  • Carvalho, G. R. & R. N. Hughes, 1983. The effect of food availability, female-density and photoperiod on ephippia production in Daphnia magna Straus (Crustacea, Cladocera). Freshwater Biology 13: 37–46.

    Article  Google Scholar 

  • Caceres, C. E., 1998. Interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology 79: 1699–1710.

    Article  Google Scholar 

  • Chen, W.-H., X. Ge, W. Wang, J. Yu & S. Hu, 2009. A gene catalogue for post-diapause development of an anhydrobiotic arthropod Artemia franciscana. BMC Genomics 10: 52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Decaestecker, E., S. Gaba, J. A. M. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert & L. De Meester, 2007. Host-parasite “Red Queen” dynamics archived in pond sediment. Nature 450: 70–873.

    Article  Google Scholar 

  • De Coninck, D., J. Asselman, S. Glaholt, C. Janssen, J. K. Colbourne, J. Shaw & K. De Schamphelaere, 2014. Genome-wide transcription profiles reveal genotype-dependent responses of biological pathways and gene-families in Daphnia exposed to single and mixed stressors. Environmental Science Technology 48: 3513–3522.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng, D., S. Zhang, Y. Li, X. Meng, W. Yang, Y. Li & X. Li, 2010. Effects of Microcystis aeruginosa on population dynamics and sexual reproduction in two Daphnia species. Journal of Plankton Research 32: 1385–1392.

    Article  Google Scholar 

  • De Stasio, B., 2007. Egg bank formation by aquatic invertebrates: a bridge across disciplinary boundaries. In Alekseev, A., B. De Stasio & J. J. Gilbert (eds.), Diapause in Aquatic Invertebrates. Theory and Human Use, Vol. 84. Springer, New York: 121–133.

    Chapter  Google Scholar 

  • Di Cera, E., 2009. Serine proteases. IUBMB Life 61(5): 510–515.

    Article  PubMed  PubMed Central  Google Scholar 

  • Falchuk, K. H. & M. Montorzi, 2001. Zinc physiology and biochemistry in oocytes and embryos. Biometals 14(3–4): 385–395.

    Article  CAS  PubMed  Google Scholar 

  • Fleming, M. D., D. R. Campagna, J. N. Haslett, C. C. Trenor 3rd & N. C. Andrews, 2001. A mutation in a mitochondrial transmembrane protein is responsible for the pleiotropic hematological and skeletal phenotype of flexed-tail (f/f) mice. Genes and Development 15: 652–657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frisch, D., P. K. Morton, P. R. Chowdhury, B. W. Culver, J. K. Colbourne, L. J. Weider & P. D. Jeyasingh, 2014. A millennial-scale chronicle of evolutionary responses to cultural eutrophication in Daphnia. Ecology Letters 17(3): 360–368.

    Article  PubMed  Google Scholar 

  • Fröhlich, T., G. J. Arnold, R. Fritsch, T. Mayr & C. Laforsch, 2009. LC-MS/MS-based proteome profiling in Daphnia pulex and Daphnia longicephala: the Daphnia pulex genome database as a key for high throughput proteomics in Daphnia. BMC Genomics 10: 171.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gerke, P., C. Börding, B. Zeis & R. J. Paul, 2011. Adaptive haemoglobin gene control in Daphnia pulex at different oxygen and temperature conditions. Comparative Biochemistry and Physiology, Part A 159: 56–65.

    Article  Google Scholar 

  • Gyllström, M., 2004. Induction and termination of diapause in a freshwater zooplankton community. Archiv für Hydrobiologie 161: 81–97.

    Article  Google Scholar 

  • Gyllström, M. & L. Hansson, 2004. Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquatic Sciences 66: 274–295.

    Article  Google Scholar 

  • Hairston Jr., N. G., R. A. Va Brunt & C. M. Kearns, 1995. Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76: 1706–1711.

    Article  Google Scholar 

  • Hairston Jr., N. G., A.-M. Hansen & W. R. Schaffner, 2000. The effect of diapause emergence on the seasonal dynamics of zooplankton assemblage. Freshwater Biology 22: 471–478.

    Google Scholar 

  • Harris, K.D.M., N.J. Bartlett & V.K. Lloyd, 2012. Daphnia as an emerging epigenetic model organism. Genetics Research International, Article ID 147892

  • Hellman, U., C. Wernstedt, J. Gonez & C. H. Heldin, 1995. Improvement of an “in-gel” digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Analytical Biochemistry 224: 451–455.

    Article  CAS  PubMed  Google Scholar 

  • Hedstrom, L., 2002. Serine protease mechanism and specificity. Chemical Reviews 102(12): 4501–4524.

    Article  CAS  PubMed  Google Scholar 

  • Kato, Y., S. Tokishita, T. Ohta & H. Yamagata, 2004. A vitellogenin chain containing a superoxide dismutase-like domain is the major component of yolk proteins in cladoceran crustacean Daphnia magna. Gene 334: 157–165.

    Article  CAS  PubMed  Google Scholar 

  • Kemp, C. J. & D. Kültz, 2012. Controlling proteome degradation in Daphnia pulex. The Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 317(10): 645–651.

    CAS  Google Scholar 

  • Koch, U., E. Von Elen & D. Straile, 2009. Food quality triggers the reproductive mode in the cyclical parthenogen Daphnia (Cladocera). Oecologia 159: 317–324.

    Article  PubMed  Google Scholar 

  • Koeppe, J. & J. Ofengand, 1976. Juvenile hormone-induced biosynthesis of vitellogenin in Leucophaea maderae. Archives of Biochemistry and Biophysics 173: 100–113.

    Article  CAS  PubMed  Google Scholar 

  • Lampert, W., K. P. Lampert & P. Larsson, 2012. Induction of male production in clones of Daphnia pulex by the juvenoid hormone methyl farnesoate under short photoperiod. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 156(2): 130–133.

    CAS  Google Scholar 

  • Latta, L. C., L. J. Weider, J. K. Colbourne & M. E. Pfrender, 2012. The evolution of salinity tolerance in Daphnia: a functional genomics approach. Ecology Letters 15: 794–802.

    Article  PubMed  Google Scholar 

  • Li, X., D. Han, R. K. T. Kam, X. Guo, M. Chen, Y. Yang, H. Zhao & Y. Chen, 2010. Developmental expression of sideroflexin family genes in Xenopus embryos. Developmental Dynamics 239: 2742–2747.

    Article  CAS  PubMed  Google Scholar 

  • MATLAB and Statistics Toolbox Release 2012b, The MathWorks, Inc., Natick, Massachusetts, United States

  • Mayer, C. & I. Grummt, 2006. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25: 6384–6391.

    Article  CAS  PubMed  Google Scholar 

  • McCarthy, F. M., N. Wang, G. B. Magee, B. Nanduri, M. L. Lawrence, E. B. Camon, D. G. Barrell, D. P. Hill, M. E. Dolan, W. P. Williams, D. S. Luthe, S. M. Bridges & S. C. Burgess, 2006. AgBase: a functional genomics resource for agriculture. BMC Genomics 7: 229.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miner, B. E., L. De Meester, M. E. Pfrender, W. Lampert & N. G. Hairston, 2012. Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proceedings of the Royal Society B 279: 1873–1882.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mutti, N. S., A. G. Dolezal, F. Wolschin, J. S. Mutti, K. S. Gill & G. V. Amdam, 2011. IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. The Journal of Experimental Biology 214: 3977–3984.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldham, S. & E. Hafen, 2003. Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends in Cell Biology 13: 79–85.

    Article  CAS  PubMed  Google Scholar 

  • Patel, A., M. K. Fondrk, O. Kaftanoglu, C. Emore, G. Hunt, K. Frederick & G. V. Amdam, 2007. The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE 2(6): e509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pauwels, K., R. Stoks & L. De Meester, 2005. Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water flea Daphnia magna. Journal of Evolutionary Biology 18: 867–872.

    Article  CAS  PubMed  Google Scholar 

  • Perez-Martınez, C., L. Jimenez, E. Moreno & J. M. Conde-Porcuna, 2013. Emergence pattern and hatching cues of Daphnia pulicaria (Crustacea, Cladocera) in an alpine lake. Hydrobiologia 707: 47–57.

    Article  Google Scholar 

  • Pijanowska, J. & G. Stolpe, 1996. Summer diapause in Daphnia as a reaction to the presence of fish. Journal of Plankton Research 18: 1407–1412.

    Article  Google Scholar 

  • Pfaffl, M. W., G. W. Horgan & L. Dempfle, 2002. Relative Expression Software Tool (REST) for group-wise comparison and statistical analysis of relative expression results in Real-Time PCR. Nucleic Acids Research 30: E36.

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team, 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Rother, A., M. Pitsch & S. Hülsmann, 2010. The importance of hatching from resting eggs for population dynamics and genetic composition of Daphnia in a deep reservoir. Freshwater Biology 55: 2319–2331.

    Google Scholar 

  • Rozenberg, A., M. Parida, F. Leese, L. C. Weiss, R. Tollrian & J. R. Manak, 2015. Transcriptional profiling of predator-induced phenotypic plasticity in Daphnia pulex. Frontiers in Zoology 12: 18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rufini, A., M. V. Niklison-Chirou, S. Inoue, R. Tomasini, I. S. Harris, A. Marino & T. W. Mak, 2012. TAp73 depletion accelerates aging through metabolic dysregulation. Genes and Development 26(18): 2009–2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sappington, T. W. & A. S. Raikhel, 1998a. Ligand-binding domains in vitellogenin receptors and other LDL-receptor family members share a common ancestral ordering of cysteine-rich repeats. Journal of Molecular Evolution 46: 476–487.

    Article  CAS  PubMed  Google Scholar 

  • Sappington, T. W. & A. S. Raikhel, 1998b. Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology 28: 277–300.

    Article  CAS  PubMed  Google Scholar 

  • Schwanhäusser, B., D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen & M. Selbach, 2011. Global quantification of mammalian gene expression control. Nature 473: 337–342.

    Article  PubMed  Google Scholar 

  • Schwerin, S., B. Zeis, T. Lamkemeyer, R. J. Paul, M. Koch, J. Madlung, C. Fladerer & R. Pirow, 2009. Acclimatory responses of the Daphnia pulex proteome to environmental changes. II. Chronic exposure to different temperatures (10 and 20°C) mainly affects protein metabolism. BMC Physiology 9: 8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shiraishi, S., C. Zhou, T. Aoki, N. Sato, T. Chiva, K. Tanaka, S. Yoshida, Y. Nabeshima, Y. I. Nabeshima & T. Tamura, 2007. TBP-interacting protein 120B (TIP120B)/cullin-associated and neddylation dissociated 2 (CAND2) inhibits SCF-dependent ubiquitination of myogenin and accelerates myogenic differentiation. The Journal of Biological Chemistry 282: 9017–9028.

    Article  CAS  PubMed  Google Scholar 

  • Slusarczyk, M., 2001. Food threshold for diapause in Daphnia under the threat of fish predation. Ecology 82: 1089–1096.

    Article  Google Scholar 

  • Sommer, U., Z. M. Gliwicz, W. Lampert & A. Duncan, 1986. The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv für Hydrobiologie 106: 433–471.

    Google Scholar 

  • Spanier, K., F. Leese, C. Mayer, J. K. Colbourne, D. Gilbert, M. E. Pfrender & R. Tollrian, 2010. Predator induced defences in Daphnia pulex: Selection and evaluation of internal reference genes for gene expression studies with real-time PCR. BMC Molecular Biology 11: 50.

    Article  PubMed  PubMed Central  Google Scholar 

  • Strepetkaitė, D., G. Alzbutas, E. Astromskas, A. Lagunavičius, R. Sabaliauskaitė, K. Arbačiauskas & J. Lazutka, 2016. Analysis of DNA methylation and hydroxymethylation in the genome of crustacean Daphnia pulex. Genes 7: 1.

    Article  Google Scholar 

  • Stross, R. G. & R. G. Hill, 1965. Diapause induction in Daphnia requires two stimuli. Science 150: 1462–1464.

    Article  CAS  PubMed  Google Scholar 

  • Toyota, K., Y. Kato, H. Miyakawa & R. Yatsu, 2014. Molecular impact of juvenile hormone agonists on neonatal Daphnia magna. Journal of Applied Toxicology 34(5): 537–544.

    Article  CAS  PubMed  Google Scholar 

  • Turek-Plewa, J. & P. Jagodzinski, 2005. The role of mammalian DNA methyltransferases in the regulation of gene expression. Cellular and Molecular Biology Letters 10: 631–647.

    CAS  PubMed  Google Scholar 

  • van den Berg, R. A., H. C. J. Hoefsloot, J. A. Westerhuis, A. K. Smilde & M. J. van der Werf, 2006. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genomics 7: 142.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe & F. Speleman, 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3(7): 0034.1–0034.11.

    Article  Google Scholar 

  • Vandegehuchte, M. B., T. Kyndt, B. Vanholme, A. Haegeman, G. Gheysen & C. R. Janssen, 2009. Occurrence of DNA methylation in Daphnia magna and influence of multigeneration Cd exposure. Environment International 35: 700–706.

    Article  CAS  PubMed  Google Scholar 

  • Walsh, M. R., 2013. The link between environmental variation and evolutionary shifts in dormancy in zooplankton. Integrative and Comparative Biology 53: 713–722.

    Article  PubMed  Google Scholar 

  • Wolschin, F., N. S. Mutti & G. V. Amdam, 2011. Insulin receptor substrate influences female caste development in honeybees. Biology Letters 7: 112–115.

    Article  PubMed  Google Scholar 

  • Wolf, H. G. & G. R. Carvalho, 1989. Testing eggs of lake-Daphnia II. In situ observations on the hatching of eggs and their contribution to population and community structure. Freshwater Biology 22: 471–478.

    Article  Google Scholar 

  • Zeis, B., T. Lamkemeyer, R. J. Paul, F. Nunes, S. Schwerin, M. Koch, W. Schutz, J. Madlung, C. Fladerer & R. Pirow, 2009. Acclimatory responses of the Daphnia pulex proteome to environmental changes. I. Chronic exposure to hypoxia affects the oxygen transport system and carbohydrate metabolism. BMC Physiology 9: 7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, Y., X.-W. Lin, Y.-R. Zhang, Y.-J. Huang, C.-H. Zhang, Q. Yang, H.-Y. Li, J.-Q. Yuan, J.-A. Cheng, R. Xu, C. Mao & Z.-R. Zhu, 2013. Identification and biochemical characterization of Laodelphax striatellus neutral ceramidase. Insect Molecular Biology 22: 366–375.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The Research Council of Lithuania supported the proteomic study, Project No. MIP-135/2010 as well as the gene expression investigation, Project No. MIP-031/2012. The manuscript substantially benefited from the comments of peer referees and the advice of Adam Petrusek, the editor of the volume.

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Authors and Affiliations

  1. Proteomics Center, Institute of Biochemistry, Vilnius University, Saulėtekio al. 7, 10257, Vilnius, Lithuania

    Algirdas Kaupinis & Mindaugas Valius

  2. Department of Botany and Genetics, Institute of Biosciences, Vilnius University, Saulėtekio al. 7, 10257, Vilnius, Lithuania

    Lina Aitmanaitė, Dovilė Strepetkaitė & Juozas R. Lazutka

  3. Nature Research Centre, Akademijos Str. 2, 08412, Vilnius, Lithuania

    Kęstutis Arbačiauskas

  4. Department of Zoology, Institute of Biosciences, Vilnius University, Saulėtekio al. 7, 10257, Vilnius, Lithuania

    Algirdas Kaupinis & Kęstutis Arbačiauskas

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Guest editors: Adam Petrusek & Piet Spaak / Proceedings of the 10th International Symposium on Cladocera

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Kaupinis, A., Aitmanaitė, L., Strepetkaitė, D. et al. Proteomic and gene expression differences between post-diapause and subitaneous offspring phenotypes in the cyclic parthenogen Daphnia pulex . Hydrobiologia 798, 87–103 (2017). https://doi.org/10.1007/s10750-016-3057-3

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