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The expression pattern of dormancy-associated genes in multiple life-history stages in the rotifer Brachionus plicatilis

  • ROTIFERA XII
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Abstract

Rotifer resting eggs retain their viability for several decades in a non-desiccated form and are of interest in discerning the processes associated with dormancy, since in most organisms this phenomenon is linked with desiccation. The expression pattern of candidate genes with biological functions associated with dormancy in several other organisms was examined in rotifers. High-throughput transcriptome profiling revealed three patterns of gene expression in resting eggs: (1) relatively highly expressed genes coding for LEA proteins and putative paralogs of the small heat shock protein family (shsp); (2) genes coding for ferritin (ferr), glutathione-6-transferase (gts) and HSP70, where some of the putative gene paralogs of these families show relatively high expression levels and other putative paralogs show relatively low expression levels in resting eggs; and (3) genes with relatively low expression levels in resting eggs, for trehalose-6-phosphate synthase (tps), fatty-acid binding proteins (fab) and of lipoprotein lipase (lpl) and the aquaporins gene family (aqp). Changes in the expression pattern of some members of putative gene families occurred during the obligatory dormant period of resting eggs. A transition was observed from an expression pattern of diapausing embryos to an expression pattern of amictic females, during hatching. Differences were also found in the expression pattern in the different types of females, especially in those carrying resting eggs, and in males compared with females. These results suggest putative functional significance to genes associated with dormancy in non-desiccated resting eggs. It could also be proposed that their occurrence in resting eggs is developmentally programmed to facilitate survival in case of desiccation.

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References

  • Audic, S. & J. M. Claverie, 1997. The significance of digital gene expression profiles. Genome Research 7: 986–995.

    CAS  PubMed  Google Scholar 

  • Avonce, N., B. Leyman, J. O. Mascorro-Gallardo, P. Van Dijk, J. M. Thevelein & G. Iturriaga, 2004. The Arabisopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiology 136: 3649–3659.

    Article  CAS  PubMed  Google Scholar 

  • Ayyadevara, S., A. Dandapat, S. P. Singh, E. R. Siegel, R. J. Shmookler Reis, L. Zimniak & P. Zimniak, 2007. Life span and stress resistance of Caenorhabditis elegans are differentially affected by glutathione transferases metabolising 4-hydroxynon-2-enal. Mechanisms of Ageing and Development 128: 196–205.

    Article  CAS  PubMed  Google Scholar 

  • Bailly, C., H. El-Maarouf-Bouteau & F. Corbineau, 2008. From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C.R. Biologies 331: 806–814.

    Article  CAS  PubMed  Google Scholar 

  • Balompapueng, M. D., A. Hagiwara, Y. Nozaki & K. Hirayama, 1997. Preservation of resting eggs of the euryhaline rotifer Brachionus plicatilis O.F. Müller by canning. Hydrobiologia 358: 163–166.

    Article  Google Scholar 

  • Berjak, B., 2006. Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Science Research 16: 1–15.

    Article  CAS  Google Scholar 

  • Briat, J.-F., K. Ravet, A. Nicolas, C. Duc, J. Voucherez, B. Touraine, F. Cellier & F. Gaymard, 2009. New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants. Annals of Botany 105(5): 811–822.

    Article  PubMed  Google Scholar 

  • Caprioli, M., A. K. Katholm, G. Melone, H. Ramlov, C. Ricci & N. Santo, 2004. Trehalose in desiccated rotifers: a comparison between a bdelloid and a monogonont species. Comparative Biochemistry and Physiology A 139: 527–532.

    Article  Google Scholar 

  • Chakrabortee, S., C. Boschetti, L. I. Walton, S. Sarkar, D. Rubinsztein & A. Tunnacliffe, 2007. Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proceedings of the National Academy of Science 104: 18073–18078.

    Article  CAS  Google Scholar 

  • Chen, T., T. S. Villeneuve, K. A. Garant, R. Amons & T. H. MacRae, 2007. Functional characterisation of artemin, a ferritin homolog synthesised in Artemia embryos during encystment and diapause. The FEBS Journal 274: 1093–1101.

    Article  CAS  PubMed  Google Scholar 

  • Clark, M. S., M. A. Thorne, J. Purać, G. Grubor-Lajsić, M. Kube, R. Reinhardt & M. R. Worland, 2007. Surviving extreme polar winters by desiccation: clues from Arctic springtail (Onychiurus arcticus) EST libraries. BMC Genomics 8: 475.

    Article  PubMed  Google Scholar 

  • Clegg, J. S., 2001. Cryptobiosis – apecular state of biological organization. Comparative Physiology and Biochemistry Molecular Biology 128: 613–624.

    Article  CAS  Google Scholar 

  • Crowe, J. H. & L. M. Crowe, 2000. Preservation of mammalian cells – learning nature’s tricks. Nature Biotechnology 18: 145–146.

    Article  CAS  PubMed  Google Scholar 

  • Dark, J., 2005. Annual lipid cycles in hibernators: integration of physiology and behavior. Annual Review of Nutrition 25: 469–497.

    Article  CAS  PubMed  Google Scholar 

  • Denekamp, N. Y., M. A. S. Thorne, M. S. Clark, M. Kube, R. Reinhardt & E. Lubzens, 2009. Discovering genes associated with dormancy in the monogont rotifer Brachionus plicatilis. BMC Genomics 10: 108.

    Article  PubMed  Google Scholar 

  • Denekamp, N. Y., M. Kube, R. Reinhardt & E. Lubzens, 2010. Presence of Late embryogenesis abundant (LEA) proteins in a non-desiccated, diapausing invertebrate embryo. Biology of Reproduction 82: 714–724.

    Article  CAS  PubMed  Google Scholar 

  • Epperson, L. E., T. A. Dahl & S. L. Martin, 2004. Quantitative analysis of liver protein expression during hibernation in the golden-mantled ground squirrel. Molecular and Cellular Proteomics 3: 920–933.

    Article  CAS  PubMed  Google Scholar 

  • Force, A., M. Lynch, F. B. Pickett, A. Amores, Y. Yan & J. Postlethwait, 1999. Preservation of duplicate genes by complementary, generative mutations. Genetics 151: 1531–1545.

    CAS  PubMed  Google Scholar 

  • Frova, C., 2006. Glutathione transferases in the genomics era: new insights and perspectives. Bioengineering 23: 149–169.

    CAS  Google Scholar 

  • Gilbert, J. J., 1989. Rorifera. In: Reproductive biology of invertebrates. In Adiyodi, K. G. & R. G. Adiyodi (eds), Sexual differentiation and behaviour, Vol V. Oxford & IBH Publishing Co. Pvt. Ltd, New Delhi: 115–136.

  • Gilbert, J. J., 2004a. Population density, sexual reproduction and diapause in monogonont rotifers: new data for Brachionus and a review. Journal of Limnology 63(Suppl 1): 32–36.

    Google Scholar 

  • Gilbert, J. J., 2004b. Females from resting eggs and parthenogenic eggs in the rotifer Brachionus calyciflorus: lipid droplets, starvation resistance and reproduction. Freshwater Biology 49: 1505–1515.

    Article  Google Scholar 

  • Gilbert, J. J., 2007. Timing of diapause in monogonont rotifers: mechanisms and strategies. In Alekseev, V. R., B. De Stasio & J. J. Gilbert (eds), Diapause in Aquatic Invertebrates: Theory and Human Use. Springer, Dordrecht: 11–27.

    Chapter  Google Scholar 

  • Hagiwara, A., 1996. Use of resting eggs for mass preservation of marine rotifers. Technical Reports of Japanese Sea Ranching Programs 24: 109–120. (In Japanese).

    Google Scholar 

  • Hagiwara, A., N. Hoshi, F. Kawahara, K. Tominaga & K. Hirayama, 1995. Resting eggs of the marine rotifer Brachionus plicatilis Muller: development and effect of irradiation on hatching. Hydrobiologia 313(314): 223–229.

    Article  Google Scholar 

  • Hagiwara, A., Y. Kadota & A. Hino, 2005. Maternal effect by stem females in Brachionus plicatilis: effect of starvation on mixis induction in offspring. Hydrobiologia 546: 275–279.

    Article  Google Scholar 

  • Hughes, L. A. & R. Friedman, 2007. Sharing of transcription factors after gene duplication in the yeast Saccharomuces cerevisiae. Genetica 129: 301–308.

    Article  CAS  PubMed  Google Scholar 

  • Kaneko, G., S. Kinoshita, T. Yoshinaga, K. Tsukamoto & S. Watabe, 2002. Changes in expression patterns of stress protein genes during population growth of the rotifer Brachionus plicatilis. Fisheries Sciences 68: 1317–1323.

    Article  CAS  Google Scholar 

  • Kaneko, G., T. Yoshinaga, Y. Yanagawa, S. Kinoshita, K. Tsukamoto & S. Watabe, 2005. Molecular characterization of Mn-superoxide dismutase and gene expression studies in dietary restricted Brachionus plicatilis rotifers. Hydrobiologia 546: 117–123.

    Article  CAS  Google Scholar 

  • Keilin, D., 1959. The problem of anabiosis of latent life: history and current concept. Proceedings of the Royal Society Biological Sciences 150: 149–191.

    Article  CAS  Google Scholar 

  • Kondrashov, F. A. & A. S. Kondrashov, 2006. Role of selection in fixation of gene duplications. Journal of Theoretical Biology 239: 141–151.

    Article  CAS  PubMed  Google Scholar 

  • Kotani, T., M. Ozaki, K. Matsuoka, T. W. Snell & A. Hagiwara, 2001. Reproductive isolation among geographically and temporally isolated marine Brachionus strains. Hydrobiologia 446(447): 283–290.

    Article  Google Scholar 

  • Li, R., Y. Li, K. Kristiansen & J. Wang, 2008. SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713–714.

    Article  CAS  PubMed  Google Scholar 

  • Lubzens, E. & O. Zmora, 2003. Production and nutritional value of rotifers. In Stottrup, J. G. & L. A. McEvoy (eds), Live Feeds in Marine Aquaculture. Blackwell Publishing, Oxford: 17–64 (Appendix I 300–303).

  • Lubzens, E., G. Minkoff & S. Marom, 1985. Salinity dependence of sexual and asexual reproduction in the rotifer Brachionus plicatilis. Marine Biology 85: 23–126.

    Article  Google Scholar 

  • Lubzens, E., O. Gibson, O. Zmora & A. Sukenik, 1995. Potential advantages of frozen algae (Nannochloropsis sp.) for rotifer (Brachionus plicatilis) culture. Aquaculture 133: 295–309.

    Article  Google Scholar 

  • Lynch, M. & A. Force, 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459–473.

    CAS  PubMed  Google Scholar 

  • Minkoff, G., E. Lubzens & D. Kahan, 1983. Environmental factors affecting hatching of rotifer (Brachionus plicatilis) resting eggs. Hydrobiolgia 104: 61–169.

    Article  Google Scholar 

  • Pauwels, K., R. Stoks, A. Verbiest & L. De Meester, 2007. Biochemical adaptation for dormancy in subitaneous and dormant eggs of Daphnia magna. Hydrobiologia 594: 91–96.

    Article  CAS  Google Scholar 

  • Pellerone, F. L., S. K. Archer, C. A. Behm, W. N. Grant, M. J. Lacey & A. C. Somerville, 2003. Trehalose metabolism genes in Caenorhabditis elegans and filarial nematodes. International Journal of Parasitology 33: 1195–1206.

    Article  CAS  PubMed  Google Scholar 

  • Plenzler, G., 2006. Presence of aquaporins in desiccation process in pea seeds. Acta Agrophysica 7: 171–178.

    Google Scholar 

  • Schröder, T., 2005. Diapause in monogonont rotifers. Hydrobiologia 546: 291–306.

    Article  Google Scholar 

  • Serra, M. & C. E. King, 1999. Optimal rates of bisexual reproduction in cyclical parthenogens with density-dependent growth. Journal of Evolutionary Biology 12: 263–271.

    Article  Google Scholar 

  • Sharon, M. A., A. Korzarova, J. S. Clegg, P. O. Vacratsis & A. H. Warner, 2009. Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia francisacana. Biochemistry and Cellular Biology 87: 415–4310.

    Article  CAS  Google Scholar 

  • Snell, T. W., J. Kubanek, W. Carter, A. B. Payne, J. Kim, M. K. Hicks & C. P. Stelzer, 2006. A protein signal triggers sexual reproduction in Brachionus plicatilis (rotifera). Marine Biology 149: 763–773.

    Article  CAS  Google Scholar 

  • Storey, K. B., 2003. Mammalian hibernation. Transcriptional and translational controls. Advances of Experimental Medicine and Biology 543: 21–38.

    CAS  Google Scholar 

  • Storey, K. B. & J. M. Storey, 2007. Tribute to P.L.Lutz: putting life on ‘pause’ – molecular regulation of hypometabolism. Journal of Experimental Biology 210: 1700–1714.

    Article  CAS  PubMed  Google Scholar 

  • Suga, K., D. Mark Welch, Y. Tanaka, Y. Sakakura & A. Hagiwara, 2007. Analysis of expressed sequence tags of the cyclically parthenogenetic rotifer Brachionus plicatilis. PLoS One 2: e671.

    Article  PubMed  Google Scholar 

  • Suga, K., D. Mark Welch, Y. Tanaka, Y. Sakakura & A. Hagiwara, 2008. Two circular chromosomes of unequal copy number make up the mitochondrial genome of the rotifer Brachionus plicatilis. Molecular Biology and Evolution 25: 1129–1137.

    Article  CAS  PubMed  Google Scholar 

  • Tunnacliffe, A. & M. J. Wise, 2007. The continuing conundrum of LEA proteins. Naturwissenschaften 94: 791–812.

    Article  CAS  PubMed  Google Scholar 

  • Tunnacliffe, A., J. Lapinski & B. McGree, 2005. A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546: 315–321.

    Article  CAS  Google Scholar 

  • Walters, C., L. M. Hill & L. J. Wheeler, 2005. Dying while dry: kinetics and mechanisms of deterioration in desiccated organisms. Integrative and Comparative Biology 45: 751–758.

    Article  Google Scholar 

  • Wang, J. & S. K. Kim, 2003. Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130: 1621–1634.

    Article  CAS  PubMed  Google Scholar 

  • Wheelock, C. E., T. A. Baumgartner, J. W. Newman, M. F. Wolfe & R. S. Tjeerdema, 2002. Effect of nutritional state on Hsp60 levels in the rotifer Brachionus plicatilis following toxicant exposure. Aquatic Toxicology 61: 89–93.

    Article  CAS  PubMed  Google Scholar 

  • Wurdak, E. S., J. J. Gilbert & R. Jagels, 1978. Fine structure of the resting eggs of the rotifers Brachionus calyciflorus and Asplanchna sieboldi. Transactions of the American Mircoscopical Society 97: 49–72.

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the European Commission (NEST #12674; Sleeping Beauty). The technical help of Irena Perkaski and Alisa Hadani is highly appreciated. We acknowledge the Illumina sequencing by the ngs-group of MPI-MG. We would also like to thank two anonymous reviewers for their useful comments and Dr. M. S. Clark (British Antarctic Survey, Natural Environment Research Council, Cambridge, UK) for useful discussions.

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Authors and Affiliations

  1. Israel Oceanographic and Limnological Research, P. O. Box 8030, Haifa, 31080, Israel

    N. Y. Denekamp & E. Lubzens

  2. Max Planck Institute for Molecular Genetics, Berlin-Dahlem, Germany

    R. Reinhardt, M. W. Albrecht, M. Drungowski & M. Kube

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  1. N. Y. Denekamp
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  2. R. Reinhardt
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  3. M. W. Albrecht
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  4. M. Drungowski
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  5. M. Kube
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  6. E. Lubzens
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Correspondence to E. Lubzens.

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Guest editors: N. Walz, R. Adrian, J.J. Gilbert, M.T. Monaghan, G. Weithoff & H. Zimmermann-Timm / Rotifera XII: New aspects in rotifer evolution, genetics, reproduction, ecology and biogeography

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Denekamp, N.Y., Reinhardt, R., Albrecht, M.W. et al. The expression pattern of dormancy-associated genes in multiple life-history stages in the rotifer Brachionus plicatilis . Hydrobiologia 662, 51–63 (2011). https://doi.org/10.1007/s10750-010-0518-y

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