Abstract
Salinity is a significant factor in affecting resting egg hatching in the euryhaline rotifers. In order to clarify the effects of salinity on resting egg hatchability, this study investigated gene expressions of resting eggs subjected to two different incubation salinities (at 17 and 33 ppt) in the rotifer Brachionus manjavacas. The resting eggs formed at 17 ppt showed a higher hatching rate at 17 ppt incubation salinity, compared to those at 33 ppt. Related to these circumstances, the resting eggs incubated at 17 ppt expressed genes which have putative functions implying cellular differentiation and embryonic development: late embryogenesis abundant protein (LEAs-1), α-amylase, and deaminase. The resting eggs incubated at 33 ppt highly expressed the genes related to the environmental stresses: AP2 transcription factors (AP2TF), and ATP decomposition: ABC transporter permease (ABC-TP), NAD + synthase, copper-translocating P-type ATPase (CTP-ATPase). It is expected that the resting eggs incubated at 33 ppt may need more energy (ATP) to endure saline stress during incubation. The obtained results indicated that the resting eggs regulate their hatching by allocating energy between embryo development and self-defense against environmental conditions like salinity stresses.
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Abogadallah GM, Nada RM, Malinowski R, Quick P (2011) Overexpression of HARDY, an AP2/ERF gene from Arabidopsis, improves drought and salt tolerance by reducing transpiration and sodium uptake in transgenic Trifolium alexandrinum L. Planta 233:1265–1276
Bahnson BJ, Anderson VE, Petsko GA (2002) Structural mechanism of enoyl-CoA hydratase: three atoms from a single water are added in either an E1cb stepwise or concerted fashion. Biochemistry 41:2621–2629
Berjak P, Pammenter NW, Adkins SW, Ashmore S, Navie SC (2007) Recent progress towards the understanding of desiccation tolerance. Seeds: biology, development and ecology. Cabi Publishing-CAB Int, Wallingford, pp 17–27
Cao H, Sekiya M, Erikci M, Burak MF, Mayers JR, White A, Inouye K, Rickey LM, Ercal BC, Furuhashi M, Tuncman G, Hotamisligil GS (2013) Adipocyte lipid chaperone aP2 is a secreted adipokine regulating hepatic glucose production. Cell Metab 17:768–778
Chinnery FE, Williams JA (2004) The influence of temperature and salinity on Acartia (Copepoda: Calanoida) nauplii survival. Mar Biol 145:733–738
Clark MS, Denekamp NY, Thorne MAS, Richard R, Mario D, Albrecht MW (2012) Long-term survival of hydrated resting eggs from Brachionus plicatilis. PLoS ONE 7:e293-65
Demontis S, Terao M, Brivio M, Zanotta S, Bruschi M, Garattini E (1999) Isolation and characterization of the gene coding for human cytidine deaminase. Biochim Biophys Acta 1443:323–333
Devreker D, Souissi S, Winkler G, Leboulenger F (2009) Effects of salinity, temperature and individual variability on the reproduction of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: a laboratory study. J Exp Mar Biol Ecol 368:113–123
Galau GA, Hughes DW, Dure L (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7:155–170
Gautam A, Liu HW (2003) Enoyl-Coa hydratase: Reaction, mechanism, and inhibition. Bioorg Med Chem 11:9–20
Gilbert JJ (2003) Environmental and endogenous control of sexuality in a rotifer lifecycle: developmental and population biology. Evol Dev 5:19–24
Hagiwara A, Hino A (1990) Feeding history and hatching of resting eggs in the marine rotifer Brachionus plicatilis. Nippon Suisan Gakkaishi 56:1965–1971
Hagiwara A, Hoshi N, Kawahara F, Tominaga K, Hirayama K (1995) Resting eggs of the marine rotifer Brachionus plicatilis Müller: development, and effect of irradiation on hatching. Hydrobiologia 313:223–229
Henze K, Martin W (2003) Evolutionary biology: essence of mitochondria. Nature 426:127–128
Inesi G, Pilankatta R, Tadinibuoninsegni F (2014) Biochemical characterization of P-type copper ATPases. Biochem J 463:167–176
John JG (2016) Resting-egg hatching and early population development in rotifers: a review and a hypothesis for differences between shallow and deep waters. Hydrobiologia 186:1–9
Kim HJ, Hagiwara A (2011a) Effect of female aging on the morphology and hatchability of resting eggs in the rotifer Brachionus plicatilis Müller. Hydrobiologia 662:107–111
Kim HJ, Hagiwara A (2011b) Effect of salinity during resting egg formation and hatching on descendent reproduction in the rotifer Brachionus rotundiformis Tschugunof. J Plankton Res 33:1033–1042
Kim RO, Rhee JS, Won EJ, Lee KW, Kang CM, Lee YM, Lee JS (2011) Ultraviolet B retards growth, induces oxidative stress, and modulates DNA repair-related gene and heat shock protein gene expression in the monogonont rotifer, Brachionus sp. Aquat Toxicol 101:529–539
Kim RO, Kim BM, Jeong CB, Nelson DR, Lee JS, Rhee JS (2013) Expression pattern of entire cytochrome P450 genes and response of defensomes in the benzo [a] pyrene-exposed monogonont rotifer Brachionus koreanus. Environ Sci Technol 47:13804–13812
Kim BM, Lee JW, Seo JS, Shin KH, Rhee JS, Lee JS (2014a) Modulated expression and enzymatic activity of the monogonont rotifer Brachionus koreanus Cu/Zn- and Mn-superoxide dismutase (SOD) in response to environmental biocides. Chemosphere 120:470–478
Kim HJ, Sawada C, Rhee JS, Lee JS, Suga K, Hagiwara A (2014b) Nutritional effects on the visual system of the rotifer Brachionus plicatilis sensu stricto (Rotifera: Monogononta). J Exp Mar Biol Ecol 460:177–183
Kim HJ, Suga K, Kim BM, Rhee JS, Lee JS, Hagiwara A (2015) Light-dependent transcriptional events during resting egg hatching of the rotifer Brachionus manjavacas. Mar Genom 20:25–31
Kuhn K, Bertling WM, Emmrich F (1993) Cloning of a functional cDNA for human cytidine deaminase (CDD) and its use as a marker of monocyte/macrophage differentiation. Biochem Biophys Res Commun 190:1–7
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408
Lowe CD, Kemp SJ, Bates AD, Montagness DJS (2005) Evidence that the rotifer Brachionus plicatili is not an osmoconformer. Mar Biol 146:923–929
Lubzens E, Fishler R, White VB (1980) Induction of sexual reproduction and resting egg production in Brachionus plicatilis reared in sea water. Hydrobiologia 73:55–58
McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr Biol 16:551–560
Michalec EG, Souissi S, Dur G, Mahjoub MS, Schmitt FG, Hwang JS (2010) Differences in behavioral responses of Eurytemora affinis (Copepoda, Calanoida) reproductive stages to salinity variations. J Plankton Res 32:805–813
Pourriot R, Snell T (1983) Resting eggs in rotifers. Hydrobiologia 104:213–224
Rhee JS, Kim RO, Choi HG, Lee J, Lee YM, Lee JS (2011) Molecular and biochemical modulation of heat shock protein 20 (Hsp20) gene by temperature stress and hydrogen peroxide (H2O2) in the monogonont rotifer, Brachionus sp. Comp Biochem Physiol C 154:19–27
Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827
Snell TW (1987) Sex, population dynamics and resting egg production in rotifers. Hydrobiologia 144:105–111
Stedman TL (2000) Stedman’s medical dictionary. 27th edn. Lippincott Williams and Wilkins. Baltimore, Maryland, USA, p 65
Thorpe C, Kim JJ (1995) Structure and mechanism of action of the acyl-CoA dehydrogenases. Faseb J Off Publ Fed Am Soc Exp Biol 9:718–725
Tunnacliffe A, Hincha DK, Leprince O, Macherel D (2010) LEA proteins: versatility of form and function. In: Lubzens E, Cerda J, Clark M (eds) Sleeping beauties: dormancy and resistance in harsh environments. Springer, Berlin, pp 91–108
Wheelock CE, Wolfe MF, Olsen H, Tjeerdema RS, Sowby ML (1999) Hsp60-induced tolerance in the rotifer Brachionus plicatilis exposed to multiple environmental contaminants. Arch Environ Contam Toxicol 36:281–367
Wolanin PW, Thomason PA, Stock JB (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3:3013.1–3013.8
Yang T, Zhang L, Zhang T, Zhang H, Xu S, An L (2005) Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci 169:987–995
Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Li W, Zhang H (2010) The Arabidopsis AP2/ERF transcription factor RAP2. 6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12
Acknowledgements
This research was supported by JSPS KAKENHI Grant Number JP17H03862 and 15K14791 to Atsushi Hagiwara. The authors deeply appreciate the comments and suggestions from Dr. Helen Marcial and the anonymous reviewers who greatly improved the manuscript.
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Han, C., Kim, HJ., Suga, K. et al. Comparison of resting egg gene expression with different hatchability related to salinity variations in the marine rotifer Brachionus manjavacas. Fish Sci 84, 663–669 (2018). https://doi.org/10.1007/s12562-018-1213-6
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DOI: https://doi.org/10.1007/s12562-018-1213-6