Stress induced «railway for pre-ribosome export» structure as a new model for studying eukaryote ribosome biogenesis

E.N. Baranova; R.M. Sarimov; A.A. Gulevich; E.N. Baranova; R.M. Sarimov; A.A. Gulevich

doi:10.3934/biophy.2019.2.47

AIMS Biophysics

2019, Volume 6, Issue 2: 47-67. doi: 10.3934/biophy.2019.2.47

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Stress induced «railway for pre-ribosome export» structure as a new model for studying eukaryote ribosome biogenesis

1.
All-Russia Research Institute of Agricultural Biotechnology, Timiriazevskaya 42, 127550 Moscow, Russia
2.
Prokhorov General Physics Institute of the Russian Academy of Sciences, GPI RAS, 38 Vavilov str., 119991 Moscow, Russia
3.
Institute of Plant Physiology of the Russian Academy of Sciences, Moscow, Russia

Received: 03 April 2019 Accepted: 01 July 2019 Published: 18 July 2019

Abstract
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The article presents the details of the process of structural organization, formation and disassembly of the nucleolus, chromatin condensation during the passage of the cell cycle studied by the method of classical transmission electron microscopy (TEM) in the cells of the meristematic zone of the wheat root. The transformations of peripheral chromosome material (PCM) in telophase, the transformations of the nucleolar nucleolonema in the interphase and prophase, and the chromatin transformations (condensation and decondensation) were studied and analyzed under the conditions of the geomagnetic field, weakened magnetic field and static magnetic field. Using an analysis of the dynamics of structural transformations of proliferating nuclei, we observed a disturbance in the formation of the chromonema and condensed chromatin in the middle interphase, a change in the structural organization of the nucleolus during the transition from late interphase to prophase, as well as a change in the structure of PCM, pre-nucleolus and chromatin in telophase. A schema for the generation of a specific conformation of nucleolonema and chromonema and its influence on the structural organization of chromosomes in anaphase and telophase was proposed. The nature of this structure is discussed. Possible mechanisms of the effect of magnetic field on the nuclear compartment, regulation of chromatin decompactization, export of pre-ribosomal particles under stress, and the fine structure of the nucleolonema are considered.
- weakened magnetic field,
- cold,
- chromonema,
- nucleolonema,
- nucleolus,
- ribosome biogenesis
Citation: E.N. Baranova, R.M. Sarimov, A.A. Gulevich. Stress induced «railway for pre-ribosome export» structure as a new model for studying eukaryote ribosome biogenesis[J]. AIMS Biophysics, 2019, 6(2): 47-67. doi: 10.3934/biophy.2019.2.47

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Abstract

The article presents the details of the process of structural organization, formation and disassembly of the nucleolus, chromatin condensation during the passage of the cell cycle studied by the method of classical transmission electron microscopy (TEM) in the cells of the meristematic zone of the wheat root. The transformations of peripheral chromosome material (PCM) in telophase, the transformations of the nucleolar nucleolonema in the interphase and prophase, and the chromatin transformations (condensation and decondensation) were studied and analyzed under the conditions of the geomagnetic field, weakened magnetic field and static magnetic field. Using an analysis of the dynamics of structural transformations of proliferating nuclei, we observed a disturbance in the formation of the chromonema and condensed chromatin in the middle interphase, a change in the structural organization of the nucleolus during the transition from late interphase to prophase, as well as a change in the structure of PCM, pre-nucleolus and chromatin in telophase. A schema for the generation of a specific conformation of nucleolonema and chromonema and its influence on the structural organization of chromosomes in anaphase and telophase was proposed. The nature of this structure is discussed. Possible mechanisms of the effect of magnetic field on the nuclear compartment, regulation of chromatin decompactization, export of pre-ribosomal particles under stress, and the fine structure of the nucleolonema are considered.

Acknowledgment

The research was performed on the state assignment AAAA-A18-118051890089-0.

Conflict of interest

The authors declare no competing financial interests.

References

[1]	Tarduno JA, Cottrell RD, Davis WJ, et al. (2015) A Hadean to Paleoarchean geodynamo recorded by single zircon crystals. Science 349: 521‒524.
[2]	Martin A, McMinn A (2018) Sea ice, extremophiles and life on extra-terrestrial ocean worlds. Int J Astrobiol 17: 1‒16.
[3]	Stevenson DJ (2003) Planetary magnetic fields. Earth Planet Sci Lett 208: 1‒11.
[4]	Purucker ME, Clark DA (2011) Mapping and interpretation of the lithospheric magnetic field. In: Mandea M, Korte M, Geomagnetic Observations and Models. Dordrecht: Springer, 311‒337.
[5]	Da Silva JAT, Dobránszki J (2016) Magnetic fields: how is plant growth and development impacted? Protoplasma 253: 231‒248.
[6]	Cucinotta FA, Cacao E (2017) Non-targeted effects models predict significantly higher mars mission cancer risk than targeted effects models. Sci Rep 7: 1832. doi: 10.1038/s41598-017-02087-3
[7]	Agliassa C, Maffei ME (2019) Reduction of geomagnetic field (GMF) to near null magnetic field (NNMF) affects some Arabidopsis thaliana clock genes amplitude in a light independent manner. J Plant Physiol 232: 23‒26.
[8]	Novitskii YI, Novitskaya GV (2016) Action of Permanent Magnetic Field on Plants, Moscow: Nauka.
[9]	Maffei ME (2014) Magnetic field effects on plant growth, development, and evolution. Front Plant Sci 5: 445.
[10]	Binhi VN, Prato FS (2017) Biological effects of the hypomagnetic field: an analytical review of experiments and theories. Plos One 12: e0179340. doi: 10.1371/journal.pone.0179340
[11]	Galland P, Pazur A (2005) Magnetoreception in plants. J Plant Res 118: 371‒389.
[12]	Belyavskaya NA (2001) Ultrastructure and calcium balance in meristem cells of pea roots exposed to extremely low magnetic fields. Adv Space Res 28: 645-650. doi: 10.1016/S0273-1177(01)00373-8
[13]	Belyavskaya NA (2004) Biological effects due to weak magnetic field on plants. Adv Space Res 34: 1566-1574. doi: 10.1016/j.asr.2004.01.021
[14]	Belyavskaya NA, Fomicheva VM, Govorun RD, et al. (1992) Structure-functional organization of meristem cells of pea, flax and lentil roots under conditions of the geomagnetic field screening. Biofizika 37: 759-768.
[15]	Baranova EN, Baranova GB, Kharchenko PN (2011) Effect of weak magnetic field and low positive temperature on chromatin and nucleolus ultrastructure of rye and barley. Russ Agric Sci 37: 453‒461.
[16]	Mo WC, Zhang ZJ, Liu Y, et al. (2013) Magnetic shielding accelerates the proliferation of human neuroblastoma cell by promoting G1-phase progression. Plos One 8: e54775. doi: 10.1371/journal.pone.0054775
[17]	Mo WC, Zhang ZJ, Wang DL, et al. (2016) Shielding of the geomagnetic field alters actin assembly and inhibits cell motility in human neuroblastoma cells. Sci Rep 6:1-15. doi: 10.1038/s41598-016-0001-8
[18]	Belyaev IY, Alipov YD, Harms-Ringdahl M (1997) Effects of zero magnetic field on the conformation of chromatin in human cells. Biochim Biophys Acta Gen Sub 1336:465-473. doi: 10.1016/S0304-4165(97)00059-7
[19]	Lee SK, Park S, Kim YW (2016) The effects of extremely low-frequency magnetic fields on reproductive function in rodents. In: Insights from Animal Reproduction.
[20]	Sarimov R, Malmgren LOG, Markova E, et al. (2004) Nonthermal GSM microwaves affect chromatin conformation in human lymphocytes similar to heat shock. IEEE Trans Plasma Sci 32: 1600‒1608.
[21]	Sarimov R, Alipov ED, Belyaev IY (2011) Fifty hertz magnetic fields individually affect chromatin conformation in human lymphocytes: dependence on amplitude, temperature, and initial chromatin state. Bioelectromagnetics 32: 570‒579.
[22]	Maffei ME (2019) Plant Responses to Electromagnetic Fields, In: Greenebaum B, Barnes F, Biological and Medical Aspects of Electromagnetic Fields, 4 Eds., CRC Press, 89‒110.
[23]	Binhi VN (2016) Primary physical mechanism of the biological effects of weak magnetic fields. Biophysics 61: 170‒176.
[24]	Shatalov VM (2009) Degasation of bioliquids as the target of weak electromagnetic field biological effects. Biophys Bull 23: 92‒99.
[25]	Silletta EV, Tuckerman ME, Jerschow A (2018) Unusual proton transfer kinetics in water at the temperature of maximum density. Phys Rev Lett 121: 076001. doi: 10.1103/PhysRevLett.121.076001
[26]	Kalinina NO, Makarova S, Makhotenko A, et al. (2018) The multiple functions of the nucleolus in plant development, disease and stress responses. Front Plant Sci 9: 132. doi: 10.3389/fpls.2018.00132
[27]	Sirri V, Jourdan N, Hernandez-Verdun D, et al. (2016) Sharing of mitotic pre-ribosomal particles between daughter cells. J Cell Sci 129: 1592‒1604.
[28]	Sato S, Myoraku A (1994) Three-dimensional organization of nuclear DNA in the higher plant nucleolonema studied by immunoelectron microscopy. Micron 25: 431‒437.
[29]	Henras AK, Plisson‐Chastang C, O'Donohue MF, et al. (2015) An overview of pre‐ribosomal RNA processing in eukaryotes. Wiley Interdiscip Rev: RNA 6: 225‒242.
[30]	Schellhaus AK, De Magistris P, Antonin W (2016) Nuclear reformation at the end of mitosis. JMol Biol 428: 1962‒1985.
[31]	Petrovská B, Šebela M, Doležel J (2015) Inside a plant nucleus: discovering the proteins. J Exp Bot 66: 1627‒1640.
[32]	Sato S (1992) Three‐dimensional architecture of the higher plant nucleolonema disclosed on serial ultrathin sections. Biol Cell 75: 225‒233.
[33]	Bernhard W (1969) A new staining procedure for electron microscopical cytology. J Ultrastruct Res 27: 250‒265.
[34]	Lafontaine JG, Lord AA (1974) Correlated light and electron microscope investigation of the structural evolution of the nucleolus during the cell cycle in plant meristematic cells (Allium porrum). J Cell Sci 16: 63‒93.
[35]	Baranova EN, Gulevich AA (2009) Structural organization of nuclei and nucleoli of wheat shoot and root meristem during germination under alkaline pH conditions. Russ Agri Sci 35: 11‒14.
[36]	Baranova EN, Gulevich AA, Lavrova NV (2010) Vliyanie kisloj rN sredy na strukturnuyu organizaciyu yader i yadryshek kletok pobegovoj i kornevoj meristem pshenicy pri prorastanii (in Russian) Influence of acid pH of the environment on the structural organization of nuclei and nucleoli of cells of shoot and root meristems of wheat during germination. Izv Timiryazevsk S Kh Akad 2: 44-51.
[37]	Wang J, Zhang F (2015) Nucleolus disassembly and distribution of segregated nucleolar material in prophase of root-tip meristematic cells in Triticum aestivum L. Arch Biol Sci 67: 405‒410.
[38]	Zharskaya OO, Zatsepina OV (2007) The dynamics and mechanisms of nucleolar reorganization during mitosis. Cell Tiss Biol 1: 277‒292.
[39]	Avetisova LV, Kadykov VA (1985) Ul'trastruktura kletok apikal'noj meristemy pobega pshenicy, razvivayushchegosya pri nizkih temperaturah (in Russian) Ultrastructure of wheat apical meristem cells at low positive temperatures, 1: Nuclear structure. Tsitologiya 27: 28-32.
[40]	Avetisova LV, Shaposhnikov JD, Kadykov VA (1988) Izmeneniya ul'trastruktury yader kletok apeksa pobega pshenicy v processe prorastaniya (in Russian) Changes in the ultrastructure of nuclei in cells of the apical meristem during germination of wheat. Ontogenez 19: 181-190.
[41]	Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Phys 55: 1859‒1863.
[42]	Baranova EN, Chaban IA, Kononenko NV, et al. (2017) Ultrastructural organization of the domains in the cell nucleus of dicotyledonous and monocotyledonous plants under abiotic stress. Russ Agri Sci 43: 199‒206.
[43]	Yang X, Timofejeva L, Ma H, et al. (2006) The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J Cell Sci 119: 3754‒3763.
[44]	West G, Inzé D, Beemster GT (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Phys 135: 1050-1058. doi: 10.1104/pp.104.040022
[45]	Skirycz A, Claeys H, De Bodt S, et al. (2011) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23: 1876-1888. doi: 10.1105/tpc.111.084160
[46]	Lord A, Lafontaine JG (1969) The organization of the nucleolus in meristematic plant cells: a cytochemical study. J Cell Biol 40: 633‒647.
[47]	Hozak P, Zatsepina O, Vasilyeva I, et al. (1986) An electron microscopic study of nucleolus‐organizing regions at some stages of the cell cycle (G0 period, G2 period, mitosis). Biol Cell 57: 197‒205.
[48]	Cuylen S, Blaukopf C, Politi AZ, et al. (2016) Ki-67 acts as a biological surfactant to disperse mitotic chromosomes. Nature 535: 308‒312.
[49]	Hayashi Y, Kato K, Kimura K (2017) The hierarchical structure of the perichromosomal layer comprises Ki67, ribosomal RNAs, and nucleolar proteins. Biochem Biophys Res Commun 493: 1043‒1049.
[50]	Sarkar A, Thoms M, Barrio-Garcia C, et al. (2017) Preribosomes escaping from the nucleus are caught during translation by cytoplasmic quality control. Nat Struct Mol Biol 24: 1107. doi: 10.1038/nsmb.3495
[51]	Azum-Gélade MC, Noaillac-Depeyre J, Caizergues-Ferrer M, et al. (1994) Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the prenucleolar bodies at telophase. J Cell Sci 107: 463‒475.
[52]	Boulon S, Westman BJ, Hutten S, et al. (2010) The nucleolus under stress. Mol Cell 40: 216‒227.
[53]	Couté Y, Burgess JA, Diaz JJ, et al. (2006) Deciphering the human nucleolar proteome. Mass Spectrom Rev 25: 215‒234.
[54]	Moisa SS, Tsetlin VV, Levinskich MA, et al. (2016) Low doses of ionized radiation and hypomagnetic field alter redox properties of water and physiological characteristics of seeds of the highest plants. J Biomed Sci Engin 9: 410‒418.
[55]	Basto S, Thompson K, Rees M (2015) The effect of soil pH on persistence of seeds of grassland species in soil. Plant Ecol 216: 1163‒1175.
[56]	Binhi VN, Prato FS (2017) A physical mechanism of magnetoreception: extension and analysis. Bioelectromagnetics 38: 41‒52.
[57]	Binhi VN, Prato FS (2018) Rotations of macromolecules affect nonspecific biological responses to magnetic fields. Sci Rep 8: 13495. doi: 10.1038/s41598-018-31847-y
[58]	Belova NA, Ermakova ON, Ermakov AM, et al. (2007) The bioeffects of extremely weak power-frequency alternating magnetic fields. Environmentalist 27: 411‒416.
[59]	Binhi VN (2011) Microwave absorption by magnetic nanoparticles in the organism. Biophysics 56: 1096‒1098.
[60]	Fu JP, Mo WC, Liu Y, et al. (2016) Elimination of the geomagnetic field stimulates the proliferation of mouse neural progenitor and stem cells. Protein Cell 7: 624-637. doi: 10.1007/s13238-016-0300-7
[61]	Mo WC, Liu Y, Bartlett PF, et al. (2014) Transcriptome profile of human neuroblastoma cells in the hypomagnetic field. Sci China: Life Sci 57: 448-461. doi: 10.1007/s11427-014-4644-z
[62]	Wiltschko W, Wiltschko R (2005) Magnetic orientation and magnetoreception in birds and other animals. J Comp Physiol A 191: 675‒693.
[63]	Dhiman SK, Galland P (2018) Effects of weak static magnetic fields on the gene expression of seedlings of Arabidopsis thaliana. J Plant Physiol 231: 9‒18.
[64]	Lednev VV (1996) Bioeffects of weak static and alternating magnetic fields. Biofizika 41: 224-232.
[65]	Alipov YD, Belyaev IY (1996) Difference in frequency spectrum of extremely-low-frequency effects on the genome conformational state of AB 1157 and EMG2 E. coli cells. Bioelectromagnetics 17: 384-387. doi: 10.1002/(SICI)1521-186X(1996)17:5<384::AID-BEM5>3.0.CO;2-#
[66]	Bunkin NF, Shkirin AV, Ignatiev PS, et al. (2012) Nanobubble clusters of dissolved gas in aqueous solutions of electrolyte. I. Experimental proof. J Chem Phys 137: 054706.
[67]	Liu S, Kawagoe Y, Makino Y, et al. (2013) Effects of nanobubbles on the physicochemical properties of water: the basis for peculiar properties of water containing nanobubbles. Chem Engin Sci 93: 250‒256.
[68]	Liu S, Oshita S, Makino Y, et al. (2016) Oxidative capacity of nanobubbles and its effect on seed germination. ACS Sustainable Chem Eng 4: 1347‒1353.
[69]	Binhi VN (2002) Magnetobiology: underlying physical problems, San Diego: Academic Press.
[70]	Wan GJ, Wang WJ, Xu JJ, et al. (2015) Cryptochromes and hormone signal transduction under near-zero magnetic fields: New clues to magnetic field effects in a rice planthopper. Plos One 10: e0132966. doi: 10.1371/journal.pone.0132966
[71]	Xu C, Yu Y, Zhang Y, et al. (2017) Gibberellins are involved in effect of near-null magnetic field on Arabidopsis flowering. Bioelectromagnetics 38: 1-10. doi: 10.1002/bem.22004
[72]	Krylov VV (2017) Biological effects related to geomagnetic activity and possible mechanisms. Bioelectromagnetics 38: 497‒510.
[73]	Polyn S, Willems A, De Veylder L (2015) Cell cycle entry, maintenance, and exit during plant development. Curr Opin Plant Biol 23: 1‒7.
[74]	Shaw PJ, Brown JWS (2004) Plant Nuclear Bodies. Curr Opin Plant Biol 7: 614-620. doi: 10.1016/j.pbi.2004.09.011
[75]	Raška I, Shaw PJ, Cmarko D (2006) New insights into nucleolar architecture and activity. Int Rev Cytol 255: 177‒235.
[76]	Hernandez-Verdun D (2011) Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2: 189‒194.
[77]	Kiryanov GI, Manamshjan TA, Polyakov VY, et al. (1976) Levels of granular organization of chromatin fibres. FEBS Lett 67: 323‒327.
[78]	Paweletz N, Risueno MC (1982) Transmission electron microscopic studies on the mitotic cycle of nucleolar proteins impregnated with silver. Chromosoma 85: 261‒273.
[79]	Van Hooser AA, Yuh P, Heald R (2005) The perichromosomal layer. Chromosoma 114: 377‒388.
[80]	Hernandez‐Verdun D, Roussel P, Thiry M, et al. (2010) The nucleolus: structure/function relationship in RNA metabolism. Wiley Interdisciplinary Reviews: RNA 1: 415‒431.
[81]	Shaw P, Brown J (2012) Nucleoli: composition, function, and dynamics. Plant Physiol 158:44‒51.
[82]	Feric M, Vaidya N, Harmon TS, et al. (2016) Coexisting liquid phases underlie nucleolar subcompartments. Cell 165: 1686‒1697.
[83]	Nerurkar P, Altvater M, Gerhardy S, et al. (2015) Eukaryotic ribosome assembly and nuclear export, In: Jeon KW, ed., International review of cell and molecular biology, Academic Press, 319: 107‒140.

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