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Rhythms, Clocks and Deterministic Chaos in Unicellular Organisms

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Rhythms in Plants

Abstract

The cell generation or cell cycle time in a clonal population of identical unicellular organisms growing under steady-state conditions in a carbon (or energy)-limited continuous culture (chemostat) shows a broad distribution. This indicates that the rate of cell division cycle traverse shows considerable variability. The basis for this variable temporal organisation has been the subject of a great deal of speculation, and many models have been suggested. This process is highly temperature dependent, and like all chemical and biochemical reactions, its rate approximately doubles for every 10 °C rise in temperature over a certain range of growth temperatures (i.e. the Q10 ♎ 2). Clock-controlled biological processes on the other hand are temperature-compensated, so that Q10 ♎ 1; two well-established examples are the circadian (τ ♎ 24 h) and ultradian clocks (τ ♎ 40 min in Saccharomyces cerevisiae). Other biological processes proceeding in faster time domains often show reactive oscillatory dynamics. A well-studied example is glycolysis, although a function for glycolytic oscillations is not yet established. As all these examples depend on three or more variables and are often in coupled sets, departure from regular oscillatory behaviour into deterministic aperiodicity is to be expected. Chaos has been demonstrated in biochemical reactions (enzyme-catalysed), as well as chemical reactions. It has also been shown in a metabolic pathway (glycolysis), and in the complex system of the cell division cycle. Chaos may also arise from coupled oscillators. One possible mechanism for spatio-temporal coherence (order) arises in unicells as an output from a tuneable multi-oscillator (controlled chaos). Self-similarity of oscillatory properties across multiple time domains indicates temporal coherence described by an inverse power law proportional to 1/fβ and long-term temporal correlations. Clocks , rhythms , oscillations, deterministic chaos and scale-free coherence are fundamental hallmarks of life on every time scale.

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References

  • Adams CA, Kuriyama H, Lloyd D, Murray DB (2003) The GTS1 protein stabilizes the autonomous oscillator in yeast. Yeast 20:463–470

    CAS  PubMed  Google Scholar 

  • Adams KJ (1990) Circadian clock control of an ultradian rhythm in Euglena gracilis. In: Morgan (Ed) Chronobiology and chronomedicine: basic research and applications. Peter Lang, Frankfurt, pp 13–22

    Google Scholar 

  • Amariel C, Machné R, Sasidharan K, Gottstein W, Tomita M, Soga T, Lloyd D, Murray DB (2013) The dynamics of cellular energetics during continuous yeast cultures. Conf Proc IEEE Eng Med Biol Soc 2013:2011–2707

    Google Scholar 

  • Amariel C, Tomita M, Murray DB (2014) Quantifying periodicity in omics data. Front Cell Dev Biol 2:40

    Google Scholar 

  • Anserinsky E, Kleitman N (1953) Regularly occurring periods of eye motility, and concomitant phenomena during sleep. Science 118:273–274

    Google Scholar 

  • Aon MA, Cortassa S (1997) Dynamic biological organization: fundamentals as applied to living systems. Chapman and Hall, London

    Google Scholar 

  • Aon MA, Cortassa S, Lloyd D (2000) Chaotic dynamics and fractal space in biochemistry: simplicity underlies complexity. Cell Biol Int 24:581–587

    CAS  PubMed  Google Scholar 

  • Aon MA, Cortassa S, Lemar KM, Hayes AJ, Lloyd D (2007a) Single and cell population respiratory oscillations in yeast: a 2-photon scanning laser microscopy study. FEBS Lett 581:8–14

    CAS  PubMed  Google Scholar 

  • Aon MA, Cortassa S, O’Rourke B (2006) The fundamental organization of cardiac mitochondria as a network of coupled oscillators. Biophys J 91:4317–4327

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aon MA, Cortassa S, Maack C, O’Rourke B (2007b) Sequential opening of mitochondrial ion channels as a function of glutathione redox thiol status. J Biol Chem 282:21889–21900

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aon MA, Cortassa S, O’Rourke B (2007c) On the network properties of mitochondria. Wiley, Hoboken

    Google Scholar 

  • Aon MA, Roussel MR, Cortassa S, O’Rourke B, Murray DB, Beckmann M, Lloyd D (2008) The scale-free dynamics of eukaryotic cells. PLoS ONE 3:e3624

    PubMed Central  PubMed  Google Scholar 

  • Aon MA, Cortassa S, Lloyd D (2011) Chaos in biochemistry and physiology. In: Encyclopedia of molecular cell biology and molecular medicine. Wiley, Hoboken

    Google Scholar 

  • Auberson LCM, Kanbier T, von Stockar (1993) Monitoring yeast cultures by calorimetry. J Biotech 29:205–215

    Google Scholar 

  • Baek SJ, Ott E (2004) Onset of synchronization in systems of globally coupled chaotic maps. Phys RenE StatNonlin Matter 69:066210

    Google Scholar 

  • Ball DA, Adames NR, Reischmann N, Barik D, Franck CT, Tyson JJ, Peccoud J (2013) Measurement and modelling of transcriptional noise in the cell cycle regulatory network. Cell Cycle 12:3203–3218

    CAS  PubMed Central  PubMed  Google Scholar 

  • Balzer I, Neuhaus-Steinmetz V, Hardeland R (1989) Temperature compensation in an ultradian rhythm of tyrosine aminotransferase in Euglena gracilis Krebs. Experientia 45:476–477

    CAS  PubMed  Google Scholar 

  • Barrio RS, Zhang L, Maini PK (1997) Hierarchically coupled ultradian oscillations generating robust circadian rhythms. Bull Math Biol 59:517–532

    CAS  PubMed  Google Scholar 

  • Battogtokh D, Tyson JJ (2004a) Bifurcation analysis of a model of the budding yeast cell cycle. Chaos 14:653–661

    CAS  PubMed  Google Scholar 

  • Battogtokh D, Tyson JJ (2004b) Turbulence near cyclic fold bifurcations in biorhythmic media. Phys Rev E: Stat, Nonlin, Soft Matter Phys 70:026212

    Google Scholar 

  • Battogtokh D, Tyson JJ (2006) Periodic forcing of a mathematical model of the eukaryotic cell cycle. Phys Rev E 73:011910

    Google Scholar 

  • Von Bertalanffy L (1952) Problems of life. Harper, New York

    Google Scholar 

  • Von Bertalanffy L (1968) General systems theory. George Braziller, New York

    Google Scholar 

  • Beuse M, Kopman K, Dickmann H, Thoma M (1999) Oxygen, pH value and carbon source changes the mode of oscillation in synchronous cultures of yeast (Saccharomyces cerevisae). Biotech Bioeng 63:410–417

    Google Scholar 

  • Boyd CAR, Noble D (1993) The logic of life: the challenge of integrative physiology. Oxford University Press, Oxford

    Google Scholar 

  • Brenner S (1999) Theoretical biology in the third millennium. Phil Trans R Soc Lond B 354:1963–1965

    CAS  Google Scholar 

  • Brodsky VY (1975) Protein synthesis rhythm. J Theor Biol 55:167–200

    Google Scholar 

  • Brodsky VY (2006) Direct cell-cell communication. A new approach due to recent data on the nature and self organization of ultradian cirahoralian intracellular rhythms. Biol Rev 81:143–162

    PubMed  Google Scholar 

  • Brodsky VY (2014) Circahoralian (Ultradian) metabolic rhythms. Biochemistry (Moscow) 79(6):483–495

    CAS  Google Scholar 

  • Brooks RF (1985) The transition probability model: successes, limitations, and deficiencies. In: Rensing L, Jaeger NI (eds) Temporal order, Springer, Berlin, pp 304–314

    Google Scholar 

  • Bunning E (1964) The physiological clock. Springer, Berlin

    Google Scholar 

  • Carlisle M (1980) From prokaryote to eukaryote gains and losses. The eukaryotic microbial cell. Lloyd D and Trinci APJ Cambridge University Press, Gooday GW, pp 1–40

    Google Scholar 

  • Carré IA, Edmunds LN Jr (1992) Oscillator control of cell division in Euglema: cyclic AMP oscillations mediate the phasing of the cell division cycle by the circadian clock. J Cell Sci 104:1163–1173

    PubMed  Google Scholar 

  • Chance B, Estabrook RW, Ghosh AK (1964) Damped sinusoidal oscillations of cytoplasmic reduced pyridine nucleotide in cells. Proc Nat Acad Sci USA 51:1244–1251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chance B, Pye EK, Ghosh AK, Hess B (eds) (1973) Biological and biochemical. Oscillations Academic Press, New York

    Google Scholar 

  • Chandrashekaran MK (2005) Time in the living world. Universities Press (India), Hyderabad

    Google Scholar 

  • Chen C-I, McDonald KA (1990) Oscillatory behaviour of yeast in continuous culture. Biotech Bioeng 36:28–38

    CAS  Google Scholar 

  • Chernavskii DS, Palamarchuk EK, Polexhaev AA, Solyanik GI, Burlakova EB (1977) Mathematical model of periodic processes in membranes with application to cell cycle regulation. Biosystems 9:183–187

    Google Scholar 

  • Chin SL, Marcus IM, Klevecz RR, Li CM (2012) Dynamics of oscillatory phenotypes in Saccharomyces cerevisiae reveal a network of genome-wide oscillators. FEBS J 279:1119–1130

    CAS  PubMed Central  PubMed  Google Scholar 

  • Conrad M (1986) What is the use of chaos? In: Holden AV (ed) Univ Press, Manchester, pp 3–14

    Google Scholar 

  • Cortassa S, O’Rourke B, Aon MA (2014) Redox-optimised ROS balance and the relationship between mitochondrial respiration and ROS. Biochim Biophys Acta 1837:287–295

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crabb R, Mackey MV, Rey AD (1996) Propagating fronts, chaos and multistability in a cell replication model. Chaos 6:477–492

    PubMed  Google Scholar 

  • Dano S, Madsen MF, Sorensen PG (2007) Quantitative characterization of cell synchronization in yeast. Proc Natl Acad Sci U S A 104:12732–12736

    PubMed Central  PubMed  Google Scholar 

  • Davey HM, Davey CL, Woodward AM, Edmonds AN, Lee AW, Kell DB (1996) Oscillatory, stochastic and chaotic growth fluctuations in permittistatically controlled yeast cultures. BioSystems 39:43–61

    CAS  PubMed  Google Scholar 

  • De Monte S, d’Ovidio F, Dano S, Sorensen PG (2007) Dynamical quorum sensing: population density encoded in cellular dynamics. Proc Natl Acad Sci U S A 104:18377–18381

    PubMed Central  PubMed  Google Scholar 

  • Dowse HB, Ringo JM (1987) Further evidence that the circadian clock in Drosophila is a population of coupled ultradian oscillators. J Biol Rhythm 2:65–76

    CAS  Google Scholar 

  • Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer CH, de Paepe R (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered and diurnal regulation. Plant Cell 15:1212–1226

    CAS  PubMed Central  PubMed  Google Scholar 

  • Duboc P, Marison L, von Stockar U (1996) Physiology of yeast during cell cycle oscillations. J Biotech 51:57–72

    CAS  Google Scholar 

  • Duysens LN, Amesz J (1957) Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact yeast cells in the near ultraviolet and visible region. Biochim Biophys Acta 24:19–26

    CAS  PubMed  Google Scholar 

  • Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290

    CAS  PubMed  Google Scholar 

  • Edmunds LN Jr (1984) Cell cycle clocks marcell. Dekker, New York

    Google Scholar 

  • Edmunds LN Jr (1988) Cellular and molecular bases of biological clocks. Springer, New York

    Google Scholar 

  • Emberley E, Wingreen NS (2006) Hourglass model for a protein-based circadian oscillator. Phy Rev Lett 96:038303

    Google Scholar 

  • Engelberg J (1968) On deterministic origins of mitotic variability. J Theoret Biol 20:249–251

    CAS  Google Scholar 

  • Edwards SW, Lloyd D (1978) Oscillations of respiration and adenine nucleotides in synchronous cultures of Acanthamoeba castellanii: mitochondrial respiratory control in vivo. J Gen Microbiol 108:197–204

    CAS  Google Scholar 

  • Edwards SW, Lloyd D (1980) Oscillations in protein and RNA content during synchronous growth of Acanthamoeba castellanii: evidence for periodic turnover of macromolecules during the cell cycle. FEBS Lett 109:21–26

    CAS  PubMed  Google Scholar 

  • Fell DA (1997) Understanding the control of metabolism. Portland Press, London

    Google Scholar 

  • Fell DA (2005) Enzymes, metabolites and fluxes. J Exp Bot 56:267–272

    CAS  PubMed  Google Scholar 

  • Fuentes-Pardo B, Sáenz EM (1988) Action of deuterium oxide upon the ERG circadian rhythm in crayfish, Procambarus bouviei. Comp Biochem Physiol 90A:435–440

    CAS  Google Scholar 

  • Fukuda H, Kodama J-I, Lai S (2004) Circadian rhythm formation in plant seedling: global synchronization and bifurcation as a coupled non-linear oscillator system. Biosystems 77:41–46

    PubMed  Google Scholar 

  • Ganitkevich V, Mattea V, Benndorf K (2010) Glycolytic oscillations in single ischemic cardiomyocytes at near anoxia. J Gen Physiol 135:307–319

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garfinkel D (1971) Simulation of the Krebs cycle and closely related metabolites in perfused rat liver. Comput Biomed Res 4:18–42

    CAS  PubMed  Google Scholar 

  • Geest T, Steinmetz GC, Larter O, Olsen LF (1992) Period doubling bifurcations and chaos in an enzyme reaction. J Phys Chem 96:5678–5680

    CAS  Google Scholar 

  • Gilbert DA (1974) The nature of the cell cycle and the control of cell proliferation. BioSystems 5:197–204

    CAS  Google Scholar 

  • Gillette MU, Sejnowski TJ (2005) Biological clocks coordinately keep life on time. Science 309:1196–1198

    CAS  PubMed  Google Scholar 

  • Goda K, Kondo T, Oyama T (2014) Effects of adenylates on the circadian interaction of KaiB with the KaiC complex in the reconstituted cyanobacterial kai protein oscillator. Biosci Biotechnol Biochem 78:1833–1838

    CAS  PubMed  Google Scholar 

  • Goldbeter A, Gonze D, Houart G, Leloup JC, Halloy J, Dupont G (2001) From simple to complex oscillatory behaviour in metabolic and genetic control networks. Chaos 11:247–260

    CAS  PubMed  Google Scholar 

  • Grasman J (1990) A deterministic model of the cell cycle. Bull Math Biol 52:535

    CAS  PubMed  Google Scholar 

  • Grassberger P, Procaccia I (1983) Measuring the strangeness of strange attractors. Physica 9D:189–208

    Google Scholar 

  • Gustavsson AK, van Niekerk DD, Adiels CB, du Preez FB, Goksor M, Snoep JL (2012) Sustained glycolytic oscillations in individual isolated yeast cells. FEBS J 279:2837–2847

    CAS  PubMed  Google Scholar 

  • Gustavsson AK, van Niekerk DD, Adiels CB, Goksor M, Snoep JL (2014) Heterogeneity of glycolytic oscillatory behaviour in individual yeast cells. FEBS Lett 588:3–7

    CAS  PubMed  Google Scholar 

  • Hardeland R, Coto-Mates A, Poeggler B (2003) Circadian rhythms, oxidative stress and antioxidant defense mechanisms. Chronobiol Int 20:921–962

    CAS  PubMed  Google Scholar 

  • Halberg F, Cornelissen G, Faraone P, Poeggeler B, Hardeland R, Katinas G, Schwartzkopff O, Otsuka K, Bakken EE (2005) Prokaryote and eukaryote unicellular chronomics. Biomed Pharmacother 59(1):S192–202

    PubMed Central  PubMed  Google Scholar 

  • Hammond KD, Savage N, Littlewood M (2000) Protein kinase C in erythroleukaemia cells: temporal variations of isoforms. Cell Biol Int 24:549–557

    CAS  PubMed  Google Scholar 

  • Harrison DEF (1973) Growth, oxygen and respiration. Crit Rev Microbiol 2:185–228

    CAS  Google Scholar 

  • Hastings A, Hom CL, Ellner S, Godfray PHCJ (1993) Chaos in ecology: is nature a strange attractor? Ann Rev Ecol System 24:1–33

    Google Scholar 

  • Hastings JW, Sweeney BM (1957) On the mechanism of temperature independence in a biological clock. Proc Nat Acad Sci USA 43:804–811

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hauck T, Schneider FW (1994) Chaos in a Farey sequence through period doubling in the peroxidase-oxidase reaction. J Phys Chem 98:2072–2077

    CAS  Google Scholar 

  • Heinrich R, Rapoport TA (1974) A linear steady-state treatment of enzymatic chains. Eur J Biochem 42:89–95

    CAS  PubMed  Google Scholar 

  • Higgins J (1963) Dynamics and control in cellular reactions. In: Chance B, Estabrook R, Williamson JR (eds) Control of energy metabolism. Academic Press, New York, pp 13–46

    Google Scholar 

  • Hurley JM et al (2014) Analysis of clock-regulated genes in Neurospora crassa reveals widespread post-transcriptional control of metabolic potential. Proc Nat Acad Sci USA 111:16995–17002

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ivleva NB, Bramlett MR, Lindahl PA, Golden SS (2005) LdpA: a component of the circadian clock senses redox state of the cell. EMBOJ 24:1202–1210

    CAS  Google Scholar 

  • Jenkins H, Griffiths AJ, Lloyd D (1989) Simultaneous operation of ultradian and circadian rhythms in Chlamydomonas reinhardii. J Interdisc Cycle Res 20:257–264

    Google Scholar 

  • Jenkins H, Griffiths AJ, Lloyd D (1990) Selection-synchronised Chlamydomonas reinhardii display ultradian but not circadian rhythms. J Interdisc Cycle Res 21:75–80

    Google Scholar 

  • Kacser H, Burns J (1973) Rate control of biological processes. In: Davies DD (ed) Cambridge University Press, Cambridge pp 65–104

    Google Scholar 

  • Kageyama H, Kondo T, Iwasaki H (2003) Circadian formation of clock protein complexes by KaiA, KaiB, KaiC and SasA in cyanpbacteria. J Biol Chem 278:2388–2395

    CAS  PubMed  Google Scholar 

  • Kamen M (1963) Primary processes in photosynthesis. Academic Press, NY, p 4

    Google Scholar 

  • Kembro JM, Cortassa S, Aon MA (2014) Complex oscillatory redox dynamics with signalling potential at the edge between normal and pathological mitochondrial function. Front Physiol 5:257

    PubMed Central  PubMed  Google Scholar 

  • Kippert F, Lloyd D (1995) A temperature-compensated clock ticks in Schizosaccharomyces pombe. Microbiol 141:883–890

    CAS  Google Scholar 

  • Klevecz RR (1976) Quantized generation times in mammalian cells as an expression of the cellular clock. Proc Natl Acad Sci USA 73:4012–4016

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klevecz RR (1992) A precise circadian clock from chaotic cell cycle oscillations. In: Lloyd D, Rossi EL (eds) Ultradian rhythms in life processes. Springer, London, pp 41–70

    Google Scholar 

  • Klevecz RR, Braly PS (1987) Circadian and ultradian rhythms of proliferation in human ovarian cancer. Chronobiol Int 4:513–523

    CAS  PubMed  Google Scholar 

  • Klevecz RR, Li CM (2007) Evolution of the cellular clock from yeast to man by period doubling folds in the cellular oscillator. Coldspring Harbor Symp Quant Biol 72:421–429

    CAS  Google Scholar 

  • Klevecz RR, Bolen J, Forrest G, Murray DB (2004) A genomewide oscillation in transcription gates DNA replication and cell cycle. Proc Nat Acad Sci USA 101:1200–1205

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kloster A, Olsen LF (2012) Oscillations in glycolysis in Saccharomyces cerevisiae: the role of autocatalysis and intracellular ATPase activity. Biophys Chem 165–166:39–47

    PubMed  Google Scholar 

  • Kucho K-I, Okamoto K, Isuchiya Y, Nomura S, Nango M, Kanehisa M, Ishiura M (2005) Global analysis of circadian expression in the cyanobacterium Synechocystis sp Strain PCC 6803. J Bact 187:2190–2199

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuenzi MT, Fiechter M (1969) Changes in carbohydrate composition and trehalase activity during the budding cycle of yeast. Arch Mikrobiol 64:396–407

    CAS  PubMed  Google Scholar 

  • Lakin-Thomas PL (2000) Circadian rhythms: new functions for old clock genes. Trends Genet 16:135–142

    CAS  PubMed  Google Scholar 

  • Lakin-Thomas PL, Brody S (2004) Circadian rhythms in microorganisms: new complexities. Annu Rev Microbiol 58:489–519

    CAS  PubMed  Google Scholar 

  • Langton CG (1991) Life at the edge of chaos. In: Langton CG, Taylor C, Farmer JD, Rasmussen S (eds) Artificial life II, studies in the science of complexity. Addison-Wesley, Santa Fe, pp 41–91

    Google Scholar 

  • Lara-Aparicio M, Barriga-Montoya C, Padilla-Longoria C, Fuentes-Pardo B (2014) Modeling some properties of circadian rhythms. Math Biosci Eng 11(2):317–330

    PubMed  Google Scholar 

  • Lemar KM, Passa O, Aon MA, Cortassa S, Muller CT, Plummer S, O’Rourke B, Lloyd D (2005) Allyl alcohol and garlic (Allium sativum) extract produce oxidative stress in Candida albicans. Microbiology (Reading, England) 151:3257–3265

    Google Scholar 

  • Lemar KM, Aon MA, Cortassa S, O’Rourke B, Muller CT, Lloyd D (2007) Diallyl disulphide depletes glutathione in Candida albicans: oxidative stress-mediated cell death studied by two-photon microscopy. Yeast (Chichester, England) 24:695–706

    Google Scholar 

  • Lillo C, Meyer C, Ruoff P (2001) The nitrate reductase system. The central clock dogma contra multiple oscillatory feedback loops. Plant Physiol 125:1554–1557

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lloyd AL, Lloyd D (1993) Hypothesis: the central oscillator of the circadian clock is a controlled chaotic oscillator. BioSystems 29:77–85

    CAS  PubMed  Google Scholar 

  • Lloyd AL, Lloyd D (1995) Chaos: its significance and detection in biology. Biol Rhythm Res 26:233–252

    Google Scholar 

  • Lloyd D (1974) The mitochondria of microorganisms. Academic Press, London

    Google Scholar 

  • Lloyd D (1992) Intracellular time keeping: epigenetic oscillations reveal the functions of an ultradian clock. In: Lloyd D, Rossi EL (eds) Ultradian rhythms in life processes. Springer, London, pp 5–22

    Google Scholar 

  • Lloyd D (1994) A controlled chaotic attractor controls life. In: What is controlling life? 50 years after Erwin Schrodinger’s. In: Gnaiger E, Gellerich FN, Wyss M (eds) What is life? Innsbruck University Press, Innsbruck, pp 77–80

    Google Scholar 

  • Lloyd D (1998) Circadian and ultradian clock controlled rhythms in unicellular microorganisms. Adv Microb Physiol 39:292–339

    Google Scholar 

  • Lloyd D (2003) Effects of uncoupling of mitochondrial energy conservation on the ultradian clock-driven oscillations in Saccharomyces cerevisiae continuous culture. Mitochondrion 3:139–146

    CAS  PubMed  Google Scholar 

  • Lloyd D (2005) Systems dynamics of biology. J Appl Biomed 3:1–12

    CAS  Google Scholar 

  • Lloyd D (2006) Ultradian rhythms and clocks in plants and yeast. Biol Rhythm Res 37:281–296

    CAS  Google Scholar 

  • Lloyd D, Murray DB, Klevecz RR, Wolf J, Kuriyama H (2008) The ultradian clock (about 40 min) in yeast. In: Lloyd D, Rossi ER (eds) Ultradian rhythms from molecules to mind, a new vision of life. Springer, Berlin, pp 11–42

    Google Scholar 

  • Lloyd D (2008) Biological time is fractal: early events reverberate over a life time. J Biosci 33:9–19

    PubMed  Google Scholar 

  • Lloyd D, Edwards SW (1984) Epigenetic oscillations during the cell cycles of lower eukaryotes are coupled to a clock: life’s slow dance to the music of time. In: Edmunds L (ed) Cell clocks and cell cycles. Plenum Press, New York, pp 26–27

    Google Scholar 

  • Lloyd D, Gilbert DA (1998) Temporal organization of the cell division cycle of eukaryote microbes. Symp Soc Gen Microbiol 56:251–278

    Google Scholar 

  • Lloyd D, Kippert F (1987) A temperature compensated ultradian clock explains temperature-dependent quantal cell cycle times. In: Bowler K and Fuller BJ (eds) Temperature and animal cells, Cambridge University Press, Cambridge, pp 135–155

    Google Scholar 

  • Lloyd D, Lloyd AL (1994) A controlled chaotic attractor could provide a tuneable oscillator for circadian clocks. Biol Rhythm Res 25:235–240

    Google Scholar 

  • Lloyd D, Murray DB (2000) Redox cycling of intracellular thiols: state variables for ultradian, cell division cycle and circadian cycles? In: Vanden Driessche T et al (eds) The redox state and circadian rhythms. Kluwer, Amsterdam, pp 85–94

    Google Scholar 

  • Lloyd D, Murray DB (2005) Ultradian metronome: timekeeper for orchestration of cellular coherence. Trends Biochem Sci 30:373–377

    CAS  PubMed  Google Scholar 

  • Lloyd D, Murray DB (2006) The temporal architecture of eukaryotic ultradian rhythms in life processes. FEBS Lett 580:2830–2835

    Google Scholar 

  • Lloyd D, Murray DB (2007) Redox rhythmicity: clocks at the core of temporal coherence. BioEssays 29:465–473

    CAS  PubMed  Google Scholar 

  • Lloyd D, Rossi ER (1992) Ultradian rhythms in life processes. Springer, London

    Google Scholar 

  • Lloyd D, Rossi ER (2008) Ultradian rhythms from molecules to mind: a new vision of life. Springer, Berlin

    Google Scholar 

  • Lloyd D, Stupfel M (1991) The occurrence and functions of ultradian rhythms. Biol Rev 66:275–299

    CAS  PubMed  Google Scholar 

  • Lloyd D, Volkov EI (1990) Quantized cell cycle times: interaction between a relaxation oscillator and ultradian clock pulses. BioSystems 23:305–310

    CAS  PubMed  Google Scholar 

  • Lloyd D, Volkov EI (1991) The ultradian clock: timekeeping for intracellular dynamics. In: Mosekilde E, Mosekilde L (eds) Complexity, chaos and biological evolution. Plenum Press, New York, pp 51–60

    Google Scholar 

  • Lloyd D, Edwards SW, Fry JC (1982a) Temperature-compensated oscillations in respiration and cellular protein content in synchronous cultures of Acanthamoeba castellanii. Proc Natl Acad Sci USA 79:3786–3788

    Google Scholar 

  • Lloyd D, Poole RK, Edwards SW (1982b) The cell division cycle: temporal organization and control of cellular growth and reproduction. Academic Press, London

    Google Scholar 

  • Lloyd D, Lloyd AL, Olsen LF (1992) The cell division cycle: a physiologically plausible dynamic model can exhibit chaotic solutions. BioSystems 27:17–24

    CAS  PubMed  Google Scholar 

  • Lloyd D, Aon MA, Cortassa S (2001) Why homeodynamics, not homeostasis? Sci World 1:133–145

    Google Scholar 

  • Lloyd D, Salgado EJ, Turner MP, Murray DB (2002a) Respiratory oscillations in yeast: clock-driven mitochondrial cycles if energization. FEBS Lett 519:41–44

    CAS  PubMed  Google Scholar 

  • Lloyd D, Salgado EJ, Turner MP, Suller MTE, Murray DB (2002b) Cycles of mitochondrial energization driven by the ultradian clock in a continuous culture of Saccharomyces cerevisiae. Microbiology 148:3715–3724

    CAS  PubMed  Google Scholar 

  • Lloyd D, Lemar KM, Salgado LEJ, Gould TM, Murray DB (2003) Respiratory oscillations in yeast: mitochondrial reactive oxygen species, apoptosis and time; an hypothesis. FEMS Yeast Res 3:333–339

    CAS  PubMed  Google Scholar 

  • Lloyd D, Lloyd A, Olsen LF, Stolyarov MN, Volkov E, Murray DB (2004) Ultradian clock timekeeping: periodic, quasiperiodic and chaotic outputs. WSEAS Trans Biol Biomed 1:390–394

    Google Scholar 

  • Lloyd D, Cortassa S, O’Rourke B, Aon MA (2012) What yeast and cardiomyocytes share: ultradian oscillatory redox mechanisms of cellular coherence and survival. Integr Biol (Camb) 4:65–74

    CAS  Google Scholar 

  • Machné R, Murray DB (2012) The ying and yang of yeast transcription elements of a global feedback between metabolism and chromatin. PLoS ONE 7:e37906

    PubMed Central  PubMed  Google Scholar 

  • Mackey MC (1985) A deterministic cell cycle model with transition probability-like behaviour. In: Rensing L, Jaeger NI (eds) Temporal order. Springer, Berlin, pp 315–320

    Google Scholar 

  • Mackey MC, Santavy M, Selepova P (1986) A mitotic oscillator with a strange attractor and distributions of cell cycle times. In: Othmer H (ed) Nonlinear oscillations in biology and chemistry. Springer, Berlin

    Google Scholar 

  • Martegani E, Porro D, Ranzi BM, Alberghina L (1990) Involvement of a cell size control mechanism in the induction and maintenance of oscillations in continuous cultures of budding yeast. Biotech Bioeng 36:453–459

    CAS  Google Scholar 

  • Markus M, Muller SC, Hess B (1985) Observations of entrainment, quasi-periodicity and chaos in glycolysing yeast extract and periodic glucose input. Ber Bunsenges Phys Chem 89:651–654

    CAS  Google Scholar 

  • Matsuo T, Onai K, Okamoto K, Minagansa J, Ishura M (2006) Real-time monitoring of chloroplast gene expression: evidence for nuclear regulation of chloroplast circadian period. Mol Cell Biol 26:863–870

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mihalcescu I, Hsing W, Leibler S (2004) Resilient circadian oscillator revealed in individual cyanobacteria. Nature 430:81–85

    CAS  PubMed  Google Scholar 

  • Mitsui K, Yaguchi S-I, Tsurugi K (1994) The GTS1 gene which contains a Gly-Thr repeat, affects the timing of budding and cell size of the yeast Saccharomyces cerevisiae. Mol Cell Biol 14:5569–5578

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mittag M, Wagner V (2003) The circadian clock of the unicellular eukaryotic model organism Chlamydomonas reinhardtii. J Biol Chem 384:689–695

    CAS  Google Scholar 

  • Mittag M, Kiaulehn S, Johnson CH (2005) The circadian clock in Chlamydomonas reinhardtii. What is it for? What is it similar to? Plant Physiol 137:399–409

    Google Scholar 

  • Monod J (1950) La technique de culture continue: theorie et applications. Ann Inst Pasteur 79:390

    CAS  Google Scholar 

  • Monto S (2012) Nested synchrony-a novel cross-scale interaction among neuronal oscillations. Front Physiol 3:384

    PubMed Central  PubMed  Google Scholar 

  • Morré DJ, Ternes P, Morré DM (2002a) Cell enlargement of plant tissue explants oscillates with a temperature-compensated period of 24 min. In-Vitro Cell Devel Biol Plant 38:18–28

    Google Scholar 

  • Morré DJ, Church PJ, Pletcher T, Tang X, Wu LY, Morré DM (2002b) Biochemical basis for the biological clock. Biochem 41:11941–11945

    Google Scholar 

  • Münch T, Sonnleitner B, Fiechter A (1992) New insights into the synchronization mechanism with forced synchronous cultures of Saccharomyces cerevisiae. J Biotech 24:299–314

    Google Scholar 

  • Murray DB (2004) On the temporal organisation of Saccharomyces cerevisiae. Curr Genomics 5:665–671

    CAS  Google Scholar 

  • Murray DB, Lloyd D (2007) A tuneable attractor underlies yeast respiratory dynamics. Biosystems 90:287–294

    CAS  PubMed  Google Scholar 

  • Murray DB, Engelen FA, Keulers M, Kuriyama H, Lloyd D (1998a) NO + , but not NO, inhibits respiratory oscillations in ethanol-grown chemostat cultures of Saccharomyces cerevisiae. FEBS Lett 431:297–299

    CAS  PubMed  Google Scholar 

  • Murray DB, Engelen FA, Keulers M, Kuriyama H, Lloyd D (1998b) NO + , but not NO, inhibits respiratory oscillations in ethanol-grown chemostat cultures of Saccharomyces cerevisiae. Biochem Soc Trans 26:S339

    CAS  PubMed  Google Scholar 

  • Murray DB, Engelen F, Lloyd D, Kuriyama H (1999) Involvement of glutathione in the regulation of respiratory oscillation during a continuous culture of Saccharomyces cerevisiae. Microbiology (Reading, England) 145:2739–2745

    Google Scholar 

  • Murray DB, Roller S, Kuriyama H, Lloyd D (2001) Clock control of ultradian respiratory oscillation found during yeast continuous culture. J Bacteriol 183:7253–7259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murray DB, Klevecz RR, Lloyd D (2003) Generation and maintenance of synchrony in Saccharomyces cerevisiae continuous culture. Exp Cell Res 287:10–15

    CAS  PubMed  Google Scholar 

  • Murray DB, Beckmann M, Kitano H (2007) Regulation of yeast oscillatory dynamics. Proc Nat Acad Sci USA 104:2241–2246

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murray DB, Amariel C, Sasidharan K, Machne R, Aon MA, Lloyd D (2013) Temporal partitioning of the yeast cellular network. In: Aon MA, Saks V, Schlattner U (eds) Systems biology of metabolic and signaling networks. Energy, mass and information transfer. Springer, Heidelberg, pp 323–349

    Google Scholar 

  • Mustafin AT, Volkov EI (1977) On the distribution of cell generation times. BioSystems 15:111–126

    Google Scholar 

  • Nakajima M, Imai K, Ito H, Mishawaka T, Mahayana Y, Iwasaki H, Osama T, Kondo T (2005) Reconstitution of circadian oscillation of cyanobacterial Kai C phosphorylation in vitro. Science 308:414–415

    CAS  PubMed  Google Scholar 

  • Nielsen K, Sorensen PG, Hymen F (1997) Chaos in glycolysis. J Theor Biol 186:303–306

    CAS  PubMed  Google Scholar 

  • Nivala M, Korge P, Weiss JN, Qu Z (2011) Linking flickering to waves and whole-cell oscillations in a mitochondrial network model. Biophys J 101:2102–2111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nivala M, Ko CY, Nivala M, Weiss JN, Qu Z (2013) The emergence of subcellular pacemaker sites for calcium waves and oscillations. J Physiol 591(5305):5320

    Google Scholar 

  • Noble D (2002) Modeling the heart—from genes to cells to the whole organ. Science 295:1678–1682

    CAS  PubMed  Google Scholar 

  • Oike H, Nagai K, Fukushima T, Ishida N, Kobori M (2011) Feeding cues and injected nutrients induce acute expression of multiple clock genes in the mouse liver. PLoS ONE 6:e23709

    CAS  PubMed Central  PubMed  Google Scholar 

  • Norel R, Agur Z (1991) A model for the adjustment of the mitotic clock by cyclon and MPF levels. Science 251:1076–1078

    CAS  PubMed  Google Scholar 

  • Novak B, Pataki Z, Giliberto A, Tyson JJ (2001) Mathematical model of the cell cycle fission yeast. Chaos 11:277–286

    CAS  PubMed  Google Scholar 

  • Oike H, Oishi K, Kobori M (2014) Nutrients, clock genes, and chrononutrition. Curr Nutr Rep 3:204–212

    CAS  PubMed Central  PubMed  Google Scholar 

  • Olsen LF, Degn H (1977) Chaos in an enzymatic reaction. Nature 267:177–178

    CAS  PubMed  Google Scholar 

  • Olsen LF, Andersen AZ, Lunding A, Brasen JC, Poulsen AK (2009) Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-ATPases. Biophys J 96:3850–3861

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ott E, Grebogi C, Yorke JA (1990) Controlling Chaos. Phys Rev Lett 64:1196–1199

    PubMed  Google Scholar 

  • Paetkau V, Edwards R, Illner R (2006) A model for generating circadian rhythm by coupling ultradian oscillators. Theoret Biol Med Mod 3:12

    Google Scholar 

  • Park J, Lee J, Choi C (2011) Mitochondrial network determines intracellular ROS dynamics and sensitivity to oxidative stress through switching inter-mitochondrial messengers. PLoS ONE 6:e23211

    CAS  PubMed Central  PubMed  Google Scholar 

  • Parulekar SJ, Semiones GB, Rolf MJ, Livense JC, Lim HC (1986) Induction and elimination of oscillations in continuous cultures of yeast (Saccharomyces cerevisiae) Biotech Bioeng 28:700–710

    Google Scholar 

  • Pirt SJ (1975) Principles of microbe and cell cultivation. Blackwell Scientific, Oxford

    Google Scholar 

  • Porro D, Martegani E, Razni BM, Alberghina L (1988) Oscillations in continuous cultures of budding yeast a segregated parameter analysis. Biotech Bioeng 32:411–417

    CAS  Google Scholar 

  • Prytz G (2001) A biophysical study of oscillatory water regulation in plants. Measurement and models. DSc thesis Norwegian Univ Sci Technol, Trondheim

    Google Scholar 

  • Pye EK (1969) Biochemical mechanisms underlying the metabolic oscillations of yeast. Canad J Bot 47:271–285

    CAS  Google Scholar 

  • Pyragas K (1992) Continuous control of chaos by self-controlling feed-back. Phys Lett 170:421–428

    Google Scholar 

  • Pyragas K (2002) Analytical properties and optimization of time-delayed feedback control. Phys Rev E: Stat, Nonlin, Soft Matter Phys 66:026207

    CAS  Google Scholar 

  • Pyragiene T, Pyragas K (2005) Delayed feedback control of forced self-sustained oscillations. Phys Rev E: Stat, Nonlin, Soft Matter Phys 72:026203

    CAS  Google Scholar 

  • Rees P, Spencer PS, Pierce I, Sivaprakasam S, Shore KA (2003) Anticipated chaos in a non-symmetric coupled external-cavity laser system. Phys Rev A68:033818

    Google Scholar 

  • Restrepo JG, Ott E, Hunt BR (2005) Onset of synchronization in large networks of coupled oscillators. Phys Rev E: Stat, Nonlin, Soft Matter Phys 71:036151

    Google Scholar 

  • Romond PC, Rustici M, Gonze D, Goldbeter A (1999) Alternating oscillations and chaos in a model of two coupled biochemical oscillators driving successive phases of the cell cycle. Ann NY Acad Sci 879:180–193

    CAS  PubMed  Google Scholar 

  • Roussel MR, Lloyd D (2007) Observation of a chaotic multioscillatory metabolic attractor by real-time monitoring of a yeast continuous culture. FEBS J 274:1011–1018

    CAS  PubMed  Google Scholar 

  • Ruoff P, Zakhartsev M, Westerhoff HV (2007) Temperature compensation through systems biology. FEBS J 274:940–950

    CAS  PubMed  Google Scholar 

  • Sahar S, Sassone-Corsi P (2012) Regulation of metabolism: the circadian clock dictates the time. Trends Endocrinol Metab 23:1–8

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sahar S, Sassoni-Corsi P (2013) The epigenetic language of circadian clocks. Handb Exp Pharmacol 217:29–44

    CAS  PubMed  Google Scholar 

  • Salgado, F, Murray DB, Lloyd (2002) Some antidepressant agents (Li+, monoamine oxidase type A inhibitors) perturb the ultradian clock in S. cerevisiae. Biol Rhythm Res 33:351–361

    Google Scholar 

  • Sasidharan K, Amariel C, Tomita M, Murray DB (2012a) Rapid DNA, RNA and protein extraction protocols optimised for slow continuously growing yeast cultures. Yeast 29:311–322

    CAS  PubMed  Google Scholar 

  • Sasidharan K, Soga T, Tomita M, Murray DB (2012b) A yeast metabolite extraction protocol optimised for time-series analyses. PLoS ONE 7:e44283

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sasidharan K, Tomita M, Aon M, Lloyd D, Murray DB (2012c) Time structure of the yeast metabolism in vivo. Adv Exp Med Biol 736:369–379

    Google Scholar 

  • Satroutdinov AD, Kuriyama H, Kobayashi H (1992) Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. FEMS Microbiol Lett 77:261–267

    CAS  PubMed  Google Scholar 

  • Schibler U, Naef F (2005) Cellular oscillators: rhythmic gene expression and metabolism. Curr Opin Cell Biol 17:223–229

    CAS  PubMed  Google Scholar 

  • Schibler U (2005) The daily rhythms of genes, cells and organs. Biological clocks and circadian timing in cells. EMBO Rep Spec No. S9–13

    Google Scholar 

  • Schneider ED, Sagan D (2005) Into the cool. Energy flow thermodynamics and live. University of Chicago Press, Chicago

    Google Scholar 

  • Schwarzländer M, Logan DC, Johnston IG, Jones NS, Meyer AJ, Fricker MD, Sweetlove LJ (2012) Pulsing of membrane potential in individual mitochondria: a stress-induced mechanism to regulate respiratory bioenergetics in Arabidopsis. Plant Cell 24:1188–1201

    PubMed Central  PubMed  Google Scholar 

  • Searcy DG (2003) Metabolic integration during the evolutionary origin of mitochondria. Cell Res 4:229–234

    Google Scholar 

  • Sel’kov EE (1970) Two alternative self-oscillating stationary states in thiol metabolism—two alternative types of cell division normal and malignant ones. Biophysika 15:1065–1073

    Google Scholar 

  • Selivanov VA, Cascante M, Friedman M, Schumaker MF, Trucco M, Votyakova TV (2012) Multistationary and oscillatory modes of free radicals generation by the mitochondrial respiratory chain revealed by a bifurcation analysis. PLoS Comput Biol 8:e1002700

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sheppard JD, Dawson PSS (1999) Cell synchrony and periodic behaviour in yeast populations. Canad J Chem Eng 77:892–902

    Google Scholar 

  • Slodzinski MK, Aon MA, O’Rourke B (2008) Glutathione oxidation as a trigger of mitochondrial depolarization and oscillation in intact hearts. J Mol Cell Cardiol 45:650–660

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sohn H-Y, Kuriyama H (2001) Ultradian metabolic oscillation of Saccharomyces cerevisiae during aerobic continuous culture: H2S, a population synchronizer is produced by sulphite reductase population synchrony. Yeast 18:125–135

    CAS  PubMed  Google Scholar 

  • Sohn H-Y, Murray DB, Kuriyama H (2000) Ultradian oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide mediates population synchrony. Yeast 16:1185–1190

    CAS  PubMed  Google Scholar 

  • Sornette D (2000) Critical phenomena in natural sciences. Chaos, fractals, self-organization and disorder: concepts and tools. Springer, Berlin

    Google Scholar 

  • Strässle C, Sonnleitner B, Fiechter A (1988) A predictive model for the spontaneous synchronization of yeast (Saccharomyces cerevisiae) grown in continuous culture. J Biotech 7:299–318

    Google Scholar 

  • Sweeney BM (1982) Interaction of the circadian cycle with the cell cycle in Pyrocystis fusiformis. Plant Physiol 70:272–276

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thoke HS, Tobiesen A, Brewer J, Hansen PL, Stock RP, Olsen LF, Bagatolli L (2015) Tight coupling of metabolic oscillations and intracellular water dynamics in Saccharomyces cerevisiae. PLoS One 10(2) e0117308

    Google Scholar 

  • Thorsen K, Agafonov O, Selso CH, Jolma IW, Ni XY, Drenstig T, Ruoff P (2014) Robust concentration and frequency control in oscillatory homeostats. PLoS ONE 9(9):e107766

    PubMed Central  PubMed  Google Scholar 

  • Tseng YY, Hunt SM, Heintzen C, Crosthwaite SK, Schwartz JM (2012) Comprehensive modelling of the Neurospora circadian clock and its temperature compensation. PLoS Comput Biol 8:e1002437

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tyson JJ, Chen KC, Novak B (2003) Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr Opin Cell Biol 15:221–231

    CAS  PubMed  Google Scholar 

  • Wagner V, Gessner G, Mittag M (2005) Functional proteomics: a promising approach to find novel components of the circadian system. Chronobiol Int 22:403–415

    CAS  PubMed  Google Scholar 

  • Weber G (1990) Whither biophysics? Ann Rev Biophys Chem 19:1–6

    Google Scholar 

  • Weiss JN, Nivala M, Garfinkel A, Qu Z (2011) Alternans and arrhythmias: from cell to heart. Circ Res 108:98–112

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weiss JN, Yang JH (2010) Oscillations at odds in the heart. J Gen Physiol 135:303–305

    CAS  PubMed Central  PubMed  Google Scholar 

  • West BJ (1999) Physiology, promiscuity and prophecy at the millennium: a tale of tails. World Scientific, Singapore

    Google Scholar 

  • Wiener N (1961) Cybernetics, 2nd edn. MIT Press, Cambridge

    Google Scholar 

  • Wicken J (1987) Evolution, thermodynamics and information: extending the Darwin program Oxford University Press, New York

    Google Scholar 

  • Wolf A, Swift JB, Swinney HL, Vastano JA (1985) Determining Lyapunov exponents from a times series. Physica 16D:285–318

    Google Scholar 

  • Yang L, Korge P, Weiss JN, Qu Z (2010) Mitochondrial oscillations and waves in cardiac myocytes: insights from computational models. Biophys J 98:1428–1438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang TH, Hunt BR, Ott E (2000) Optimal periodic orbits of continuous time chaotic systems. Phys Rev E Stat Phys Plasmas Fluids Rel Inter Topics 62:1950–1959

    CAS  Google Scholar 

  • Yates FE (1992a) Fractal applications in biology. Scaling in biochemical networks. Meth Enzymol 210:636–675

    CAS  PubMed  Google Scholar 

  • Yates FE (1992b) Outline of a physical theory of physiological systems. J Physiol Pharmacol 60:217–248

    Google Scholar 

  • Yates FE (1993) Self-organizing systems. In: Boyd CAR, Noble D (eds) The logic of life. The challenge of integrative physiology. Oxford University Press, New York, pp 189–218

    Google Scholar 

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Lloyd, D., Aon, M.A., Cortassa, S. (2015). Rhythms, Clocks and Deterministic Chaos in Unicellular Organisms. In: Mancuso, S., Shabala, S. (eds) Rhythms in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-20517-5_14

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