Abstract
Tic-tac, tic-tac, the sound of time is familiar to us, yet, it also silently shapes daily biological processes conferring 24-hour rhythms in, among others, cellular and systemic signaling, gene expression, and metabolism. Indeed, circadian clocks are molecular machines that permit temporal control of a variety of processes in individuals, with a close to 24-hour period, optimizing cellular dynamics in synchrony with daily environmental cycles. For over three decades, the molecular bases of these clocks have been extensively described in the filamentous fungus Neurospora crassa, yet, there have been few molecular studies in fungi other than Neurospora, despite evidence of rhythmic phenomena in many fungal species, including pathogenic ones. This chapter will revise the mechanisms underlying clock regulation in the model fungus N. crassa, as well as recent findings obtained in several fungi. In particular, this chapter will review the effect of circadian regulation of virulence and organismal interactions, focusing on the phytopathogen Botrytis cinerea, as well as several entomopathogenic fungi, including the behavior-manipulating species Ophiocordyceps kimflemingiae and Entomophthora muscae. Finally, this review will comment current efforts in the study of mammalian pathogenic fungi, while highlighting recent circadian lessons from parasites such as Trypanosoma and Plasmodium. The clock keeps on ticking, whether we can hear it or not.
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Aronson BD, Johnson KA, Loros JJ, Dunlap JC (1994) Negative feedback defining a circadian clock—autoregulation of the clock gene-frequency. Science 263(5153):1578–1584. https://doi.org/10.1126/science.8128244
Austin B (1968) An endogenous rhythm of spore discharge in Sordaria fimicola. Ann Bot 32(2):262–278
Belden WJ, Larrondo LF, Froehlich AC, Shi M, Chen CH, Loros JJ, Dunlap JC (2007) The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian output. Genes Dev 21(12):1494–1505. https://doi.org/10.1101/gad.1551707
Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, Zoran MJ (2005) Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6(7):544–556. https://doi.org/10.1038/nrg1633
Bell-Pedersen D, Garceau N, Loros JJ (1996) Circadian rhythms in fungi. J Genet 75(3):387–401
Bellini R, Mullens BA, Jespersen JB (1992) Infectivity of two members of the Entomophthora muscae complex [Zygomycetes: Entomophthorales] for Musca domestica [Dipt.: Muscidae]. Entomophaga 37:11–19. https://doi.org/10.1007/bf02372969
Bhardwaj V, Meier S, Petersen LN, Ingle RA, Roden LC (2011) Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLoS ONE 6(10):e26968. https://doi.org/10.1371/journal.pone.0026968 (PONE-D-11-15640 [pii])
Blackwell M (2011) The fungi: 1, 2, 3 … 5.1 million species? Am J Bot 98(3):426–438. https://doi.org/10.3732/ajb.1000298
Bluhm BH, Burnham AM, Dunkle LD (2010) A circadian rhythm regulating hyphal melanization in Cercospora kikuchii. Mycologia 102(6):1221–1228. https://doi.org/10.3852/09-041 (09-041 [pii])
Buttner P, Koch F, Voigt K, Quidde T, Risch S, Blaich R, Bruckner B, Tudzynski P (1994) Variations in ploidy among isolates of Botrytis cinerea: implications for genetic and molecular analyses. Curr Genet 25(5):445–450
Callaghan AA (1969) Light and spore discharge in Entomophthorales. Trans Br Mycol Soc 53:87–97. https://doi.org/10.1016/S0007-1536(69)80010-0
Canessa P, Schumacher J, Hevia MA, Tudzynski P, Larrondo LF (2013) Assessing the effects of light on differentiation and virulence of the plant pathogen Botrytis cinerea: characterization of the white collar complex. PLoS ONE 8(12):e84223. https://doi.org/10.1371/journal.pone.0084223
Casas-Flores S, Rios-Momberg M, Bibbins M, Ponce-Noyola P, Herrera-Estrella A (2004) BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiology 150(Pt 11):3561–3569. https://doi.org/10.1099/mic.0.27346-0 (150/11/3561 [pii])
Causton HC, Feeney KA, Ziegler CA, O’Neill JS (2015) Metabolic cycles in yeast share features conserved among circadian rhythms. Curr Biol 25(8):1056–1062. https://doi.org/10.1016/j.cub.2015.02.035
Chen CH, Dunlap JC, Loros JJ (2010) Neurospora illuminates fungal photoreception. Fungal Genet Biol 47(11):922–929. https://doi.org/10.1016/j.fgb.2010.07.005 (S1087-1845(10)00131-3 [pii])
Chen S, Fuller KK, Dunlap JC, Loros JJ (2018) Circadian clearance of a fungal pathogen from the lung is not based on cell-intrinsic macrophage rhythms. J Biol Rhythms 33(1):99–105. https://doi.org/10.1177/0748730417745178
Crosthwaite SK, Heintzen C (2010) Detection and Response of the Neurospora crassa circadian clock to light and temperature. Fungal Biol Rev 24:114–122
Crosthwaite SK, Loros JJ, Dunlap JC (1995) Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81(7):1003–1012
Curtis AM, Bellet MM, Sassone-Corsi P, O’Neill LA (2014) Circadian clock proteins and immunity. Immunity 40(2):178–186. https://doi.org/10.1016/j.immuni.2014.02.002
Daub ME, Ehrenshaft M (2000) THE PHOTOACTIVATED CERCOSPORA TOXIN CERCOSPORIN: contributions to plant disease and fundamental biology. Annu Rev Phytopathol 38:461–490. https://doi.org/10.1146/annurev.phyto.38.1.461
de Bekker C, Merrow M, Hughes DP (2014) From behavior to mechanisms: an integrative approach to the manipulation by a parasitic fungus (Ophiocordyceps unilateralis s.l.) of its host ants (Camponotus spp.). Integr Comp Biol 54(2):166–176. https://doi.org/10.1093/icb/icu063
de Bekker C, Ohm RA, Loreto RG, Sebastian A, Albert I, Merrow M, Brachmann A, Hughes DP (2015) Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genom 16:620. https://doi.org/10.1186/s12864-015-1812-x
de Bekker C, Will I, Hughes DP, Brachmann A, Merrow M (2017) Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiae. PLoS ONE 12(11):e0187170. https://doi.org/10.1371/journal.pone.0187170
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13(4):414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
Deng YZ, Qu Z, Naqvi NI (2015) Twilight, a novel circadian-regulated gene, integrates phototropism with nutrient and redox homeostasis during fungal development. PLoS Pathog 11(6):e1004972. https://doi.org/10.1371/journal.ppat.1004972
Dibner C, Schibler U (2017) Body clocks: time for the Nobel Prize. Acta Physiol (Oxf). https://doi.org/10.1111/apha.13024
Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309(5734):630–633
Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96(2):271–290
Dunlap JC (2008) Salad days in the rhythms trade. Genetics 178(1):1–13
Dunlap JC, Loros JJ (2018) Just-so stories and origin myths: phosphorylation and structural disorder in circadian clock proteins. Mol Cell 69(2):165–168. https://doi.org/10.1016/j.molcel.2017.11.028
Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer Associates, Sunderland, Mass
Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O’Neill NS, Reddy AB (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485(7399):459–464. https://doi.org/10.1038/nature11088 (nature11088 [pii])
Edmunds LN Jr, Apter RI, Rosenthal PJ, Shen WK, Woodward JR (1979) Light effects in yeast: persisting oscillations in cell division activity and amino acid transport in cultures of Saccharomyces cerevisiae entrained by light-dark cycles. Photochem Photobiol 30(5):595–601
Eelderink-Chen Z, Mazzotta G, Sturre M, Bosman J, Roenneberg T, Merrow M (2010) A circadian clock in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 107 (5):2043–2047. https://doi.org/10.1073/pnas.0907902107
Elad Y, Williamson B, Tudzynski P, Delen N (2007) Botrytis spp. and diseases they cause in agricultural systems—an introduction. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Springer Netherlands, pp 1–8. https://doi.org/10.1007/978-1-4020-2626-3_1
Elya C, Lok TC, Spencer QE, McCausland H, Martinez CC, Eisen M (2018) Robust manipulation of the behavior of Drosophila melanogaster by a fungal pathogen in the laboratory. Elife 7. https://doi.org/10.7554/elife.34414
Feeney KA, Hansen LL, Putker M, Olivares-Yanez C, Day J, Eades LJ, Larrondo LF, Hoyle NP, O’Neill JS, van Ooijen G (2016) Daily magnesium fluxes regulate cellular timekeeping and energy balance. Nature 532(7599):375–379. https://doi.org/10.1038/nature17407
Feigin RD, San Joaquin VH, Haymond MW, Wyatt RG (1969) Daily periodicity of susceptibility of mice to pneumococcal infection. Nature 224(5217):379–380
Franco DL, Canessa P, Bellora N, Risau-Gusman S, Olivares-Yanez C, Perez-Lara R, Libkind D, Larrondo LF, Marpegan L (2017) Spontaneous circadian rhythms in a cold-adapted natural isolate of Aureobasidium pullulans. Sci Rep 7(1):13837. https://doi.org/10.1038/s41598-017-14085-6
Froehlich AC, Liu Y, Loros JJ, Dunlap JC (2002) White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297(5582):815–819. https://doi.org/10.1126/science.1073681 (1073681 [pii])
Froehlich AC, Loros JJ, Dunlap JC (2003) Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc Natl Acad Sci USA 100 (10):5914–5919. https://doi.org/10.1073/pnas.1030057100 1030057100 [pii]
Fuller KK, Loros JJ, Dunlap JC (2015) Fungal photobiology: visible light as a signal for stress, space and time. Curr Genet 61(3):275–288. https://doi.org/10.1007/s00294-014-0451-0
Fuller KK, Ringelberg CS, Loros JJ, Dunlap JC (2013) The fungal pathogen Aspergillus fumigatus regulates growth, metabolism, and stress resistance in response to light. MBio 4(2). doi:mBio.00142-13 [pii] https://doi.org/10.1128/mbio.00142-13
Gooch VD, Johnson AE, Bourne BJ, Nix BT, Maas JA, Fox JA, Loros JJ, Larrondo LF, Dunlap JC (2014) A kinetic study of the effects of light on circadian rhythmicity of the frq Promoter of Neurospora crassa. J Biol Rhythms 29(1):38–48. https://doi.org/10.1177/0748730413517981
Gooch VD, Mehra A, Larrondo LF, Fox J, Touroutoutoudis M, Loros JJ, Dunlap JC (2008) Fully codon-optimized luciferase uncovers novel temperature characteristics of the Neurospora clock. Eukaryot Cell 7(1):28–37. https://doi.org/10.1128/ec.00257-07
Goodspeed D, Chehab EW, Covington MF, Braam J (2013) Circadian control of jasmonates and salicylates: the clock role in plant defense. Plant Signal Behav 8(2):e23123. https://doi.org/10.4161/psb.23123
Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF (2012) Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc Natl Acad Sci USA 109(12):4674–4677. https://doi.org/10.1073/pnas.1116368109
Greene AV, Keller N, Haas H, Bell-Pedersen D (2003) A circadian oscillator in Aspergillus spp. Regulates daily development and gene expression. Eukaryot Cell 2(2):231–237. https://doi.org/10.1128/ec.2.2.231-237.2003
Guo J, Liu Y (2010) Molecular mechanism of the Neurospora circadian oscillator. Protein Cell 1(4):331–341. https://doi.org/10.1007/s13238-010-0053-7
Hajek AE, Soper RS (1992) Temporal dynamics of Entomophaga maimaiga after death of gypsy moth (Lepidoptera: Lymantriidae) larval hosts. Environ Entomol 21(1):129–135. https://doi.org/10.1093/ee/21.1.129
Hamilton ED (1959) Studies on the air spora. Acta Allergol 13(2):143–173
Hawking F, Worms MJ, Gammage K (1968) Host temperature and control of 24-hour and 48-hour cycles in malaria parasites. Lancet 1(7541):506–509
He Q, Liu Y (2005) Degradation of the Neurospora circadian clock protein FREQUENCY through the ubiquitin-proteasome pathway. Biochem Soc Trans 33(Pt 5):953–956
Hernandez RR, Allen MF (2013) Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the soil ecosystem observatory. New Phytol 200(2):547–557. https://doi.org/10.1111/nph.12393
Hevia MA, Canessa P, Larrondo LF (2016) Circadian clocks and the regulation of virulence in fungi: getting up to speed. Semin Cell Dev Biol 57:147–155. https://doi.org/10.1016/j.semcdb.2016.03.021
Hevia MA, Canessa P, Muller-Esparza H, Larrondo LF (2015) A circadian oscillator in the fungus Botrytis cinerea regulates virulence when infecting Arabidopsis thaliana. Proc Natl Acad Sci USA 112(28):8744–8749. https://doi.org/10.1073/pnas.1508432112
Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schussler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111(Pt 5):509–547. https://doi.org/10.1016/j.mycres.2007.03.004
Hirako IC, Assis PA, Hojo-Souza NS, Reed G, Nakaya H, Golenbock DT, Coimbra RS, Gazzinelli RT (2018) Daily rhythms of TNFalpha expression and food intake regulate synchrony of plasmodium stages with the host circadian cycle. Cell Host Microbe 23(6):796–808 e796. https://doi.org/10.1016/j.chom.2018.04.016
Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecol 11:13. https://doi.org/10.1186/1472-6785-11-13
Hurley J, Loros JJ, Dunlap JC (2015) Dissecting the mechanisms of the clock in Neurospora. Methods Enzymol 551:29–52. https://doi.org/10.1016/bs.mie.2014.10.009
Hurley JM, Dasgupta A, Emerson JM, Zhou X, Ringelberg CS, Knabe N, Lipzen AM, Lindquist EA, Daum CG, Barry KW, Grigoriev IV, Smith KM, Galagan JE, Bell-Pedersen D, Freitag M, Cheng C, Loros JJ, Dunlap JC (2014) Analysis of clock-regulated genes in Neurospora reveals widespread posttranscriptional control of metabolic potential. Proc Natl Acad Sci USA 111 (48):16995–17002. https://doi.org/10.1073/pnas.1418963111
Hurley JM, Larrondo LF, Loros JJ, Dunlap JC (2013) Conserved RNA helicase FRH acts nonenzymatically to support the intrinsically disordered neurospora clock protein FRQ. Mol Cell 52(6):832–843. https://doi.org/10.1016/j.molcel.2013.11.005
Idnurm A, Heitman J (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol 3(4):e95. https://doi.org/10.1371/journal.pbio.0030095 (04-PLBI-RA-0453R3 [pii])
Ingle RA, Stoker C, Stone W, Adams N, Smith R, Grant M, Carre I, Roden LC, Denby KJ (2015) Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. Plant J 84(5):937–948. https://doi.org/10.1111/tpj.13050
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lucking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443(7113):818–822. https://doi.org/10.1038/nature05110
Jarvis WR (1977) Botryotinia and botrytis species. Taxonomy and pathogenicity. Agriculture and agri-food canada—agriculture et Agroalimentaire Canada 15
Jensen C, Lysek G (1983) Differences in the mycelial growth rhythms in a population of Sclerotinia fructigena Experientia
Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk HD, Kramer A, Maier B (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci USA 106(50):21407–21412. https://doi.org/10.1073/pnas.0906361106
Kim H, Ridenour JB, Dunkle LD, Bluhm BH (2011a) Regulation of stomatal tropism and infection by light in Cercospora zeae-maydis: evidence for coordinated host/pathogen responses to photoperiod? PLoS Pathog 7(7):e1002113. https://doi.org/10.1371/journal.ppat.1002113 (PPATHOGENS-D-10-00513 [pii])
Kim S, Singh P, Park J, Park S, Friedman A, Zheng T, Lee YH, Lee K (2011b) Genetic and molecular characterization of a blue light photoreceptor MGWC-1 in Magnaporth oryzae. Fungal Genet Biol: FG & B 48(4):400–407. https://doi.org/10.1016/j.fgb.2011.01.004
Korneli C, Danisman S, Staiger D (2014) Differential control of pre-invasive and post-invasive antibacterial defense by the Arabidopsis circadian clock. Plant Cell Physiol 55(9):1613–1622. https://doi.org/10.1093/pcp/pcu092
Krasnoff SB, Watson DW, Gibson DM, Kwan EC (1995) Behavioral effects of the entomopathogenic fungus, Entomophthora muscae on its host Musca domestica: postural changes in dying hosts and gated pattern of mortality. J Insect Physiol 41:895–903. https://doi.org/10.1016/0022-1910(95)00026-Q
Labrecque N, Cermakian N (2015) Circadian clocks in the immune system. J Biol Rhythms 30(4):277–290. https://doi.org/10.1177/0748730415577723
Lacey ME (1962) The summer air-spora of two contrasting adjacent rural sites. J Gen Microbiol 29:485–501. https://doi.org/10.1099/00221287-29-3-485
Larrondo LF, Colot HV, Baker CL, Loros JJ, Dunlap JC (2009) Fungal functional genomics: tunable knockout-knock-in expression and tagging strategies. Eukaryot Cell 8(5):800–804. https://doi.org/10.1128/ec.00072-09
Larrondo LF, Loros JJ, Dunlap JC (2012) High-resolution spatiotemporal analysis of gene expression in real time: in vivo analysis of circadian rhythms in Neurospora crassa using a FREQUENCY-luciferase translational reporter. Fungal Genet Biol 49(9):681–683. https://doi.org/10.1016/j.fgb.2012.06.001
Larrondo LF, Olivares-Yanez C, Baker CL, Loros JJ, Dunlap JC (2015) Circadian rhythms. Decoupling circadian clock protein turnover from circadian period determination. Science 347(6221):1257277. https://doi.org/10.1126/science.1257277
Latorre B, Rioja M (2002) Efecto de la Temperatura y de la Humedad Relativa Sobre la Germinación de Conidias de Botrytis cinerea. Ciencia e investigación agraria: revista latinoamericana de ciencias de la agricultura 29(2):66–72
Lee JE, Edery I (2008) Circadian regulation in the ability of Drosophila to combat pathogenic infections. Curr Biol 18(3):195–199. https://doi.org/10.1016/j.cub.2007.12.054 (S0960-9822(07)02486-4 [pii])
Lee K, Dunlap JC, Loros JJ (2003) Roles for WHITE COLLAR-1 in circadian and general photoperception in Neurospora crassa. Genetics 163(1):103–114
Lee K, Singh P, Chung WC, Ash J, Kim TS, Hang L, Park S (2006) Light regulation of asexual development in the rice blast fungus, Magnaporthe oryzae. Fungal Genet Biol: FG & B 43(10):694–706. https://doi.org/10.1016/j.fgb.2006.04.005
Lee SJ, Kong M, Morse D, Hijri M (2018) Expression of putative circadian clock components in the arbuscular mycorrhizal fungus Rhizoglomus irregulare. Mycorrhiza. https://doi.org/10.1007/s00572-018-0843-y
Lowrey PL, Takahashi JS (2011) Genetics of circadian rhythms in Mammalian model organisms. Adv Genet 74:175–230. https://doi.org/10.1016/b978-0-12-387690-4.00006-4
Mackey SR, Golden SS, Ditty JL (2011) The itty-bitty time machine genetics of the cyanobacterial circadian clock. Adv Genet 74:13–53. https://doi.org/10.1016/b978-0-12-387690-4.00002-7
McClung C (2006) Plant circadian rhythms. The Plant cell 18(4):792–803
McClung CR (2001) Circadian rhythms in plants. Annu Rev Plant Physiol Plant Mol Biol 52:139–162. https://doi.org/10.1146/annurev.arplant.52.1.139
Mehra A, Shi M, Baker CL, Colot HV, Loros JJ, Dunlap JC (2009) A role for casein kinase 2 in the mechanism underlying circadian temperature compensation. Cell 137(4):749–760
Merrow MW, Dunlap JC (1994) Intergeneric complementation of a circadian rhythmicity defect: phylogenetic conservation of structure and function of the clock gene frequency. EMBO J 13(10):2257–2266
Mideo N, Reece SE, Smith AL, Metcalf CJ (2013) The Cinderella syndrome: why do malaria-infected cells burst at midnight? Trends Parasitol 29(1):10–16. https://doi.org/10.1016/j.pt.2012.10.006
Milner RJ, Holdom DG, Glare TR (1983) Diurnal patterns of mortality in aphids infected by entomophthoran fungi. Entomol Exp Appl 36:37–42. https://doi.org/10.1111/j.1570-7458.1984.tb03404.x
Montenegro-Montero A, Canessa P, Larrondo LF (2015) Around the fungal clock: recent advances in the molecular study of circadian clocks in neurospora and other fungi. Adv Genet 92:107–184. https://doi.org/10.1016/bs.adgen.2015.09.003
Montenegro-Montero A, Larrondo LF (2013) The neurospora circadian system: from genes to proteins and back in less than 24 hours. In: McCluskey K, Kasbekar D (eds) Neurospora. Genomics and molecular biology. Caister Academic Press, Norfolk, UK
Montenegro-Montero A, Larrondo LF (2016) In the driver’s seat: the case for transcriptional regulation and coupling as relevant determinants of the circadian transcriptome and proteome in Eukaryotes. J Biol Rhythms 31(1):37–47. https://doi.org/10.1177/0748730415607321
Mouahid G, Idris MA, Verneau O, Theron A, Shaban MM, Mone H (2012) A new chronotype of Schistosoma mansoni: adaptive significance. Trop Med Int Health 17(6):727–732. https://doi.org/10.1111/j.1365-3156.2012.02988.x
Newman GG, Carner GR (1974) Diel periodicity of Entomophthora gammae in the soybean looper. Environ Entomol 3:888–890
Nielsen C, Hajek AE (2006) Diurnal pattern of death and sporulation in Entomophaga maimaiga-infected Lymantria dispar. Entomol Exp Appl 118(3):237–243. https://doi.org/10.1111/j.1570-7458.2006.00382.x
Olivares-Yanez C, Emerson J, Kettenbach A, Loros JJ, Dunlap JC, Larrondo LF (2016) Modulation of circadian gene expression and metabolic compensation by the RCO-1 co-repressor of Neurospora crassa. Genetics. https://doi.org/10.1534/genetics.116.191064
Oliveira AG, Stevani CV, Waldenmaier HE, Viviani V, Emerson JM, Loros JJ, Dunlap JC (2015) Circadian control sheds light on fungal bioluminescence. Curr Biol 25(7):964–968. https://doi.org/10.1016/j.cub.2015.02.021
Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95(15):8660–8664
Paschos GK, FitzGerald GA (2017) Circadian clocks and metabolism: implications for microbiome and aging. Trends Genet 33(10):760–769. https://doi.org/10.1016/j.tig.2017.07.010
Perelis M, Ramsey KM, Bass J (2015) The molecular clock as a metabolic rheostat. Diabetes Obes Metab 17(Suppl 1):99–105. https://doi.org/10.1111/dom.12521
Pregueiro AM, Price-Lloyd N, Bell-Pedersen D, Heintzen C, Loros JJ, Dunlap JC (2005) Assignment of an essential role for the Neurospora frequency gene in circadian entrainment to temperature cycles. Proc Natl Acad Sci USA 102(6):2210–2215
Prior KF, van der Veen DR, O’Donnell AJ, Cumnock K, Schneider D, Pain A, Subudhi A, Ramaprasad A, Rund SSC, Savill NJ, Reece SE (2018) Timing of host feeding drives rhythms in parasite replication. PLoS Pathog 14(2):e1006900. https://doi.org/10.1371/journal.ppat.1006900
Proietto M, Bianchi MM, Ballario P, Brenna A (2015) Epigenetic and posttranslational modifications in light signal transduction and the circadian clock in Neurospora crassa. Int J Mol Sci 16(7):15347–15383. https://doi.org/10.3390/ijms160715347
Ramsdale M (2008) Circadian rhythms in filamentous fungi. In: Gow NAR, Robson GD, Gadd GM (eds) The fungal colony, vol First digitally printed version 2008. British Mycological Society Symposia, pp 75–107
Rijo-Ferreira F, Carvalho T, Afonso C, Sanches-Vaz M, Costa RM, Figueiredo LM, Takahashi JS (2018) Sleeping sickness is a circadian disorder. Nat Commun 9(1):62. https://doi.org/10.1038/s41467-017-02484-2
Rijo-Ferreira F, Pinto-Neves D, Barbosa-Morais NL, Takahashi JS, Figueiredo LM (2017a) Trypanosoma brucei metabolism is under circadian control. Nat Microbiol 2:17032. https://doi.org/10.1038/nmicrobiol.2017.32
Rijo-Ferreira F, Takahashi JS, Figueiredo LM (2017b) Circadian rhythms in parasites. PLoS Pathog 13(10):e1006590. https://doi.org/10.1371/journal.ppat.1006590
Roden LC, Ingle RA (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell 21(9):2546–2552. https://doi.org/10.1105/tpc.109.069922 (tpc.109.069922 [pii])
Romanowski A, Yanovsky MJ (2015) Circadian rhythms and post-transcriptional regulation in higher plants. Front Plant Sci 6:437. https://doi.org/10.3389/fpls.2015.00437
Rosbash M (2009) The implications of multiple circadian clock origins. PLoS Biol 7(3):e62. https://doi.org/10.1371/journal.pbio.1000062
Ruiz-Roldan MC, Garre V, Guarro J, Marine M, Roncero MI (2008) Role of the white collar 1 photoreceptor in carotenogenesis, UV resistance, hydrophobicity, and virulence of Fusarium oxysporum. Eukaryot Cell 7(7):1227–1230. https://doi.org/10.1128/ec.00072-08 (EC.00072-08 [pii])
Salichos L, Rokas A (2010) The diversity and evolution of circadian clock proteins in fungi. Mycologia 102(2):269–278
Sancar C, Sancar G, Ha N, Cesbron F, Brunner M (2015) Dawn- and dusk-phased circadian transcription rhythms coordinate anabolic and catabolic functions in Neurospora. BMC Biol 13(1):17. https://doi.org/10.1186/s12915-015-0126-4
Sancar G, Sancar C, Brugger B, Ha N, Sachsenheimer T, Gin E, Wdowik S, Lohmann I, Wieland F, Hofer T, Diernfellner A, Brunner M (2011) A global circadian repressor controls antiphasic expression of metabolic genes in Neurospora. Mol Cell 44(5):687–697. https://doi.org/10.1016/j.molcel.2011.10.019 (S1097-2765(11)00902-6 [pii])
Santamaria-Hernando S, Rodriguez-Herva JJ, Martinez-Garcia PM, Rio-Alvarez I, Gonzalez-Melendi P, Zamorano J, Tapia C, Rodriguez-Palenzuela P, Lopez-Solanilla E (2018) Pseudomonas syringae pv. tomato exploits light signals to optimize virulence and colonization of leaves. Environ Microbiol. https://doi.org/10.1111/1462-2920.14331
Sargent ML, Briggs WR, Woodward DO (1966) Circadian nature of a rhythm expressed by an invertaseless strain of Neurospora crassa. Plant Physiol 41(8):1343–1349
Scheiermann C, Gibbs J, Ince L, Loudon A (2018) Clocking into immunity. Nat Rev Immunol 18(7):423–437. https://doi.org/10.1038/s41577-018-0008-4
Schmidle A (1951) Die Tagesperiodizität der asexuellen Reproduktion von Pilobolus spaerosporus. Arch Mikrobiol 16:80–100
Schumacher J (2017) How light affects the life of Botrytis. Fungal Genet Biol 106:26–41. https://doi.org/10.1016/j.fgb.2017.06.002
Schumacher J, Tudzynski P (2012) Morphogenesis and infection in Botrytis cinerea. In: Perez-Martın J, Di Pietro A (eds) Morphogenesis and pathogenicity in fungi. Topics in current genetics, vol 22. Springer-Verlag Berlin Heidelberg 2012, pp 225–241. https://doi.org/10.1007/978-3-642-22916-9_11
Sharma M, Bhatt D (2014) The circadian clock and defence signalling in plants. Molecular Plant Pathology. https://doi.org/10.1111/mpp.12178
Shi M, Larrondo LF, Loros JJ, Dunlap JC (2007) A developmental cycle masks output from the circadian oscillator under conditions of choline deficiency in Neurospora. Proc Natl Acad Sci USA 104(50):20102–20107. https://doi.org/10.1073/pnas.0706631104
Shin J, Heidrich K, Sanchez-Villarreal A, Parker JE, Davis SJ (2012) TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis. Plant Cell 24(6):2470–2482. https://doi.org/10.1105/tpc.111.095430
Slepecky RA, Starmer WT (2009) Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101(6):823–832
Smith KM, Sancar G, Dekhang R, Sullivan CM, Li S, Tag AG, Sancar C, Bredeweg EL, Priest HD, McCormick RF, Thomas TL, Carrington JC, Stajich JE, Bell-Pedersen D, Brunner M, Freitag M (2010) Transcription factors in light and circadian clock signaling networks revealed by genomewide mapping of direct targets for Neurospora white collar complex. Eukaryot Cell 9(10):1549–1556. https://doi.org/10.1128/ec.00154-10 (EC.00154-10 [pii])
Steinkraus DC, Hajek AE, Liebherr JK (2017) Zombie soldier beetles: epizootics in the goldenrod soldier beetle, Chauliognathus pensylvanicus (Coleoptera: Cantharidae) caused by Eryniopsis lampyridarum (Entomophthoromycotina: Entomophthoraceae). J Invertebr Pathol 148:51–59. https://doi.org/10.1016/j.jip.2017.05.002
Steinkraus DC, Hollingsworth RG, Boys GO (1996) Aerial spores of Neozygites fresenii (EntoInophthorales: Neozygitaceae): density, periodicity, and potential role in CoUon Aphid (HoInoptera: Aphididae) Epizootics. Environ Entomol 25:48–57
Steyaert JM, Weld RJ, Loguercio LL, Stewart A (2010) Rhythmic conidiation in the blue-light fungus Trichoderma pleuroticola. Fungal Biol 114(2–3):219–223. https://doi.org/10.1016/j.funbio.2010.01.001 (S1878-6146(10)00003-6 [pii])
Thaiss CA, Levy M, Korem T, Dohnalova L, Shapiro H, Jaitin DA, David E, Winter DR, Gury-BenAri M, Tatirovsky E, Tuganbaev T, Federici S, Zmora N, Zeevi D, Dori-Bachash M, Pevsner-Fischer M, Kartvelishvily E, Brandis A, Harmelin A, Shibolet O, Halpern Z, Honda K, Amit I, Segal E, Elinav E (2016) Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell 167 (6):1495–1510 e1412. https://doi.org/10.1016/j.cell.2016.11.003
Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abramson L, Katz MN, Korem T, Zmora N, Kuperman Y, Biton I, Gilad S, Harmelin A, Shapiro H, Halpern Z, Segal E, Elinav E (2014) Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159(3):514–529. https://doi.org/10.1016/j.cell.2014.09.048
Traeger S, Altegoer F, Freitag M, Gabaldon T, Kempken F, Kumar A, Marcet-Houben M, Poggeler S, Stajich JE, Nowrousian M (2013) The genome and development-dependent transcriptomes of Pyronema confluens: a window into fungal evolution. PLoS Genet 9(9):e1003820. https://doi.org/10.1371/journal.pgen.1003820
Traeger S, Nowrousian M (2015) Analysis of circadian rhythms in the basal filamentous Ascomycete Pyronema confluens. G3 (Bethesda). https://doi.org/10.1534/g3.115.020461
Tudzynski P, Siewers V (2004) Approaches to molecular genetics and genomics of Botrytis. In: Elad Y WB, Tudzynski P, Delen Neds (ed) Botrytis: biology, pathology and control, vol XIX. p 428
Tuzdynski P, Kokkelink L (2009) Botrytis cinerea: molecular aspects of a necrotrophic life style. In: H D (ed) The Mycota V: plant relationships, 2nd edn. Springer-Verlag, Berlin, Heidelberg, pp 29–50
Uebelmesser ER (1954) Uber den endonomen Tagesrhythmus der Sporangientragerbildung bon Pilobolus. Arch Mikrobiol 20:1–33
Veloso J, van Kan JAL (2018) Many shades of grey in botrytis-host plant interactions. Trends Plant Sci 23(7):613–622. https://doi.org/10.1016/j.tplants.2018.03.016
Wang B, Kettenbach AN, Gerber SA, Loros JJ, Dunlap JC (2014) Neurospora WC-1 recruits SWI/SNF to remodel frequency and initiate a circadian cycle. PLoS Genet 10(9):e1004599. https://doi.org/10.1371/journal.pgen.1004599
Wang W, Barnaby JY, Tada Y, Li H, Tor M, Caldelari D, Lee DU, Fu XD, Dong X (2011) Timing of plant immune responses by a central circadian regulator. Nature 470(7332):110–114
Welsh DK, Imaizumi T, Kay SA (2005) Real-time reporting of circadian-regulated gene expression by luciferase imaging in plants and mammalian cells. Methods Enzymol 393:269–288
West AC, Bechtold DA (2015) The cost of circadian desynchrony: evidence, insights and open questions. BioEssays 37(7):777–788. https://doi.org/10.1002/bies.201400173
Wilding N (1970) Entomophthora conidia in the air-spora. J Gen Microbiol 62(2):149–157. https://doi.org/10.1099/00221287-62-2-149
Yerushalmi S, Green RM (2009) Evidence for the adaptive significance of circadian rhythms. Ecol Lett 12(9):970–981. https://doi.org/10.1111/j.1461-0248.2009.01343.x (ELE1343 [pii])
Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR, McDowell JM, Kong D, Kwak JM, Lu H (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog 9(6):e1003370. https://doi.org/10.1371/journal.ppat.1003370
Zhao X, Spraker JE, Bok JW, Velk T, He ZM, Keller NP (2017) A cellular fusion cascade regulated by LaeA is required for sclerotial development in Aspergillus flavus. Front Microbiol 8:1925. https://doi.org/10.3389/fmicb.2017.01925
Zhou Z, Liu X, Hu Q, Zhang N, Sun G, Cha J, Wang Y, Liu Y, He Q (2013) Suppression of WC-independent frequency transcription by RCO-1 is essential for Neurospora circadian clock. Proc Natl Acad Sci USA 110(50):E4867-4874. https://doi.org/10.1073/pnas.1315133110
Acknowledgements
Work in our laboratories is funded by iBio, Iniciativa Científica Milenio-MINECON (L.F.L and P.C.), and CONICYT/FONDECYT 1171151 and International Research Scholar of the Howard Hughes Medical Institute, both to L.F.L.
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Larrondo, L.F., Canessa, P. (2018). The Clock Keeps on Ticking: Emerging Roles for Circadian Regulation in the Control of Fungal Physiology and Pathogenesis. In: Rodrigues, M. (eds) Fungal Physiology and Immunopathogenesis . Current Topics in Microbiology and Immunology, vol 422. Springer, Cham. https://doi.org/10.1007/82_2018_143
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