The clock in growing hyphae and their synchronization in Neurospora crassa.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
18 Jun 2024
18 Jun 2024
Historique:
received:
26
04
2023
accepted:
07
06
2024
medline:
19
6
2024
pubmed:
19
6
2024
entrez:
18
6
2024
Statut:
epublish
Résumé
Utilizing a microfluidic chip with serpentine channels, we inoculated the chip with an agar plug with Neurospora crassa mycelium and successfully captured individual hyphae in channels. For the first time, we report the presence of an autonomous clock in hyphae. Fluorescence of a mCherry reporter gene driven by a clock-controlled gene-2 promoter (ccg-2p) was measured simultaneously along hyphae every half an hour for at least 6 days. We entrained single hyphae to light over a wide range of day lengths, including 6,12, 24, and 36 h days. Hyphae tracked in individual serpentine channels were highly synchronized (K = 0.60-0.78). Furthermore, hyphae also displayed temperature compensation properties, where the oscillation period was stable over a physiological range of temperatures from 24 °C to 30 °C (Q
Identifiants
pubmed: 38890525
doi: 10.1038/s42003-024-06429-6
pii: 10.1038/s42003-024-06429-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
735Subventions
Organisme : National Science Foundation (NSF)
ID : 1713746
Organisme : National Science Foundation (NSF)
ID : 2041546
Informations de copyright
© 2024. The Author(s).
Références
Kitano, H. Systems biology: a brief overview. Science 295, 1662–1664 (2002).
pubmed: 11872829
doi: 10.1126/science.1069492
Deng, Z. et al. Synchronizing stochastic circadian oscillators in single cells of Neurospora crassa. Sci. Rep. 6, 35828 (2016).
pubmed: 27786253
pmcid: 5082370
doi: 10.1038/srep35828
Deng, Z. et al. Single cells of Neurospora crassa show circadian oscillations as well light entrainment and temperature compensation. IEEE Access 7, 49403–49417 (2019).
doi: 10.1109/ACCESS.2019.2910731
Gould, P. D. et al. Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression. eLife 7, e31700 (2018).
pubmed: 29697372
pmcid: 5988422
doi: 10.7554/eLife.31700
Grima, B., Chélot, E., Xia, R. & Rouyer, F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869–873 (2004).
pubmed: 15483616
doi: 10.1038/nature02935
Yamaguchi, S. et al. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 302, 1408–1412 (2003).
pubmed: 14631044
doi: 10.1126/science.1089287
Gooch, V. D. et al. Fully codon-optimized luciferase uncovers novel temperature characteristics of the Neurospora clock. Eukaryot. Cell 7, 28–37 (2008).
pubmed: 17766461
doi: 10.1128/EC.00257-07
Dharmananda, S. Studies of the Circadian Clock of Neurospora Crassa: Light-Induced Phase Shifting. (University of California, Santa Cruz, 1980).
Lindgren, K. M. Characterization of ccg-1, a Clock-Controlled Gene of Neurospora crassa. PhD dissertation. (Dartmouth College, 1994).
Paijmans, J., Bosman, M., Wolde, P. R. T. & Lubensky, D. K. Discrete gene replication events drive coupling between the cell cycle and circadian clocks. Proc. Natl Acad. Sci. USA 113, 4063–4068 (2015).
doi: 10.1073/pnas.1507291113
Yang, Q., Pando, B. F., Dong, G., Golden, S. S. & van Oudenaarden, A. Circadian gating of the cell cycle revealed in single cyanobacterial cells. Science 327, 1522 (2010).
pubmed: 20299597
pmcid: 3118046
doi: 10.1126/science.1181759
Hong, C. I. et al. Circadian rhythms synchronize mitosis in Neurospora crassa. Proc. Natl Acad. Sci. USA 111, 1397–1402 (2014).
pubmed: 24474764
pmcid: 3910635
doi: 10.1073/pnas.1319399111
Nudleman, E., Wall, D. & Kaiser, D. Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309, 125–127 (2005).
pubmed: 15994555
doi: 10.1126/science.1112440
Arbel-Goren, R. et al. Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments. Elife 10, e64348 (2021).
pubmed: 33749592
pmcid: 8064755
doi: 10.7554/eLife.64348
Ko, C. H. et al. Emergence of noise-induced oscillations in the central circadian pacemaker. PLoS Biol. 8, e1000513 (2010).
pubmed: 20967239
pmcid: 2953532
doi: 10.1371/journal.pbio.1000513
Caranica, C., Al-Omari, A., Schuttler, H. B. & Arnold, J. Identifying a stochastic clock network with light entrainment for single cells of Neurospora crassa. Sci. Rep. 10, 15168 (2020).
pubmed: 32938998
pmcid: 7495483
doi: 10.1038/s41598-020-72213-1
Lee, K. K., Labiscsak, L., Ahn, C. H. & Hong, C. I. Spiral-based microfluidic device for long-term time course imaging of Neurospora crassa with single nucleus resolution. Fungal Genet. Biol. 94, 11–14 (2016).
pubmed: 27345439
doi: 10.1016/j.fgb.2016.06.004
Geng, T. et al. Compartmentalized microchannel array for high-throughput analysis of single cell polarized growth and dynamics. Sci. Rep. 5, 16111 (2015).
pubmed: 26530004
pmcid: 4632079
doi: 10.1038/srep16111
Voorsluijs, V., Dawson, S. P., De Decker, Y. & Dupont, G. Deterministic limit of intracellular calcium spikes. Phys. Rev. Lett. 122, 088101 (2019).
pubmed: 30932600
doi: 10.1103/PhysRevLett.122.088101
Roper, M., Lee, C., Hickey, P. C. & Gladfelter, A. S. Life as a moving fluid: fate of cytoplasmic macromolecules in dynamic fungal syncytia. Curr. Opin. Microbiol. 26, 116–122 (2015).
pubmed: 26226449
pmcid: 4577449
doi: 10.1016/j.mib.2015.07.001
Ramos-García, S. L., Roberson, R. W., Freitag, M., Bartnicki-García, S. & Mouriño-Pérez, R. R. Cytoplasmic bulk flow propels nuclei in mature hyphae of Neurospora crassa. Eukaryot. Cell 8, 1880 (2009).
pubmed: 19684281
pmcid: 2794216
doi: 10.1128/EC.00062-09
Bartnicki-Garcia, S., Hergert, F. & Gierz, G. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma 153, 46–57 (1989).
doi: 10.1007/BF01322464
Schnepf, A., Roose, T. & Schweiger, P. Growth model for arbuscular mycorrhizal fungi. J. R. Soc. Interface 5, 773–784 (2008).
pubmed: 18077246
doi: 10.1098/rsif.2007.1250
Dong, W. et al. Systems biology of the clock in Neurospora crassa. PloS ONE 3, e3105 (2008).
pubmed: 18769678
pmcid: 2518617
doi: 10.1371/journal.pone.0003105
Bell-Pedersen, D., Dunlap, J. C. & Loros, J. J. The Neurospora circadian clock-controlled gene, ccg-2, is allelic to eas and encodes a fungal hydrophobin required for formation of the conidial rodlet layer. Genes Dev. 6, 2382–2394 (1992).
pubmed: 1459460
doi: 10.1101/gad.6.12a.2382
Castro-Longoria, E., Ferry, M., Bartnicki-Garcia, S., Hasty, J. & Brody, S. Circadian rhythms in Neurospora crassa: dynamics of the clock component frequency visualized using a fluorescent reporter. Fungal Genet. Biol. 47, 332–341 (2010).
pubmed: 20051268
pmcid: 2935182
doi: 10.1016/j.fgb.2009.12.013
Cheong, J. H. et al. The macroscopic limit to synchronization of cellular clocks in single cells of Neurospora crassa. Sci. Rep. 12, 6750 (2022).
pubmed: 35468928
pmcid: 9039089
doi: 10.1038/s41598-022-10612-2
Judge, M., Griffith, J. & Arnold, J. Aging and the biological clock. Healthy Ageing Long. 7, 211–234 (2017).
doi: 10.1007/978-3-319-64543-8_10
Crosthwaite, S. K., Dunlap, J. C. & Loros, J. J. Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science 276, 763–769 (1997).
pubmed: 9115195
doi: 10.1126/science.276.5313.763
Freitag, M., Hickey, P. C., Raju, N. B., Selker, E. U. & Read, N. D. GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 41, 897–910 (2004).
pubmed: 15341912
doi: 10.1016/j.fgb.2004.06.008
Shinomoto, S. & Kuramoto, Y. Phase transitions in active rotator systems. Prog. Theor. Phys. 75, 1105–1110 (1986).
doi: 10.1143/PTP.75.1105
Caranica, C. et al. What is phase in cellular clocks? Yale J. Biol. Med. 92, 169–178 (2019).
pubmed: 31249477
pmcid: 6585513
Gardner, G. F. & Feldman, J. F. Temperature compensation of circadian period length in clock mutants of Neurospora crassa 1. Plant Physiol. 68, 1244–1248 (1981).
pubmed: 16662086
pmcid: 426081
doi: 10.1104/pp.68.6.1244
Kurosawa, G., Fujioka, A., Koinuma, S., Mochizuki, A. & Shigeyoshi, Y. Temperature-amplitude coupling for stable biological rhythms at different temperatures. PloS Comput. Biol. 13, e1005501 (2017).
pubmed: 28594845
pmcid: 5464531
doi: 10.1371/journal.pcbi.1005501
Yu, Y. et al. A genetic network for the clock of Neurospora crassa. Proc. Natl Acad. Sci. USA 104, 2809–2814 (2007).
pubmed: 17301235
pmcid: 1797628
doi: 10.1073/pnas.0611005104
Mouriño-Pérez, R. R., Roberson, R. W. & Bartnicki-García, S. Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa. Fungal Genet. Biol. 43, 389–400 (2006).
pubmed: 16621627
doi: 10.1016/j.fgb.2005.10.007
Pieuchot, L. et al. Cellular subcompartments through cytoplasmic streaming. Dev. Cell 34, 410–420 (2015).
pubmed: 26305593
doi: 10.1016/j.devcel.2015.07.017
Lai, J. et al. Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity. Proc. Natl Acad. Sci. USA 109, 15781–15786 (2012).
pubmed: 22955885
pmcid: 3465371
doi: 10.1073/pnas.1207467109
Markham, P. Occlusions of septal pores in filamentous fungi. Mycol. Res. 98, 1089–1106 (1994).
doi: 10.1016/S0953-7562(09)80195-0
Martegani, E., Levi, M., Trezzi, F. & Alberghina, L. Nuclear division cycle in Neurospora crassa hyphae under different growth conditions. J. Bacteriol. 142, 268–275 (1980).
pubmed: 6445357
pmcid: 293945
doi: 10.1128/jb.142.1.268-275.1980
Aronson, B. D., Johnson, K. A., Loros, J. J. & Dunlap, J. C. Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263, 1578–1584 (1994).
pubmed: 8128244
doi: 10.1126/science.8128244
Roper, M. & Seminara, A. Mycofluidics: the fluid mechanics of fungal adaptation. Annu. Rev. Fluid Mech. 51, 511–538 (2019).
doi: 10.1146/annurev-fluid-122316-045308
Roper, M., Simonin, A., Hickey, P. C., Leeder, A. & Glass, N. L. Nuclear dynamics in a fungal chimera. Proc. Natl Acad. Sci. USA 110, 12875–12880 (2013).
pubmed: 23861490
pmcid: 3740868
doi: 10.1073/pnas.1220842110
Teng, S. W., Mukherji, S., Moffitt, J. R., de Buyl, S. & O’Shea, E. K. Robust circadian oscillations in growing cyanobacteria require transcriptional feedback. Science 340, 737–740 (2013).
pubmed: 23661759
pmcid: 3696982
doi: 10.1126/science.1230996
Lee, K. K., Ahn, C. H. & Hong, C. I. Circadian rhythms in Neurospora crassa on a polydimethylsiloxane microfluidic device for real-time gas perturbations. Biomicrofluidics 7, 44129 (2013).
pubmed: 24404062
doi: 10.1063/1.4819478
Danino, T., Mondragón-Palomino, O., Tsimring, L. & Hasty, J. A synchronized quorum of genetic clocks. Nature 463, 326–330 (2010).
pubmed: 20090747
pmcid: 2838179
doi: 10.1038/nature08753
Gagliano, O. et al. Synchronization between peripheral circadian clock and feeding-fasting cycles in microfluidic device sustains oscillatory pattern of transcriptome. Nat. Commun. 12, 6185 (2021).
pubmed: 34702819
pmcid: 8548598
doi: 10.1038/s41467-021-26294-9
Held, M., Kaspar, O., Edwards, C. & Nicolau, D. V. Intracellular mechanisms of fungal space searching in microenvironments. Proc. Natl Acad. Sci. USA 116, 13543–13552 (2019).
pubmed: 31213536
pmcid: 6613077
doi: 10.1073/pnas.1816423116
Fukuda, S. et al. Trade-off between plasticity and velocity in mycelial growth. Mbio 12, e30196–30120 (2021).
doi: 10.1128/mBio.03196-20
Mossu, A. et al. A silicon nanomembrane platform for the visualization of immune cell trafficking across the human blood–brain barrier under flow. J. Cereb. Blood Flow. Metab. 39, 395–410 (2019).
pubmed: 30565961
doi: 10.1177/0271678X18820584
Hopke, A. et al. Crowdsourced analysis of fungal growth and branching on microfluidic platforms. PloS ONE 16, e0257823 (2021).
pubmed: 34587206
pmcid: 8480888
doi: 10.1371/journal.pone.0257823
Chung, K., Rivet, C. A., Kemp, M. L. & Lu, H. Imaging single-cell signaling dynamics with a deterministic high-density single-cell trap array. Anal. Chem. 83, 7044–7052 (2011).
pubmed: 21809821
pmcid: 3190639
doi: 10.1021/ac2011153
Duffy, D. C., McDonald, J. C., Schueller, O. J. & Whitesides, G. M. Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal. Chem. 70, 4974–4984 (1998).
pubmed: 21644679
doi: 10.1021/ac980656z
McQuin, C. et al. CellProfiler 3.0: next-generation image processing for biology. PLOS Biol. 16, e2005970 (2018).
pubmed: 29969450
pmcid: 6029841
doi: 10.1371/journal.pbio.2005970
Marple, S. L. Computing the discrete-time “Analytic” Signal via FFT. IEEE Trans. 47, 2600–2603 (1999).
doi: 10.1109/78.782222