The Essential and the Nonessential Roles of Four Clock Elements in the Circadian Rhythm of

Overview

Journal J Fungi (Basel)

Date 2022 Jun 23

PMID 35736041

Authors

Han Peng

Yi-Lu Zhang

Sheng-Hua Ying

Ming-Guang Feng

Affiliations

Soon will be listed here.

Abstract

FRQ (frequency protein), FRH (FRQ-interacting RNA helicase), and WC1 and WC2 (white collar proteins) are major clock elements that govern the circadian rhythm in . However, deletion of is lethal for the viability of , making it elusive whether FRH is essential or nonessential for the circadian rhythm. This needs clarification in a fungus where deletion is not lethal. Here, the nuclear FRH ortholog proved nonessential for the circadian rhythm of . The nucleocytoplasmic shuttling of FRQ, WC1, and WC2 orthologs was light-dependent. Yeast two-hybrid assay validated interactions of FRQ with FRH and WC1 instead of FRH with WC1 and WC2 or FRQ with WC2. The circadian rhythm well, shown as conidiation rings of tint and dark in 15 d-old plate cultures grown at 25 °C in a light/dark cycle of 12:12, was abolished in the absence of or , partially disturbed in the absence of , but unaffected in the absence of . These results indicate a requirement of either FRQ or WC1 instead of FRH for the fungal circadian rhythm. Further analyses of and mutants revealed the dispensable and the limited roles of FRQ and FRH in the insect-pathogenic lifecycle of , respectively.

Citing Articles

The Frq-Frh Complex Light-Dependently Delays Sfl1-Induced Microsclerotia Formation in .

Nagel A, Leonard M, Maurus I, Starke J, Schmitt K, Valerius O J Fungi (Basel). 2023; 9(7).

PMID: 37504714 PMC: 10381341. DOI: 10.3390/jof9070725.

Co-Regulatory Roles of WC1 and WC2 in Asexual Development and Photoreactivation of .

Xu S, Yu L, Luo X, Ying S, Feng M J Fungi (Basel). 2023; 9(3).

PMID: 36983459 PMC: 10056576. DOI: 10.3390/jof9030290.

Comparative Roles of Rad4A and Rad4B in Photoprotection of from Solar Ultraviolet Damage.

Yu L, Xu S, Luo X, Ying S, Feng M J Fungi (Basel). 2023; 9(2).

PMID: 36836269 PMC: 9961694. DOI: 10.3390/jof9020154.

Rad1 and Rad10 Tied to Photolyase Regulators Protect Insecticidal Fungal Cells from Solar UV Damage by Photoreactivation.

Yu L, Xu S, Luo X, Ying S, Feng M J Fungi (Basel). 2022; 8(11).

PMID: 36354891 PMC: 9692854. DOI: 10.3390/jof8111124.

Circadian oscillations in and the role of core clock components in secondary metabolism, development, and mycoparasitism against the phytopathogen .

Henriquez-Urrutia M, Spanner R, Olivares-Yanez C, Seguel-Avello A, Perez-Lara R, Guillen-Alonso H Elife. 2022; 11.

PMID: 35950750 PMC: 9427114. DOI: 10.7554/eLife.71358.

References

Cheng P, Yang Y, Heintzen C, Liu Y . Coiled-coil domain-mediated FRQ-FRQ interaction is essential for its circadian clock function in Neurospora. EMBO J. 2001; 20(1-2):101-8. PMC: 140186. DOI: 10.1093/emboj/20.1.101. View

Schafmeier T, Haase A, Kaldi K, Scholz J, Fuchs M, Brunner M . Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell. 2005; 122(2):235-46. DOI: 10.1016/j.cell.2005.05.032. View

Froehlich A, Loros J, Dunlap J . Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc Natl Acad Sci U S A. 2003; 100(10):5914-9. PMC: 156301. DOI: 10.1073/pnas.1030057100. View

Crosthwaite S, Dunlap J, Loros J . Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science. 1997; 276(5313):763-9. DOI: 10.1126/science.276.5313.763. View

Tong S, Feng M . Molecular basis and regulatory mechanisms underlying fungal insecticides' resistance to solar ultraviolet irradiation. Pest Manag Sci. 2021; 78(1):30-42. DOI: 10.1002/ps.6600. View

Baker C, Loros J, Dunlap J . The circadian clock of Neurospora crassa. FEMS Microbiol Rev. 2011; 36(1):95-110. PMC: 3203324. DOI: 10.1111/j.1574-6976.2011.00288.x. View

Cha J, Yuan H, Liu Y . Regulation of the activity and cellular localization of the circadian clock protein FRQ. J Biol Chem. 2011; 286(13):11469-78. PMC: 3064202. DOI: 10.1074/jbc.M111.219782. View

Hurley J, Larrondo L, Loros J, Dunlap J . Conserved RNA helicase FRH acts nonenzymatically to support the intrinsically disordered neurospora clock protein FRQ. Mol Cell. 2013; 52(6):832-43. PMC: 3900029. DOI: 10.1016/j.molcel.2013.11.005. View

Lauinger L, Diernfellner A, Falk S, Brunner M . The RNA helicase FRH is an ATP-dependent regulator of CK1a in the circadian clock of Neurospora crassa. Nat Commun. 2014; 5:3598. DOI: 10.1038/ncomms4598. View

10.

de Paula R, Lewis Z, Greene A, Seo K, Morgan L, Vitalini M . Two circadian timing circuits in Neurospora crassa cells share components and regulate distinct rhythmic processes. J Biol Rhythms. 2006; 21(3):159-68. DOI: 10.1177/0748730406288338. View

11.

Denault D, Loros J, Dunlap J . WC-2 mediates WC-1-FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora. EMBO J. 2001; 20(1-2):109-17. PMC: 140181. DOI: 10.1093/emboj/20.1.109. View

12.

Cheng P, Yang Y, Liu Y . Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc Natl Acad Sci U S A. 2001; 98(13):7408-13. PMC: 34682. DOI: 10.1073/pnas.121170298. View

13.

Salichos L, Rokas A . The diversity and evolution of circadian clock proteins in fungi. Mycologia. 2010; 102(2):269-78. DOI: 10.3852/09-073. View

14.

Shi M, Collett M, Loros J, Dunlap J . FRQ-interacting RNA helicase mediates negative and positive feedback in the Neurospora circadian clock. Genetics. 2009; 184(2):351-61. PMC: 2828717. DOI: 10.1534/genetics.109.111393. View

15.

Fang W, Zhang Y, Yang X, Zheng X, Duan H, Li Y . Agrobacterium tumefaciens-mediated transformation of Beauveria bassiana using an herbicide resistance gene as a selection marker. J Invertebr Pathol. 2004; 85(1):18-24. DOI: 10.1016/j.jip.2003.12.003. View

16.

Luo C, Loros J, Dunlap J . Nuclear localization is required for function of the essential clock protein FRQ. EMBO J. 1998; 17(5):1228-35. PMC: 1170471. DOI: 10.1093/emboj/17.5.1228. View

17.

Hong C, Ruoff P, Loros J, Dunlap J . Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus. Genes Dev. 2008; 22(22):3196-204. PMC: 2593610. DOI: 10.1101/gad.1706908. View

18.

Shang Y, Xiao G, Zheng P, Cen K, Zhan S, Wang C . Divergent and Convergent Evolution of Fungal Pathogenicity. Genome Biol Evol. 2016; 8(5):1374-87. PMC: 4898799. DOI: 10.1093/gbe/evw082. View

19.

Dunlap J . Molecular bases for circadian clocks. Cell. 1999; 96(2):271-90. DOI: 10.1016/s0092-8674(00)80566-8. View

20.

Liu Y, Garceau N, Loros J, Dunlap J . Thermally regulated translational control of FRQ mediates aspects of temperature responses in the neurospora circadian clock. Cell. 1997; 89(3):477-86. DOI: 10.1016/s0092-8674(00)80228-7. View