Skip to main content
SpringerLink
Log in

Expression of putative circadian clock components in the arbuscular mycorrhizal fungus Rhizoglomus irregulare

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal fungi (AMF) are obligatory plant symbionts that live underground, so few studies have examined their response to light. Responses to blue light by other fungi can be mediated by White Collar-1 (WC-1) and WC-2 proteins. These wc genes, together with the frequency gene (frq), also form part of the endogenous circadian clock. The clock mechanism has never been studied in AMF, although circadian growth of their hyphae in the field has been reported. Using both genomic and transcriptomic data, we have found homologs of wc-1, wc-2, and frq and related circadian clock genes in the arbuscular mycorrhizal fungus Rhizoglomus irregulare (synonym Rhizophagus irregularis). Gene expression of wc-1, wc-2, and frq was analyzed using RT-qPCR on RNA extracted from germinating spores and from fungal material cultivated in vitro with transformed carrot roots. We found that all three core clock genes were expressed in both pre- and post-mycorrhizal stages of R. irregulare growth. Similar to the model fungus Neurospora crassa, the core circadian oscillator gene frq was induced by brief light stimulation. The presence of circadian clock and output genes in R. irregulare opens the door to the study of circadian clocks in the fungal partner of plant-AMF symbiosis. Our finding also provides new insight into the evolution of the circadian frq gene in fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ambra R, Grimaldi B, Zamboni S, Filetici P, Macino G, Ballario P (2004) Photomorphogenesis in the hypogeous fungus Tuber borchii: isolation and characterization of Tbwc-1, the homologue of the blue-light photoreceptor of Neurospora crassa. Fungal Genet Biol 41:688–697

    Article  CAS  Google Scholar 

  • Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108–124

    Article  CAS  Google Scholar 

  • Bell-Pedersen D, Shinohara ML, Loros JJ, Dunlap JC (1996) Circadian clock-controlled genes isolated from Neurospora crassa are late night- to early morning-specific. Proc Natl Acad Sci U S A 93:13096–13101

    Article  CAS  Google Scholar 

  • Cheng P, Yang Y, Heintzen C, Liu Y (2001) Coiled-coil domain-mediated FRQ-FRQ interaction is essential for its circadian clock function in Neurospora. EMBO J 20:101–108

    Article  CAS  Google Scholar 

  • Ciani A, Goss KU, Schwarzenbach RP (2005) Light penetration in soil and particulate minerals. Eur J Soil Sci 56:561–574. https://doi.org/10.1111/j.1365-2389.2005.00688.x

    Article  CAS  Google Scholar 

  • Corrochano LM (2011) Fungal photobiology: a synopsis. IMA Fungus 2:25–28

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    Article  CAS  Google Scholar 

  • Dunlap JC, Loros JJ (2017) Making time: conservation of biological clocks from fungi to animals Microbiol Spectr 5(3): FUNK–0039–2016

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  Google Scholar 

  • Estrada AF, Avalos J (2008) The White Collar protein WcoA of Fusarium fujikuroi is not essential for photocarotenogenesis, but is involved in the regulation of secondary metabolism and conidiation. Fungal Genet Biol 45:705–718

    Article  CAS  Google Scholar 

  • Ferguson JJ, Menge JA (1982) Factors that affect production of endomycorrhizal inoculum. Proc Fla State Hort Soc 95:37–39

    Google Scholar 

  • Franken P, Lapopin L, Meyer-Gauen G, Gianinazzi-Pearson V (1997) RNA accumulation and genes expressed in spores of the arbuscular mycorrhizal fungus, Gigaspora rosea. Mycologia 89:293–297. https://doi.org/10.2307/3761085

    Article  CAS  Google Scholar 

  • Gallego M, Virshup DM (2007) Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol 8:139–148

    Article  CAS  Google Scholar 

  • Greene AV, Keller N, Haas H, Bell-Pedersen D (2003) A circadian oscillator in Aspergillus spp. regulates daily development and gene expression. Eukaryot Cell 2:231–237

    Article  CAS  Google Scholar 

  • Grimaldi B, Coiro P, Filetici P, Berge E, Dobosy JR, Freitag M, Selker EU, Ballario P (2006) The Neurospora crassa White Collar-1 dependent blue light response requires acetylation of histone H3 lysine 14 by NGF-1. Mol Biol Cell 17:4576–4583

    Article  CAS  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  • Hernandez RR, Allen MF (2013) Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the Soil Ecosystem Observatory. New Phytol 200:547–557

    Article  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking 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, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miądlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüßler 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 111:509–547

    Article  Google Scholar 

  • Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, von Mering C, Bork P (2016) eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293

    Article  CAS  Google Scholar 

  • 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 U S A 111:16995–17002

    Article  CAS  Google Scholar 

  • Hurley JM, Loros JJ, Dunlap JC (2016a) Circadian oscillators: around the transcription-translation feedback loop and on to output. Trends Biochem Sci 41:834–846

    Article  CAS  Google Scholar 

  • Hurley JM, Loros JJ, Dunlap JC (2016b) The circadian system as an organizer of metabolism. Fungal Genet Biol 90:39–43

    Article  CAS  Google Scholar 

  • Idnurm A, Heitman J (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol 3:e95

    Article  Google Scholar 

  • Idnurm A, Rodriguez-Romero J, Corrochano LM, Sanz C, Iturriaga EA, Eslava AP, Heitman J (2006) The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc Natl Acad Sci U S A 103:4546–4551

    Article  CAS  Google Scholar 

  • Idnurm A, Verma S, Corrochano LM (2010) A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet Biol 47:881–892

    Article  Google Scholar 

  • James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, Nimmo HG (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322:1832–1835

    Article  CAS  Google Scholar 

  • Jansa J, Bukovska P, Gryndler M (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts—or just soil free-riders? Front Plant Sci 4:134

    Article  Google Scholar 

  • Lee S-J, Kong M, Harrison P, Hijri M (2018) Conserved proteins of the RNA interference system in the arbuscular mycorrhizal fungus Rhizoglomus irregulare provide new insight into the evolutionary history of Glomeromycota. Genome Biol Evol 10:328–343. https://doi.org/10.1093/gbe/evy002

    Article  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43:D257–D260

    Article  CAS  Google Scholar 

  • Liu Y, Bell-Pedersen D (2006) Circadian rhythms in Neurospora crassa and other filamentous fungi. Eukaryot Cell 5:1184–1193

    Article  CAS  Google Scholar 

  • Lombardi LM, Brody S (2005) Circadian rhythms in Neurospora crassa: clock gene homologues in fungi. Fungal Genet Biol 42:887–892

    Article  CAS  Google Scholar 

  • Loros JJ, Dunlap JC (2001) Genetic and molecular analysis of circadian rhythms in Neurospora. Annu Rev Physiol 63:757–794

    Article  CAS  Google Scholar 

  • Loros JJ, Denome SA, Dunlap JC (1989) Molecular cloning of genes under control of the circadian clock in Neurospora. Science 243:385–388

    Article  CAS  Google Scholar 

  • Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164

    Article  CAS  Google Scholar 

  • Maeght J-L, Rewald B, Pierret A (2013) How to study deep roots-and why it matters. Front Plant Sci 4:299

    Article  Google Scholar 

  • McClung CR (2006) Plant circadian rhythms. Plant Cell 18:792–803

    Article  CAS  Google Scholar 

  • McDowall J, Hunter S (2011) InterPro protein classification. Methods Mol Biol 694:37–47

    Article  CAS  Google Scholar 

  • Nadimi M, Beaudet D, Forget L, Hijri M, Lang BF (2012) Group I intron-mediated trans-splicing in mitochondria of Gigaspora rosea and a robust phylogenetic affiliation of arbuscular mycorrhizal fungi with Mortierellales. Mol Biol Evol 29:2199–2210

    Article  CAS  Google Scholar 

  • Nagahashi G, Douds DD Jr (2003) Action spectrum for the induction of hyphal branches of an arbuscular mycorrhizal fungus: exposure sites versus branching sites. Mycol Res 107:1075–1082

    Article  Google Scholar 

  • Nagahashi G, Douds DD Jr (2004) Synergism between blue light and root exudate compounds and evidence for a second messenger in the hyphal branching response of Gigaspora gigantea. Mycologia 96:948–954

    Article  Google Scholar 

  • Olmedo M, Ruger-Herreros C, Corrochano LM (2010) Regulation by blue light of the fluffy gene encoding a major regulator of conidiation in Neurospora crassa. Genetics 184:651–658

    Article  CAS  Google Scholar 

  • Oosterhuis DM (1990) Growth and development of a cotton plant. Publications of the American Society of Agronomy, Madison, MP332-4M-9-92R

  • Purschwitz J, Muller S, Kastner C, Fischer R (2006) Seeing the rainbow: light sensing in fungi. Curr Opin Microbiol 9:566–571

    Article  CAS  Google Scholar 

  • Querfurth C, Diernfellner ACR, Gin E, Malzahn E, Hofer T, Brunner M (2011) Circadian conformational change of the Neurospora clock protein FREQUENCY triggered by clustered hyperphosphorylation of a basic domain. Mol Cell 43:713–722

    Article  CAS  Google Scholar 

  • Redecker D, Schussler A, Stockinger H, Sturmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531

    Article  Google Scholar 

  • Rodriguez-Romero J, Hedtke M, Kastner C, Muller S, Fischer R (2010) Fungi, hidden in soil or up in the air: light makes a difference. Annu Rev Microbiol 64:585–610

    Article  CAS  Google Scholar 

  • Roenneberg T, Merrow M (1999) Circadian clocks—from genes to complex behaviour. Reprod Nutr Dev 39:277–294

    Article  CAS  Google Scholar 

  • Salichos L, Rokas A (2010) The diversity and evolution of circadian clock proteins in fungi. Mycologia 102:269–278

    Article  CAS  Google Scholar 

  • Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421. https://doi.org/10.1017/S0953756201005196

    Article  Google Scholar 

  • Serikawa M, Miwa K, Kondo T, Oyama T (2008) Functional conservation of clock-related genes in flowering plants: overexpression and RNA interference analyses of the circadian rhythm in the monocotyledon Lemna gibba. Plant Physiol 146:1952–1963

    Article  CAS  Google Scholar 

  • Shinohara ML, Correa A, Bell-Pedersen D, Dunlap JC, Loros JJ (2002) Neurospora clock-controlled gene 9 (ccg-9) encodes trehalose synthase: circadian regulation of stress responses and development. Eukaryot Cell 1:33–43

    Article  CAS  Google Scholar 

  • Shukla A, Vyas D, Anuradha, J (2013) Soil depth: an overriding factor for distribution of arbuscular mycorrhizal fungi. Journal of Soil Science and Plant Nutrition 13:23–33.

  • Simon NML, Dodd AN (2017) A new link between plant metabolism and circadian rhythms? Plant Cell Environ 40:995–996

    Article  CAS  Google Scholar 

  • Smith A (1932) Seasonal subsoil temperature variations. J Agric Res 44:421–428

    Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    Article  CAS  Google Scholar 

  • Stone EL, Kalisz PJ (1991) On the maximum extent of tree roots. For Ecol Manag 46:59–102. https://doi.org/10.1016/0378-1127(91)90245-Q

    Article  Google Scholar 

  • Takemiya A, Inoue S-I, Doi M, Kinoshita T, Shimazaki K-I (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17:1120–1127

    Article  CAS  Google Scholar 

  • Tester M, Morris C (1987) The penetration of light through soil. Plant Cell Environ 10:281–286. https://doi.org/10.1111/j.1365-3040.1987.tb01607.x

    Article  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JPW, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  CAS  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Becard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JPW, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122

    Article  CAS  Google Scholar 

  • Uebelmesser E (1954) The endogenous daily rhythm of conidiospore formation of Pilobolus. Arch Mikrobiol 20:1–33

    Article  CAS  Google Scholar 

  • White MJ, Hirsch JP, Henry SA (1991) The OPI1 gene of Saccharomyces cerevisiae, a negative regulator of phospholipid biosynthesis, encodes a protein containing polyglutamine tracts and a leucine zipper. J Biol Chem 266:863–872

    CAS  PubMed  Google Scholar 

  • Yang T, Xiong W, Dong C (2014) Cloning and analysis of the Oswc-1 gene encoding a putative blue light photoreceptor from Ophiocordyceps sinensis. Mycoscience 55:241–245. https://doi.org/10.1016/j.myc.2013.09.003

    Article  CAS  Google Scholar 

  • Yazdanbakhsh N, Sulpice R, Graf A, Stitt M, Fisahn J (2011) Circadian control of root elongation and C partitioning in Arabidopsis thaliana. Plant Cell Environ 34:877–894

    Article  Google Scholar 

  • Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou YJ, Jin G, Ye M, Zou H, Zhao ZK (2012) A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun 3:1112

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by an NSERC Discovery grant to MH which is gratefully acknowledged. We thank Miss Yerim Heo for assistance in designing and editing some figures. We also thank Dr. Dave Janos and two anonymous reviewers for their helpful comments.

Author information

Authors and Affiliations

  1. Institut de Recherche en Biologie Végétale, Université de Montréal, 4101 Rue Sherbrooke Est, Montréal, Québec, H1X 2B2, Canada

    Soon-Jae Lee, Mengxuan Kong, David Morse & Mohamed Hijri

Authors
  1. Soon-Jae Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mengxuan Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Morse
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed Hijri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohamed Hijri.

Electronic supplementary material

ESM 1

(DOCX 681 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, SJ., Kong, M., Morse, D. et al. Expression of putative circadian clock components in the arbuscular mycorrhizal fungus Rhizoglomus irregulare. Mycorrhiza 28, 523–534 (2018). https://doi.org/10.1007/s00572-018-0843-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-018-0843-y

Keywords

Search

Navigation