First published online January 20, 2006; 10.1104/pp.105.074864
Plant Physiology 140:933-945 (2006)
© 2006 American Society of Plant Biologists
GENETICS, GENOMICS, AND MOLECULAR EVOLUTION
Forward Genetic Analysis of the Circadian Clock Separates the Multiple Functions of ZEITLUPE1,[W]
Éva Kevei,
Péter Gyula,
Anthony Hall,
László Kozma-Bognár,
Woe-Yeon Kim,
Maria E. Eriksson,
Réka Tóth,
Shigeru Hanano,
Balázs Fehér,
Megan M. Southern,
Ruth M. Bastow,
András Viczián,
Victoria Hibberd,
Seth J. Davis,
David E. Somers,
Ferenc Nagy and
Andrew J. Millar*
Institute of Plant Biology, Biological Research Centre of the Hungarian Academy of Sciences, H–6726 Szeged, Hungary (É.K., P.G., B.F., F.N.); School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, United Kingdom (A.H.); Institute of Molecular Plant Science, University of Edinburgh, Edinburgh EH9 3JH, United Kingdom (L.K.-B., A.J.M.); Department of Plant Cellular and Molecular Biology, Ohio State University, Columbus, Ohio 43210 (W.-Y.K., D.E.S.); Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, SE–901 87 Umea, Sweden (M.E.E.); Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, D–50829 Cologne, Germany (R.T., S.H., S.J.D.); Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, United Kingdom (M.M.S., R.M.B., V.H.); and Biologie II/Institut für Botanik, University of Freiburg, D–79104 Freiburg, Germany (A.V.)
The circadian system of Arabidopsis (Arabidopsis thaliana) includes feedback loops of gene regulation that generate 24-h oscillations. Components of these loops remain to be identified; none of the known components is completely understood, including ZEITLUPE (ZTL), a gene implicated in regulated protein degradation. ztl mutations affect both circadian and developmental responses to red light, possibly through ZTL interaction with PHYTOCHROME B (PHYB). We conducted a large-scale genetic screen that identified additional clock-affecting loci. Other mutants recovered include 11 new ztl alleles encompassing mutations in each of the ZTL protein domains. Each mutation lengthened the circadian period, even in dark-grown seedlings entrained to temperature cycles. A mutation of the LIGHT, OXYGEN, VOLTAGE (LOV)/Period-ARNT-Sim (PAS) domain was unique in retaining wild-type responses to red light both for the circadian period and for control of hypocotyl elongation. This uncoupling of ztl phenotypes indicates that interactions of ZTL protein with multiple factors must be disrupted to generate the full ztl mutant phenotype. Protein interaction assays showed that the ztl mutant phenotypes were not fully explained by impaired interactions with previously described partner proteins Arabidopsis S-phase kinase-related protein 1, TIMING OF CAB EXPRESSION 1, and PHYB. Interaction with PHYB was unaffected by mutation of any ZTL domain. Mutation of the kelch repeat domain affected protein binding at both the LOV/PAS and the F-box domains, indicating that interaction among ZTL domains leads to the strong phenotypes of kelch mutations. Forward genetics continues to provide insight regarding both known and newly discovered components of the circadian system, although current approaches have saturated mutations at some loci.
1 This work was supported in part by a long-term fellowship of the European Molecular Biology Organization (to L.K.B.), by a Marie Curie fellowship of the European Union (to M.E.E.), in part by a Japanese Society for the Promotion of Science postdoctoral fellowship (to S.H.), by a Biotechnology and Biological Science Research Council (BBSRC) postgraduate studentship (to M.M.S.), by a studentship from the Gatsby Charitable Foundation (to R.M.B.), by a Department of Energy Biosciences fellowship of the Life Science Research Foundation (to S.J.D.), by the National Science Foundation (grant no. IBN 0344377) and U.S. Department of Agriculture/Cooperative State Research, Education and Extension Service (grant no.CRIS 2002 35304 12594 to D.E.S.), and by the Alexander von Humboldt Foundation (grant no. IV–UNG/1118446 STP to A.V.); work in Szeged was supported by the Hungarian Scientific Research Fund (grant no. OTKA T046710) and the Howard Hughes Medical Institute (grant no. INTNL 55000325 to F.N.); work in Warwick was supported by the BBSRC (grant nos. G08667, G13967, and G15231) and the imaging facility was supported by grants from the Gatsby Charitable Foundation, the BBSRC, and the Royal Society (to A.J.M.).
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Andrew J. Millar (andrew.millar{at}ed.ac.uk).
[W] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.074864.
* Corresponding author; e-mail andrew.millar{at}ed.ac.uk; fax 44–0131–650–5392.
Received November 29, 2005;
returned for revision November 29, 2005;
accepted December 21, 2005.
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