Magnesium maintains the length of the circadian period in Arabidopsis.

The circadian clock coordinates the physiological responses of a biological system to day and night rhythms through complex loops of transcriptional/translational regulation. It can respond to external stimuli and adjust generated circadian oscillations accordingly to maintain an endogenous period close to 24 h. However, the interaction between nutritional status and circadian rhythms in plants is poorly understood. Magnesium (Mg) is essential for numerous biological processes in plants, and its homeostasis is crucial to maintain optimal development and growth. Magnesium deficiency in young Arabidopsis thaliana seedlings increased the period of circadian oscillations of the CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) promoter (pCCA1:LUC) activity and dampened their amplitude under constant light in a dose-dependent manner. Although the circadian period increase caused by Mg deficiency was light dependent, it did not depend on active photosynthesis. Mathematical modeling of the Mg input into the circadian clock reproduced the experimental increase of the circadian period and suggested that Mg is likely to affect global transcription/translation levels rather than a single component of the circadian oscillator. Upon addition of a low dose of cycloheximide to perturb translation, the circadian period increased further under Mg deficiency, which was rescued when sufficient Mg was supplied, supporting the model's prediction. These findings suggest that sufficient Mg supply is required to support proper timekeeping in plants.

[1]  H. Liao,et al.  Diel magnesium fluctuations in chloroplasts contribute to photosynthesis in rice , 2020, Nature Plants.

[2]  Merle Tränkner,et al.  Critical Leaf Magnesium Thresholds and the Impact of Magnesium on Plant Growth and Photo-Oxidative Defense: A Systematic Review and Meta-Analysis From 70 Years of Research , 2019, Front. Plant Sci..

[3]  C. Caldana,et al.  Continuous dynamic adjustment of the plant circadian oscillator , 2019, Nature Communications.

[4]  David Hayden,et al.  Dynamical differential expression (DyDE) reveals the period control mechanisms of the Arabidopsis circadian oscillator , 2019, PLoS Comput. Biol..

[5]  F. Kawamura,et al.  Magnesium Suppresses Defects in the Formation of 70S Ribosomes as Well as in Sporulation Caused by Lack of Several Individual Ribosomal Proteins , 2018, bioRxiv.

[6]  W. Gruissem,et al.  Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism , 2017, bioRxiv.

[7]  Jian Li,et al.  Functional dissection and transport mechanism of magnesium in plants. , 2017, Seminars in cell & developmental biology.

[8]  J. Leloup,et al.  Modeling the photoperiodic entrainment of the plant circadian clock. , 2017, Journal of theoretical biology.

[9]  M. Stitt,et al.  Photoperiod-dependent changes in the phase of core clock transcripts and global transcriptional outputs at dawn and dusk in Arabidopsis. , 2016, Plant, cell & environment.

[10]  M. Putker,et al.  Daily magnesium fluxes regulate cellular timekeeping and energy balance , 2016, Nature.

[11]  Didier Gonze,et al.  A Compact Model for the Complex Plant Circadian Clock , 2016, Front. Plant Sci..

[12]  K. Aihara,et al.  A Hierarchical Multi-oscillator Network Orchestrates the Arabidopsis Circadian System , 2015, Cell.

[13]  C. Robertson McClung,et al.  Integrating circadian dynamics with physiological processes in plants , 2015, Nature Reviews Genetics.

[14]  Kazuyuki Aihara,et al.  A Hierarchical Multi-oscillator Network Orchestrates the Arabidopsis Circadian System , 2015, Cell.

[15]  Q. Jia,et al.  The Circadian Clock Modulates Global Daily Cycles of mRNA Ribosome Loading[OPEN] , 2015, Plant Cell.

[16]  Michael J. Haydon,et al.  Nutrient homeostasis within the plant circadian network , 2015, Front. Plant Sci..

[17]  Andrew J. Millar,et al.  Strengths and Limitations of Period Estimation Methods for Circadian Data , 2014, PloS one.

[18]  Polly Yingshan Hsu,et al.  Wheels within wheels: the plant circadian system. , 2014, Trends in plant science.

[19]  Fiona C. Robertson,et al.  Photosynthetic entrainment of the Arabidopsis circadian clock , 2013, Nature.

[20]  S. Conn,et al.  An update on magnesium homeostasis mechanisms in plants. , 2013, Metallomics : integrated biometal science.

[21]  C. Hermans,et al.  Physiological and molecular responses to magnesium nutritional imbalance in plants , 2013, Plant and Soil.

[22]  Y. Wang,et al.  Iron Is Involved in the Maintenance of Circadian Period Length in Arabidopsis12[W][OA] , 2013, Plant Physiology.

[23]  C. Robertson McClung,et al.  Reciprocal Interaction of the Circadian Clock with the Iron Homeostasis Network in Arabidopsis1[W][OA] , 2012, Plant Physiology.

[24]  D. Weigel,et al.  Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function , 2012, The EMBO journal.

[25]  Ioana Visan,et al.  Circadian rhythms , 2012, Nature Immunology.

[26]  M. Hirai,et al.  Establishment of an in planta magnesium monitoring system using CAX3 promoter-luciferase in Arabidopsis , 2011, Journal of experimental botany.

[27]  Fiona C. Robertson,et al.  The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose , 2011, Proceedings of the National Academy of Sciences.

[28]  Frederik Coppens,et al.  Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. , 2010, The New phytologist.

[29]  Frederik Coppens,et al.  Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. , 2010, The New phytologist.

[30]  S. Puig,et al.  Deregulated Copper Transport Affects Arabidopsis Development Especially in the Absence of Environmental Cycles1[C][W] , 2010, Plant Physiology.

[31]  S. Harmer,et al.  The circadian system in higher plants. , 2009, Annual review of plant biology.

[32]  Fiona C. Robertson,et al.  Interactions between circadian and hormonal signalling in plants , 2009, Plant Molecular Biology.

[33]  Rodrigo A Gutiérrez,et al.  Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1 , 2008, Proceedings of the National Academy of Sciences.

[34]  Neil Dalchau,et al.  Modulation of environmental responses of plants by circadian clocks. , 2007, Plant, cell & environment.

[35]  B. Usadel,et al.  Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. , 2007, The Plant journal : for cell and molecular biology.

[36]  W. Luo,et al.  Characterisation of magnesium nutrition and interaction of magnesium and potassium in rice , 2006 .

[37]  C. Robertson McClung,et al.  Plant Circadian Rhythms , 2006, The Plant Cell Online.

[38]  C. Hermans,et al.  Physiological characterization of Mg deficiency in Arabidopsis thaliana. , 2005, Journal of experimental botany.

[39]  Anthony Hall,et al.  Plant Circadian Clocks Increase Photosynthesis, Growth, Survival, and Competitive Advantage , 2005, Science.

[40]  C Robertson McClung,et al.  PSEUDO-RESPONSE REGULATOR 7 and 9 Are Partially Redundant Genes Essential for the Temperature Responsiveness of the Arabidopsis Circadian Clock , 2005, The Plant Cell Online.

[41]  S. Delrot,et al.  Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves , 2005, Planta.

[42]  Stacey L. Harmer,et al.  Overlapping and Distinct Roles of PRR7 and PRR9 in the Arabidopsis Circadian Clock , 2005, Current Biology.

[43]  R. Strasser,et al.  Physiological characterisation of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II , 2004, Planta.

[44]  T. Steitz,et al.  The contribution of metal ions to the structural stability of the large ribosomal subunit. , 2004, RNA.

[45]  Alex A R Webb,et al.  The physiology of circadian rhythms in plants. , 2003, The New phytologist.

[46]  E. Tobin,et al.  Circadian Rhythms Confer a Higher Level of Fitness to Arabidopsis Plants1 , 2002, Plant Physiology.

[47]  Stacey L. Harmer,et al.  Critical Role for CCA1 and LHY in Maintaining Circadian Rhythmicity in Arabidopsis , 2002, Current Biology.

[48]  J. Dunlap.  Molecular Bases for Circadian Clocks , 1999, Cell.

[49]  J. Cowan.  Metal Activation of Enzymes in Nucleic Acid Biochemistry. , 1998, Chemical reviews.

[50]  D. E. Somers,et al.  Conditional Circadian Dysfunction of the Arabidopsis early-flowering 3 Mutant , 1996, Science.

[51]  K. Guan,et al.  Phosphorylation and Activation of the ATP-Mg-dependent Protein Phosphatase by the Mitogen-activated Protein Kinase (*) , 1995, The Journal of Biological Chemistry.

[52]  H. Marschner,et al.  Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants , 1994 .

[53]  J. Weinstein,et al.  Further characterization of the magnesium chelatase in isolated developing cucumber chloroplasts : substrate specificity, regulation, intactness, and ATP requirements. , 1991, Plant physiology.

[54]  B. Sweeney,et al.  Nitrate deficiency shortens the circadian period in gonyaulax. , 1984, Plant physiology.

[55]  A. Jagendorf,et al.  A Mg2+ requirement for rapid ATP-driven protein synthesis by intact pea chloroplasts☆ , 1983 .

[56]  L. Spremulli,et al.  Quantitation of cation binding to wheat germ ribosomes: influences on subunit association equilibria and ribosome activity. , 1983, Nucleic acids research.

[57]  R. Strasser,et al.  Energy transfer and the distribution of excitation energy in the photosynthetic apparatus of spinach chloroplasts. , 1977, Biochimica et biophysica acta.

[58]  R. Lilley,et al.  MAGNESIUM ACTIVATION OF PHOTOSYNTHETIC CO2‐FIXATION IN A RECONSTITUTED CHLOROPLAST SYSTEM , 1974 .

[59]  D. Morris,et al.  Cations and ribosome structure. I. Effects on the 30S subunit of substituting polyamines for magnesium ion. , 1973, Biochemistry.

[60]  R. Cox,et al.  Sodium, potassium, magnesium, calcium and strontium in sea water , 1966 .

[61]  M. Fleischer.  The abundance and distribution of the chemical elements in the earth's crust , 1954 .

[62]  L. S. Levitt.  The role of magnesium in photosynthesis. , 1954, Science.

[63]  Michael J. Haydon,et al.  Assessing the Impact of Photosynthetic Sugars on the Arabidopsis Circadian Clock. , 2016, Methods in molecular biology.

[64]  Volker Römheld,et al.  Diagnosis of Deficiency and Toxicity of Nutrients , 2012 .

[65]  W. Grzebisz.  MAGNESIUM - FOOD AND HUMAN HEALTH , 2011 .

[66]  R. Parker.  Composition of the Earth's crust , 1967 .

[67]  Frank Wigglesworth Clarke,et al.  The composition of the Earth's crust , 1924 .