Os-GIGANTEA Confers Robust Diurnal Rhythms on the Global Transcriptome of Rice in the Field[C][W][OA]

An extensive analysis of a circadian clock–related mutant of rice in the field revealed that the circadian clock confers robust diurnal rhythms on the global transcriptome in the field. Net photosynthetic rates and grain yields, however, were not affected in the mutant. Thus, unexpectedly, net primary assimilation was still robust despite this circadian clock defect in the field. The circadian clock controls physiological traits such as flowering time, photosynthesis, and growth in plants under laboratory conditions. Under natural field conditions, however, little is known about the significance of the circadian clock in plants. By time-course transcriptome analyses of rice (Oryza sativa) leaves, using a newly isolated rice circadian clock–related mutant carrying a null mutation in Os-GIGANTEA (Os-GI), we show here that Os-GI controlled 75% (false discovery rate = 0.05) of genes among 27,201 genes tested and was required for strong amplitudes and fine-tuning of the diurnal rhythm phases of global gene expression in the field. However, transcripts involved in primary metabolism were not greatly affected by osgi. Time-course metabolome analyses of leaves revealed no trends of change in primary metabolites in osgi plants, and net photosynthetic rates and grain yields were not affected. By contrast, some transcripts and metabolites in the phenylpropanoid metabolite pathway were consistently affected. Thus, net primary assimilation of rice was still robust in the face of such osgi mutation-related circadian clock defects in the field, unlike the case with defects caused by Arabidopsis thaliana toc1 and ztl mutations in the laboratory.

[1]  Daniël P. Melters,et al.  Disruption of Hepatic Leptin Signaling Protects Mice From Age- and Diet-Related Glucose Intolerance , 2010, Diabetes.

[2]  M. Yano,et al.  A pair of floral regulators sets critical day length for Hd3a florigen expression in rice , 2010, Nature Genetics.

[3]  Mark Stitt,et al.  Circadian control of carbohydrate availability for growth in Arabidopsis plants at night , 2010, Proceedings of the National Academy of Sciences.

[4]  Takeshi Itoh,et al.  SALAD database: a motif-based database of protein annotations for plant comparative genomics , 2009, Nucleic Acids Res..

[5]  G. Coupland,et al.  Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. , 2009, Developmental cell.

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

[7]  Kazuki Saito,et al.  Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination , 2009, Proceedings of the National Academy of Sciences.

[8]  Takeshi Mizuno,et al.  Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. , 2009, Plant & cell physiology.

[9]  Brook T. Moyers,et al.  Effects of Genetic Perturbation on Seasonal Life History Plasticity , 2009, Science.

[10]  M. Hirai,et al.  Widely Targeted Metabolomics Based on Large-Scale MS/MS Data for Elucidating Metabolite Accumulation Patterns in Plants , 2008, Plant & cell physiology.

[11]  C. R. McClung,et al.  Comes a time. , 2008, Current opinion in plant biology.

[12]  K. Halliday,et al.  β-AMYLASE4, a Noncatalytic Protein Required for Starch Breakdown, Acts Upstream of Three Active β-Amylases in Arabidopsis Chloroplasts[W][OA] , 2008, The Plant Cell Online.

[13]  Dmitri A. Nusinow,et al.  FKF1 and GIGANTEA Complex Formation Is Required for Day-Length Measurement in Arabidopsis , 2007, Science.

[14]  Karine David,et al.  ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. , 2007, Nature.

[15]  T. Izawa,et al.  Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. , 2007, Journal of experimental botany.

[16]  Shoichi Matsuo,et al.  Hd3a Protein Is a Mobile Flowering Signal in Rice , 2007, Science.

[17]  Fabio Fornara,et al.  FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis , 2007, Science.

[18]  Anthony C. Davison,et al.  Rapid Classification of Phenotypic Mutants of Arabidopsis via Metabolite Fingerprinting1[W][OA] , 2007, Plant Physiology.

[19]  M. Nordborg,et al.  Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. , 2006, Genes & development.

[20]  S. Harmer,et al.  GIGANTEA Acts in Blue Light Signaling and Has Biochemically Separable Roles in Circadian Clock and Flowering Time Regulation1[C][W][OA] , 2006, Plant Physiology.

[21]  S. Kay,et al.  Photoperiodic control of flowering: not only by coincidence. , 2006, Trends in plant science.

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

[23]  Paul E. Brown,et al.  Extension of a genetic network model by iterative experimentation and mathematical analysis , 2005, Molecular systems biology.

[24]  M. Nordborg,et al.  Role of FRIGIDA and FLOWERING LOCUS C in Determining Variation in Flowering Time of Arabidopsis1[w] , 2005, Plant Physiology.

[25]  A. Makino,et al.  Changes in the thermal dissipation and the electron flow in the water-water cycle in rice grown under conditions of physiologically low temperature. , 2004, Plant & cell physiology.

[26]  T. Mizuno,et al.  The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm. , 2003, Plant & cell physiology.

[27]  C. R. McClung,et al.  Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock , 2003, Science.

[28]  Takashi Araki,et al.  Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. , 2002, Plant & cell physiology.

[29]  S. Knudsen,et al.  A new non-linear normalization method for reducing variability in DNA microarray experiments , 2002, Genome Biology.

[30]  M. Yano,et al.  Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. , 2002, Genes & development.

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

[32]  K. Shimamoto,et al.  Isolation of rice genes possibly involved in the photoperiodic control of flowering by a fluorescent differential display method. , 2002, Plant & cell physiology.

[33]  Steve A. Kay,et al.  Reciprocal Regulation Between TOC1 and LHY/CCA1 Within the Arabidopsis Circadian Clock , 2001, Science.

[34]  K. Shimamoto,et al.  Light regulation of circadian clock-controlled gene expression in rice. , 2001, The Plant journal : for cell and molecular biology.

[35]  M. Yano,et al.  Hd1, a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS , 2000, Plant Cell.

[36]  B. Logan,et al.  Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[37]  D. E. Somers,et al.  Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. , 2000, Science.

[38]  K. Shimamoto,et al.  Phytochromes confer the photoperiodic control of flowering in rice (a short-day plant). , 1999, The Plant journal : for cell and molecular biology.

[39]  D. E. Somers,et al.  Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. , 1999, Science.

[40]  G. Coupland,et al.  GIGANTEA: a circadian clock‐controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane‐spanning domains , 1999, The EMBO journal.

[41]  S. Golden,et al.  Resonating circadian clocks enhance fitness in cyanobacteria. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Zhi-Yong Wang,et al.  Constitutive Expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) Gene Disrupts Circadian Rhythms and Suppresses Its Own Expression , 1998, Cell.

[43]  Jychian Chen,et al.  Monogenic Recessive Mutations Causing Both Late Floral Initiation and Excess Starch Accumulation in Arabidopsis. , 1995, The Plant cell.

[44]  J. Conroy,et al.  Diurnal Regulation of Leaf Blade Elongation in Rice by CO2 (Is it Related to Sucrose-Phosphate Synthase Activity?) , 1995, Plant physiology.

[45]  J. Watson,et al.  Characterization of a cDNA Encoding Ribosomal Protein S16 in Rice , 1995, Plant physiology.

[46]  R. Simon,et al.  The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors , 1995, Cell.

[47]  C. Strayer,et al.  Circadian clock mutants in Arabidopsis identified by luciferase imaging , 1995, Science.

[48]  S. Kay,et al.  Circadian Control of cab Gene Transcription and mRNA Accumulation in Arabidopsis. , 1991, The Plant cell.

[49]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[50]  A. Makino,et al.  Differences between wheat and rice in the enzymic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase and the relationship to photosynthetic gas exchange , 1988, Planta.

[51]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[52]  K. Halliday,et al.  Edinburgh Research Explorer Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts , 2008 .

[53]  Alison M. Smith,et al.  The diurnal metabolism of leaf starch. , 2007, The Biochemical journal.

[54]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[55]  A. Pokhilko,et al.  Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model , 2010, Molecular systems biology.