Significance of Light, Sugar, and Amino Acid Supply for Diurnal Gene Regulation in Developing Barley Caryopses

The caryopses of barley ( Hordeum vulgare ), as of all cereals, are complex sink organs optimized for starch accumulation and embryo development. While their early to late development has been studied in great detail, processes underlying the caryopses’ diurnal adaptation to changes in light, temperature, and the fluctuations in phloem-supplied carbon and nitrogen have remained unknown. In an attempt to identify diurnally affected processes in developing caryopses at the early maturation phase, we monitored global changes of both gene expression and metabolite levels. We applied the 22 K Barley1 GeneChip microarray and identified 2,091 differentially expressed (DE) genes that were assigned to six major diurnal expression clusters. Principal component analysis and other global analyses demonstrated that the variability within the data set relates to genes involved in circadian regulation, storage compound accumulation, embryo development, response to abiotic stress, and photosynthesis. The correlation of amino acid and sugar profiles with expression trajectories led to the identification of several hundred potentially metabolite-regulated DE genes. A comparative analysis of our data set and publicly available microarray data disclosed suborgan-specific expression of almost all diurnal DE genes, with more than 350 genes specifically expressed in the pericarp, endosperm, or embryo tissues. Our data reveal a tight linkage between day/night cycles, changes in light, and the supply of carbon and nitrogen. We present a model that suggests several phases of diurnal gene expression in developing barley caryopses, summarized as starvation and priming, energy collection and carbon fixation, light protection and chaperone activity, storage and growth, and embryo development.

[1]  M. Tegeder,et al.  AAP1 regulates import of amino acids into developing Arabidopsis embryos. , 2009, The Plant journal : for cell and molecular biology.

[2]  J. Thevelein,et al.  Extensive expression regulation and lack of heterologous enzymatic activity of the Class II trehalose metabolism proteins from Arabidopsis thaliana. , 2009, Plant, cell & environment.

[3]  P. D’Silva,et al.  Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors , 2009, Functional & Integrative Genomics.

[4]  Zhi-Liang Zheng Carbon and nitrogen nutrient balance signaling in plants , 2009, Plant signaling & behavior.

[5]  Qian Qian,et al.  Short panicle1 encodes a putative PTR family transporter and determines rice panicle size. , 2009, The Plant journal : for cell and molecular biology.

[6]  H. Rolletschek,et al.  Spatiotemporal Profiling of Starch Biosynthesis and Degradation in the Developing Barley Grain1[W] , 2009, Plant Physiology.

[7]  F. Navari-Izzo,et al.  The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2. , 2009, Physiologia plantarum.

[8]  S. Zeeman,et al.  Starch Granule Biosynthesis in Arabidopsis Is Abolished by Removal of All Debranching Enzymes but Restored by the Subsequent Removal of an Endoamylase[W][OA] , 2008, The Plant Cell Online.

[9]  Marc Strickert,et al.  Different Hormonal Regulation of Cellular Differentiation and Function in Nucellar Projection and Endosperm Transfer Cells: A Microdissection-Based Transcriptome Study of Young Barley Grains1[W] , 2008, Plant Physiology.

[10]  A. Covarrubias,et al.  The Enigmatic LEA Proteins and Other Hydrophilins1[W] , 2008, Plant Physiology.

[11]  A. Fernie,et al.  Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. , 2008, The Plant journal : for cell and molecular biology.

[12]  K. Harter,et al.  The Arabidopsis thaliana response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds , 2008, BMC Plant Biology.

[13]  C. Frohberg,et al.  Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. , 2008, The Plant journal : for cell and molecular biology.

[14]  C. Jansson,et al.  Sugar-mediated semidian oscillation of gene expression in the cassava storage root regulates starch synthesis , 2008, Plant signaling & behavior.

[15]  L. C. Hannah,et al.  The complexities of starch biosynthesis in cereal endosperms. , 2008, Current opinion in biotechnology.

[16]  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.

[17]  Yves Gibon,et al.  Global Transcript Levels Respond to Small Changes of the Carbon Status during Progressive Exhaustion of Carbohydrates in Arabidopsis Rosettes1[W][OA] , 2008, Plant Physiology.

[18]  Uwe Scholz,et al.  Barley Grain Maturation and Germination: Metabolic Pathway and Regulatory Network Commonalities and Differences Highlighted by New MapMan/PageMan Profiling Tools1[W][OA] , 2008, Plant Physiology.

[19]  Connor W. McEntee,et al.  Network Discovery Pipeline Elucidates Conserved Time-of-Day–Specific cis-Regulatory Modules , 2007, PLoS genetics.

[20]  B. Larkins,et al.  The Development of Endosperm in Grasses 1 , 2008 .

[21]  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 .

[22]  Joachim Kilian,et al.  Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots , 2008, BMC Genomics.

[23]  B. Svensson,et al.  The NADPH-Dependent Thioredoxin Reductase/Thioredoxin System in Germinating Barley Seeds: Gene Expression, Protein Profiles, and Interactions between Isoforms of Thioredoxin h and Thioredoxin Reductase1[W] , 2007, Plant Physiology.

[24]  G. Hoch Cell wall hemicelluloses as mobile carbon stores in non‐reproductive plant tissues , 2007 .

[25]  M. Stitt,et al.  Coordination of carbon supply and plant growth. , 2007, Plant, cell & environment.

[26]  O. Van Wuytswinkel,et al.  Combined networks regulating seed maturation. , 2007, Trends in plant science.

[27]  P. Barre,et al.  Cloning, gene mapping, and functional analysis of a fructan 1-exohydrolase (1-FEH) from Lolium perenne implicated in fructan synthesis rather than in fructan mobilization. , 2007, Journal of experimental botany.

[28]  Réjane Pratelli,et al.  Altered Amino Acid Metabolism in Glutamine Dumper1 Plants , 2007, Plant signaling & behavior.

[29]  M. Foolad,et al.  Roles of glycine betaine and proline in improving plant abiotic stress resistance , 2007 .

[30]  Eun-Jeong Lee,et al.  Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. , 2007, Plant & cell physiology.

[31]  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.

[32]  R. Green,et al.  Regulation of output from the plant circadian clock , 2007, The FEBS journal.

[33]  Sanjay Kumar,et al.  A quick method to isolate RNA from wheat and other carbohydrate-rich seeds , 2003, Plant Molecular Biology Reporter.

[34]  M. Steup,et al.  Glucan, Water Dikinase Activity Stimulates Breakdown of Starch Granules by Plastidial b-Amylases , 2007 .

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

[36]  Michael W Young,et al.  Interplay of circadian clocks and metabolic rhythms. , 2006, Annual review of genetics.

[37]  S. Walter,et al.  The molecular chaperone Hsp104--a molecular machine for protein disaggregation. , 2006, Journal of structural biology.

[38]  Marc Strickert,et al.  Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA- regulated maturation in developing barley seeds. , 2006, The Plant journal : for cell and molecular biology.

[39]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[40]  S. Baginsky,et al.  Identification of a Vacuolar Sucrose Transporter in Barley and Arabidopsis Mesophyll Cells by a Tonoplast Proteomic Approach1 , 2006, Plant Physiology.

[41]  Nick Cai,et al.  A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Yves Gibon,et al.  Sugars and Circadian Regulation Make Major Contributions to the Global Regulation of Diurnal Gene Expression in Arabidopsis[W][OA] , 2005, The Plant Cell Online.

[43]  T. Sharkey,et al.  Daylength and Circadian Effects on Starch Degradation and Maltose Metabolism1 , 2005, Plant Physiology.

[44]  Manash S. Chatterjee,et al.  Reduced expression of a protein homologous to glycogenin leads to reduction of starch content in Arabidopsis leaves , 2005 .

[45]  P. Geigenberger,et al.  Identification of a Novel Enzyme Required for Starch Metabolism in Arabidopsis Leaves. The Phosphoglucan, Water Dikinase1[w] , 2005, Plant Physiology.

[46]  Alison M. Smith,et al.  Starch degradation. , 2005, Annual Review of Plant Biology.

[47]  T. Boller,et al.  Cloning and functional characterization of a cDNA encoding barley soluble acid invertase (HvINV1) , 2005 .

[48]  Sang-Jin Kim,et al.  Transcriptome Profiling of the Response of Arabidopsis Suspension Culture Cells to Suc Starvation1[w] , 2004, Plant Physiology.

[49]  N. Patron,et al.  The lys5 Mutations of Barley Reveal the Nature and Importance of Plastidial ADP-Glc Transporters for Starch Synthesis in Cereal Endosperm1 , 2004, Plant Physiology.

[50]  Rafael A. Irizarry,et al.  A Model-Based Background Adjustment for Oligonucleotide Expression Arrays , 2004 .

[51]  H. Rolletschek,et al.  Seed development and differentiation: a role for metabolic regulation. , 2004, Plant biology.

[52]  David Meinke,et al.  Identification of Genes Required for Embryo Development in Arabidopsis1[w] , 2004, Plant Physiology.

[53]  W. Frommer,et al.  Overexpression of GLUTAMINE DUMPER1 Leads to Hypersecretion of Glutamine from Hydathodes of Arabidopsis Leaves , 2004, The Plant Cell Online.

[54]  T. Abebe,et al.  Cloning and identification of highly expressed genes in barley lemma and palea , 2004 .

[55]  T. Boller,et al.  Distinct regulation of sucrose: sucrose-1-fructosyltransferase (1-SST) and sucrose: fructan-6-fructosyltransferase (6-SFT), the key enzymes of fructan synthesis in barley leaves: 1-SST as the pacemaker. , 2004, The New phytologist.

[56]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[57]  Rod A Wing,et al.  A New Resource for Cereal Genomics: 22K Barley GeneChip Comes of Age1 , 2004, Plant Physiology.

[58]  C. Jansson,et al.  Analyses of isoamylase gene activity in wild-type barley indicate its involvement in starch synthesis , 1999, Plant Molecular Biology.

[59]  P. Shewry,et al.  Differential expression of two barley SNF1-related protein kinase genes , 1995, Plant Molecular Biology.

[60]  C. Jansson,et al.  A Novel WRKY Transcription Factor, SUSIBA2, Participates in Sugar Signaling in Barley by Binding to the Sugar-Responsive Elements of the iso1 Promoter Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.0145 , 2003, The Plant Cell Online.

[61]  Huawu Jiang,et al.  Cloning and characterization of the granule-bound starch synthase II gene in rice: gene expression is regulated by the nitrogen level, sugar and circadian rhythm , 2003, Planta.

[62]  U. Wobus,et al.  Peptide and Amino Acid Transporters Are Differentially Regulated during Seed Development and Germination in Faba Bean1 , 2003, Plant Physiology.

[63]  G. Coruzzi,et al.  Overexpression of the ASN1 Gene Enhances Nitrogen Status in Seeds of Arabidopsis1 , 2003, Plant Physiology.

[64]  B. Svensson,et al.  Identification, cloning and characterization of two thioredoxin h isoforms, HvTrxh1 and HvTrxh2, from the barley seed proteome. , 2003, European journal of biochemistry.

[65]  S. Clerens,et al.  Fructan 1-Exohydrolases. β-(2,1)-Trimmers during Graminan Biosynthesis in Stems of Wheat? Purification, Characterization, Mass Mapping, and Cloning of Two Fructan 1-Exohydrolase Isoforms1,212 , 2003, Plant Physiology.

[66]  N. Patron,et al.  A Low-Starch Barley Mutant, Risø 16, Lacking the Cytosolic Small Subunit of ADP-Glucose Pyrophosphorylase, Reveals the Importance of the Cytosolic Isoform and the Identity of the Plastidial Small Subunit1 , 2003, Plant Physiology.

[67]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[68]  U. Wobus,et al.  The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. , 2003, The Plant journal : for cell and molecular biology.

[69]  Chungui Lu,et al.  Balancing supply and demand: the spatial regulation of carbon metabolism in grass and cereal leaves. , 2003, Journal of experimental botany.

[70]  M. Paul,et al.  Carbon metabolite feedback regulation of leaf photosynthesis and development. , 2003, Journal of experimental botany.

[71]  M. Yamamoto,et al.  The structural organisation of the gene encoding class II starch synthase of wheat and barley and the evolution of the genes encoding starch synthases in plants , 2003, Functional & Integrative Genomics.

[72]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[73]  N. Patron,et al.  The Altered Pattern of Amylose Accumulation in the Endosperm of Low-Amylose Barley Cultivars Is Attributable to a Single Mutant Allele of Granule-Bound Starch Synthase I with a Deletion in the 5′-Non-Coding Region1 , 2002, Plant Physiology.

[74]  D. Laurie,et al.  Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. , 2002, The Plant journal : for cell and molecular biology.

[75]  Alex E. Lash,et al.  Gene Expression Omnibus: NCBI gene expression and hybridization array data repository , 2002, Nucleic Acids Res..

[76]  F. Speleman,et al.  Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes , 2002, Genome Biology.

[77]  G M Coruzzi,et al.  Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects'. , 2001, Current opinion in plant biology.

[78]  Alison M. Smith,et al.  The biosynthesis of starch granules. , 2001, Biomacromolecules.

[79]  C. Offler,et al.  Compartmentation of transport and transfer events in developing seeds. , 2001, Journal of experimental botany.

[80]  Seth J Davis,et al.  Watching the hands of the Arabidopsis biological clock , 2001, Genome Biology.

[81]  M. Stitt,et al.  Diurnal changes in sucrose, nucleotides, starch synthesis and AGPS transcript in growing potato tubers that are suppressed by decreased expression of sucrose phosphate synthase. , 2000, The Plant journal : for cell and molecular biology.

[82]  U. Wobus,et al.  Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. , 2000, The Plant journal : for cell and molecular biology.

[83]  S. Smeekens,et al.  Photosynthesis, sugars and the regulation of gene expression. , 2000, Journal of experimental botany.

[84]  S. Smeekens,et al.  Fructan: more than a reserve carbohydrate? , 1999, Plant physiology.

[85]  R. Burton,et al.  A single limit dextrinase gene is expressed both in the developing endosperm and in germinated grains of barley. , 1999, Plant physiology.

[86]  Alison M. Smith,et al.  Making starch. , 1999, Current opinion in plant biology.

[87]  C. Jansson,et al.  The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. , 1998, Plant physiology.

[88]  C. Jansson,et al.  Identification of four starch-branching enzymes in barley endosperm: partial purification of forms I, IIa and IIb. , 1997, The New phytologist.

[89]  P. Carbonero,et al.  The Spatial Distribution of Sucrose Synthase Isozymes in Barley , 1997, Plant physiology.

[90]  A. Déjardin,et al.  Molecular cloning and expression of the large subunit of ADP-glucose pyrophosphorylase from barley (Hordeum vulgare) leaves. , 1997, Gene.

[91]  K. Koch CARBOHYDRATE-MODULATED GENE EXPRESSION IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[92]  L. Kleczkowski,et al.  A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). , 1996, The Biochemical journal.

[93]  G. Coruzzi,et al.  Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. , 1995, The Plant cell.

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

[95]  L. Kleczkowski,et al.  ADP-Glucose Pyrophosphorylase Large Subunit cDNA from Barley Endosperm. , 1992, Plant physiology.