Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000877.

We have used cDNA microarrays to examine changes in gene expression during Arabidopsis seed development and to compare wild-type and mutant wrinkled1 (wri1) seeds that have an 80% reduction in oil. Between 5 and 13 days after flowering, a period preceding and including the major accumulation of storage oils and proteins, ∼35% of the genes represented on the array changed at least twofold, but a larger fraction (65%) showed little or no change in expression. Genes whose expression changed most tended to be expressed more in seeds than in other tissues. Genes related to the biosynthesis of storage components showed several distinct temporal expression patterns. For example, a number of genes encoding core fatty acid synthesis enzymes displayed a bell-shaped pattern of expression between 5 and 13 days after flowering. By contrast, the expression of storage proteins, oleosins, and other known abscisic acid–regulated genes increased later and remained high. Genes for photosynthetic proteins followed a pattern very similar to that of fatty acid synthesis proteins, implicating a role in CO2 refixation and the supply of cofactors for oil synthesis. Expression profiles of key carbon transporters and glycolytic enzymes reflected shifts in flux from cytosolic to plastid metabolism. Despite major changes in metabolism between wri1 and wild-type seeds, <1% of genes differed by more than twofold, and most of these were involved in central lipid and carbohydrate metabolism. Thus, these data define in part the downstream responses to disruption of the WRI1 gene.

[1]  J. Ohlrogge,et al.  Protocol for small-scale RNA isolation and transcriptional profiling of developing Arabidopsis seeds. , 2001, BioTechniques.

[2]  G. Ditta,et al.  Abundance, diversity, and regulation of mRNA sequence sets in soybean embryogenesis. , 1981, Developmental biology.

[3]  M. Van Montagu,et al.  Differential Expression of the Arabidopsis 2S Albumin Genes and the Effect of Increasing Gene Family Size. , 1990, The Plant cell.

[4]  S. Merlot,et al.  The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. , 1997, The Plant cell.

[5]  P. Eastmond,et al.  Photosynthesis by developing embryos of oilseed rape (Brassica napus L.) , 1996 .

[6]  Alison M. Smith,et al.  A Mutant of Arabidopsis Lacking a Chloroplastic Isoamylase Accumulates Both Starch and Phytoglycogen , 1998, Plant Cell.

[7]  Tong Zhu,et al.  Multiple transcription-factor genes are early targets of phytochrome A signaling , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Furbank,et al.  CO2 refixation characteristics of developing canola seeds and silique wall , 1998 .

[9]  The Arabidopsis Genome Initiative.  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[10]  A. Kinney,et al.  Developmental and Growth Temperature Regulation of Two Different Microsomal [omega]-6 Desaturase Genes in Soybeans , 1996, Plant physiology.

[11]  C. Benning,et al.  wrinkled1: A novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. , 1998, Plant physiology.

[12]  P. Brown,et al.  DNA arrays for analysis of gene expression. , 1999, Methods in enzymology.

[13]  Fan Kang,et al.  Starch and fatty acid synthesis in plastids from developing embryos of oilseed rape (Brassica napus L.) , 1994 .

[14]  E. Wurtele,et al.  Coordinate regulation of the nuclear and plastidic genes coding for the subunits of the heteromeric acetyl-coenzyme A carboxylase. , 2000, Plant physiology.

[15]  J. Ohlrogge,et al.  A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. , 2000, Plant physiology.

[16]  U. Wobus,et al.  A sucrose-synthase gene of Vicia faba L.: Expression pattern in developing seeds in relation to starch synthesis and metabolic regulation , 2004, Planta.

[17]  R. Furbank,et al.  Carbohydrate Content and Enzyme Metabolism in Developing Canola Siliques , 1997, Plant physiology.

[18]  P. McCourt,et al.  Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. , 1986, Analytical biochemistry.

[19]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[20]  P. Eastmond,et al.  Coordinate changes in carbon partitioning and plastidial metabolism during the development of oilseed rape embryos. , 2000, Plant physiology.

[21]  M. Emes,et al.  NONPHOTOSYNTHETIC METABOLISM IN PLASTIDS. , 2003, Annual review of plant physiology and plant molecular biology.

[22]  J. Shumway,et al.  Role of ABA in Maturation of Rapeseed Embryos. , 1985, Plant physiology.

[23]  O. Folkerts,et al.  Expression Profiling of the Maize Flavonoid Pathway Genes Controlled by Estradiol-Inducible Transcription Factors CRC and P , 2000, Plant Cell.

[24]  K. Shinozaki,et al.  Characterization of two cDNAs that encode MAP kinase homologues in Arabidopsis thaliana and analysis of the possible role of auxin in activating such kinase activities in cultured cells. , 1994, The Plant journal : for cell and molecular biology.

[25]  U. Wobus,et al.  Seed maturation: genetic programmes and control signals. , 1999, Current opinion in plant biology.

[26]  J. Zou,et al.  Induction of Lipid and Oleosin Biosynthesis by (+)-Abscisic Acid and Its Metabolites in Microspore-Derived Embryos of Brassica napus L.cv Reston (Biological Responses in the Presence of 8[prime]-Hydroxyabscisic Acid) , 1995, Plant physiology.

[27]  S. Mansfield,et al.  Cotyledon cell development in Arabidopsis thaliana during reserve deposition , 1992 .

[28]  D. Meinke,et al.  Analysis of storage proteins in normal and aborted seeds from embryo-lethal mutants of Arabidopsis thaliana , 1986, Planta.

[29]  J. Ohlrogge,et al.  Regulation of plant lipid biosynthesis: an example of developmental regulation superimposed on a ubiquitous pathway. , 1993 .

[30]  P. Beyer,et al.  Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. , 2000, Science.

[31]  C. Somerville,et al.  Three Classes of Abscisic Acid (ABA)-Insensitive Mutations of Arabidopsis Define Genes that Control Overlapping Subsets of ABA Responses. , 1990, Plant physiology.

[32]  J. Ohlrogge,et al.  Microarray analysis of developing Arabidopsis seeds. , 2000, Plant physiology.

[33]  J. Sheen,et al.  Feedback control of gene expression , 1994, Photosynthesis Research.

[34]  Y. Hihara,et al.  DNA Microarray Analysis of Cyanobacterial Gene Expression during Acclimation to High Light , 2001, Plant Cell.

[35]  T. Voelker,et al.  Genetic engineering of a quantitative trait: metabolic and genetic parameters influencing the accumulation of laurate in rapeseed , 1996 .

[36]  D. Northcote,et al.  The use of acetyl-CoA carboxylase activity and changes in wall composition as measures of embryogenesis in tissue cultures of oil palm (Elaeis guineensis). , 1982, The Biochemical journal.

[37]  D. Northcote,et al.  Changes in the activity of acetyl-CoA carboxylase during rape-seed formation. , 1983, The Biochemical journal.

[38]  P. Brown,et al.  Exploring the metabolic and genetic control of gene expression on a genomic scale. , 1997, Science.

[39]  M. Moloney,et al.  Oilbody Proteins in Microspore-Derived Embryos of Brassica napus: Hormonal, Osmotic, and Developmental Regulation of Synthesis. , 1991, Plant physiology.

[40]  E. Brown,et al.  Genomic analysis of gene expression in C. elegans. , 2000, Science.

[41]  E. Krebbers,et al.  Gene discovery and product development for grain quality traits. , 1999, Science.

[42]  D. Dennis,et al.  Respiratory pathways and fat synthesis in the developing castor oil seed , 1979 .