The Plant Cell, Vol. 14, 1191-1206,
June 2002, Copyright © 2002,
American Society of Plant Biologists
Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling
Sari A. Ruuska1,a,
Thomas Girke2,b,
Christoph Benningc and
John B. Ohlroggea
a Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
b Dow AgroSciences, 5501 Oberlin Drive, San Diego, California 92121
c Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824
1 To whom correspondence should be addressed. E-mail ruuska{at}pilot.msu.edu; fax 517-353-1926
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 acidregulated 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.
This article has been cited by other articles:

|
 |

|
 |
 
A.-B. Feria, R. Alvarez, L. Cochereau, J. Vidal, S. Garcia-Maurino, and C. Echevarria
Regulation of Phosphoenolpyruvate Carboxylase Phosphorylation by Metabolites and Abscisic Acid during the Development and Germination of Barley Seeds
Plant Physiology,
October 1, 2008;
148(2):
761 - 774.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. B. Xu, T. Li, Z. Y. Deng, K. Chong, Y. Xue, and T. Wang
Dynamic Proteomic Analysis Reveals a Switch between Central Carbon Metabolism and Alcoholic Fermentation in Rice Filling Grains
Plant Physiology,
October 1, 2008;
148(2):
908 - 925.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Mu, H. Tan, Q. Zheng, F. Fu, Y. Liang, J. Zhang, X. Yang, T. Wang, K. Chong, X.-J. Wang, et al.
LEAFY COTYLEDON1 Is a Key Regulator of Fatty Acid Biosynthesis in Arabidopsis
Plant Physiology,
October 1, 2008;
148(2):
1042 - 1054.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Fallahi, G. N. Scofield, M. R. Badger, W. S. Chow, R. T. Furbank, and Y.-L. Ruan
Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development
J. Exp. Bot.,
September 1, 2008;
59(12):
3283 - 3295.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Verdier and R. D. Thompson
Transcriptional Regulation of Storage Protein Synthesis During Dicotyledon Seed Filling
Plant Cell Physiol.,
September 1, 2008;
49(9):
1263 - 1271.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. K. Agrawal, M. Hajduch, K. Graham, and J. J. Thelen
In-Depth Investigation of the Soybean Seed-Filling Proteome and Comparison with a Parallel Study of Rapeseed
Plant Physiology,
September 1, 2008;
148(1):
504 - 518.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Zhang, S. D. Rider Jr., J. T. Henderson, M. Fountain, K. Chuang, V. Kandachar, A. Simons, H. J. Edenberg, J. Romero-Severson, W. M. Muir, et al.
The CHD3 Remodeler PICKLE Promotes Trimethylation of Histone H3 Lysine 27
J. Biol. Chem.,
August 15, 2008;
283(33):
22637 - 22648.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Gallardo, C. Firnhaber, H. Zuber, D. Hericher, M. Belghazi, C. Henry, H. Kuster, and R. Thompson
A Combined Proteome and Transcriptome Analysis of Developing Medicago truncatula Seeds: Evidence for Metabolic Specialization of Maternal and Filial Tissues
Mol. Cell. Proteomics,
December 1, 2007;
6(12):
2165 - 2179.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Ruttink, M. Arend, K. Morreel, V. Storme, S. Rombauts, J. Fromm, R. P. Bhalerao, W. Boerjan, and A. Rohde
A Molecular Timetable for Apical Bud Formation and Dormancy Induction in Poplar
PLANT CELL,
August 1, 2007;
19(8):
2370 - 2390.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Hudson, T. Bruggink, S. H. Chang, W. Yu, B. Han, X. Wang, P. van der Toorn, and T. Zhu
Analysis of Gene Expression during Brassica Seed Germination Using a Cross-Species Microarray Platform
Crop Sci.,
July 16, 2007;
47(S2):
S-96 - S-112.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Andre, J. E. Froehlich, M. R. Moll, and C. Benning
A Heteromeric Plastidic Pyruvate Kinase Complex Involved in Seed Oil Biosynthesis in Arabidopsis
PLANT CELL,
June 1, 2007;
19(6):
2006 - 2022.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. O'Hara, A. R. Slabas, and T. Fawcett
Antisense Expression of 3-Oxoacyl-ACP Reductase Affects Whole Plant Productivity and Causes Collateral Changes in Activity of Fatty Acid Synthase Components
Plant Cell Physiol.,
May 1, 2007;
48(5):
736 - 744.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Chopin, M. Orsel, M.-F. Dorbe, F. Chardon, H.-N. Truong, A. J. Miller, A. Krapp, and F. Daniel-Vedele
The Arabidopsis ATNRT2.7 Nitrate Transporter Controls Nitrate Content in Seeds
PLANT CELL,
May 1, 2007;
19(5):
1590 - 1602.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Carrera, T. Holman, A. Medhurst, W. Peer, H. Schmuths, S. Footitt, F. L. Theodoulou, and M. J. Holdsworth
Gene Expression Profiling Reveals Defined Functions of the ATP-Binding Cassette Transporter COMATOSE Late in Phase II of Germination
Plant Physiology,
April 1, 2007;
143(4):
1669 - 1679.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Dhaubhadel, M. Gijzen, P. Moy, and M. Farhangkhoee
Transcriptome Analysis Reveals a Critical Role of CHS7 and CHS8 Genes for Isoflavonoid Synthesis in Soybean Seeds
Plant Physiology,
January 1, 2007;
143(1):
326 - 338.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Fait, R. Angelovici, H. Less, I. Ohad, E. Urbanczyk-Wochniak, A. R. Fernie, and G. Galili
Arabidopsis Seed Development and Germination Is Associated with Temporally Distinct Metabolic Switches
Plant Physiology,
November 1, 2006;
142(3):
839 - 854.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Gutierrez, G. Conejero, M. Castelain, S. Guenin, J.-L. Verdeil, B. Thomasset, and O. Van Wuytswinkel
Identification of new gene expression regulators specifically expressed during plant seed maturation
J. Exp. Bot.,
June 1, 2006;
57(9):
1919 - 1932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Cernac, C. Andre, S. Hoffmann-Benning, and C. Benning
WRI1 Is Required for Seed Germination and Seedling Establishment
Plant Physiology,
June 1, 2006;
141(2):
745 - 757.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Hajduch, J. E. Casteel, K. E. Hurrelmeyer, Z. Song, G. K. Agrawal, and J. J. Thelen
Proteomic Analysis of Seed Filling in Brassica napus. Developmental Characterization of Metabolic Isozymes Using High-Resolution Two-Dimensional Gel Electrophoresis
Plant Physiology,
May 1, 2006;
141(1):
32 - 46.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Radchuk, V. Radchuk, W. Weschke, L. Borisjuk, and H. Weber
Repressing the Expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE Gene in Pea Embryo Causes Pleiotropic Defects of Maturation Similar to an Abscisic Acid-Insensitive Phenotype
Plant Physiology,
January 1, 2006;
140(1):
263 - 278.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. E. Tripodi, W. L. Turner, S. Gennidakis, and W. C. Plaxton
In Vivo Regulatory Phosphorylation of Novel Phosphoenolpyruvate Carboxylase Isoforms in Endosperm of Developing Castor Oil Seeds
Plant Physiology,
October 1, 2005;
139(2):
969 - 978.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Mazzella, M. V. Arana, R. J. Staneloni, S. Perelman, M. J. Rodriguez Batiller, J. Muschietti, P. D. Cerdan, K. Chen, R. A. Sanchez, T. Zhu, et al.
Phytochrome Control of the Arabidopsis Transcriptome Anticipates Seedling Exposure to Light
PLANT CELL,
September 1, 2005;
17(9):
2507 - 2516.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Baxter, M. Sabar, W. P. Quick, and L. J. Sweetlove
Comparison of changes in fruit gene expression in tomato introgression lines provides evidence of genome-wide transcriptional changes and reveals links to mapped QTLs and described traits
J. Exp. Bot.,
June 1, 2005;
56(416):
1591 - 1604.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Masaki, N. Mitsui, H. Tsukagoshi, T. Nishii, A. Morikami, and K. Nakamura
ACTIVATOR of Spomin::LUC1/WRINKLED1 of Arabidopsis thaliana Transactivates Sugar-inducible Promoters
Plant Cell Physiol.,
April 1, 2005;
46(4):
547 - 556.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Hajduch, A. Ganapathy, J. W. Stein, and J. J. Thelen
A Systematic Proteomic Study of Seed Filling in Soybean. Establishment of High-Resolution Two-Dimensional Reference Maps, Expression Profiles, and an Interactive Proteome Database
Plant Physiology,
April 1, 2005;
137(4):
1397 - 1419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Niewiadomski, S. Knappe, S. Geimer, K. Fischer, B. Schulz, U. S. Unte, M. G. Rosso, P. Ache, U.-I. Flugge, and A. Schneider
The Arabidopsis Plastidic Glucose 6-Phosphate/Phosphate Translocator GPT1 Is Essential for Pollen Maturation and Embryo Sac Development
PLANT CELL,
March 1, 2005;
17(3):
760 - 775.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Baxter, F. Carrari, A. Bauke, S. Overy, S. A. Hill, P. W. Quick, A. R. Fernie, and L. J. Sweetlove
Fruit Carbohydrate Metabolism in an Introgression Line of Tomato with Increased Fruit Soluble Solids
Plant Cell Physiol.,
March 1, 2005;
46(3):
425 - 437.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Dian, H. Jiang, and P. Wu
Evolution and expression analysis of starch synthase III and IV in rice
J. Exp. Bot.,
February 1, 2005;
56(412):
623 - 632.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Soeda, M. C.J.M. Konings, O. Vorst, A. M.M.L. van Houwelingen, G. M. Stoopen, C. A. Maliepaard, J. Kodde, R. J. Bino, S. P.C. Groot, and A. H.M. van der Geest
Gene Expression Programs during Brassica oleracea Seed Maturation, Osmopriming, and Germination Are Indicators of Progression of the Germination Process and the Stress Tolerance Level
Plant Physiology,
January 1, 2005;
137(1):
354 - 368.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Collin, P. Lamkemeyer, M. Miginiac-Maslow, M. Hirasawa, D. B. Knaff, K.-J. Dietz, and E. Issakidis-Bourguet
Characterization of Plastidial Thioredoxins from Arabidopsis Belonging to the New y-Type
Plant Physiology,
December 1, 2004;
136(4):
4088 - 4095.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Penfield, E. L. Rylott, A. D. Gilday, S. Graham, T. R. Larson, and I. A. Graham
Reserve Mobilization in the Arabidopsis Endosperm Fuels Hypocotyl Elongation in the Dark, Is Independent of Abscisic Acid, and Requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1
PLANT CELL,
October 1, 2004;
16(10):
2705 - 2718.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. H. Hobbs, J. E. Flintham, and M. J. Hills
Genetic Control of Storage Oil Synthesis in Seeds of Arabidopsis
Plant Physiology,
October 1, 2004;
136(2):
3341 - 3349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Ruuska, J. Schwender, and J. B. Ohlrogge
The Capacity of Green Oilseeds to Utilize Photosynthesis to Drive Biosynthetic Processes
Plant Physiology,
September 1, 2004;
136(1):
2700 - 2709.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. T. Furbank, R. White, J. A. Palta, and N. C. Turner
Internal recycling of respiratory CO2 in pods of chickpea (Cicer arietinum L.): the role of pod wall, seed coat, and embryo
J. Exp. Bot.,
August 1, 2004;
55(403):
1687 - 1696.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. Kubis, M. J. Pike, C. J. Everett, L. M. Hill, and S. Rawsthorne
The import of phosphoenolpyruvate by plastids from developing embryos of oilseed rape, Brassica napus (L.), and its potential as a substrate for fatty acid synthesis
J. Exp. Bot.,
July 1, 2004;
55(402):
1455 - 1462.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Hennig, W. Gruissem, U. Grossniklaus, and C. Kohler
Transcriptional Programs of Early Reproductive Stages in Arabidopsis
Plant Physiology,
July 1, 2004;
135(3):
1765 - 1775.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W.A. Rensink and C. R. Buell
Arabidopsis to Rice. Applying Knowledge from a Weed to Enhance Our Understanding of a Crop Species
Plant Physiology,
June 1, 2004;
135(2):
622 - 629.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Lin, J. E. Cluette-Brown, and H. M. Goodman
The Peroxisome Deficient Arabidopsis Mutant sse1 Exhibits Impaired Fatty Acid Synthesis
Plant Physiology,
June 1, 2004;
135(2):
814 - 827.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. T. Henderson, H.-C. Li, S. D. Rider, A. P. Mordhorst, J. Romero-Severson, J.-C. Cheng, J. Robey, Z. R. Sung, S. C. de Vries, and J. Ogas
PICKLE Acts throughout the Plant to Repress Expression of Embryonic Traits and May Play a Role in Gibberellin-Dependent Responses
Plant Physiology,
March 1, 2004;
134(3):
995 - 1005.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Baud, M.-N. Vaultier, and C. Rochat
Structure and expression profile of the sucrose synthase multigene family in Arabidopsis
J. Exp. Bot.,
February 1, 2004;
55(396):
397 - 409.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Moire, E. Rezzonico, S. Goepfert, and Y. Poirier
Impact of Unusual Fatty Acid Synthesis on Futile Cycling through {beta}-Oxidation and on Gene Expression in Transgenic Plants
Plant Physiology,
January 1, 2004;
134(1):
432 - 442.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Gallardo, C. Le Signor, J. Vandekerckhove, R. D. Thompson, and J. Burstin
Proteomics of Medicago truncatula Seed Development Establishes the Time Frame of Diverse Metabolic Processes Related to Reserve Accumulation
Plant Physiology,
October 1, 2003;
133(2):
664 - 682.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Schwender, J. B. Ohlrogge, and Y. Shachar-Hill
A Flux Model of Glycolysis and the Oxidative Pentosephosphate Pathway in Developing Brassica napus Embryos
J. Biol. Chem.,
August 8, 2003;
278(32):
29442 - 29453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Ogawa, A. Hanada, Y. Yamauchi, A. Kuwahara, Y. Kamiya, and S. Yamaguchi
Gibberellin Biosynthesis and Response during Arabidopsis Seed Germination
PLANT CELL,
July 1, 2003;
15(7):
1591 - 1604.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Schluepmann, T. Pellny, A. van Dijken, S. Smeekens, and M. Paul
Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana
PNAS,
May 27, 2003;
100(11):
6849 - 6854.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. J.K. Koo and J. B. Ohlrogge
The Predicted Candidates of Arabidopsis Plastid Inner Envelope Membrane Proteins and Their Expression Profiles
Plant Physiology,
October 1, 2002;
130(2):
823 - 836.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Schwender and J. B. Ohlrogge
Probing in Vivo Metabolism by Stable Isotope Labeling of Storage Lipids and Proteins in Developing Brassica napus Embryos
Plant Physiology,
September 1, 2002;
130(1):
347 - 361.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|