First published online September 8, 2006; 10.1104/pp.106.086694
Plant Physiology 142:839-854 (2006)
© 2006 American Society of Plant Biologists
BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES
Arabidopsis Seed Development and Germination Is Associated with Temporally Distinct Metabolic Switches1,[W]
Aaron Fait2,
Ruthie Angelovici2,
Hadar Less,
Itzhak Ohad,
Ewa Urbanczyk-Wochniak,
Alisdair R. Fernie and
Gad Galili*
Department of Plant Sciences, the Weizmann Institute of Science, 76100 Rehovot, Israel (A.F., R.A., H.L., G.G.); Minerva Avron Evenari Center for Photosynthesis Research, Department of Biological Chemistry, The Hebrew University, 91904 Jerusalem, Israel (I.O.); and Abteitlung Willmitzer, Max-Planck-Institut für Molekulare Pflanzenphysiologie, 14476 Golm-Potsdam, Germany (E.U.-W., A.R.F.)
While the metabolic networks in developing seeds during the period of reserve accumulation have been extensively characterized, much less is known about those present during seed desiccation and subsequent germination. Here we utilized metabolite profiling, in conjunction with selective mRNA and physiological profiling to characterize Arabidopsis (Arabidopsis thaliana) seeds throughout development and germination. Seed maturation was associated with a significant reduction of most sugars, organic acids, and amino acids, suggesting their efficient incorporation into storage reserves. The transition from reserve accumulation to seed desiccation was associated with a major metabolic switch, resulting in the accumulation of distinct sugars, organic acids, nitrogen-rich amino acids, and shikimate-derived metabolites. In contrast, seed vernalization was associated with a decrease in the content of several of the metabolic intermediates accumulated during seed desiccation, implying that these intermediates might support the metabolic reorganization needed for seed germination. Concomitantly, the levels of other metabolites significantly increased during vernalization and were boosted further during germination sensu stricto, implying their importance for germination and seedling establishment. The metabolic switches during seed maturation and germination were also associated with distinct patterns of expression of genes encoding metabolism-associated gene products, as determined by semiquantitative reverse transcription-polymerase chain reaction and analysis of publicly available microarray data. When taken together our results provide a comprehensive picture of the coordinated changes in primary metabolism that underlie seed development and germination in Arabidopsis. They furthermore imply that the metabolic preparation for germination and efficient seedling establishment initiates already during seed desiccation and continues by additional distinct metabolic switches during vernalization and early germination.
1 This work was supported by the German Federal Ministry of Education and Research within the framework of German-Israeli Project Cooperation as well as the Charles W. and Tillie K. Lubin Centre for Plant Biotechnology at the Weizmann Institute of Science. G.G. is an incumbent of the Bronfman Chair of Plant Science at the Weizmann Institute of Science. A.F. is a Postdoc fellow sponsored by the Alexander von Humboldt foundation.
2 These authors contributed equally to the paper.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Gad Galili (gad.galili{at}weizmann.ac.il).
[W] The online version of this article contains Web-only data.
www.plantphysiol.org/cgi/doi/10.1104/pp.106.086694
* Corresponding author; e-mail gad.galili{at}weizmann.ac.il; fax 972–8–9344181.
Received July 13, 2006;
accepted August 29, 2006;
published September 8, 2006.
This article has been cited by other articles:
|
|
|
|
 
M. Hansen, C. Friis, S. Bowra, P. B. Holm, and E. Vincze
A pathway-specific microarray analysis highlights the complex and co-ordinated transcriptional networks of the developing grain of field-grown barley
J. Exp. Bot.,
November 17, 2008;
(2008)
ern270v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Fait, K. Hanhineva, R. Beleggia, N. Dai, I. Rogachev, V. J. Nikiforova, A. R. Fernie, and A. Aharoni
Reconfiguration of the Achene and Receptacle Metabolic Networks during Strawberry Fruit Development
Plant Physiology,
October 1, 2008;
148(2):
730 - 750.
[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. 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]
|
|
|
|
|
|
|
J. Catusse, J.-M. Strub, C. Job, A. Van Dorsselaer, and D. Job
Proteome-wide characterization of sugarbeet seed vigor and its tissue specific expression
PNAS,
July 22, 2008;
105(29):
10262 - 10267.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Jumtee, T. Bamba, A. Okazawa, E. Fukusaki, and A. Kobayashi
Integrated metabolite and gene expression profiling revealing phytochrome A regulation of polyamine biosynthesis of Arabidopsis thaliana
J. Exp. Bot.,
April 1, 2008;
59(6):
1187 - 1200.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Sreenivasulu, B. Usadel, A. Winter, V. Radchuk, U. Scholz, N. Stein, W. Weschke, M. Strickert, T. J. Close, M. Stitt, et al.
Barley Grain Maturation and Germination: Metabolic Pathway and Regulatory Network Commonalities and Differences Highlighted by New MapMan/PageMan Profiling Tools
Plant Physiology,
April 1, 2008;
146(4):
1738 - 1758.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Vigeolas, C. Chinoy, E. Zuther, B. Blessington, P. Geigenberger, and C. Domoney
Combined Metabolomic and Genetic Approaches Reveal a Link between the Polyamine Pathway and Albumin 2 in Developing Pea Seeds
Plant Physiology,
January 1, 2008;
146(1):
74 - 82.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Andre and C. Benning
Arabidopsis Seedlings Deficient in a Plastidic Pyruvate Kinase Are Unable to Utilize Seed Storage Compounds for Germination and Establishment
Plant Physiology,
December 1, 2007;
145(4):
1670 - 1680.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Martinelli, A. Whittaker, A. Bochicchio, C. Vazzana, A. Suzuki, and C. Masclaux-Daubresse
Amino acid pattern and glutamate metabolism during dehydration stress in the 'resurrection' plant Sporobolus stapfianus: a comparison between desiccation-sensitive and desiccation-tolerant leaves
J. Exp. Bot.,
August 1, 2007;
58(11):
3037 - 3046.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Footitt, D. Dietrich, A. Fait, A. R. Fernie, M. J. Holdsworth, A. Baker, and F. L. Theodoulou
The COMATOSE ATP-Binding Cassette Transporter Is Required for Full Fertility in Arabidopsis
Plant Physiology,
July 1, 2007;
144(3):
1467 - 1480.
[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]
|
|
|
|
|
