A Genome-Wide Analysis of the Effects of Sucrose on Gene Expression in Arabidopsis Seedlings under Anoxia[w]

Exogenous sucrose (Suc) greatly enhances anoxia tolerance of Arabidopsis (Arabidopsis thaliana) seedlings. We used the Affymetrix ATH1 GeneChip containing more than 22,500 probe sets to explore the anaerobic transcriptome of Arabidopsis seedlings kept under anoxia for 6 h in presence or absence of exogenous Suc. Functional clustering was performed using the MapMan software. Besides the expected induction of genes encoding enzymes involved in Suc metabolism and alcoholic fermentation, a large number of genes not related to these pathways were affected by anoxia. Addition of exogenous Suc mitigated the effects of anoxia on auxin responsive genes that are repressed under oxygen deprivation. Anoxia-induced Suc synthases showed a lower induction in presence of exogenous Suc, suggesting that induction of these genes might be related to an anoxia-dependent sugar starvation. Anoxic induction of genes coding for heat shock proteins was much stronger in presence of exogenous Suc. Interestingly, a short heat treatment enhanced anoxia tolerance, suggesting that heat shock proteins may play a role in survival to low oxygen. These results provide insight into the effects of Suc on the anoxic transcriptome and provide a list of candidate genes that enhance anoxia tolerance of Suc-treated seedlings.

[1]  B. Vartapetian,et al.  Mitochondrial Ultrastructure of Three Hygrophyte Species at Anoxia and in Anoxic Glucose-Supplemented Medium , 1986 .

[2]  Christopher D Town,et al.  Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. , 2004, The Plant journal : for cell and molecular biology.

[3]  P. Perata,et al.  Sugar modulation of alpha-amylase genes under anoxia. , 2003, Annals of botany.

[4]  M. Jackson,et al.  Plant adaptations to anaerobic stress , 1997 .

[5]  P. Perata,et al.  Amylolytic Activities in Cereal Seeds under Aerobic and Anaerobic Conditions , 1995, Plant physiology.

[6]  R. Reggiani,et al.  Anaerobic Amino Acid Metabolism , 2003, Russian Journal of Plant Physiology.

[7]  R S Reneman,et al.  Heat shock proteins and cardiovascular pathophysiology. , 2001, Physiological reviews.

[8]  M. Ellis,et al.  Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. , 1999, Plant physiology.

[9]  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.

[10]  V. Germain,et al.  The Role of Sugars, Hexokinase, and Sucrose Synthase in the Determination of Hypoxically Induced Tolerance to Anoxia in Tomato Roots , 1997, Plant physiology.

[11]  Bush,et al.  Mitochondrial contribution to the anoxic Ca2+ signal in maize suspension-cultured cells , 1998, Plant physiology.

[12]  P. Perata,et al.  Mobilization of Endosperm Reserves in Cereal Seeds under Anoxia , 1997 .

[13]  J. Bailey-Serres,et al.  Post-transcriptional regulation of gene expression in oxygen-deprived roots of maize , 1995 .

[14]  J. Pozueta-Romero,et al.  Effect of anoxia on starch breakdown in rice and wheat seeds , 1992, Planta.

[15]  M. Stam,et al.  Review Article: The Silence of Genes in Transgenic Plants , 1997 .

[16]  O. Pisarenko,et al.  Substrate accessibility to cytosolic aspartate aminotransferase improves posthypoxic recovery of isolated rat heart. , 1995, Biochemical and molecular medicine.

[17]  S. Baud,et al.  Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. , 2004, Journal of experimental botany.

[18]  K E Koch,et al.  Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. , 2000, Journal of experimental botany.

[19]  I. P. Maslova,et al.  Functional electron microscopy in studies of plant response and adaptation to anaerobic stress. , 2003, Annals of botany.

[20]  S. Lindquist,et al.  Heat Shock Protein 101 Plays a Crucial Role in Thermotolerance in Arabidopsis , 2000, Plant Cell.

[21]  B. Trevaskis,et al.  Strategies of Gene Action in Arabidopsis during Hypoxia , 1997 .

[22]  L. Voesenek,et al.  Flooding and Plant Growth , 2003 .

[23]  P. Perata,et al.  Carbohydrate metabolism and anoxia tolerance in cereal grains , 1998 .

[24]  M. Sachs,et al.  Differential expression and sequence analysis of the maize glyceraldehyde-3-phosphate dehydrogenase gene family. , 1989, The Plant cell.

[25]  P. Perata,et al.  Sucrose Synthesis in Cereal Grains under Oxygen Deprivation , 1999, Journal of Plant Research.

[26]  P. Perata,et al.  Plant responses to anaerobiosis , 1993 .

[27]  P. Perata,et al.  Sugar Repression of a Gibberellin-Dependent Signaling Pathway in Barley Embryos. , 1997, The Plant cell.

[28]  E. J. Klok,et al.  Enhancing the anaerobic response. , 2003, Annals of botany.

[29]  A. Pradet,et al.  Rice embryos can express heat-shock genes under anoxia. , 1987, Biochimie.

[30]  S. Chapman,et al.  Expression Profile Analysis of the Low-Oxygen Response in Arabidopsis Root Cultures Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004747. , 2002, The Plant Cell Online.

[31]  Martin M. Sachs,et al.  Anaerobic gene expression and flooding tolerance in maize , 1996 .

[32]  T. Kozlowski Flooding and Plant Growth , 1985 .

[33]  A. Fernie,et al.  A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers1 , 2003, Plant Physiology.

[34]  V. Germain,et al.  Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Cris Kuhlemeier,et al.  The Pyruvate decarboxylase1 Gene of Arabidopsis Is Required during Anoxia But Not Other Environmental Stresses[w] , 2003, Plant Physiology.