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Title: Exogenous trehalose promotes non-structural carbohydrate accumulation and induces chemical detoxification and stress response proteins in Arabidopsis thaliana grown in liquid culture

item Bae, Hanhong
item Herman, Eliot
item Sicher, Richard

Submitted to: Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/7/2005
Publication Date: 3/5/2005
Citation: Bae, H., Herman, E.M., Sicher Jr, R.C. 2005. Exogenous trehalose promotes non-structural carbohydrate accumulation and induces chemical detoxification and stress response proteins in Arabidopsis thaliana grown in liquid culture. Plant Science. 168:1293-1301.

Interpretive Summary: Carbon dioxide levels in the atmosphere are rising rapidly and this is expected to impact agricultural production in the near future. Increased atmospheric carbon dioxide also may affect plant growth and development. Sugar concentrations almost always increase when plants are grown with enhanced carbon dioxide. Sugars are essential constituents of plants and are involved in both growth and metabolism. Although the exact mechanisms are unknown, specific sugars also affect plant gene expression. One sugar known to alter plant gene expression is trehalose. Trehalose has many important functions in lower organisms including yeasts, fungi, and certain insects. Trehalose is present in trace amounts in all flowering plants but externally applied trehalose is toxic and drastically inhibits root growth. The objective of this research was to determine how external trehalose altered the expression of genes using the experimental higher plant, thale cress. Total proteins from control and trehalose treated leaves were separated on gels and were identified using a database containing all of the thale cress genes. Gel images showed that ten proteins were either positively or negatively affected by external trehalose and seven of these proteins were identified using available sequence information. The proteins that were increased by trehalose treatment were primarily involved in removing toxic chemicals and in relieving environmental stress. The genes we have identified will now be studied in crop plants. This research will benefit scientists studying the control of plant gene expression and will be used for engineering plants to survive chemical stress caused by plant pathogens.

Technical Abstract: Trehalose is a nonreducing disaccharide that occurs in most living organisms, and it functions as the principal storage carbohydrate and as an important osmoprotectant in yeast and certain fungi. Although trehalose is only present in trace amounts in flowering plants, it was shown to be essential for embryo maturation. Exogenous trehalose in millimolar amounts was toxic to higher plants and strongly inhibited root growth and leaf expansion of Arabidopsis thaliana (L.) Henyh. In the current study, either 30 mM trehalose or sterile water was added to two week old liquid cultures containing Arabidopsis seedlings (Columbia) and samples were collected after 2 and 72 h of treatment. Densely stained particles, possibly glycans or proteoglycans, were detected by transmission electron microscopy in the extracellular regions of both cotyledons and roots of trehalose treated seedlings. Starch, sucrose and glutamate were increased, ATP levels were reduced and glutamine, hexoses and chlorophyll were unchanged in response to 3 days treatment with 30 mM exogenous trehalose. Using two-dimensional gel electrophoresis, ten protein spots were detected that responded to treatment with 30 mM exogenous trehalose for 2 and 12 h. Seven of these polypeptides were identified by sequence analysis determined by mass spectrometry. Two of the identified proteins, Phi glutathione S-transferase 2 (AtGSTF2) and flavin mononucleotide-binding flavodoxin-like quinone reductase 1 (FQR1), were involved in detoxification reactions. Two other identified proteins, cytosolic dehydroascorbate reductase 1 (DHAR1) and S-adenosylmethionine synthetase 2 (SAMS2), were stress response proteins. Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase was the only protein in the present study that was decreased by exogenous trehalose. It was concluded that Arabidopsis synthesized detoxifying and stress response proteins in order to cope with high concentrations of exogenous trehalose and that similar mechanisms are likely involved in plant defense systems directed against trehalose producing pathogens and other organisms in the environment.