Gamma-hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms

Abstract

Enzymes that reduce the aldehyde chemical grouping (i.e. H-C=O) to its corresponding alcohol are probably crucial in maintaining plant health during stress. Succinic semialdehyde (SSA) is a mitochondrially-generated intermediate in the metabolism of gamma-aminobutyrate (GABA), which accumulates in response to a variety of biotic and abiotic stresses. SSA can be reduced to gamma-hydroxybutyrate (GHB) under oxygen deficiency and high light conditions. Recent evidence indicates that distinct cytosolic and plastidial glyoxylate reductase isoforms from Arabidopsis (designated herein after as AtGR1 and AtGR2, respectively) catalyse the in vitro conversion of SSA to GHB, as well as glyoxylate to glycolate, via NADPH-dependent reactions. In the present report, the responses of GHB and related amino acids, as well as NADP(+) and NADPH, were monitored in leaves from Arabidopsis or tobacco plants subjected to various abiotic stresses (i.e. Arabidopsis during exposure to salinity, drought, submergence, cold, or heat; tobacco during exposure to, and recovery from, submergence). Time-course experiments revealed that GHB accumulated in both Arabidopsis and tobacco plants subjected to stress, and that this accumulation was generally accompanied by higher GABA and alanine levels, higher NADPH/NADP(+) ratio, and lower glutamate levels. Furthermore, the analysis of gene expression in Arabidopsis revealed that the relative abundance of GR1 (salinity, drought, submergence, cold, and heat) and GR2 (cold and heat) transcripts was enhanced by the stress tested. Thus, GHB accumulation in plants is a general response to abiotic stress and appears to be regulated by both biochemical and transcriptional processes.

Fig. 1.

Response of metabolites in mature rosette leaves of Arabidopsis plants (A) and mature leaves of tobacco plants (B) subjected to salinity, drought, submergence, cold or heat. Closed and open circles represent control and experimental plants, respectively. Data represent the mean ±SE; where the bar is not shown, it is within the symbol. Note that the drought data only are expressed on a DM basis, rather than a FM basis. TAA represents total amino acids.

Fig. 2.

Response of phosphorylated pyridine nucleotides in mature rosette leaves of Arabidopsis plants (A) and mature leaves of tobacco plants (B) subjected to cold, heat or submergence. Closed and open circles represent control and experimental plants, respectively. Data represent the mean ±SE; where the bar is not shown, it is within the symbol.

Fig. 3.

Recovery of GHB and related metabolites (A), as well as phosphorylated pyridine nucleotides (B), in mature leaves of tobacco plants after being subjected to submergence. The column headings indicate the duration of submergence (3, 6, or 9 h) before transfer to air for an additional 9 h. Data for control and submerged plants for the first 9 h are taken from Figs 1B and 2B. Closed circles, open circles, and closed triangles, respectively, represent control plants, submerged plants, and plants returned to air after a period of submergence. Data represent the mean ±SE; where the bar is not shown, it is within the symbol.

Fig. 4.

Response of GR transcripts in mature rosette leaves of Arabidopsis plants subjected to salinity, drought, submergence, cold, or heat. Closed and open circles represent control and experimental plants, respectively. Data represent the mean ±SE; where the bar is not shown, it is within the symbol.