Characterization of the Arabidopsis thermosensitive mutant atts02 reveals an important role for galactolipids in thermotolerance

Abstract

Plants are constantly challenged with various abiotic stresses in their natural environment. Elevated temperatures have a detrimental impact on overall plant growth and productivity. Many plants increase their tolerance to high temperatures through an adaptation response known as acquired thermotolerance. To identify the various mechanisms that plants have evolved to cope with high temperature stress, we have isolated a series of Arabidopsis mutants that are defective in the acquisition of thermotolerance after an exposure to 38 ∞ C, a treatment that induces acquired thermotolerance in wild-type plants. One of these mutants, atts02 , was not only defective in acquiring thermotolerance after the treatment, but also displayed a reduced level of basal thermotolerance in a 30 ∞ C growth assay. The affected gene in atts02 was identified by positional cloning and encodes digalactosyldiacylglycerol synthase 1 (DGD1) (the atts02 mutant was, at that point, renamed dgd1-2 ). An additional dgd1 allele, dgd1-3 , was identified in two other mutant lines displaying altered acquired thermotolerance, atts100 and atts104 . Expression patterns of several heat shock proteins (HSPs) in heattreated dgd1-2 homozygous plants were similar to those from identically treated wild-type plants, suggesting that the thermosensitivity in the dgd1-2 mutant was not caused by a defect in HSP induction. Lipid analysis of wild-type and mutant plants indicated a close correlation between the ability to acquire thermotolerance and the increases in digalactosyldiacylglycerol (DGDG) level and in the ratio of DGDG to monogalactosyldiacylglycerol (MGDG). Thermosensitivity in dgd1-2 and dgd1-3 was associated with (1) a decreased DGDG level and (2) an inability to increase the ratio of DGDG to MGDG upon exposure to a 38 ∞ C sublethal temperature treatment. Our results suggest that the DGDG level and/or the ratio of DGDG to MGDG may play an important role in basal as well as acquired thermotolerance in Arabidopsis .

Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

“…Under phosphate starvation, phospholipids are replaced by galactolipids in not only the thylakoid membrane, but also the extraplastidic membranes (Härtel et al, 2000), thereby reducing the need for phosphorus consumption for membrane lipid biosynthesis. Proportional changes of glycerolipid species have also been documented in plants subjected to temperature fluctuations (Pearcy, 1978;Johnson and Williams, 1989;Harwood, 1991Harwood, , 1994Chen et al, 2006). An increased proportion of DGDG was observed at high temperature in Arabidopsis (Chen et al, 2006), whereas biosynthesis of MGDG in canola (Brassica napus) was induced by low temperature (Johnson and Williams, 1989).…”

Plant lipidomics: Discerning biological function by profiling plant complex lipids using mass spectrometry

“…Increases in the saturation level of other major polar lipids in response to heat treatment were also observed in this study (data not shown). Taken together, the results (22) suggest that acquired thermotolerance induced by heat acclimation in wild-type Arabidopsis is associated with an increase in relative amount of GalGalDG, a dramatic increase in GalGalDG to GalDG ratio, and a moderate increase in saturation of fatty acids.…”

“…DGD1 knock-out mutants also show defective growth phenotypes. In contrast to dgd1-1 and the knockout mutants, the growth and development of dgd1-2 and dgd1-3 mutant plants are similar to wild-type plants under normal conditions (22). To determine if DGD1 function is indeed affected by the mutations in dgd1-2/dgd1-3, their lipid and fatty acid profile changes were examined in comparison to those of wild-type plants under normal growth conditions, using ESI-MS/MS (5, 6).…”

“…One of the identified loci, defined by two allelic mutants, atts02 and atts104 (renamed as dgd1-2 and dgd1-3, respectively), was shown by map-based cloning to encode digalactosyldiacylglycerol synthase 1 (DGD1) (22). Mutations in DGD1 resulted in plants both defective in acquired thermotolerance and susceptible to moderately elevated temperatures (reduced level of basal thermotolerance).…”

Genetic engineering for heat tolerance in plants

“…How Hsps (or other methods of eliciting thermotolerance discussed in this chapter) can play a role in protecting such important cellular reactions need to be taken up for further research. Chen et al (2006) recently isolated series of Arabidopsis mutants that are defective in the acquisition of thermotolerance in response to sublethal high temperature treatment. In the specific mutant type named dgd1-2 which has lesion with respect to loss of acquired as well as basal thermotolerance, affected gene was shown to encode for digalactosyldiacylglycerol synthase 1 (DGD1).…”