Abstract
Fatty acid beta-oxidation is essential for seedling establishment of oilseed plants, but little is known about its role in leaf metabolism of adult plants. Arabidopsis thaliana plants with loss-of-function mutations in the peroxisomal ABC-transporter1 (PXA1) or the core beta-oxidation enzyme keto-acyl-thiolase 2 (KAT2) have impaired peroxisomal beta-oxidation. pxa1 and kat2 plants developed severe leaf necrosis, bleached rapidly when returned to light, and died after extended dark treatment, whereas the wild type was unaffected. Dark-treated pxa1 plants showed a decrease in photosystem II efficiency early on and accumulation of free fatty acids, mostly alpha-linolenic acid [18:3(n-3)] and pheophorbide a, a phototoxic chlorophyll catabolite causing the rapid bleaching. Isolated wild-type and pxa1 chloroplasts challenged with comparable alpha-linolenic acid concentrations both showed an 80% reduction in photosynthetic electron transport, whereas intact pxa1 plants were more susceptible to the toxic effects of alpha-linolenic acid than the wild type. Furthermore, starch-free mutants with impaired PXA1 function showed the phenotype more quickly, indicating a link between energy metabolism and beta-oxidation. We conclude that the accumulation of free polyunsaturated fatty acids causes membrane damage in pxa1 and kat2 plants and propose a model in which fatty acid respiration via peroxisomal beta-oxidation plays a major role in dark-treated plants after depletion of starch reserves.
Highlights
Fatty acid b-oxidation is essential for seedling establishment of oilseed plants, but little is known about its role in leaf metabolism of adult plants
At a night temperature of 248C, no visible phenotypic alterations of pxa1 and kat2 plants compared with the wild type were observed after exposure to only 16 h of darkness
We demonstrate a severe phenotype of mature pxa1 plants exposed to extended darkness that indicates an important role for peroxisomal ABC-transporter1 (PXA1) and peroxisomal b-oxidation during extended darkness
Summary
Fatty acid b-oxidation is essential for seedling establishment of oilseed plants, but little is known about its role in leaf metabolism of adult plants. B-oxidation is localized exclusively in peroxisomes, where the enzymatic reactions involved lead to the sequential degradation of long-chain fatty acids to acetylCoA. This pathway is essential in oilseeds for providing growing seedlings with carbon skeletons and energy via the glyoxylate cycle in combination with either gluconeogenesis or the citrate cycle (Baker et al, 2006; Goepfert and Poirier, 2007). PXA1 was initially identified as peroxisomal defective 3 (PED3) in a screen for Arabidopsis mutants resistant to 2,4-dichlorophenoxybutyric acid (Hayashi et al, 1998), and pxa mutants were subsequently shown to be resistant to indole butyric acid (IBA) (Zolman et al, 2001). Microarray experiments investigating transcriptional alterations on a genome-wide scale showed that the transcripts of many genes involved in b-oxidation were increased in abundance during dark-induced and natural senescence (Buchanan-Wollaston et al, 2005; van der Graaff et al, 2006), indicating a physiological function for b-oxidation in extended darkness
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