The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness.
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.
Department of Botany II, University of Cologne, Koeln, Germany.
Hans-Henning
HH
Kunz
Michael
M
Scharnewski
Kirstin
K
Feussner
Ivo
I
Feussner
Ulf-Ingo
UI
Flügge
Martin
M
Fulda
Markus
M
Gierth
D018528:ATP-Binding Cassette Transporters / Q000235:genetics / Q000378:metabolism*; D000251:Adenosine Triphosphatases; D000255:Adenosine Triphosphate / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002734:Chlorophyll / Q000031:analogs & derivatives / Q000378:metabolism; D003001:Cloning, Molecular; D004269:DNA, Bacterial / Q000235:genetics; D003624:Darkness; D016254:Mutagenesis, Insertional; D009154:Mutation; D010084:Oxidation-Reduction; D020675:Peroxisomes / Q000235:genetics / Q000378:metabolism*; D010788:Photosynthesis; D045332:Photosystem II Protein Complex / Q000378:metabolism; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism*; D024642:Potassium Channels, Voltage-Gated / Q000235:genetics / Q000378:metabolism; D013213:Starch / Q000378:metabolism; D017962:alpha-Linolenic Acid / Q000378:metabolism
D018528:ATP-Binding Cassette Transporters; D029681:Arabidopsis Proteins; D004269:DNA, Bacterial; C428126:KAT2 protein, Arabidopsis; D045332:Photosystem II Protein Complex; D024642:Potassium Channels, Voltage-Gated; C036483:T-DNA; D017962:alpha-Linolenic Acid; D002734:Chlorophyll; D000255:Adenosine Triphosphate; D013213:Starch; D000251:Adenosine Triphosphatases; C456843:At4g39850 protein, Arabidopsis; C032623:pheophorbide a