Sucrose Production Mediated by Lipid Metabolism Suppresses the Physical Interaction of Peroxisomes and Oil Bodies during Germination of Arabidopsis thaliana

J Biol Chem. 2016 Sep 16;291(38):19734-45. doi: 10.1074/jbc.M116.748814. Epub 2016 Jul 27.

Abstract

Physical interaction between organelles is a flexible event and essential for cells to adapt rapidly to environmental stimuli. Germinating plants utilize oil bodies and peroxisomes to mobilize storage lipids for the generation of sucrose as the main energy source. Although membrane interaction between oil bodies and peroxisomes has been widely observed, its underlying molecular mechanism is largely unknown. Here we present genetic evidence for control of the physical interaction between oil bodies and peroxisomes. We identified alleles of the sdp1 mutant altered in oil body morphology. This mutant accumulates bigger and more oil body aggregates compared with the wild type and showed defects in lipid mobilization during germination. SUGAR DEPENDENT 1 (SDP1) encodes major triacylglycerol lipase in Arabidopsis Interestingly, sdp1 seedlings show enhanced physical interaction between oil bodies and peroxisomes compared with the wild type, whereas exogenous sucrose supplementation greatly suppresses the interaction. The same phenomenon occurs in the peroxisomal defective 1 (ped1) mutant, defective in lipid mobilization because of impaired peroxisomal β-oxidation, indicating that sucrose production is a key factor for oil body-peroxisomal dissociation. Peroxisomal dissociation and subsequent release from oil bodies is dependent on actin filaments. We also show that a peroxisomal ATP binding cassette transporter, PED3, is the potential anchor protein to the membranes of these organelles. Our results provide novel components linking lipid metabolism and oil body-peroxisome interaction whereby sucrose may act as a negative signal for the interaction of oil bodies and peroxisomes to fine-tune lipolysis.

Keywords: ABC transporter; lipid droplet; lipolysis; membrane; oil body; organelle; peroxisome; sucrose production.

MeSH terms

  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism
  • Adenosine Triphosphatases
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / metabolism
  • Germination / physiology*
  • Lipid Droplets / metabolism*
  • Lipid Metabolism / physiology*
  • Peroxisomes / genetics
  • Peroxisomes / metabolism*
  • Sucrose / metabolism*

Substances

  • ATP-Binding Cassette Transporters
  • Arabidopsis Proteins
  • Sucrose
  • Carboxylic Ester Hydrolases
  • SDP1 protein, Arabidopsis
  • Adenosine Triphosphatases
  • At4g39850 protein, Arabidopsis