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

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 ␤-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.

Membrane Dynamics and Multiple Functions of Oil Bodies in Seeds and Leaves

“…Fatty acids may be transported from oil bodies to glyoxysomes via small vesicles originating from the oil body, rather than free diffusion through the cytosol. In support of this hypothesis, PED3 is enriched significantly on the dendritic tubule membrane where the vesicles may dock (Cui et al, 2016). A recent study observed the retrograde flow of membranous structures from glyoxysomes to oil bodies in plant cells (Thazar-Poulot et al, 2015).…”

“…Cytological observations of the Arabidopsis specific triacylglycerol lipase (sdp1) mutant revealed that the close proximity of oil bodies and glyoxysomes is strictly regulated by the intracellular Suc concentration, which is an end product of triacylglycerol catabolism (Cui et al, 2016). Arabidopsis cells contain substantial oil body aggregates during early seedling growth.…”

Disparate peroxisome‐related defects in Arabidopsis pex6 and pex26 mutants link peroxisomal retrotranslocation and oil body utilization

“…Although peroxisomes and oil bodies interact in Arabidopsis (Hayashi et al ., ; Schumann et al ., ; Thazar‐Poulot et al ., ), the molecular details of the relationship are incompletely understood. Peroxisome–oil body clustering is heightened when Arabidopsis seedlings are grown without sucrose (Cui et al ., ). We observed peroxisomes nestled around persisting oil bodies in pex6‐1 , pex6‐3, pex6‐4 , and pex26‐1 even when supplemented with sucrose (Figure ).…”

Plant peroxisomes: A nitro-oxidative cocktail

“…In some cases, these metabolic interactions may involve dynamic and reversible functional and morphological adaptations between peroxisomes and other organelles such as chloroplasts and oil bodies during physiological processes such as photorespiration [19], [51], [84] and seed germination [35] which enable metabolic exchanges between the organelles to be optimized [63]. So far, over 300 plant peroxisomal proteins have been identified [69], [93]; however, innovative approaches using proteomic and bioinformatic technologies, with the combination of highly purified peroxisomes from different plant tissues at different developmental stages, have brought to light new and unexpected components with hitherto unknown functions [3], [47], [60], [62], [71], [88], [99].…”