Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics

Abstract

Peroxisomes are essential for life in plants. These organelles house a variety of metabolic processes that generate and inactivate reactive oxygen species. Our knowledge of pathways and mechanisms that depend on peroxisomes and their constituent enzymes continues to grow, and in this review we highlight recent advances in understanding the identity and biological functions of peroxisomal enzymes and metabolic processes. We also review how peroxisomal matrix and membrane proteins enter the organelle from their sites of synthesis. Peroxisome homeostasis is regulated by specific degradation mechanisms, and we discuss the contributions of specialized autophagy and a peroxisomal protease to the degradation of entire peroxisomes and peroxisomal enzymes that are damaged or superfluous. Finally, we review how peroxisomes can flexibly change their morphology to facilitate inter-organellar contacts.

Figure 1. Peroxisome dynamics

Peroxisomal membrane proteins (PMPs) are inserted directly into peroxisomes or into the ER membrane from which pre-peroxisomes can bud. PMPs include a subset of the PEX proteins necessary for import of matrix proteins into the organelle (Figure 2). Mature peroxisomes extend and retract peroxules, tubulate, and divide by fission, which is considered to be the predominant mode of peroxisome proliferation. Peroxisomal quality control includes degrading damaged or obsolete matrix proteins and eliminating dysfunctional or superfluous peroxisomes via pexophagy, a specialized form of autophagy.

Figure 2. Import of matrix proteins into peroxisomes

Import of peroxisomal matrix proteins (green) is facilitated by peroxins (numbered ovals), some of which are integral membrane proteins (purple). The PEX5 and PEX7 receptors (blue) bind to PTS1 and PTS2 proteins in the cytosol, respectively, and dock at the peroxisomal membrane via interactions with each other and with PEX13 and PEX14. After cargo delivery into the matrix, the N-terminal PTS2 domain is cleaved. Membrane-associated PEX5 is ubiquitinated, presumably with the assistance of the PEX4 ubiquitin (Ub)-conjugating enzyme (gray) and the PEX2-PEX10-PEX12 ubiquitin-protein ligase complex. PEX5 retrotranslocation back to the cytosol for reuse requires the PEX1-PEX6 heterohexameric ATPase (pink). When retrotranslocation is impeded, PEX5 can be polyubiquitinated and degraded by the proteasome.