Peroxisomes Extend Peroxules in a Fast Response to Stress via a Reactive Oxygen Species-Mediated Induction of the Peroxin PEX11a

Abstract

Peroxisomes are highly dynamic and metabolically active organelles that play an important role in cellular functions, including reactive oxygen species (ROS) metabolism. Peroxisomal dynamics, such as the proliferation, movement, and production of dynamic extensions called peroxules, have been associated with ROS in plant cells. However, the function and regulation of peroxules are largely unknown. Using confocal microscopy, we have shown that treatment of Arabidopsis leaves with the heavy metal cadmium produces time course-dependent changes in peroxisomal dynamics, starting with peroxule formation, followed by peroxisome proliferation, and finally returning to the normal morphology and number. These changes during Cd treatment were regulated by NADPH oxidase (C and F)-related ROS production. Peroxule formation is a general response to stimuli such as arsenic and is regulated by peroxin 11a (PEX11a), as Arabidopsis pex11a RNA i lines are unable to produce peroxules under stress conditions. The pex11a line showed higher levels of lipid peroxidation content and lower expression of genes involved in antioxidative defenses and signaling, suggesting that these extensions are involved in regulating ROS accumulation and ROSdependent gene expression in response to stress. Our results demonstrate that PEX11a and peroxule formation play a key role in regulating stress perception and fast cell responses to environmental cues.Peroxisomes are highly versatile organelles that adapt to changes in their cellular environment through morphological and metabolic adjustments (Hu et al., 2012;Sandalio et al., 2013). Plant peroxisomes perform essential functions such as photorespiration and fatty acid b-oxidation, ureide, and phytohormone (auxin and jasmonic acid) metabolisms, and also act as a source of signal molecules such as reactive oxygen and nitrogen species (ROS and RNS; Sandalio and RomeroPuertas, 2015). Peroxisomes contain a large battery of antioxidants to control ROS and RNS accumulation (Sandalio and Romero-Puertas, 2015). These organelles proliferate in response to environmental cues through a complex process involving elongation, constriction, and fission (Hu et al., 2012;Baker and Paudyal, 2014). Deciphering the signaling pathways governing the regulation of peroxisome proliferation under different environmental and metabolic conditions presents a major challenge in this field of research. Before peroxisomal division, organelle elongation occurs in a process regulated by peroxins 11 (PEX11), with the final division requiring dynamin-like or dynamin-related proteins and fission proteins (Hu et al., 2012, Schrader et al., 2012. There is evidence to suggest that ROS are involved in regulating peroxisome proliferation, as some peroxisomal biogenesis genes (PEX) are transcriptionally regulated by H 2 O 2 in both plant and animal cells (López-Huertas et al., 2000). The formation of peroxisomal extensions, known as peroxules, has also been observed to be regulated by exogenous applications of H 2 O 2 (Sinclair et al., 2009;Ba...

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

“…The tubulated peroxisomes become constricted and eventually undergo fission to increase peroxisome numbers [82]. Similarly, cadmium treatment induces cytosolic ROS and rapid PEX11a-dependent peroxule formation, followed by peroxisome elongation and division [83]. Beyond increasing surface and contact areas, peroxule-mediated inter-organellar contacts might assist in delivering enzymes from peroxisomes to their final subcellular destination.…”

Peroxisome Function, Biogenesis, and Dynamics in Plants

“…2). Furthermore, loss of PEX11a decreases catalase and superoxide dismutase gene expression, linking ROS signaling and peroxisomal division (Rodríguez-Serrano et al, 2016).…”

“…Additionally, PEX11a is implicated in forming peroxisomal membrane extensions called "peroxules" (Rodríguez-Serrano et al, 2016). Peroxule formation is induced by ROS (Sinclair et al, 2009;Rodríguez-Serrano et al, 2016) and may promote the peroxisomal elongation that precedes division (Fig. 2).…”

“…Although decreasing PEX11 expression via RNAi does not notably impact b-oxidation or matrix protein import, Arabidopsis pex11 RNAi lines (Nito et al, 2007;Orth et al, 2007) and moss pex11 mutants (Kamisugi et al, 2016) exhibit enlarged peroxisomes, suggesting a conserved division role. Additionally, PEX11a is implicated in forming peroxisomal membrane extensions called "peroxules" (Rodríguez-Serrano et al, 2016). Peroxule formation is induced by ROS (Sinclair et al, 2009;Rodríguez-Serrano et al, 2016) and may promote the peroxisomal elongation that precedes division (Fig.…”

“…2). Plant peroxisomes proliferate during cell division (Lingard et al, 2008) and in response to salinity (Mitsuya et al, 2010;Fahy et al, 2017), light (Desai and Hu, 2008), and cadmium treatments (Rodríguez-Serrano et al, 2016). Division involves the PMP PEX11, which has five isoforms (a to e) in Arabidopsis (Lingard and Trelease, 2006).…”