Peroxule extension over ER‐defined paths constitutes a rapid subcellular response to hydroxyl stress

Abstract

SUMMARYPlants survive against myriad environmental odds while remaining rooted to a single spot. The time scale over which plant cells can respond to environmental cues is seldom appreciated. Fluorescent protein-assisted live imaging of peroxisomes reveals that they respond within seconds of exposure to hydrogen peroxide and hydroxyl radicals by producing dynamic extensions called peroxules. Observations of the Arabidopsis flu mutant and treatments with xenobiotics eliciting singlet oxygen and superoxide reactive oxygen species suggest that the observed responses are specific for hydroxyl radicals. Prolonged exposure to hydroxyl radicals inhibits peroxule extension, and instead causes motile and spherical peroxisomes in a cell to become immotile and elongate several-fold. Expression of photo-convertible EosFP-PTS1 demonstrates that vermiform peroxisomes result from rapid stretching of individual peroxisomes, while the subsequent 'beads-on-a-string' morphology results from differential protein distribution within an elongated tubule. Over time, the beads in elongated peroxisomes also extend peroxules randomly before undergoing asynchronous, asymmetrical fission. Peroxule extension does not appear to involve cytoskeletal elements directly, but is closely aligned with and reflects the dynamics of ER tubules. Peroxisomal responses reveal a rapidly invoked subcellular machinery that is involved in recognition of hydroxyl stress thresholds, and its possible remediation locally through extension of peroxules or globally by increasing peroxisome numbers. A matrix protein retro-flow mechanism that supports peroxisome-ER connectivity in plant cells is suggested.

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

“…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;Barton et al, 2013). The term "peroxule" was coined by Scott et al (2007) to refer to dynamic extensions, which are similar to those observed in chloroplasts (stromules).…”

“…The term "peroxule" was coined by Scott et al (2007) to refer to dynamic extensions, which are similar to those observed in chloroplasts (stromules). It has been 1 suggested that peroxules are involved in the elongation of peroxisomes (Sinclair et al, 2009), although little is known about the function and regulation of peroxules. Furthermore, the speed of peroxisome movement can change under stress conditions imposed by Cd and herbicide 2,4-D and is also regulated by ROS (Rodríguez-Serrano et al, 2009.…”

Peroxisome Function, Biogenesis, and Dynamics in Plants

“…Moreover, peroxules can respond to environmental signals. For example, peroxules are induced by oxidative stress (Sinclair et al, 2009), and high light rapidly induces peroxule interactions with mitochondria (Jaipargas et al, 2016). The study of peroxule dynamics is in its infancy, and how proteins on the peroxisome and target organelle mediate these interactions awaits discovery.…”

“…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).…”

“…Peroxules can mediate interorganellar contacts, such as among peroxisomes and ER (Sinclair et al, 2009), oil bodies (Thazar-Poulot et al, 2015), mitochondria (Jaipargas et al, 2016), and chloroplasts (Gao et al, 2016). Moreover, peroxules can respond to environmental signals.…”