High Light Intensity Leads to Increased Peroxule-Mitochondria Interactions in Plants

Abstract

Peroxules are thin protrusions from spherical peroxisomes produced under low levels of reactive oxygen species (ROS) stress. Whereas, stress mitigation favors peroxule retraction, prolongation of the ROS stress leads to the elongation of the peroxisome into a tubular form. Subsequently, the elongated form becomes constricted through the binding of proteins such as dynamin related proteins 3A and 3B and eventually undergoes fission to increase the peroxisomal population within a cell. The events that occur in the short time window between peroxule initiation and the tubulation of the entire peroxisome have not been observed in living plant cells. Here, using fluorescent protein aided live-imaging, we show that peroxules are formed after only 4 min of high light (HL) irradiation during which there is a perceptible increase in the cytosolic levels of hydrogen peroxide. Using a stable, double transgenic line of Arabidopsis thaliana expressing a peroxisome targeted YFP and a mitochondrial targeted GFP probe, we observed sustained interactions between peroxules and small, spherical mitochondria. Further, it was observed that the frequency of HL-induced interactions between peroxules and mitochondria increased in the Arabidopsis anisotropy1 mutant that has reduced cell wall crystallinity and where we show accumulation of higher H2O2 levels than wild type plants. Our observations suggest a testable model whereby peroxules act as interaction platforms for ROS-distressed mitochondria that may release membrane proteins and fission factors. These proteins might thus become easily available to peroxisomes and facilitate their proliferation for enhancing the ROS-combating capability of a plant cell.

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

“…High light intensity induces ROS and increases peroxule-mitochondria interactions [82]. The tubulated peroxisomes become constricted and eventually undergo fission to increase peroxisome numbers [82].…”

“…High light intensity induces ROS and increases peroxule-mitochondria interactions [82]. 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].…”

Peroxisomes: versatile organelles with diverse roles in plants

“…Accumulating evidence has demonstrated convincingly that peroxules are key to the interaction of peroxisomes with organelles known to have close metabolic and physical ties with peroxisomes, including the ER, oil bodies, mitochondria and chloroplasts (Sinclair et al, 2009;Thazar-Poulot et al, 2015;Gao et al, 2016;Jaipargas et al, 2016). It is possible that during plant response to physiological signals, peroxules serve as a platform for the connection of peroxisomes and other organelles to facilitate the exchange of metabolites and proteins.…”

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.…”

“…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.…”