MSD2, an apoplastic Mn-SOD, contributes to root skotomorphogenic growth by modulating ROS distribution in Arabidopsis

Abstract

Reactive oxygen species (ROS) play essential roles as a second messenger in various physiological processes in plants. Due to their oxidative nature, ROS can also be harmful. Thus, the generation and homeostasis of ROS are tightly controlled by multiple enzymes. Membrane-localized NADPH oxidases are well known to generate ROS during developmental and stress responses, but the metabolic pathways of the superoxide (O2·−) generated by them in the apoplast are poorly understood, and the identity of the apoplastic superoxide dismutase (SOD) is unknown in Arabidopsis. Here, we show that a putative manganese SOD, MSD2 is secreted and possesses a SOD activity that can be inhibited by nitration at tyrosine 68. The expression of MSD2 in roots is light condition-dependent, suggesting that MSD2 may act on ROS metabolism in roots during the light-to-dark transition. Root architecture is governed by ROS distribution that exhibits opposite gradient of H2O2 and O2·−, which is indeed altered in etiolated msd2 mutants and accompanied by changes in the onset of differentiation. These results provide a missing link in our understanding of ROS metabolism and suggest that MSD2 plays a role in root skotomorphogenesis by regulating ROS distribution, thereby playing a pivotal role in plant growth and development.

MSD2‐mediated ROS metabolism fine‐tunes the timing of floral organ abscission in Arabidopsis

“…Reactive oxygen species are important mediators of various environmental stress‐related signalling pathways (Huang et al ., 2019) and might contribute to organ abscission, as they also accumulate in AZs (Sakamoto et al ., 2008a; Bar‐Dror et al ., 2011; Yang et al ., 2015; Liao et al ., 2016; Lee et al ., 2018). To investigate the link between ROS and the timing of abscission, we focused on the secretory Mn SOD MSD2 (Chen et al ., 2022) and tested its role in regulating abscission. MSD2 was preferentially expressed in the floral AZ starting in S13 flowers, when the buds open (Smyth et al ., 1990); MSD2 expression levels increased as flower development progressed (Figs 1a, S1a).…”

“…To investigate the effects of MSD2 on abscission, we analysed the abscission phenotype of two independent T‐DNA insertional mutants (Fig. S1b,c; Chen et al ., 2022). In the msd2‐1 and msd2‐2 mutants, floral organ abscission occurred when fruit length was markedly shorter than that of the wild‐type (Fig.…”

“…Msd2‐1 (GABI_100H05), msd2‐2 (SM_3_35975), UBQ10pro:MSD2‐mCherry , and MSD2pro:nlsGFP‐GUS were described by Chen et al . (2022).…”

“…Their subcellular localizations vary, with CSD2 and FSD1–3 in chloroplasts (Kliebenstein et al ., 1998; Myouga et al ., 2008; Dvorak et al ., 2021), MSD1 in mitochondria (Morgan et al ., 2008), CSD3 in peroxisomes (Kliebenstein et al ., 1998; Huang et al ., 2012), CSD1 and FSD1 in the cytoplasm (Kliebenstein et al ., 1998; Dvorak et al ., 2021), and FSD1 in the nucleus (Dvorak et al ., 2021). MSD2 is an apoplastic SOD with Mn SOD activity that is secreted into vacuoles or the apoplast (Chen et al ., 2022). SODs, which convert into H 2 O 2 , not only detoxify accumulated from various stress conditions and metabolic processes, but also affect the redox balance.…”

“…In this study, we demonstrated that MSD2, a recently identified secretory SOD (Chen et al ., 2022), is involved in the regulation of abscission signalling. MSD2 was preferentially expressed in the AZ of flowers, and the encoded MSD2 enzyme was secreted into the vacuole and extracellular spaces.…”