Dynamic Changes in Reactive Oxygen Species in the Shoot Apex Contribute to Stem Cell Death in Arabidopsis thaliana

Abstract

In monocarpic plants, stem cells are fated to die. However, the potential mechanism of stem cell death has remained elusive. Here, we reveal that the levels of two forms of reactive oxygen species (ROS), superoxide anion free radical (O2·−) and hydrogen peroxide (H2O2), show dynamic changes in the shoot apex during the plant life cycle of Arabidopsis thaliana. We found that the level of O2·− decreased and disappeared at four weeks after bolting (WAB), while H2O2 appeared at 3 WAB and showed a burst at 5 WAB. The timing of dynamic changes in O2·− and H2O2 was delayed for approximately three weeks in clv3-2, which has a longer lifespan. Moreover, exogenous application of H2O2 inhibited the expression of the stem cell determinant WUSCHEL (WUS) and promoted the expression of the developmentally programmed cell death (dPCD) marker gene ORESARA 1 (ORE1). These results indicate that H2O2 triggers an important signal inducing dPCD in stem cells. Given that O2·− plays roles in maintaining WUS expression and stem cell activity, we speculate that the dynamic shift from O2·− to H2O2 in the shoot apex results in stem cell death. Our findings provide novel insights for understanding ROS-mediated regulation during plant stem cell death.

Flowering also has to end: knowns and unknowns of reproductive arrest in monocarpic plants

“…Previous studies also suggest that H 2 O 2 may repress WUS expression. Both the study on proliferative arrest carried out by Wuest et al (2016) and the study by Wang et al (2022) showed that O 2 · – was detectable in active IMs but undetectable in arrested IMs, correlating with the WUS spatiotemporal expression pattern ( Balanzà et al , 2018 ; Merelo et al , 2022 ; Wang et al , 2022 ). Moreover, Y. Wang et al (2020 , 2022 ) showed that H 2 O 2 accumulated in arrested SAMs, suggesting that ROS may play a role in the control of meristem arrest ( Y. Wang et al, 2020) .…”

“…Both the study on proliferative arrest carried out by Wuest et al (2016) and the study by Wang et al (2022) showed that O 2 · – was detectable in active IMs but undetectable in arrested IMs, correlating with the WUS spatiotemporal expression pattern ( Balanzà et al , 2018 ; Merelo et al , 2022 ; Wang et al , 2022 ). Moreover, Y. Wang et al (2020 , 2022 ) showed that H 2 O 2 accumulated in arrested SAMs, suggesting that ROS may play a role in the control of meristem arrest ( Y. Wang et al, 2020) . These data were also supported by a transcriptomic analysis that identify a set of ROS-related genes over-represented in arrested apices in comparison with active apices ( Wang et al , 2022 ).…”

The central role of stem cells in determining plant longevity variation

“…It has recently been reported that the age-dependent cellular accumulation of reactive oxygen species at the Arabidopsis SAM shuts down stem cell activity by initiating programmed cell death ( Wang et al., 2020a , 2022 ). Future studies are required to understand age-dependent programmed cell death in stem cells and how it contributes to the control of plant longevity.…”

Paradigm and Framework of WUS-CLV Feedback Loop in Stem Cell Niche for SAM Maintenance and Cell Identity Transition

“…•− for proliferation [87]. ROS play a critical role in abiotic and biotic responses to plant development and maintaining homeostasis [88].…”

“…•− /H 2 O 2 balance serves as a key switch for stem cell maintenance and differentiation. Antioxidant enzymes such as SOD and POD plays a major role in keeping ROS under controlled level [86,87]. Decrease in the O 2…”