Redox regulation of plant stem cell fate

Abstract

Despite the importance of stem cells in plant and animal development, the common mechanisms of stem cell maintenance in both systems have remained elusive. Recently, the importance of hydrogen peroxide (H 2 O 2 ) signaling in priming stem cell differentiation has been extensively studied in animals. Here, we show that different forms of reactive oxygen species ( ROS ) have antagonistic roles in plant stem cell regulation, which were established by distinct spatiotemporal patterns of ROS ‐metabolizing enzymes. The superoxide anion ( ) is markedly enriched in stem cells to activate WUSCHEL and maintain stemness, whereas H 2 O 2 is more abundant in the differentiating peripheral zone to promote stem cell differentiation. Moreover, H 2 O 2 negatively regulates biosynthesis in stem cells, and increasing H 2 O 2 levels or scavenging leads to the termination of stem cells. Our results provide a mechanistic framework for ROS ‐mediated control of plant stem cell fate and demonstrate that the balance between and H 2 O 2 is key to stem cell maintenance and differentiation. image Superoxide regulates plant stem cell fate, and the balance between superoxide and H 2 O 2 serves as a key switch for stem cell maintenance versus differentiation by antagonistically regulating expression of stem cell fate transcription factor WUSCHEL . Superoxide specifically accumulates in plant stem cells to determine the stem‐cell fate. H 2 O 2 is enriched in the differentiating peripheral zone to promote plant stem cell differentiation. Repression of superoxide dismutases and activation of peroxidases establishes the high superoxide and low H 2 O 2 distribution patterns in plant stem cells. H 2 O 2 negatively regulates superoxide accumulation in stem cells by inhibiting key enzymes in superoxide anabolism. The superoxide/H 2 O 2 balance controls plant stem cell fate by antagonistically regulating WUSCHEL expression.