The RhWRKY33a-RhPLATZ9 regulatory module delays petal senescence by suppressing rapid reactive oxygen species accumulation in rose flowers

Redox homeostasis in plant cells is critical for maintaining normal growth and development because reactive oxygen species (ROS) can function as signaling molecules or toxic compounds. However, how plants fine-tune redox homeostasis during natural or stress-induced senescence remains unclear. Cut roses (Rosa hybrida), an economically important ornamental product worldwide, often undergo stress-induced precocious senescence at the post-harvest bud stage. Here, we identified RhPLATZ9, an age- and dehydration-induced PLATZ (plant AT-rich sequence and zinc-binding) protein, and determined that it functions as a transcriptional repressor in rose flowers during senescence. We also showed that RhWRKY33a regulates RhPLATZ9 expression during flower senescence. RhPLATZ9-silenced flowers and RhWRKY33a-silenced flowers showed accelerated senescence, with higher ROS contents than the control. By contrast, overexpression of RhWRKY33a or RhPLATZ9 delayed flower senescence, and overexpression in rose calli showed lower ROS accumulation than the control. RNA-sequencing analysis revealed that apoplastic NADPH oxidase genes (RhRbohs) were enriched among the upregulated differentially expressed genes in RhPLATZ9-silenced flowers compared to wild-type flowers. Yeast one-hybrid assays, electrophoretic mobility shift assays, dual luciferase assays and chromatin immunoprecipitation quantitative PCR confirmed that the RhRbohD gene is a direct target of RhPLATZ9. These findings suggest that the RhWRKY33a-RhPLATZ9-RhRbohD regulatory module acts as a brake to help maintain ROS homeostasis in petals and thus antagonize age- and stress-induced precocious senescence in rose flowers.

Automated summary

Redox homeostasis is crucial for plant growth and development. However, the regulation of redox homeostasis during senescence is not well understood. In this study, a PLATZ protein called RhPLATZ9 was identified and found to function as a transcriptional repressor during senescence in cut roses. The expression of RhPLATZ9 is regulated by RhWRKY33a, and their overexpression delays senescence and reduces ROS accumulation. Furthermore, RhPLATZ9 was found to directly target the RhRbohD gene, which is involved in ROS production. These findings reveal a regulatory module that helps maintain ROS homeostasis and counteract precocious senescence in roses.