Differential regulation of 26S proteasome activity, abundance and transcription during leaf development and senescence

J Exp Bot. 2025 Jun 25:eraf274. doi: 10.1093/jxb/eraf274. Online ahead of print.

Abstract

Protein homeostasis controlled by the 26S proteasome plays a pivotal role in the adaption of plants to environmental stress, contributing to survival and longevity. During ageing in animals, proteasome activity declines resulting in senescence, however, in plants this is so far largely unexplored. Both in Arabidopsis and barley we found that genes encoding for proteasomal subunits are upregulated at the transcript level during the onset of leaf senescence. In contrast, at the protein level a decrease in proteasomal subunit abundance was observed. Moreover, in Arabidopsis 26S proteasome capacity deteriorates with leaf age, while 20S proteasome activity increases. In contrast, in barley a potential increase in proteasome activity was observed with age. As ribosome-associated RNAs levels of proteasomal subunits increase in Arabidopsis during senescence, it suggests a high-turnover. Furthermore, chemical inhibition of the proteasome results in accelerated leaf senescence in Arabidopsis and barley. In Arabidopsis, 26S proteasome activity could be restored by external cytokinin application, resulting in delayed senescence. Finally, we identified several senescence-associated transcription factors that acts as novel transcriptional regulator of proteasomal genes in Arabidopsis. Taken together, this work provides new insights into the dynamic regulation of proteasome activity which deepens our understanding on leaf senescence in plants.

Keywords: Arabidopsis; barley; cytokinin; leaf senescence; proteasome; transcription factors.