Age-dependent nuclear accumulation of a membrane-associated NAC transcription factor GER1 activates SA biosynthesis to promote leaf senescence in Arabidopsis

Prof. Genji Qin published a paper in Molecular Plant.

Leaf senescence is a programmed physiological process that enhances nutrient use efficiency, thereby promoting plant adaptation and crop productivity. However, the molecular mechanisms that govern the initiation and precisely control the progression of senescence remain poorly understood. Here, we identify GERAS1 (GER1), a membrane-associated NAC transcription factor that acts as an age-dependent integrator of the leaf senescence program. As leaves age, GER1 expression is induced and its protein undergoes age-dependent translocation from the plasma membrane to the nucleus. The activation tagging mutant ger1-D exhibits early leaf senescence, while the disruption of GER1 and its three homologs in a quadruple ger1 ger2 ger3 ger4 mutant causes significantly delayed leaf senescence. We further show that the nucleus-localized GER1 directly binds and activates the promoter of the central senescence regulator ORE1. Moreover, GER1 and ORE1 form a transcriptional activation complex that directly upregulates SID2 encoding a key salicylic acid (SA) biosynthetic enzyme. The accumulation of SA in turn promotes the expression of ORE1, establishing a positive feedforward loop that drives leaf senescence. Our findings not only unveil that GER1 acts as a central spatiotemporal regulator of leaf senescence, but also uncover a straightforward membrane-to-nucleus signaling pathway that finely controls leaf aging.