A sucrose-jasmonic acid feedback loop drives stem cell senescence in Arabidopsis

The lifespan of annual plants is tightly linked to stem cell senescence and the cessation of proliferative activity in the inflorescence meristem (IM). A "senescence factor" originating in developing fruits has long been proposed to trigger proliferative arrest in the IM. Here, we show that jasmonic acid (JA) accumulates in the aging IM, where the JA-responsive transcription factor MYC2 directly represses WUSCHEL (WUS) expression and cytokinin accumulation. We demonstrate that sucrose originating in the siliques triggers local JA biosynthesis in the IM and induces stem cell senescence and meristematic arrest. Moreover, expression of SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTER (SWEET) genes increases in the IM at late developmental stages and is directly activated by MYC2. Mobile sucrose and local JA signaling form a positive feedback loop that reinforces stem cell repression in the IM. Our results suggest that sucrose from siliques acts as a senescence factor and, together with the previously described auxin and FRUITFULL/miR172 pathways, defines the timing of IM aging, which has important implications for plant fitness and agricultural productivity.