Sugar Signaling Induces Dynamic Changes during Meristem Development to Regulate Flowering in Arabidopsis

Aerial parts of plants originate from pluripotent stem cells in the shoot apical meristem. Their population is maintained via the maintenance regulators WUSCHEL and CLAVATA3 in a negative feed-back loop. Meristem size is dynamic and undergoes a more than 2-fold expansion upon the transition to reproductive growth. The mechanism controlling this doming is largely unknown, but coinciding increased trehalose 6-phosphate and changed meristem size in overexpressing or knockdown lines of TREHALOSE PHOSPHATE SYNTHASE1 suggest a participation of sugar signaling. Here we show that TREHALOSE PHOSPHATE PHOSPHATASEJ is directly regulated by WUSCHEL. Plants with reduced levels of TREHALOSE PHOSPHATE PHOSPHATASEJ in the outer meristem layer are flowering early and its reduction in the late flowering clavata3 mutant, restores wild-type flowering. This is caused by a reduction of mature miR156 and increased expression of SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes. We demonstrate that these are important for age pathway-induced flowering, in a negative feed-back loop with WUSCHEL downstream of the trehalose 6-phosphate pathway. In summary, our findings demonstrate a dynamic feed-back regulation between central maintenance and flowering time regulators with sugar signaling.