The trehalose 6-phosphate pathway coordinates dynamic changes at the shoot apical meristem in Arabidopsis thaliana

Abstract

A plant’s stem cell population in the shoot apical meristem (SAM) is maintained by WUSCHEL (WUS) and CLAVATA3 (CLV3). SAM size is dynamic and undergoes a more than 2-fold expansion upon transition to reproductive growth. The mechanism controlling this doming is largely unknown; however, coinciding increased trehalose 6-phosphate (T6P) levels suggest a participation of the T6P pathway in Arabidopsis (Arabidopsis thaliana). Moreover, lines misexpressing or with reduced expression of TREHALOSE PHOSPHATE SYNTHASE1 (TPS1) have smaller and larger SAMs, respectively. Here, we show that TREHALOSE PHOSPHATE PHOSPHATASEJ (TPPJ) is directly regulated by WUS. Changing TPPJ transcript levels in the outer layer affects SAM size and flowering time, and its reduction in the late-flowering clv3 mutant restores wild-type flowering. This is associated with altered mature miR156 abundance and expression of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes SPL3, SPL4, SPL5, and SPL9. Furthermore, SPL4 is controlled by WUS, whilst SPL4 directly represses WUS, establishing negative feedback regulation. This feedback loop is important for age pathway-induced flowering involving the T6P pathway and suggests dynamic feedback regulations between central meristem maintenance and flowering time regulators with sugar signaling throughout development.