Arabidopsis WRKY1 promotes monocarpic senescence by integrative regulation of flowering, leaf senescence, and nitrogen remobilization

Monocarpic senescence, characterized by whole plant senescence following a single flowering phase, is widespread in seed plants, particularly in crops, determining seed harvest time and quality. However, how external and internal signals are systemically integrated into monocarpic senescence remains largely unknown. Here, we disclose that Arabidopsis thaliana transcription factor WRKY1 plays essential roles in multiple key steps of monocarpic senescence. WRKY1 expression is induced by age, SA, and nitrogen (N) deficiency. Flowering and leaf senescence are promoted in the WRKY1 overexpression lines but are delayed in the wrky1 mutants. The joint analyses of DAP-Seq and RNA-Seq uncover the direct target genes of WRKY1. Further studies show that WRKY1 coordinately regulates three processesin monocarpic senescence: 1) suppressing FLOWERING LOCUS C gene expression to initiate flowering; 2) inducing SA biosynthesis genes to promote leaf senescence; and 3) activating the N-assimilation and transport genes to trigger N remobilization. In summary, we reveal how one stress-responsive transcription factor, WRKY1, synergistically integrates flowering and leaf senescence into monocarpic senescence, providing important insights into plant lifetime regulation.