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 report that the Arabidopsis thaliana transcription factor WRKY1 plays essential roles in multiple key steps of monocarpic senescence. WRKY1 expression is induced by age, salicylic acid (SA), and nitrogen (N) deficiency. Flowering and leaf senescence are accelerated in the WRKY1 overexpression lines but are delayed in the wrky1 mutants. The combined DNA affinity purification sequencing and RNA sequencing analyses uncover the direct target genes of WRKY1. Further studies show that WRKY1 coordinately regulates three processes in 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, our study reveals how one stress-responsive transcription factor, WRKY1, integrates flowering, leaf senescence, and N remobilization processes into monocarpic senescence, providing important insights into plant lifetime regulation.