Arabidopsis BECLIN1-induced autophagy mediates reprogramming in tapetal programmed cell death by altering the gross cellular homeostasis.

In flowering plants, the tapetum degeneration in post-meiotic anther occurs through developmental programmed cell death (dPCD), which is one of the most critical and sensitive steps for the proper development of male gametophytes and fertility. Yet the pathways of dPCD, its regulation, and its interaction with autophagy remain elusive. Here, we report that high-level expression of Arabidopsis autophagy-related gene BECLIN1 (BECN1 or AtATG6) in the tobacco tapetum prior to their dPCD resulted in developmental defects. BECN1 induces severe autophagy and multiple cytoplasm-to-vacuole pathways, which alters tapetal cell reactive oxygen species (ROS)-homeostasis that represses the tapetal dPCD. The transcriptome analysis reveals that BECN1- expression caused major changes in the pathway, resulting in altered cellular homeostasis in the tapetal cell. Moreover, BECN1-mediated autophagy reprograms the execution of tapetal PCD by altering the expression of the key developmental PCD marker genes: SCPL48 , CEP1 , DMP4 , BFN1 , MC9 , EXI1, and Bcl-2 member BAG5 , and BAG6. This study demonstrates that BECN1-mediated autophagy is inhibitory to the dPCD of the tapetum, but the severity of autophagy leads to autophagic death in the later stages. The delayed and altered mode of tapetal degeneration resulted in male sterility. • Arabidopsis BECN1 overexpression in post-meiotic tobacco tapetum affects its development. • BECN1 triggers severe autophagy and disrupts tapetal cell ROS homeostasis. • BECN1-induced autophagy reprograms the execution of tapetal PCD and inhibits it. • Transcriptome analysis showed altered gross cellular homeostasis in tapetal cells due to BECN1. • Delayed and altered mode of tapetal degeneration ultimately leads to male sterility. [ABSTRACT FROM AUTHOR]