ZHOUPI, a unique and highly conserved bHLH transcription factor, controls both endosperm breakdown and embryonic surface formation during Arabidopsis seed development. We have demonstrated that these two processes are distinct, and that ZHOUPI regulates embryonic surface formation via a signaling pathway mediated by the subtilisin-like serine protease ABNORMAL LEAF SHAPE1, and the receptor-kinases GASSHO1 and GASSHO2. Gene expression profiling in mutant backgrounds has permitted the identification of genes whose expression depends on both ZHOUPI and ABNORMAL LEAF SHAPE1 and genes whose expression depends uniquely on ZHOUPI. The latter are presumably involved specifically in endosperm breakdown, and we discuss this poorly understood process in the light of our results. Finally, we consider the potential ancestral role of ZHOUPI and discuss how its relationship with ABNORMAL LEAF SHAPE1 may have evolved.