Spatiotemporal Restriction of <i>FUSCA3</i> Expression by Class I BPCs Promotes Ovule Development and Coordinates Embryo and Endosperm Growth

Abstract

Spatiotemporal regulation of gene expression is critical for proper developmental timing in plants and animals. The transcription factor <i>FUSCA3 (FUS3)</i> regulates developmental phase transitions by acting as a link between hormonal pathways in Arabidopsis (<i>Arabidopsis thaliana</i>). However, the mechanisms governing its spatiotemporal expression pattern are poorly understood. Here, we show that <i>FUS3</i> is repressed in the ovule integuments and seed endosperm. <i>FUS3</i> repression requires class I BASIC PENTACYSTEINE (BPC) proteins, which directly bind GA/CT <i>cis</i>-elements in <i>FUS3</i> and restrict its expression pattern. During vegetative and reproductive development, <i>FUS3</i> derepression in <i>bpc1-1 bpc2</i> (<i>bpc1/2</i>) double mutant or misexpression in <i>ProML1:FUS3</i> lines causes dwarf plants carrying defective flowers and aborted ovules. After fertilization, ectopic <i>FUS3</i> expression in <i>bpc1/2</i> endosperm or <i>ProML1:FUS3</i> endosperm and endothelium increases endosperm nuclei proliferation and seed size, causing delayed or arrested embryo development. These phenotypes are rescued in <i>bpc1/2 fus3-3</i> Finally, class I BPCs interact with FIS-PRC2 (FERTILIZATION-INDEPENDENT SEED-Polycomb Repressive Complex2), which represses <i>FUS3</i> in the endosperm during early seed development. We propose that BPC1 and 2 promote the transition from reproductive to seed development by repressing <i>FUS3</i> in ovule integuments. After fertilization, BPC1 and 2 and FIS-PRC2 repress <i>FUS3</i> in the endosperm to coordinate early endosperm and embryo growth.