SnRK1 phosphorylation of FUSCA3 positively regulates embryogenesis, seed yield, and plant growth at high temperature in Arabidopsis

The transcription factor FUSCA3 (FUS3) acts as a major regulator of seed maturation in Arabidopsis. FUS3 is phosphorylated by the SnRK1 catalytic subunit AKIN10/SnRK1α1, which belongs to a conserved eukaryotic kinase complex involved in energy homeostasis. Here we show that AKIN10 and FUS3 share overlapping expression patterns during embryogenesis, and that FUS3 is phosphorylated by AKIN10 in embryo cell extracts. To understand the role of FUS3 phosphorylation, we generated fus3-3 plants carrying FUS3 phosphorylation-null (FUS3(S>A)) and phosphorylation-mimic (FUS3(S>D)) variants. While FUS3(S>A) and FUS3(S>D) rescued all the fus3-3 seed maturation defects, FUS3(S>A) showed reduced transcriptional activity and enhanced fus3-3 previously uncharacterized phenotypes. FUS3(S>A) embryos displayed increased seed abortion due to maternal FUS3(S>A) and delayed embryo development, which correlated with a strong decrease in seed yield (~50%). Accordingly, the akin10 and akin11 mutants displayed a frequency of seed abortion similar to fus3-3. When plants were grown at elevated temperature, most phenotypes were exaggerated in FUS3(S>A) plants, and progeny seedlings overall grew poorly, suggesting that phosphorylation of FUS3 plays an important role during early embryogenesis and under heat stress. Collectively, these results suggest that FUS3 phosphorylation and SnRK1 are required for embryogenesis and integration of environmental cues to ensure the survival of the progeny.