REVOLUTA regulates cell fate and wall patterning in the fruit endocarp

Abstract

Explosive seed dispersal distinguishes Cardamine species from Arabidopsis and depends on polarized secondary cell wall (SCW) deposition in fruit endocarp b (endb) cells. How this SCW pattern is specified and environmentally modulated remains unclear. The polyploid Cardamine chenopodiifolia produces explosive aerial fruit and non-explosive subterranean fruit, creating a tractable system to address this problem. We show light triggers underground fruit to explode by reprogramming endb SCW patterning from uniform to polar. We identify the HD-ZIPIII transcription factor REVOLUTA as a central regulator of endb cell fate, SCW formation, and organ polarity in Arabidopsis and Cardamine hirsuta. In C. hirsuta, duplicated REVOLUTA paralogs are required for endb SCW deposition, while other HD-ZIPIII genes contribute redundantly to cell fate and organ polarity. REVOLUTA over-expression converts polar endb SCWs to uniform, producing non-explosive fruit. Together, these findings reveal a tunable developmental module underlying evolutionary transitions between explosive and non-explosive seed dispersal strategies.