Recruitment of an ancient branching program to suppress carpel development in maize flowers.

Abstract

Carpels in maize undergo programmed cell death in half of the flowers initiated in ears and in all flowers in tassels. The HD-ZIP I transcription factor gene <i>GRASSY TILLERS1</i> (<i>GT1</i>) is one of only a few genes known to regulate this process. To identify additional regulators of carpel suppression, we performed a <i>gt1</i> enhancer screen and found a genetic interaction between <i>gt1</i> and <i>ramosa3</i> (<i>ra3</i>). <i>RA3</i> is a classic inflorescence meristem determinacy gene that encodes a trehalose-6-phosphate (T6P) phosphatase (TPP). Dissection of floral development revealed that <i>ra3</i> single mutants have partially derepressed carpels, whereas <i>gt1</i>;<i>ra3</i> double mutants have completely derepressed carpels. Surprisingly, <i>gt1</i> suppresses <i>ra3</i> inflorescence branching, revealing a role for <i>gt1</i> in meristem determinacy. Supporting these genetic interactions, GT1 and RA3 proteins colocalize to carpel nuclei in developing flowers. Global expression profiling revealed common genes misregulated in single and double mutant flowers, as well as in derepressed <i>gt1</i> axillary meristems. Indeed, we found that <i>ra3</i> enhances <i>gt1</i> vegetative branching, similar to the roles for the trehalose pathway and <i>GT1</i> homologs in the eudicots. This functional conservation over ∼160 million years of evolution reveals ancient roles for <i>GT1</i>-like genes and the trehalose pathway in regulating axillary meristem suppression, later recruited to mediate carpel suppression. Our findings expose hidden pleiotropy of classic maize genes and show how an ancient developmental program was redeployed to sculpt floral form.