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 GRASSY TILLERS1 (GT1) is one of only a few genes known to regulate this process. To identify additional regulators of carpel suppression, we performed a gt1 enhancer screen and found a genetic interaction between gt1 and ramosa3 (ra3). RA3 is a classic inflorescence meristem determinacy gene that encodes a trehalose-6-phosphate (T6P) phosphatase (TPP). Dissection of floral development revealed that ra3 single mutants have partially derepressed carpels, whereas gt1;ra3 double mutants have completely derepressed carpels. Surprisingly, gt1 suppresses ra3 inflorescence branching, revealing a role for gt1 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 gt1 axillary meristems. Indeed, we found that ra3 enhances gt1 vegetative branching, similar to the roles for the trehalose pathway and GT1 homologs in the eudicots. This functional conservation over ∼160 million years of evolution reveals ancient roles for GT1-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.

Duplicate transcription factorsGT1andVRS1regulate branching and fertile flower number in maize andBrachypodium distachyon

“…3). However, upon backcrossing to B73, the strength of this phenotype decreased to that described previously for gt1 (Klein et al, 2022;Whipple et al, 2011). This suggests that the silky tassel phenotypes of double mutants are subject to the regulation of a modifier in the initial background that is not present in the B73 background (Suppl Fig 3).…”

“…Floral organs are also derepressed in gt1; ra3 double mutant tassels (Klein et al, 2022). We compared the gene expression changes accompanying the derepression of pistils in tassel inflorescences in gt1; ra3 maize plants (Klein et al, 2022) with the gene expression changes observed here. Only three genes were shared between the wildtype versus gt1; vrl1 DE genes and the pre-pistil suppression stage wild-type versus gt1; ra3 DE genes (Klein et al, 2022).…”

“…gt1 plants develop tillers, have more ear-bearing branches, and sometimes develop pistils in the typically staminate tassel flowers (Whipple et al, 2011). In double mutants between gt1 and the trehalose-phosphate phosphatase (TPP) gene ramosa3 (ra3), pistil development in tassels is no longer suppressed, with receptive silks growing out of tassel flowers (Klein et al, 2022). In rice (Oryza sativa), an ortholog of GT1 also represses lateral tillering when targeted by RNAi (V. Kumar et al, 2021).…”

Singlet oxygen-induced signalling depends on the metabolic status of the Chlamydomonas cell

“…its function aside from the catalysis of Tre6P dephosphorylation 53 . Subsequent study also demonstrated “moonlighting” function of RA3 in carpel suppression 54 . Rather regulatory than a catalytic function was also proposed for TPP7 in Oryza sativa , due to its low activity in vitro and no apparent effect on Tre6P content in knockout mutants of TPP7 55 .…”

Killing me softly - Programmed cell death in plant reproduction from sporogenesis to fertilization

“…Interestingly, RA3 and GT1 appear to regulate genes implicated in PCD, including homologs of the Arabidopsis (Arabidopsis thaliana) NAC transcription factors (TFs) KIRA1 and ANAC087 [13][14][15].…”