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

Klein, Harry, Gallagher, Joseph, Demesa-Arevalo, Edgar, Abraham-Juárez, María Jazmín, Heeney, Michelle, Feil, Regina, Lunn, John E, Xiao, Yuguo, Chuck, George, Whipple, Clinton, Jackson, David, Bartlett, Madelaine (January 2022) Recruitment of an ancient branching program to suppress carpel development in maize flowers. Proceedings of the National Academy of Sciences of USA, 119 (2). e2115871119-e2115871119. ISSN 0027-8424

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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.

Item Type:	Paper
Subjects:	bioinformatics bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification bioinformatics > genomics and proteomics > genetics & nucleic acid processing bioinformatics > genomics and proteomics organism description > plant > maize organs, tissues, organelles, cell types and functions > cell types and functions > cell functions > apoptosis organs, tissues, organelles, cell types and functions > cell types and functions > cell functions organs, tissues, organelles, cell types and functions > cell types and functions bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > genes, structure and function > gene expression bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > genes, structure and function > gene regulation bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > genes, structure and function > gene regulation bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > genes, structure and function organs, tissues, organelles, cell types and functions > tissues types and functions > inflorescence organs, tissues, organelles, cell types and functions > tissues types and functions > meristem organs, tissues, organelles, cell types and functions organs, tissues, organelles, cell types and functions > tissues types and functions
CSHL Authors:	Jackson, David P. Demesa Arevalo, Edgar
Communities:	CSHL labs > Jackson lab
SWORD Depositor:	CSHL Elements
Depositing User:	CSHL Elements
Date:	11 January 2022
Date Deposited:	12 Jan 2022 15:09
Last Modified:	11 Jan 2024 20:53
PMCID:	PMC8764674
URI:	https://repository.cshl.edu/id/eprint/40477

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