Gene Duplication at the Fascicled Ear1 Locus Controls the Fate of Inflorescence Meristem Cells in Maize.

Significance The maize ear is unbranched and terminates in a single point. The ear and tassel inflorescences of Fascicled ear mutants fail to grow as a single point and instead are branched. This phenotype results from the misexpression of duplicated transcription factors, ZMM8 and DRL2. We hypothesize that these gene rearrangements create regulatory sequences that cause misexpression in early inflorescence meristems, thus activating a laminar program, ablating the meristem, and producing branches. This work demonstrates that zmm8 and drl2 must be restricted from the inflorescence meristem to maintain its terminal point, and conversely, a mechanism by which branching may be imposed. Manipulation of these genes can be used to alter plant architecture, potentially to improve agronomic traits. Plant meristems are self-renewing groups of pluripotent stem cells that produce lateral organs in a stereotypical pattern. Of interest is how the radially symmetrical meristem produces laminar lateral organs. Both the male and female inflorescence meristems of the dominant Fascicled ear (Fas1) mutant fail to grow as a single point and instead show deep branching. Positional cloning of two independent Fas1 alleles identified an ∼160 kb region containing two floral genes, the MADS-box gene, zmm8, and the YABBY gene, drooping leaf2 (drl2). Both genes are duplicated within the Fas1 locus and spatiotemporally misexpressed in the mutant inflorescence meristems. Increased zmm8 expression alone does not affect inflorescence development; however, combined misexpression of zmm8, drl2, and their syntenic paralogs zmm14 and drl1, perturbs meristem organization. We hypothesize that misexpression of the floral genes in the inflorescence and their potential interaction cause ectopic activation of a laminar program, thereby disrupting signaling necessary for maintenance of radially symmetrical inflorescence meristems. Consistent with this hypothesis, RNA sequencing and in situ analysis reveal altered expression patterns of genes that define distinct zones of the meristem and developing leaf. Our findings highlight the importance of strict spatiotemporal patterns of expression for both zmm8 and drl2 and provide an example of phenotypes arising from tandem gene duplications.