Gene duplication at the Fascicled ear1 locus controls fate of inflorescence meristem cells in maize

Authors: Hake, Sarah; DU, YANFANG - University Of California; LUNDE, CHINA - University Of California; LI, YUNFU - Huazhong Agricultural University; JACKSON, DAVID - Cold Spring Harbor Laboratory; ZHANG, ZUXIN - Huazhong Agricultural University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/13/2021
Publication Date: 2/16/2021
Citation: Hake, S.C., Du, Y., Lunde, C., Li, Y., Jackson, D., Zhang, Z. 2021. Gene duplication at the Fascicled ear1 locus controls fate of inflorescence meristem cells in maize. Proceedings of the National Academy of Sciences(PNAS). 118(7). Article e2019218118. https://doi.org/10.1073/pnas.2019218118.
DOI: https://doi.org/10.1073/pnas.2019218118

Interpretive Summary: The maize inflorescence is unbranched and terminates in a single point. Here we found the ear and tassel inflorescences of two independent Fascicled ear (Fas1) alleles fail to grow as a single point and instead show deep branching. This phenotype results from gene duplications of a pair of tightly linked transcription factors, Zea mays MADS8 and drooping leaf2 (zmm8 and drl2). We hypothesize that these gene rearrangements create novel promoters that cause misexpression at the inflorescence transition stage thus activating a laminar program. Although these promoters are yet unknown, the 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. Temporal misexpression of the zmm8 drl2 gene pair molecularly ablates the meristem and gives rise to branching, thus, manipulation of these genes can be used to alter tassel and ear architecture, potentially to improve crop yield or other agronomic traits.

Technical Abstract: 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 a ~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 novel phenotypes arising from gene copy number variation.