Reconstructing the transcriptional ontogeny of maize and sorghum supports an inverse hourglass model of inflorescence development

Authors: LEIBOFF, SAMUEL - University Of California; Hake, Sarah

Submitted to: Current Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/19/2019
Publication Date: 10/21/2019
Citation: Leiboff, S., Hake, S.C. 2019. Reconstructing the transcriptional ontogeny of maize and sorghum supports an inverse hourglass model of inflorescence development. Current Biology. 29:3410-3419. https://doi.org/10.1016/j.cub.2019.08.044.
DOI: https://doi.org/10.1016/j.cub.2019.08.044

Interpretive Summary: A comparative ontogeny of terminal inflorescence development in maize and sorghum is presented. By collecting individual transcriptomes from immature maize tassels and sorghum panicles throughout development, the transcriptional ontogeny of both species is reconstructed. The appearance of species-specific morphological characteristics is correlated with molecularly-defined developmental stages. Examining the relative timing and sequence of known genetic master regulators from maize and their syntenic orthologs in sorghum revealed that extended tissue indeterminacy in sorghum results from the prolonged and/or heterochronic activity of multiple proliferative tissue types. We detected high transcriptional similarity between maize and sorghum during floral meristem formation, representing the termination of indeterminate, proliferative pluripotent growth. Measuring selective signatures during maize and sorghum inflorescence ontogeny detected hourglass-like mid-transition stages for each species. Despite their relatively small evolutionary distance, comparing the hourglass-like stage from each species identified their least similar transcriptional phase, providing evidence of an inverse hourglass between maize and sorghum inflorescence development.

Technical Abstract: Assembling meaningful comparisons between species is a major limitation in studying the evolution of organismal form. To understand development in maize and sorghum, closely-related species with architecturally distinct inflorescences, we collected RNAseq profiles encompassing inflorescence body plan specification in both species. We reconstructed molecular ontogenies from 40 B73 maize tassels and 47 BTx623 sorghum panicles and separated them into transcriptional stages. To discover new markers of inflorescence development, we used random forest machine learning to determine stage by RNAseq. We used two descriptions of transcriptional conservation to identify hourglass-like developmental stages. Despite short evolutionary ancestry of 12 million years, we found maize and sorghum inflorescences are most different during their hourglass-like stages of development, following an ‘inverse-hourglass’ model of development. We discuss if agricultural selection may account for the rapid divergence signatures in these species and the observed separation of evolutionary pressure and developmental reprogramming.