Interspecific analysis of diurnal gene regulation in panicoid grasses identifies known and novel regulatory motifs

Authors: LAI, XIANJUN - University Of Nebraska; BENDIX, CLAIRE - University Of California; YAN, LANG - University Of Nebraska; ZHANG, YANG - University Of Nebraska; SCHNABLE, JAMES - University Of Nebraska; Harmon, Frank

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/12/2020
Publication Date: 6/25/2020
Citation: Lai, X., Bendix, C., Yan, L., Zhang, Y., Schnable, J., Harmon, F.G. 2020. Interspecific analysis of diurnal gene regulation in panicoid grasses identifies known and novel regulatory motifs. BMC Genomics. 21. Article 428. https://doi.org/10.1186/s12864-020-06824-3.
DOI: https://doi.org/10.1186/s12864-020-06824-3

Interpretive Summary: Maize, sorghum, and foxtail millet are each leading crop plants from the Panacoid family of grass plants. The goal of this work was to identify genes important for regulation of daily activities in these plants. The working hypothesis was critical regulatory features will be retained through evolution and, therefore, these will be discovered by finding aspects of the genomes shared between these plants. Of particular interest was understanding how plants anticipate and prepare for changes in the environment throughout the day-night cycle. With several comparative computational biology approaches, this study found probable key regulatory genes and sets of genes with shared expression that are predicted to be involved in common physiological processes. Also discovered within these three grass species were short DNA sequences, called motifs, near genes with the same expression pattern. This is typical of DNA regions used to control gene expression. By analysis of the DNA sequence of these genomic regions, it was clear these represented both previously known motifs with described activity and novel, previously undiscovered motifs with unknown activity. Overall, this study provides an overview of the divergence and conservation of daily expression patterns and associated DNA sequence motifs amongst related genes in three crop grass species of the same family.

Technical Abstract: The circadian clock drives endogenous 24-hour rhythms that allow organisms to adapt and prepare for predictable and repeated changes in their environment throughout the day-night (diurnal) cycle. Many components of the circadian clock in Arabidopsis thaliana have been functionally characterized, but comparatively little is known about circadian clocks in grass species including major crops like maize and sorghum. Comparative research based on protein homology and diurnal gene expression patterns suggests the function of some predicted clock components in grasses is conserved with their Arabidopsis thaliana counterparts, while others have diverged in function. Our analysis of diurnal gene expression in three panicoid grasses sorghum, maize, and foxtail millet revealed conserved and divergent evolution of expression for core circadian clock genes and for the overall transcriptome. We find that several classes of core circadian clock genes in these grasses differ in copy number compared to Arabidopsis, but mostly exhibit conservation of both protein sequence and diurnal expression pattern with the notable exception of maize paralogous genes. We predict conserved cis-regulatory motifs shared between maize, sorghum, and foxtail millet through identification of diurnal co-expression clusters for a subset of 57,803 orthologous syntenic genes. In this analysis, a Cochran–Mantel–Haenszel based method to control for background variation identified significant enrichment for both expected and novel 6-8 nucleotide motifs in the promoter regions of genes with shared diurnal regulation predicted to function in common physiological activities. This study illustrates the divergence and conservation of circadian clocks and diurnal regulatory networks across syntenic orthologous genes in panacoid grass species.