The regulatory landscape of early maize inflorescence development

Authors: PARVATHANENI, RAJIV - Danforth Plant Science Center; BERTOLINI, EDOARDO - Danforth Plant Science Center; Shamimuzzaman, Md - Shamim; VERA, DANIEL - Harvard Medical School; LUNG, PEI-YAU - Florida State University; RICE, BRIAN - University Of Illinois; BROWN, PATRICK - University Of California, Davis; LIPKA, ALEXANDER - University Of Illinois; BASS, HANK - Florida State University; EVELAND, ANDREA - Danforth Plant Science Center

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/11/2020
Publication Date: 7/6/2020
Citation: Parvathaneni, R.K., Bertolini, E., Shamimuzzaman, M., Vera, D., Lung, P., Rice, B.R., Brown, P.J., Lipka, A.E., Bass, H.W., Eveland, A.L. 2020. The regulatory landscape of early maize inflorescence development. Genome Biology. 21:165. https://doi.org/10.1186/s13059-020-02070-8.
DOI: https://doi.org/10.1186/s13059-020-02070-8

Interpretive Summary: Maize is an economically important cereal crop. About 98% of the maize genome consists of non-coding regions, which include elements such as promoters and enhancers that are often associated with binding of transcription factors and other regulatory machinery to control gene expression. This study used an approach to map accessible functional genomic regions in developing maize tassel and ear primordia. At the early primordia stages, maize tassel and ear looks morphologically similar and share common developmental programs. However, variations in later developmental programs, at the molecular level, results in distinct sutural features. Transcription factor binding motifs and several long non-coding(lnc)RNAs identified in this study provides a deeper understanding of the key regulatory mechanisms driving gene expression during early developmental transitions for maize tassel and ear morphogenesis.

Technical Abstract: The functional genome of agronomically important plant species remains largely unexplored, yet presents a virtually untapped resource for targeted crop improvement. Functional elements of regulatory DNA revealed through profiles of chromatin accessibility can be harnessed for fine-tuning gene expression to optimal phenotypes in specific environments. Here, we investigate the non-coding regulatory space in the maize (Zea mays) genome during early reproductive development of pollen- and grain-bearing inflorescences. Using an assay for differential sensitivity of chromatin to micrococcal nuclease (MNase) digestion, we profiled accessible chromatin and nucleosome occupancy in these largely undifferentiated tissues and classified approximately 1.6 percent of the genome as accessible, with the majority of MNase hypersensitive sites marking proximal promoters, but also 3' ends of maize genes. This approach mapped regulatory elements to footprint-level resolution. Integration of complementary transcriptome profiles and transcription factor (TF) occupancy data were used to annotate regulatory factors, such as combinatorial TF binding motifs and long non-coding RNAs, that potentially contribute to organogenesis, including tissue-specific regulation between male and female inflorescence structures. Finally, genome-wide association studies for inflorescence architecture traits based only on functional regions delineated by MNase hypersensitivity revealed new SNP-trait associations in known regulators of inflorescence development as well as new candidates. These analyses provide a comprehensive look into the cisregulatory landscape during inflorescence differentiation in a major cereal crop, which ultimately shapes architecture and influences yield potential.