MaizeCODE reveals bi-directionally expressed enhancers that harbor molecular signatures of maize domestication.

Authors: CAHN, JONATHAN - Howard Hughes Medical Institute; REGULSKI, MICHAEL - Cold Spring Harbor Laboratory; LYNN, JASON - Cold Spring Harbor Laboratory; ERNST, EVAN - Howard Hughes Medical Institute; DE SANTIS ALVES, CRISTIANE - Howard Hughes Medical Institute; RAMAKRISHNAN, SRIVIDYA - Johns Hopkins University; CHOUGULE, KAPEEL - Cold Spring Harbor Laboratory; WEI, SHARON - Cold Spring Harbor Laboratory; LU, ZHENYUAN - Cold Spring Harbor Laboratory; MARTIENSSEN, ROBERT - Howard Hughes Medical Institute; XIAOSA, XU - Cold Spring Harbor Laboratory; DRENKOW, JORG - Cold Spring Harbor Laboratory; KRAMER, MELISSA - Cold Spring Harbor Laboratory; MCCOMBIE, RICHARD - Cold Spring Harbor Laboratory; Ware, Doreen; JACKSON, DAVID - Cold Spring Harbor Laboratory; SCHATZ, MICHAEL - Cold Spring Harbor Laboratory; GINGERAS, THOMAS - Cold Spring Harbor Laboratory

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 2/23/2024
Publication Date: 2/23/2024
Citation: Cahn, J., Regulski, M., Lynn, J., Ernst, E., De Santis Alves, C., Ramakrishnan, S., Chougule, K., Wei, S., Lu, Z., Martienssen, R.A., Xiaosa, X., Drenkow, J., Kramer, M., Mccombie, R., Ware, D., Jackson, D., Schatz, M., Gingeras, T. 2024. MaizeCODE reveals bi-directionally expressed enhancers that harbor molecular signatures of maize domestication.. bioRxiv. https://doi.org/10.1101/2024.02.22.581585.
DOI: https://doi.org/10.1101/2024.02.22.581585

Interpretive Summary: Modern maize originated from Teosinte parviglumis, and over centuries was domesticated to have more kernels and softer seeds. This process involved complex gene networks. The MaizeCODE project used advanced methods to study the maize genome, examining how genes are regulated across different maize types and tissues, including an ancient maize relative. This work identified key areas in the genome controlling these traits, highlighting the unique genetic makeup of pollen grains and showing significant changes in the ear, the most altered part post-domestication. These findings help understand maize's evolution and guide future breeding by pinpointing genetic changes linked to domestication.

Technical Abstract: Modern maize was domesticated from Teosinte parviglumis, with subsequent introgressions from Teosinte mexicana, yielding increased kernel row number, loss of the hard fruit case and dissociation from the cob upon maturity, as well as fewer tillers. Molecular approaches have identified several transcription factors involved in the development of these traits, yet revealed that a complex regulatory network is at play. MaizeCODE deploys ENCODE strategies to catalog regulatory regions in the maize genome, generating histone modification and transcription factor ChIP-seq in parallel with transcriptomics datasets in 5 tissues of 3 inbred lines which span the phenotypic diversity of maize, as well as the teosinte inbred TIL11. Integrated analysis of these datasets resulted in the identification of a comprehensive set of regulatory regions in each inbred, and notably of distal enhancers with bi-directionally expressed enhancer RNAs, reminiscent of “super enhancers” in animal genomes. We show that pollen grains are the most differentiated tissue at the transcriptomic level, and share features with endosperm that may be related to McClintock’s chromosome breakage-fusion-bridge cycle. On the other hand, ears have the least conservation between maize and teosinte, both in gene expression and within regulatory regions, reflecting conspicuous morphological differences selected during domestication. The identification of molecular signatures of domestication in transcriptional regulatory regions provides a framework for directed breeding strategies in maize.