Constraint of Accessible Chromatins Maps Regulatory Loci Involved in Maize Speciation and Domestication

Overview

Journal Nat Commun

Specialty Biology

Date 2025 Mar 13

PMID 40075057

Authors

Yuting Liu

Xiang Gao

Hongjun Liu

Xuerong Yang

Xiao Liu

Fang Xu

Yuzhi Zhu

Qingyun Li

Liangliang Huang

Fang Yang

Jinsheng Lai

Junpeng Shi

Affiliations

Soon will be listed here.

Abstract

Comparative genomic studies can identify genes under evolutionary constraint or specialized for trait innovation. Growing evidence suggests that evolutionary constraint also acts on non-coding regulatory sequences, exerting significant impacts on fitness-related traits, although it has yet to be thoroughly explored in plants. Using the assay for transposase-accessible chromatin by sequencing (ATAC-seq), we profile over 80,000 maize accessible chromatin regions (ACRs), revealing that ACRs evolve faster than coding genes, with about one-third being maize-specific and regulating genes associated with speciation. We highlight the role of transposable elements (TEs) in driving intraspecific innovation of ACRs and identify hundreds of candidate ACRs potentially involved in transcriptional rewiring during maize domestication. Additionally, we demonstrate the importance of accessible chromatin in maintaining subgenome dominance and controlling complex trait variations. This study establishes a framework for analyzing the evolutionary trajectory of plant regulatory sequences and offers candidate loci for downstream exploration and application in maize breeding.

References

Sigmon B, Vollbrecht E . Evidence of selection at the ramosa1 locus during maize domestication. Mol Ecol. 2010; 19(7):1296-311. DOI: 10.1111/j.1365-294X.2010.04562.x. View

Hatfield R, Rancour D, Marita J . Grass Cell Walls: A Story of Cross-Linking. Front Plant Sci. 2017; 7:2056. PMC: 5241289. DOI: 10.3389/fpls.2016.02056. View

Ricci W, Lu Z, Ji L, Marand A, Ethridge C, Murphy N . Author Correction: Widespread long-range cis-regulatory elements in the maize genome. Nat Plants. 2020; 6(3):328. DOI: 10.1038/s41477-020-0600-z. View

Zhang D, Gan Y, Le L, Pu L . Epigenetic variation in maize agronomical traits for breeding and trait improvement. J Genet Genomics. 2024; 52(3):307-318. DOI: 10.1016/j.jgg.2024.01.006. View

Kang H, Sul J, Service S, Zaitlen N, Kong S, Freimer N . Variance component model to account for sample structure in genome-wide association studies. Nat Genet. 2010; 42(4):348-54. PMC: 3092069. DOI: 10.1038/ng.548. View

Chow C, Yang C, Wu N, Wang H, Tseng K, Chiu Y . PlantPAN 4.0: updated database for identifying conserved non-coding sequences and exploring dynamic transcriptional regulation in plant promoters. Nucleic Acids Res. 2023; 52(D1):D1569-D1578. PMC: 10767843. DOI: 10.1093/nar/gkad945. View

Fang C, Yang M, Tang Y, Zhang L, Zhao H, Ni H . Dynamics of -regulatory sequences and transcriptional divergence of duplicated genes in soybean. Proc Natl Acad Sci U S A. 2023; 120(44):e2303836120. PMC: 10622917. DOI: 10.1073/pnas.2303836120. View

Liu J, Fernie A, Yan J . The Past, Present, and Future of Maize Improvement: Domestication, Genomics, and Functional Genomic Routes toward Crop Enhancement. Plant Commun. 2021; 1(1):100010. PMC: 7747985. DOI: 10.1016/j.xplc.2019.100010. View

Li E, Liu H, Huang L, Zhang X, Dong X, Song W . Long-range interactions between proximal and distal regulatory regions in maize. Nat Commun. 2019; 10(1):2633. PMC: 6572780. DOI: 10.1038/s41467-019-10603-4. View

Oka R, Zicola J, Weber B, Anderson S, Hodgman C, Gent J . Genome-wide mapping of transcriptional enhancer candidates using DNA and chromatin features in maize. Genome Biol. 2017; 18(1):137. PMC: 5522596. DOI: 10.1186/s13059-017-1273-4. View

10.

Hedges S, Marin J, Suleski M, Paymer M, Kumar S . Tree of life reveals clock-like speciation and diversification. Mol Biol Evol. 2015; 32(4):835-45. PMC: 4379413. DOI: 10.1093/molbev/msv037. View

11.

Huang W, Zhang L, Columbus J, Hu Y, Zhao Y, Tang L . A well-supported nuclear phylogeny of Poaceae and implications for the evolution of C photosynthesis. Mol Plant. 2022; 15(4):755-777. DOI: 10.1016/j.molp.2022.01.015. View

12.

Bukowski R, Guo X, Lu Y, Zou C, He B, Rong Z . Construction of the third-generation Zea mays haplotype map. Gigascience. 2018; 7(4):1-12. PMC: 5890452. DOI: 10.1093/gigascience/gix134. View

13.

Rodgers-Melnick E, Vera D, Bass H, Buckler E . Open chromatin reveals the functional maize genome. Proc Natl Acad Sci U S A. 2016; 113(22):E3177-84. PMC: 4896728. DOI: 10.1073/pnas.1525244113. View

14.

Ma J, Bennetzen J . Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A. 2004; 101(34):12404-10. PMC: 515075. DOI: 10.1073/pnas.0403715101. View

15.

Zhu T, Xia C, Yu R, Zhou X, Xu X, Wang L . Comprehensive mapping and modelling of the rice regulome landscape unveils the regulatory architecture underlying complex traits. Nat Commun. 2024; 15(1):6562. PMC: 11297339. DOI: 10.1038/s41467-024-50787-y. View

16.

Haas B, Delcher A, Wortman J, Salzberg S . DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics. 2004; 20(18):3643-6. DOI: 10.1093/bioinformatics/bth397. View

17.

Hufford M, Seetharam A, Woodhouse M, Chougule K, Ou S, Liu J . De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science. 2021; 373(6555):655-662. PMC: 8733867. DOI: 10.1126/science.abg5289. View

18.

Sun S, Zhou Y, Chen J, Shi J, Zhao H, Zhao H . Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nat Genet. 2018; 50(9):1289-1295. DOI: 10.1038/s41588-018-0182-0. View

19.

Mantica F, Iniguez L, Marquez Y, Permanyer J, Torres-Mendez A, Cruz J . Evolution of tissue-specific expression of ancestral genes across vertebrates and insects. Nat Ecol Evol. 2024; 8(6):1140-1153. DOI: 10.1038/s41559-024-02398-5. View