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Title: G-quadruplex (G4) motifs in the maize (Zea mays L.) genome are enriched at specific locations in thousands of genes coupled to energy status, hypoxia, low sugar, and nutrient deprivation

item Andorf, Carson
item KOPYLOV, MYKHAILO - Florida State University
item DOBBS, DRENA - Iowa State University
item KOCH, KAREN - University Of Florida
item STROUPE, MARGARET - Florida State University
item Lawrence, Carolyn
item BASS, HANK - Florida State University

Submitted to: Journal of Genetics and Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2014
Publication Date: 12/20/2014
Citation: Andorf, C.M., Kopylov, M., Dobbs, D., Koch, K., Stroupe, M., Lawrence, C.J., Bass, H. 2014. G-quadruplex (G4) motifs in the maize (Zea mays L.) genome are enriched at specific locations in thousands of genes coupled to energy status, hypoxia, low sugar, and nutrient deprivation. Journal of Genetics and Genomics. 41(12):627-647. DOI: 10.1016/j.jgg.2014.10.004.

Interpretive Summary: Flooding causes many metabolic changes in plants. This work shows that in maize, other plants, and potentially all eukaryotes regulatory elements associated with genes and metabolic pathways associated with hypoxia (e.g., lack of oxygen as caused by flooding) are regulated by newly discovered mechanisms related to a DNA structure called a G-quadruplex. Understanding how to regulate these genes is anticipated to first steps toward controlling them, which could result in greater control of plant reaction to the stress induced in flooding conditions.

Technical Abstract: The prevalence of non-telomeric G-quadruplex elements in prokaryotes and several species within the opisthokont kingdom suggests they play ancient and conserved roles in regulating DNA and RNA template processes. To explore the potential role of G-quadruplexes in flowering plants, we carried out a computational genome-wide screen for potential G4-Qs in maize. We found G4-Qs in the non-repetitive fraction of the maize genome. These elements were found to be enriched in specific locations within genes and with regard to strand. On the template strand, they were in regions with potential for transcriptional regulation. Several prominent location signatures were discovered in specific locations relative to gene structure. Two in the template strand just downstream of the TSS and in the 5’ end of the 1st intron. In addition, we looked at genes with coding strand G4-Qs that may represent translational regulatory elements near the start codon. Analysis of functional classification of genes with these elements visualized with metabolic pathway databases revealed a striking tendency for enrichment in genes associated with electron transport, sugar degradation, and notable overlap with genes identified by others as hypoxia inducible (anaerobic respiration, inositol metabolism, phytate, glycol, TCA, sucrose, and stachyose degradation). To examine functional significance, we looked at genes conserved across several grass species and found conserved gene families more likely to have G4s than those lacking known syntenic orthologs. Hypoxia response genes, HRE and RAP2.2, have G4s, as do a high proportion of the genes associated with hypoxia-mediated germ-cell specification in maize. This study indicates that G4s may represent a missing link that functions to coordinate regulation of gene expression in response to hypoxia to control carbohydrate metabolism for anaerobic metabolism.