Symmetric and asymmetric DNA N6-adenine methylation regulates different biological responses in Mucorales

Carlos Lax, Stephen J. Mondo, Macario Osorio-Concepción, Anna Muszewska, María Corrochano-Luque, Gabriel Gutiérrez, Robert Riley, Anna Lipzen, Jie Guo, Hope Hundley, Mojgan Amirebrahimi, Vivian Ng, Damaris Lorenzo-Gutiérrez, Ulrike Binder, Junhuan Yang, Yuanda Song, David Cánovas, Eusebio Navarro, Michael Freitag, Toni Gabaldón, Igor V. Grigoriev, Luis M. Corrochano (), Francisco E. Nicolás () and Victoriano Garre ()
Additional contact information
Carlos Lax: Universidad de Murcia
Stephen J. Mondo: Lawrence Berkeley National Laboratory
Macario Osorio-Concepción: Universidad de Murcia
Anna Muszewska: Polish Academy of Sciences
María Corrochano-Luque: Universidad de Sevilla
Gabriel Gutiérrez: Universidad de Sevilla
Robert Riley: Lawrence Berkeley National Laboratory
Anna Lipzen: Lawrence Berkeley National Laboratory
Jie Guo: Lawrence Berkeley National Laboratory
Hope Hundley: Lawrence Berkeley National Laboratory
Mojgan Amirebrahimi: Lawrence Berkeley National Laboratory
Vivian Ng: Lawrence Berkeley National Laboratory
Damaris Lorenzo-Gutiérrez: Universidad de Murcia
Ulrike Binder: Medical University of Innsbruck
Junhuan Yang: Lingnan Normal University
Yuanda Song: Shandong University of Technology
David Cánovas: Universidad de Sevilla
Eusebio Navarro: Universidad de Murcia
Michael Freitag: Oregon State University
Toni Gabaldón: Barcelona Supercomputing Centre (BSC-CNS)
Igor V. Grigoriev: Lawrence Berkeley National Laboratory
Luis M. Corrochano: Universidad de Sevilla
Francisco E. Nicolás: Universidad de Murcia
Victoriano Garre: Universidad de Murcia

Nature Communications, 2024, vol. 15, issue 1, 1-21

Abstract: Abstract DNA N6-adenine methylation (6mA) has recently gained importance as an epigenetic modification in eukaryotes. Its function in lineages with high levels, such as early-diverging fungi (EDF), is of particular interest. Here, we investigated the biological significance and evolutionary implications of 6mA in EDF, which exhibit divergent evolutionary patterns in 6mA usage. The analysis of two Mucorales species displaying extreme 6mA usage reveals that species with high 6mA levels show symmetric methylation enriched in highly expressed genes. In contrast, species with low 6mA levels show mostly asymmetric 6mA. Interestingly, transcriptomic regulation throughout development and in response to environmental cues is associated with changes in the 6mA landscape. Furthermore, we identify an EDF-specific methyltransferase, likely originated from endosymbiotic bacteria, as responsible for asymmetric methylation, while an MTA-70 methylation complex performs symmetric methylation. The distinct phenotypes observed in the corresponding mutants reinforced the critical role of both types of 6mA in EDF.

Date: 2024
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DOI: 10.1038/s41467-024-50365-2

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