Mapping genetic modifiers of epimutation rates in Arabidopsis thaliana

• Applicant: Professor Dr. Frank Johannes
• Subject Area: Plant Genetics and Genomics ; General Genetics and Functional Genome Biology ; Bioinformatics and Theoretical Biology
• Term: from 2021 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 460890770

• Final Report Year: 2025

Final Report Abstract

DNA methylation in plants is a chemical modification that regulates gene activity, maintains genome stability, and silences “jumping” genes known as transposons. It occurs when a small molecule, called a methyl group, attaches to specific regions of the DNA, mainly at cytosine bases, and is controlled by specialized enzymes. Unlike in animals, plants can add, remove, or adjust this modification, and changes in DNA methylation can be passed on to the next generation. In plants, random changes in DNA methylation patterns often occur independently of changes in the DNA sequence. These so-called "spontaneous epimutations" appear to result from incomplete maintenance of DNA methylation during plant development. There is growing interest in understanding the broader effects of these random changes, as multiple studies suggest that they can sometimes lead to heritable changes in gene expression, strongly influence the diversity of methylation patterns within and between plant populations, and respond to various environmental factors. In this project, we used the model plant Arabidopsis thaliana to show that certain genotypes are much more prone to errors in maintaining DNA methylation during meiotic cell divisions than others. To investigate this, we tracked DNA methylation changes across generations in different plant genotypes and quantified epimutation rates for each genotype. We then used these epimutation rates as a molecular trait to link variations in these rates to specific genetic differences between plants. Our analysis identified a single region on a chromosome that has a major impact on DNA methylation stability across generations. Further investigation revealed that this region carries a mutation in a gene involved in the DNA methylation pathway, which explains its effect. Additionally, we found that this region also influences variation in plant traits.

Publications

• An evolutionary epigenetic clock in plants. Science, 381(6665), 1440–1445.
  Yao, N.; Zhang, Z.; Yu, L.; Hazarika, R.; Yu, C.; Jang, H.; Smith, L. M.; Ton, J.; Liu, L.; Stachowicz, J. J.; Reusch, T. B. H.; Schmitz, R. J. & Johannes, F.
  
• Stochasticity in gene body methylation. Current Opinion in Plant Biology, 75, 102436.
  Goeldel, Constantin & Johannes, Frank
  
• Time's up: Epigenetic clocks in plants. Current Opinion in Plant Biology, 81, 102602.
  Vo, Binh Thanh; Mas, Paloma & Johannes, Frank