Frontiers in Plant Science (Jun 2023)

Distinct regulatory pathways contribute to dynamic CHH methylation patterns in transposable elements throughout Arabidopsis embryogenesis

  • Jaehoon Lee,
  • Jaehoon Lee,
  • Seunga Lee,
  • Seunga Lee,
  • Kyunghyuk Park,
  • Sang-Yoon Shin,
  • Sang-Yoon Shin,
  • Jennifer M. Frost,
  • Ping-Hung Hsieh,
  • Chanseok Shin,
  • Chanseok Shin,
  • Robert L. Fischer,
  • Tzung-Fu Hsieh,
  • Tzung-Fu Hsieh,
  • Yeonhee Choi,
  • Yeonhee Choi

DOI
https://doi.org/10.3389/fpls.2023.1204279
Journal volume & issue
Vol. 14

Abstract

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CHH methylation (mCHH) increases gradually during embryogenesis across dicotyledonous plants, indicating conserved mechanisms of targeting and conferral. Although it is suggested that methylation increase during embryogenesis enhances transposable element silencing, the detailed epigenetic pathways underlying this process remain unclear. In Arabidopsis, mCHH is regulated by both small RNA-dependent DNA methylation (RdDM) and RNA-independent Chromomethylase 2 (CMT2) pathways. Here, we conducted DNA methylome profiling at five stages of Arabidopsis embryogenesis, and classified mCHH regions into groups based on their dependency on different methylation pathways. Our analysis revealed that the gradual increase in mCHH in embryos coincided with the expansion of small RNA expression and regional mCHH spreading to nearby sites at numerous loci. We identified distinct methylation dynamics in different groups of mCHH targets, which vary according to transposon length, location, and cytosine frequency. Finally, we highlight the characteristics of transposable element loci that are targeted by different mCHH machinery, showing that short, heterochromatic TEs with lower mCHG levels are enriched in loci that switch from CMT2 regulation in leaves, to RdDM regulation during embryogenesis. Our findings highlight the interplay between the length, location, and cytosine frequency of transposons and the mCHH machinery in modulating mCHH dynamics during embryogenesis.

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