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Plant Cell Reports

, Volume 37, Issue 3, pp 501–513 | Cite as

DDM1 guards against telomere truncation in Arabidopsis

  • Xiaoyuan Xie
  • Dorothy E. Shippen
Original Article

Abstract

Key message

Prolonged hypomethylation of DNA leads to telomere truncation correlated with increased telomere recombination, transposon mobilization and stem cell death.

Abstract

Epigenetic pathways, including DNA methylation, are crucial for telomere maintenance. Deficient in DNA Methylation 1 (DDM1) encodes a nucleosome remodeling protein, required to maintain DNA methylation in Arabidopsis thaliana. Plants lacking DDM1 can be self-propagated, but in the sixth generation (G6) hypomethylation leads to rampant transposon activation and infertility. Here we examine the role of DDM1 in telomere length homeostasis through a longitudinal study of successive generations of ddm1-2 mutants. We report that bulk telomere length remains within the wild-type range for the first five generations (G1–G5), and then precipitously drops in G6. While telomerase activity becomes more variable in later generation ddm1-2 mutants, there is no correlation between enzyme activity and telomere length. Plants lacking DDM1 also exhibit no dysregulation of several known telomere-associated transcripts, including TERRA. Instead, telomere shortening coincides with increased G-overhangs and extra-chromosomal circles, consistent with deletional recombination. Telomere shortening also correlates with transcriptional activation of retrotransposons, and a hypersensitive DNA damage response in root apical meristems. Since abiotic stresses, including DNA damage, stimulate homologous recombination, we hypothesize that telomere deletion in G6 ddm1-2 mutants is a by-product of elevated genome-wide recombination in response to transposon mobilization. Further, we speculate that telomere truncation may be beneficial in adverse environmental conditions by accelerating the elimination of stem cells with aberrant genomes.

Keywords

Telomerase Recombination DNA damage Stem cell DNA methylation 

Notes

Acknowledgements

We thank Keith Slotkin for providing mutant seeds, Lanying Zeng for sharing her fluorescence microscope, members of the Shippen lab for insightful comments and Jeff Kapler and Eugene Shakirov for critically reading the manuscript. This work was supported by the National Institutes of Health (GM065383 to D.E.S.).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

299_2017_2245_MOESM1_ESM.pdf (987 kb)
Supplementary material 1 (PDF 986 KB)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biochemistry and BiophysicsTexas A&M UniversityCollege StationUSA

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