Transgenerational phenotype aggravation in CAF-1 mutants reveals parent-of-origin specific epigenetic inheritance

New Phytol. 2018 Nov;220(3):908-921. doi: 10.1111/nph.15082. Epub 2018 Mar 24.

Abstract

Chromatin is assembled by histone chaperones such as chromatin assembly factor CAF-1. We had noticed that vigor of Arabidopsis thaliana CAF-1 mutants decreased over several generations. Because changes in mutant phenotype severity over generations are unusual, we asked how repeated selfing of Arabidopsis CAF-1 mutants affects phenotype severity. CAF-1 mutant plants of various generations were grown, and developmental phenotypes, transcriptomes and DNA cytosine-methylation profiles were compared quantitatively. Shoot- and root-related growth phenotypes were progressively more affected in successive generations of CAF-1 mutants. Early and late generations of the fasciata (fas)2-4 CAF-1 mutant displayed only limited changes in gene expression, of which increasing upregulation of plant defense-related genes reflects the transgenerational phenotype aggravation. Likewise, global DNA methylation in the sequence context CHG but not CG or CHH (where H = A, T or C) changed over generations in fas2-4. Crossing early and late generation fas2-4 plants established that the maternal contribution to the phenotype severity exceeds the paternal contribution. Together, epigenetic rather than genetic mechanisms underlie the progressive developmental phenotype aggravation in the Arabidopsis CAF-1 mutants and preferred maternal transmission reveals a more efficient reprogramming of epigenetic information in the male than the female germline.

Keywords: Arabidopsis thaliana; CAF-1; Chromatin; DNA methylation; Development; epigenetics; histone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Arabidopsis / genetics*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Base Sequence
  • DNA Methylation / genetics
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Plant
  • Gene Ontology
  • Inheritance Patterns / genetics*
  • Mutation / genetics*
  • Ovule / embryology
  • Phenotype
  • Plant Infertility
  • RNA Splicing Factors / genetics*
  • RNA Splicing Factors / metabolism
  • Seeds / embryology
  • Stress, Physiological / genetics
  • Transcriptome / genetics

Substances

  • Arabidopsis Proteins
  • At2g20020 protein, Arabidopsis
  • FAS protein, Arabidopsis
  • RNA Splicing Factors