ATM controls meiotic DNA double-strand break formation and recombination and affects synaptonemal complex organization in plants

Marie-Therese Kurzbauer, Michael Peter Janisiw, Luis F Paulin, Ignacio Prusén Mota, Konstantin Tomanov, Ondrej Krsicka, Arndt von Haeseler, Veit Schubert, Peter Schlögelhofer

Publications: Contribution to journalArticlePeer Reviewed

Abstract

Meiosis is a specialized cell division that gives rise to genetically distinct gametic cells. Meiosis relies on the tightly controlled formation of DNA double-strand breaks (DSBs) and their repair via homologous recombination for correct chromosome segregation. Like all forms of DNA damage, meiotic DSBs are potentially harmful and their formation activates an elaborate response to inhibit excessive DNA break formation and ensure successful repair. Previous studies established the protein kinase ATM as a DSB sensor and meiotic regulator in several organisms. Here we show that Arabidopsis ATM acts at multiple steps during DSB formation and processing, as well as crossover (CO) formation and synaptonemal complex (SC) organization, all vital for the successful completion of meiosis. We developed a single-molecule approach to quantify meiotic breaks and determined that ATM is essential to limit the number of meiotic DSBs. Local and genome-wide recombination screens showed that ATM restricts the number of interference-insensitive COs, while super-resolution STED nanoscopy of meiotic chromosomes revealed that the kinase affects chromatin loop size and SC length and width. Our study extends our understanding of how ATM functions during plant meiosis and establishes it as an integral factor of the meiotic program.
Original languageEnglish
Pages (from-to)1633–1656
Number of pages24
JournalThe Plant Cell
Volume33
Issue number5
Early online date5 Feb 2021
DOIs
Publication statusPublished - May 2021

Austrian Fields of Science 2012

  • 106023 Molecular biology

Keywords

  • ARABIDOPSIS-THALIANA
  • CELLULAR-RESPONSE
  • CHIASMA FORMATION
  • CHROMOSOME SYNAPSIS
  • CROSSOVER INTERFERENCE
  • DAMAGE RESPONSE
  • DISTINCT
  • MEIOSIS
  • PROTEIN ZYP1
  • VISUAL ASSAY

Cite this