Maize ATR safeguards genome stability during kernel development to prevent early endosperm endocycle onset and cell death

Plant Cell. 2021 Aug 31;33(8):2662-2684. doi: 10.1093/plcell/koab158.

Abstract

The ataxia-telangiectasia mutated (ATM) and ATM and Rad3-related (ATR) kinases coordinate the DNA damage response. The roles described for Arabidopsis thaliana ATR and ATM are assumed to be conserved over other plant species, but molecular evidence is scarce. Here, we demonstrate that the functions of ATR and ATM are only partially conserved between Arabidopsis and maize (Zea mays). In both species, ATR and ATM play a key role in DNA repair and cell cycle checkpoint activation, but whereas Arabidopsis plants do not suffer from the absence of ATR under control growth conditions, maize mutant plants accumulate replication defects, likely due to their large genome size. Moreover, contrarily to Arabidopsis, maize ATM deficiency does not trigger meiotic defects, whereas the ATR kinase appears to be crucial for the maternal fertility. Strikingly, ATR is required to repress premature endocycle onset and cell death in the maize endosperm. Its absence results in a reduction of kernel size, protein and starch content, and a stochastic death of kernels, a process being counteracted by ATM. Additionally, while Arabidopsis atr atm double mutants are viable, no such mutants could be obtained for maize. Therefore, our data highlight that the mechanisms maintaining genome integrity may be more important for vegetative and reproductive development than previously anticipated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • CRISPR-Cas Systems
  • Cell Death / genetics
  • DNA Breaks, Double-Stranded
  • DNA Repair / genetics*
  • DNA Replication / genetics
  • Endosperm / cytology
  • Endosperm / genetics*
  • Genomic Instability
  • Mutation
  • Plant Cells
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Plants, Genetically Modified
  • Seeds / cytology
  • Seeds / genetics
  • Seeds / growth & development
  • Zea mays / cytology
  • Zea mays / genetics*
  • Zea mays / growth & development

Substances

  • Arabidopsis Proteins
  • Plant Proteins
  • ATR protein, Arabidopsis
  • Ataxia Telangiectasia Mutated Proteins