Different functional roles of RTR complex factors in DNA repair and meiosis in Arabidopsis and tomato

Plant J. 2021 May;106(4):965-977. doi: 10.1111/tpj.15211. Epub 2021 Mar 25.

Abstract

The RTR (RecQ/Top3/Rmi1) complex has been elucidated as essential for ensuring genome stability in eukaryotes. Fundamental for the dissolution of Holliday junction (HJ)-like recombination intermediates, the factors have been shown to play further, partly distinct roles in DNA repair and homologous recombination. Across all kingdoms, disruption of this complex results in characteristic phenotypes including hyper-recombination and sensitivity to genotoxins. The type IA topoisomerase TOP3α has been shown as essential for viability in various animals. In contrast, in the model plant species Arabidopsis, the top3α mutant is viable. rmi1 mutants are deficient in the repair of DNA damage. Moreover, as opposed to other eukaryotes, TOP3α and RMI1 were found to be indispensable for proper meiotic progression, with mutants showing severe meiotic defects and sterility. We now established mutants of both TOP3α and RMI1 in tomato using CRISPR/Cas technology. Surprisingly, we found phenotypes that differed dramatically from those of Arabidopsis: the top3α mutants proved to be embryo-lethal, implying an essential role of the topoisomerase in tomato. In contrast, no defect in somatic DNA repair or meiosis was detectable for rmi1 mutants in tomato. This points to a differentiation of function of RTR complex partners between plant species. Our results indicate that there are relevant differences in the roles of basic factors involved in DNA repair and meiosis within dicotyledons, and thus should be taken as a note of caution when generalizing knowledge regarding basic biological processes obtained in the model plant Arabidopsis for the entire plant kingdom.

Keywords: Arabidopsis thaliana; Solanum lycopersicum; dissolution; helicase; topoisomerase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / enzymology
  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • DNA Repair / genetics*
  • DNA Topoisomerases, Type I / genetics
  • DNA Topoisomerases, Type I / metabolism
  • Genomic Instability
  • Homologous Recombination
  • Meiosis / genetics*
  • Mutation
  • Phenotype
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • RecQ Helicases / genetics
  • RecQ Helicases / metabolism
  • Solanum lycopersicum / enzymology
  • Solanum lycopersicum / genetics*
  • Solanum lycopersicum / physiology

Substances

  • Arabidopsis Proteins
  • Carrier Proteins
  • Plant Proteins
  • RMI1 protein, Arabidopsis
  • RecQ Helicases
  • DNA Topoisomerases, Type I