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

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 TOP3 alpha has been shown as essential for viability in various animals. In contrast, in the model plant species Arabidopsis, the top3 alpha mutant is viable. rmi1 mutants are deficient in the repair of DNA damage. Moreover, as opposed to other eukaryotes, TOP3 alpha 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 TOP3 alpha and RMI1 in tomato using CRISPR/Cas technology. Surprisingly, we found phenotypes that differed dramatically from those of Arabidopsis: the top3 alpha 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.

Automated summary

The RTR complex is essential for genome stability in eukaryotes, with TOP3α and RMI1 mutants in tomato showing significantly different phenotypes compared to Arabidopsis. While the TOP3α mutant in tomato is embryo-lethal, the RMI1 mutant does not exhibit detectable defects in somatic DNA repair or meiosis. This differentiation of function in RTR complex partners between plant species suggests caution in generalizing knowledge obtained in Arabidopsis to the entire plant kingdom.