DNA double-strand break formation and repair in Tetrahymena meiosis

Abstract

The molecular details of meiotic recombination have been determined for a small number of model organisms. From these studies, a general picture has emerged that shows that most, if not all, recombination is initiated by a DNA double-strand break (DSB) that is repaired in a recombinogenic process using a homologous DNA strand as a template. However, the details of recombination vary between organisms, and it is unknown which variant is representative of evolutionarily primordial meiosis or most prevalent among eukaryotes. To answer these questions and to obtain a better understanding of the range of recombination processes among eukaryotes, it is important to study a variety of different organisms. Here, the ciliate Tetrahymena thermophila is introduced as a versatile meiotic model system, which has the additional bonus of having the largest phylogenetic distance to all of the eukaryotes studied to date. Studying this organism can contribute to our understanding of the conservation and diversification of meiotic recombination processes.

A Zip3-like protein plays a role in crossover formation in the SC-less meiosis of the protistTetrahymena

“…Findings in Tetrahymena are compatible with a role for MutSγ in protecting CO precursors (Shodhan et al. , 2014), whereas a Mer3 orthologue has not been found (Loidl and Lorenz, 2016). …”

E2fl1 is a meiosis-specific transcription factor in the protistTetrahymena thermophila

“…In contrast, no evidence of DNA repair synthesis (by BrdU incorporation) was found. An alternative method of meiotic DSB repair by synthesis-independent nonhomologous end joining in T. thermophila is unlikely, 29 but remains a possible explanation. It is also conceivable that strand invasion and heteroduplex formation occurs, but the subsequent elongation of invading strands fails.…”

A DP-like transcription factor protein interacts with E2fl1 to regulate meiosis inTetrahymena thermophila

“…Rad51 and Dmc1 mark DSBs for repair and promote DNA strand exchange [8]. Hop2 and its partner Mnd1 promote recombination repair to form crossovers [4,9]. Due to lack of synaptonemal complexes during meiosis, crossover formation depends on the class II pathway, which is largely independent of ZMM (Zip1/2/3/4, Msh4/5, and Mer3) [38,39].…”

“…thermophila is a unicellular ciliate with two functionally distinct nuclei: a diploid (2n) germline micronucleus (MIC) and a polyploid (»45n) somatic macronucleus (MAC) [3]. As meiosis and the function of many meiotic genes have been extensively studied in T. thermophila [4][5][6][7][8][9][10][11][12][13][14], T. thermophila is an excellent eukaryotic model for studying meiosis regulation. Given the importance of achieving accurate chromosome separation during meiosis, this process must be strictly regulated by a number of factors, including transcription factors.…”