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These genetic and in vitro observations were rationalized by proposing that, during lagging strand DNA synthesis, extended Polδ- and Pif1-dependent strand displacement events generate long DNA flaps that must be cut by Dna2.Here we used conditional alleles of DNA2 to show that a single unperturbed S phase, following Dna2 depletion, generates toxic and lethal DNA structures activating the DNA damage response (DDR), without inducing fork pausing and chromosome fragmentation.While PIF1 deletion rescues the lethality of Dna2 depletion, RAD9 ablation relieves the first cell cycle arrest causing genotoxicity after few cell divisions.Slow fork speed attenuates DDR in Dna2 deprived cells.a–d Dna2 was depleted in G1 in the indicated strains and cells were released into unperturbed S phase (a, b), S phase in the presence of a low dose of HU (c) or at a low temperature (d).a, c Non-depleted cells were kept in parallel as control.We propose that this Dna2 function has been hijacked by Break Induced Replication in DSB processing.Okazaki fragment maturation depends on the strand displacement activity of Pol δ, which peels off the 5’end of the previous Okazaki fragment, Rad27/FEN1, which cuts the resulting DNA flap, and DNA nick ligation mediated by the DNA ligase I. USA 98, 5122–5127 (2001)." href="/articles/s41467-018-07378-5#ref-CR8" id="ref-link-section-d21795e414", contributes to the displacement of a fraction of 5’ ends of Okazaki fragments, forming long ss DNA tails that are cleaved, sequentially, by Dna2 and Fen1, through a secondary pathway of Okazaki fragment maturation known as alternative pathway of Okazaki fragment processing (APO).

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b–d Black arrows and grey arrows indicate, respectively, lack of Rad53 activation and cells that initiate the second cell cycle While Pif1 ablation rescued the lethality of Dna2-depleted cells, RAD9 deletion allowed CL-dna2 rad9Δ mutants to perform only few cell divisions on plates and liquid cultures at 28 °C (Fig. This is in line with previous studies showing that, although RAD9 deletion suppresses the cell lethality of dna2Δ cells at low temperatures (20–23 °C), the rad9Δ dna2Δ strain is temperature sensitive and has a reduced fitness at 28–30 °C.

Overall, previous data and the observations presented in this study suggest that under fast replication conditions, Rad9, in the absence of Dna2, promotes a first cell cycle barrier preventing the propagation of genotoxicity to the next cell cycles; without Rad9, fast replication still kills Dna2-depleted cells, by causing the accumulation of lethal DNA structures after 4–5 divisions (Fig. Slowing down fork speed did not ameliorate the viability of Dna2-depleted cells, likely due to residual DDR activation (Fig. In fact, low HU doses or low temperatures restored cell viability in Dna2-depleted rad9 mutants (Fig. We note that while slowing down replication in Dna2-depleted cells suppressed the first cell cycle arrest (Fig.

1c, d), the three major pathways causing lethality in Dna2 depleted cells (namely Pif1, DNA replication fork speed, and DNA damage checkpoint) were still functional.

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Hence, it is reasonable to think that a slow replication mode, in the absence of Dna2, can lead to the accumulation of Pif1-dependent toxic DNA structures that would activate the DNA damage checkpoint and generate genome damage over few cell cycles, ultimately causing cell cycle arrest or cell death.In this context, recent work provides evidence that Dna2 can cut at the junction between ss DNA and double-stranded DNA (ds DNA) at the base of a DNA flap, suggesting that Dna2 could also work as sole nuclease in the processing of Okazaki fragments. In in vitro reactions simulating Okazaki fragment processing, Dna2 was shown to cut a sub-fraction of long Pif1-dependent DNA flaps generated during lagging strand DNA synthesis.

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