DNA Replication Control During <i>Drosophila</i> Development: Insights into the Onset of S Phase, Replication Initiation, and Fork Progression

Hua, Brian L; Orr‐Weaver, Terry L.

doi:10.1534/genetics.115.186627

Cited by 36 publications

(36 citation statements)

References 157 publications

(258 reference statements)

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“…To determine if the SUUR ∆SNF protein was still able to associate with chromatin, we localized 184 SUUR and the SUUR ∆SNF mutant proteins in ovarian follicle cells. During follicle cell 185 development, these cells undergo programmed changes in their cell cycle and DNA replication 186 programs (Claycomb and Orr-Weaver, 2005;Hua and Orr-Weaver, 2017). At a precise time in 187 their differentiation program, follicle cells cease genomic replication and amplify six defined 188 sites of their genome through a re-replication based mechanism.…”

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confidence: 99%

Rif1 inhibits replication fork progression and controls DNA copy number in Drosophila

Munden

Rong

Gangula

et al. 2018

Preprint

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Control of DNA copy number is essential to maintain genome stability and ensure proper cell and tissue function. In Drosophila polyploid cells, the SNF2-domain-containing SUUR protein inhibits replication fork progression within specific regions of the genome to promote DNA underreplication. While dissecting the function of SUUR’s SNF2 domain, we identified a physical interaction between SUUR and Rif1. Rif1 has many roles in DNA metabolism and regulates the replication timing program. We demonstrate that repression of DNA replication is dependent on Rif1. Rif1 localizes to active replication forks in an SUUR-dependent manner and directly regulates replication fork progression. Importantly, SUUR associates with replication forks in the absence of Rif1, indicating that Rif1 acts downstream of SUUR to inhibit fork progression. Our findings uncover an unrecognized function of the Rif1 protein as a regulator of replication fork progression.

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confidence: 99%

Rif1 inhibits replication fork progression and controls DNA copy number in Drosophila

Munden

Rong

Gangula

et al. 2018

Preprint

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“…Flight performance in honeybees is associated with a reduction in polyploidy with age [19]. Further, while it is known that endocyclic cells are large and metabolically active, have multiple sites of origin firing, and variable levels of transcription [10,14,15], it remains to be seen whether underreplication is a mechanism to meet the metabolic demands of flight with a minimal increase in nuclear size. The identification of differing patterns of underreplication in indirect flight muscle tissues opens an interesting resource to pursue questions of underreplication, development, and tissue specific adaptation.…”

Section: Discussionmentioning

confidence: 99%

“…While recent work has investigated the machinery involved in this stalling of replication, the mechanisms behind this process are not fully understood [2,7,8]. UR does not alter origin firing, or the initiation of replication [9], Genes 2020, 11, 246 2 of 12 but rather determines how far the replication fork may progress during synthesis [10]. Estimations of the percent UR have been proposed to indicate the amount of heterochromatic DNA in the genome [11].…”

Section: Introductionmentioning

confidence: 99%

“…UR is typically accompanied by the endocycle, which produces UR polytene or polyploid nuclei [13]. In these cells, origin firing has been linked to the initiation of active gene transcription; cells that undergo polyploidy through the endocycle are large and highly metabolically active [9,10,14,15]. A variant of this process is seen in the thorax of Drosophila.…”

Section: Introductionmentioning

confidence: 99%

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Flying High—Muscle-Specific Underreplication in Drosophila

Johnston

Zapalac

Hjelmen

2020

Genes

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Drosophila underreplicate the DNA of thoracic nuclei, stalling during S phase at a point that is proportional to the total genome size in each species. In polytene tissues, such as the Drosophila salivary glands, all of the nuclei initiate multiple rounds of DNA synthesis and underreplicate. Yet, only half of the nuclei isolated from the thorax stall; the other half do not initiate S phase. Our question was, why half? To address this question, we use flow cytometry to compare underreplication phenotypes between thoracic tissues. When individual thoracic tissues are dissected and the proportion of stalled DNA synthesis is scored in each tissue type, we find that underreplication occurs in the indirect flight muscle, with the majority of underreplicated nuclei in the dorsal longitudinal muscles (DLM). Half of the DNA in the DLM nuclei stall at S phase between the unreplicated G0 and fully replicated G1. The dorsal ventral flight muscle provides the other source of underreplication, and yet, there, the replication stall point is earlier (less DNA replicated), and the endocycle is initiated. The differences in underreplication and ploidy in the indirect flight muscles provide a new tool to study heterochromatin, underreplication and endocycle control.

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“…Both under-replication and over-replication (amplification) have been observed in multiple animal systems, notably including Drosophila (reviewed in [17]). In addition to the well-known amplification of chorion genes and under-replication of heterochromatin, underreplication also occurs in a number of euchromatic regions, with a degree of tissue specificity suggesting a possible role in differentiation [18][19][20].…”

Section: Introductionmentioning

confidence: 99%

Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

Wear

Song

Zynda

et al. 2020

Preprint

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39 Plant cells undergo two types of cell cycles -the mitotic cycle in which DNA replication is 40 coupled to mitosis, and the endocycle in which DNA replication occurs in the absence of cell 41 division. To investigate DNA replication programs in these two types of cell cycles, we pulse 42 labeled intact root tips of maize (Zea mays) with 5-ethynyl-2'-deoxyuridine (EdU) and used flow 43 sorting of nuclei to examine DNA replication timing (RT) during the transition from a mitotic 44 cycle to an endocycle. Here, we compare sequence-based RT profiles and found that most 45 regions of the maize genome replicate at the same time during S phase in mitotic and 46 endocycling cells, despite the need to replicate twice as much DNA in the endocycle. However, 47 regions collectively corresponding to 2% of the genome displayed significant changes in timing 48 between the two types of cell cycles. The majority of these regions are small, with a median size 49 of 135 kb, and shift to a later RT in the endocycle. However, we found larger regions that shifted 50 RT in centromeres of seven of the ten maize chromosomes. These regions covered the majority 51 of the previously defined functional centromere in each case, which are ~1-2 Mb in size in the 52 reference genome. They replicate mainly during mid S phase in mitotic cells, but primarily in 53 late S phase of the endocycle. Strikingly, the immediately adjacent pericentromere sequences are 54 primarily late replicating in both cell cycles. Analysis of CENH3 enrichment levels in nuclei of 55 different ploidies suggested that there is only a partial replacement of CENH3 nucleosomes after 56 endocycle replication is complete. The shift to later replication of centromeres and reduced 57 CENH3 enrichment after endocycle replication is consistent with the hypothesis that centromeres 58 are being inactivated as their function is no longer needed. Wear et al. 3 59 AUTHOR SUMMARY60 In traditional cell division, or mitosis, a cell's genetic material is duplicated and then split 61 between two daughter cells. In contrast, in some specialized cell types, the DNA is duplicated a 62 second time without an intervening division step, resulting in cells that carry twice as much DNA 63 -a phenomenon called an endocycle, which is common during plant development. At each step, 64 DNA replication follows an ordered program, in which highly compacted DNA is unraveled and 65 replicated in sections at different times during the synthesis (S) phase. In plants, it is unclear 66 whether traditional and endocycle programs are the same. Using root tips of maize, we found a 67 small portion of the genome whose replication in the endocycle is shifted in time, usually to later 68 in S phase. Some of these regions are scattered around the genome, and mostly coincide with 69 active genes. However, the most prominent shifts occur in centromeres. This location is 70 noteworthy because centromeres orchestrate the process of separating duplicated chromosomes 71 into daughter cells, a function that is not needed in...

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DNA Replication Control During Drosophila Development: Insights into the Onset of S Phase, Replication Initiation, and Fork Progression

Cited by 36 publications

References 157 publications

Rif1 inhibits replication fork progression and controls DNA copy number in Drosophila

Rif1 inhibits replication fork progression and controls DNA copy number in Drosophila

Flying High—Muscle-Specific Underreplication in Drosophila

Comparing DNA replication programs reveals large timing shifts at centromeres of endocycling cells in maize roots

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