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      Arabidopsis AN3 and OLIGOCELLULA genes link telomere maintenance mechanisms with cell division and expansion control

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          Abstract

          Telomeres are conserved chromosomal structures necessary for continued cell division and proliferation. In addition to the classical telomerase pathway, multiple other genes including those involved in ribosome metabolism and chromatin modification contribute to telomere length maintenance. We previously reported that Arabidopsis thaliana ribosome biogenesis genes OLI2/NOP2A, OLI5/RPL5A and OLI7/RPL5B have critical roles in telomere length regulation. These three OLIGOCELLULA genes were also shown to function in cell proliferation and expansion control and to genetically interact with the transcriptional co-activator ANGUSTIFOLIA3 (AN3). Here we show that AN3-deficient plants progressively lose telomeric DNA in early homozygous mutant generations, but ultimately establish a new shorter telomere length setpoint by the fifth mutant generation with a telomere length similar to oli2/nop2a - deficient plants. Analysis of double an3 oli2 mutants indicates that the two genes are epistatic for telomere length control. Telomere shortening in an3 and oli mutants is not caused by telomerase inhibition; wild type levels of telomerase activity are detected in all analyzed mutants in vitro. Late generations of an3 and oli mutants are prone to stem cell damage in the root apical meristem, implying that genes regulating telomere length may have conserved functional roles in stem cell maintenance mechanisms. Multiple instances of anaphase fusions in late generations of oli5 and oli7 mutants were observed, highlighting an unexpected effect of ribosome biogenesis factors on chromosome integrity. Overall, our data implicate AN3 transcription coactivator and OLIGOCELLULA proteins in the establishment of telomere length set point in plants and further suggest that multiple regulators with pleiotropic functions can connect telomere biology with cell proliferation and cell expansion pathways.

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          Isolation of plant DNA from fresh tissue

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            The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.

            Nucleosome remodelers of the DDM1/Lsh family are required for DNA methylation of transposable elements, but the reason for this is unknown. How DDM1 interacts with other methylation pathways, such as small-RNA-directed DNA methylation (RdDM), which is thought to mediate plant asymmetric methylation through DRM enzymes, is also unclear. Here, we show that most asymmetric methylation is facilitated by DDM1 and mediated by the methyltransferase CMT2 separately from RdDM. We find that heterochromatic sequences preferentially require DDM1 for DNA methylation and that this preference depends on linker histone H1. RdDM is instead inhibited by heterochromatin and absolutely requires the nucleosome remodeler DRD1. Together, DDM1 and RdDM mediate nearly all transposon methylation and collaborate to repress transposition and regulate the methylation and expression of genes. Our results indicate that DDM1 provides DNA methyltransferases access to H1-containing heterochromatin to allow stable silencing of transposable elements in cooperation with the RdDM pathway. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Identification of seven loci affecting mean telomere length and their association with disease

              Interindividual variation in mean leukocyte telomere length (LTL) is associated with cancer and several age-associated diseases. We report here a genome-wide meta-analysis of 37,684 individuals with replication of selected variants in an additional 10,739 individuals. We identified seven loci, including five new loci, associated with mean LTL (P < 5 × 10(-8)). Five of the loci contain candidate genes (TERC, TERT, NAF1, OBFC1 and RTEL1) that are known to be involved in telomere biology. Lead SNPs at two loci (TERC and TERT) associate with several cancers and other diseases, including idiopathic pulmonary fibrosis. Moreover, a genetic risk score analysis combining lead variants at all 7 loci in 22,233 coronary artery disease cases and 64,762 controls showed an association of the alleles associated with shorter LTL with increased risk of coronary artery disease (21% (95% confidence interval, 5-35%) per standard deviation in LTL, P = 0.014). Our findings support a causal role of telomere-length variation in some age-related diseases.
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                Author and article information

                Contributors
                Journal
                Res Sq
                ResearchSquare
                Research Square
                American Journal Experts
                28 October 2023
                : rs.3.rs-3438810
                Affiliations
                Kazan Federal University: Kazanskij Privolzskij federal’nyj universitet
                Kazan Federal University: Kazanskij Privolzskij federal’nyj universitet
                Kazan Federal University: Kazanskij Privolzskij federal’nyj universitet
                Texas A&M University
                Marshall University
                Marshall University
                Marshall University
                Kazan Federal University: Kazanskij Privolzskij federal’nyj universitet
                Texas A&M University
                The University of Texas at Austin
                Marshall University
                Author notes

                Author Contributions

                All authors contributed significantly to this work. I.A.A., D.E.S., T.E.J., and E.V.S. designed the research. I.A.A., L.R.A, A.Y.L., P.G.Y., L.R.V., O.B., and E.G.L. performed the research. I.A.A., L.R.A, M.R.S., D.E.S., T.E.J., and E.V.S. analyzed the results. I.A.A. created the figures. I.A.A., D.E.S., T.E.J., and E.V.S. wrote the article with contributions from all other authors.

                [] Correspondence and requests for materials should be addressed to D.E.S., T.E.J. or E.V.S. shakirov@ 123456marshall.edu
                Author information
                http://orcid.org/0000-0003-2689-7410
                Article
                10.21203/rs.3.rs-3438810
                10.21203/rs.3.rs-3438810/v1
                10635316
                37961382
                4cda9699-05da-4113-8083-10e99caf2388

                This work is licensed under a Creative Commons Attribution 4.0 International License, which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.

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                arabidopsis thaliana,nop2,ribosomal proteins,telomere dynamics,telomerase,tert

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