Low dose ribosomal DNA P-loop mutation affects development and enforces autophagy in Arabidopsis

References

• Keller E, Zamenick P, Loftfield R. The role of microsomes in the incorporation of amino acids into proteins. J Histochem Cytochem. 1954;2(5):378–386. doi: 10.1177/2.5.378
   PubMed Web of Science ®Google Scholar
• Zhou X, Liao WJ, Liao JM, et al. Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol. 2015;7(2):92–104. doi: 10.1093/jmcb/mjv014
   PubMed Web of Science ®Google Scholar
• Miller OLJ, Beatty BR. Visualization of nucleolar genes. Science. 1969;164(3882):955–957. doi: 10.1126/science.164.3882.955
   PubMed Web of Science ®Google Scholar
• Russell J, Zomerdijk JCBM. RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci. 2005;30:87–96. doi: 10.1016/j.tibs.2004.12.008
   PubMed Web of Science ®Google Scholar
• Nomura M. Bacterial Ribosome. Bacteriol Rev. 1970;34(3):228–277. doi: 10.1128/br.34.3.228-277.1970
   PubMedGoogle Scholar
• Mohannath G, Pontvianne F, Pikaard CS. Selective nucleolus organizer inactivation in arabidopsis is a chromosome position-effect phenomenon. Proc Natl Acad Sci USA. 2016;113(47):13426–13431. doi: 10.1073/pnas.1608140113
   PubMed Web of Science ®Google Scholar
• Pontvianne F, Abou-Ellail M, Douet J, et al. Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in arabidopsis thaliana. PLoS Genet. 2010;6(11):1–13. doi: 10.1371/journal.pgen.1001225
   Web of Science ®Google Scholar
• Chandrasekhara C, Mohannath G, Blevins T, et al. Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in arabidopsis. Genes Dev. 2016;30(2):177–190. doi: 10.1101/gad.273755.115
   PubMed Web of Science ®Google Scholar
• Sweeney BA, Hoksza D, Nawrocki EP, et al. R2DT is a framework for predicting and visualising RNA secondary structure using templates. Nat Commun. 2021;12:1–12. doi: 10.1038/s41467-021-23555-5
   PubMed Web of Science ®Google Scholar
• Abou-Ellail M, Cooke R, Sáez-Vásquez J. Variations in a team: major and minor variants of arabidopsis thaliana rDNA genes. Nucleus. 2011;2(4):294–299. doi: 10.4161/nucl.2.4.16561
   PubMed Web of Science ®Google Scholar
• Barakat A, Szick-Miranda K, Chang IF, et al. The organization of cytoplasmic ribosomal protein genes in the arabidopsis genome. Plant Physiol. 2001;127(2):398–415. doi: 10.1104/pp.010265
   PubMed Web of Science ®Google Scholar
• de La Cruz J, Karbstein K, Woolford JL. Functions of ribosomal proteins in assembly of eukaryotic ribosomes in vivo. Annu Rev Biochem. 2015;84(1):93–129. doi: 10.1146/annurev-biochem-060614-033917
   PubMedGoogle Scholar
• Weis BL, Kovacevic J, Missbach S, et al. Plant-specific features of ribosome biogenesis. Trends Plant Sci. 2015;20(11):729–740. doi: 10.1016/j.tplants.2015.07.003
   PubMed Web of Science ®Google Scholar
• Sáez-Vásquez J, Delseny M. Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell. 2019;31(9):1945–1967. doi: 10.1105/tpc.18.00874
   PubMed Web of Science ®Google Scholar
• Genuth NR, Barna M. The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life. Mol Cell. 2018;71(3):364–374. doi: 10.1016/j.molcel.2018.07.018
   PubMed Web of Science ®Google Scholar
• Giavalisco P, Wilson D, Kreitler T, et al. High heterogeneity within the ribosomal proteins of the arabidopsis thaliana 80S ribosome. Plant Mol Biol. 2005;57(4):577–591. doi: 10.1007/s11103-005-0699-3
   PubMed Web of Science ®Google Scholar
• Kovacevic J, Palm D, Jooss D, et al. Co-orthologues of ribosome biogenesis factors in A. thaliana are differentially regulated by transcription factors. Plant Cell Rep. 2019;38:937–949. doi: 10.1007/s00299-019-02416-y
   PubMed Web of Science ®Google Scholar
• Norris K, Hopes T, Aspden JL. Ribosome heterogeneity and specialization in development. Wiley Interdiscip Rev RNA. 2021;12(4):1–23. doi: 10.1002/wrna.1644
   Web of Science ®Google Scholar
• Carroll AJ, Heazlewood JL, Ito J, et al. Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol & Cell Proteomics. 2008;7:347–369. doi: 10.1074/mcp.M700052-MCP200
   PubMed Web of Science ®Google Scholar
• Simm S, Fragkostefanakis S, Paul P, et al. Identification and expression analysis of ribosome biogenesis factor co-orthologs in solanum lycopersicum. Bioinform Biol Insights. 2015;9:1–17. doi: 10.4137/BBI.S20751
   PubMedGoogle Scholar
• Xue S, Barna M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol. 2012;13(6):355–369. doi: 10.1038/nrm3359
   PubMed Web of Science ®Google Scholar
• Sims J, Sestini G, Elgert C, et al. Sequencing of the Arabidopsis NOR2 reveals its distinct organization and tissue-specific rRNA ribosomal variants. Nat Commun. 2021;12:1–13. doi: 10.1038/s41467-020-20728-6
   PubMed Web of Science ®Google Scholar
• Azevedo-Favory J, Gaspin C, Ayadi L, et al. Mapping rRNA 2’-O-methylations and identification of C/D snoRnas in arabidopsis thaliana plants. RNA Biol. 2021;18:1760–1777. doi: 10.1080/15476286.2020.1869892
   PubMed Web of Science ®Google Scholar
• Streit D, Schleiff E. The arabidopsis 2′-O-Ribose-methylation and pseudouridylation landscape of rRNA in comparison to human and yeast. Front Plant Sci. 2021;12:1–19. doi: 10.3389/fpls.2021.684626
   Web of Science ®Google Scholar
• Byrne ME. A role for the ribosome in development. Trends Plant Sci. 2009;14(9):512–519. doi: 10.1016/j.tplants.2009.06.009
   PubMed Web of Science ®Google Scholar
• Martinez-Seidel F, Beine-Golovchuk O, Hsieh YC, et al. Systematic review of plant ribosome heterogeneity and specialization. Front Plant Sci. 2020;11:1–23. doi: 10.3389/fpls.2020.00948
   PubMed Web of Science ®Google Scholar
• Gunderson JH, Sogin ML, Wolletr G, et al. Structurally Distinct, Stage-Specific Ribosomes Occur in Plasmodium. Science. 1987;238(4829):933–937. (1979) doi: 10.1126/science.3672135
   PubMed Web of Science ®Google Scholar
• Rogers MJ, Gutell RR, Damberger SH, et al. Structural features of the large subunit rRNA expressed in Plasmodium falciparum sporozoites that distinguish it from the asexually expressed subunit rRNA. RNA. 1996;2(2):134–145. doi: 10.1016/j.cirp.2016.06.001%0A
   PubMed Web of Science ®Google Scholar
• Velichutina IV, Rogers MJ, McCutchan TF, et al. Chimeric rRnas containing the GTPase centers of the developmentally regulated ribosomal rRnas of Plasmodium falciparum are functionally distinct. RNA. 1998;4:594–602. doi: 10.1017/S1355838298980049
   PubMed Web of Science ®Google Scholar
• Locati MD, Pagano JFB, Girard G, et al. Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development. RNA. 2017;23(8):1188–1199. doi: 10.1261/rna.061515.117
   PubMed Web of Science ®Google Scholar
• Parks MM, Kurylo CM, Dass RA, et al. Variant ribosomal RNA alleles are conserved and exhibit tissue-specific expression. Sci Adv. 2018;4(2):4. doi: 10.1126/sciadv.aao0665
   Web of Science ®Google Scholar
• Kurylo CM, Parks MM, Juette MF, et al. Endogenous rRNA sequence variation can regulate stress response gene expression and phenotype. Cell Rep. 2018;25(1):236–248.e6. doi: 10.1016/j.celrep.2018.08.093
   PubMed Web of Science ®Google Scholar
• Klinge S, Voigts-Hoffmann F, Leibundgut M, et al. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science (1979). 2011;334:941–948. doi: 10.1126/science.1211204
   PubMed Web of Science ®Google Scholar
• Streit D, Shanmugam T, Garbelyanski A, et al. The existence and localization of nuclear snoRnas in arabidopsis thaliana revisited. Plants. 2020;9(8):1016–1018. doi: 10.3390/plants9081016
   Google Scholar
• Pontvianne F, Carpentier MC, Durut N, et al. Identification of nucleolus-associated chromatin domains reveals a role for the nucleolus in 3D organization of the A. thaliana genome. Cell Rep. 2016;16(6):1574–1587. doi: 10.1016/j.celrep.2016.07.016
   PubMed Web of Science ®Google Scholar
• Horlbeck MA, Witkowsky LB, Guglielmi B, et al. Nucleosomes impede Cas9 access to DNA in vivo and in vitro. Elife. 2016;5: doi: 10.7554/eLife.12677
   Web of Science ®Google Scholar
• Daer RM, Cutts JP, Brafman DA, et al. The Impact of Chromatin Dynamics on Cas9-mediated genome editing in human cells. ACS Synth Biol. 2017;6(3):428–438. doi: 10.1021/acssynbio.5b00299
   PubMed Web of Science ®Google Scholar
• Chari R, Mali P, Moosburner M, et al. Unraveling CRISPR-Cas9 genome engineering parameters via a library-on-library approach. Nat Methods. 2015;12:823–826. doi: 10.1038/nmeth.3473
   PubMed Web of Science ®Google Scholar
• Lopez FB, Fort A, Tadini L, et al. Gene dosage compensation of rRNA transcript levels in arabidopsis thaliana lines with reduced ribosomal gene copy number. Plant Cell. 2021;33(4):1135–1150. doi: 10.1093/plcell/koab020
   PubMed Web of Science ®Google Scholar
• Schindele A, Gehrke F, Schmidt C, et al. Using CRISPR-Kill for organ specific cell elimination by cleavage of tandem repeats. Nat Commun. 2022;13(1):1502. Available from. https://www.nature.com/articles/s41467-022-29130-w
   PubMed Web of Science ®Google Scholar
• Durut N, Abou-Ellail M, Pontvianne F, et al. A duplicated NUCLEOLIN gene with antagonistic activity is required for chromatin organization of silent 45S rDNA in arabidopsis. Plant Cell. 2014;26(3):1330–1344. doi: 10.1105/tpc.114.123893
   PubMed Web of Science ®Google Scholar
• Earley K, Lawrence RJ, Pontes O, et al. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 2006;20(10):1283–1293. doi: 10.1101/gad.1417706
   PubMed Web of Science ®Google Scholar
• Chen X, Lu L, Qian S, et al. Canonical and noncanonical actions of arabidopsis histone deacetylases in ribosomal RNA processing. Plant Cell. 2018;30(1):134–152. doi: 10.1105/tpc.17.00626
   PubMed Web of Science ®Google Scholar
• Shanmugam T, Streit D, Schroll F, et al. Dynamics and thermal sensitivity of rRNA maturation paths in plants. J Exp Bot. 2021;72:7626–7644. doi: 10.1093/jxb/erab434
   Web of Science ®Google Scholar
• Wang M, Parshin AV, Shcherbik N, et al. Reduced expression of the mouse ribosomal protein Rpl17 alters the diversity of mature ribosomes by enhancing production of shortened 5.8S rRNA. RNA. 2015;21:1240–1248. doi: 10.1261/rna.051169.115
   PubMed Web of Science ®Google Scholar
• Leshin JA, Heselpoth R, Belew AT, et al. High throughput structural analysis of yeast ribosomes using hSHAPE. RNA Biol. 2011;8(3):478–487. doi: 10.4161/rna.8.3.14453
   PubMed Web of Science ®Google Scholar
• Stephani M, Picchianti L, Gajic A, et al. A cross-kingdom conserved er-phagy receptor maintains endoplasmic reticulum homeostasis during stress. Elife. 2020;9:e58396. doi: 10.7554/eLife.58396
   PubMed Web of Science ®Google Scholar
• Bao Y, Mugume Y, Bassham DC. Biochemical methods to monitor autophagic responses in plants. Methods Enzymol. 2017;588:497–513.
   PubMed Web of Science ®Google Scholar
• Bao Y, Song WM, Wang P, et al. COST1 regulates autophagy to control plant drought tolerance. Proc Natl Acad Sci USA. 2020;117(13):7482–7493. doi: 10.1073/pnas.1918539117
   PubMed Web of Science ®Google Scholar
• Cheong H, Klionsky DJ. Biochemical methods to monitor autophagy-related processes in yeast [internet]. 1st ed. Meth Enzymol Elsevier Inc. 2008. doi: 10.1016/S0076-6879(08)03201-1
   Google Scholar
• Mesihovic A, Ullrich S, Rosenkranz RRE, et al. HsfA7 coordinates the transition from mild to strong heat stress response by controlling the activity of the master regulator HsfA1a in tomato. Cell Rep. 2022;38:110224. doi: 10.1016/j.celrep.2021.110224
   PubMed Web of Science ®Google Scholar
• Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of arabidopsis thaliana. Plant J. 1998;16(6):735–743. doi: 10.1046/j.1365-313x.1998.00343.x
   PubMed Web of Science ®Google Scholar
• Zhu X, Xu Y, Yu S, et al. An efficient genotyping method for genome-modified animals and human cells generated with CRISPR/Cas9 system. Sci Rep. 2014;4(1):1–8. doi: 10.1038/srep06420
   Google Scholar
• Ghatak A, Chaturvedi P, Bachmann G, et al. Physiological And proteomic signatures reveal mechanisms of superior drought resilience in pearl millet compared to wheat. Front Plant Sci. 2020;11:600278. doi: 10.3389/fpls.2020.600278
   PubMed Web of Science ®Google Scholar
• Chaturvedi P, Ischebeck T, Egelhofer V, et al. Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. J Proteome Res. 2013;12(11):4892–4903. doi: 10.1021/pr400197p
   PubMed Web of Science ®Google Scholar
• Zhang S, Ghatak A, Bazargani MM, et al. Spatial distribution of proteins and metabolites in developing wheat grain and their differential regulatory response during the grain filling process. Plant J. 2021;107(3):669–687. doi: 10.1111/tpj.15410
   PubMed Web of Science ®Google Scholar
• Paoletti AC, Parmely TJ, Tomomori-Sato C, et al. Quantitative proteomic analysis of distinct mammalian mediator complexes using normalized spectral abundance factors. Proc Natl Acad Sci USA. 2006;103(50):18928–18933. doi: 10.1073/pnas.0606379103
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012;9(4):357–359. doi: 10.1038/nmeth.1923
   PubMed Web of Science ®Google Scholar
• Li H, Handsaker B, Wysoker A, et al. The sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–2079. doi: 10.1093/bioinformatics/btp352
   PubMed Web of Science ®Google Scholar
• Wilm A, PPK A, Bertrand D, et al. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res. 2012;40(22):11189–11201. doi: 10.1093/nar/gks918
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25(4):402–408. Available from. https://www.sciencedirect.com/science/article/pii/S1046202301912629
   PubMed Web of Science ®Google Scholar
• Palm D, Streit D, Shanmugam T, et al. Plant-specific ribosome biogenesis factors in arabidopsis thaliana with essential function in rRNA processing. Nucleic Acids Res. 2019;47(4):1880–1895. doi: 10.1093/nar/gky1261
   PubMed Web of Science ®Google Scholar
• Firmino AAP, Gorka M, Graf A, et al. Separation and paired proteome profiling of plant chloroplast and cytoplasmic ribosomes. Plants. 2020;9(7):1–29. doi: 10.3390/plants9070892
   Google Scholar