Telomerase, an essential enzyme that maintains chromosome ends, is important for genome integrity and organism development. Various hypotheses have been proposed in human, ciliate and yeast systems to explain the coordination of telomerase holoenzyme assembly and the timing of telomerase performance at telomeres during DNA replication or repair. However, a general model is still unclear, especially pathways connecting telomerase with proposed non-telomeric functions. To strengthen our understanding of telomerase function during its intracellular life, we report on interactions of several groups of proteins with the Arabidopsis telomerase protein subunit (AtTERT) and/or a component of telomerase holoenzyme, POT1a protein. Among these are the nucleosome assembly proteins (NAP) and the minichromosome maintenance (MCM) system, which reveal new insights into the telomerase interaction network with links to telomere chromatin assembly and replication. A targeted investigation of 176 candidate proteins demonstrated numerous interactions with nucleolar, transport and ribosomal proteins, as well as molecular chaperones, shedding light on interactions during telomerase biogenesis. We further identified protein domains responsible for binding and analyzed the subcellular localization of these interactions. Moreover, additional interaction networks of NAP proteins and the DOMINO1 protein were identified. Our data support an image of functional telomerase contacts with multiprotein complexes including chromatin remodeling and cell differentiation pathways.

Department of Cell Biology and Radiobiology Institute of Biophysics of the Czech Academy of Sciences CZ 61265 Brno Czech Republic

Mendel Centre for Plant Genomics and Proteomics Central European Institute of Technology Masaryk University CZ 62500 Brno Czech Republic

National Centre for Biomolecular Research Faculty of Science Masaryk University CZ 61137 Brno Czech Republic

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Chan H., Wang Y., Feigon J. Progress in Human and Tetrahymena Telomerase Structure Determination. Annu. Rev. Biophys. 2017;46:199–225. doi: 10.1146/annurev-biophys-062215-011140. PubMed DOI PMC

Schmidt J.C., Cech T.R. Human telomerase: Biogenesis, trafficking, recruitment, and activation. Genes Dev. 2015;29:1095–1105. doi: 10.1101/gad.263863.115. PubMed DOI PMC

Wellinger R.J., Zakian V.A. Everything you ever wanted to know about Saccharomyces cerevisiae telomeres: Beginning to end. Genetics. 2012;191:1073–1105. doi: 10.1534/genetics.111.137851. PubMed DOI PMC

Jeong S.A., Kim K., Lee J.H., Cha J.S., Khadka P., Cho H.S., Chung I.K. Akt-mediated phosphorylation increases the binding affinity of hTERT for importin alpha to promote nuclear translocation. J. Cell Sci. 2015;128:2951. doi: 10.1242/jcs.176453. PubMed DOI

Jeong Y.Y., Her J., Oh S.Y., Chung I.K. Hsp90-binding immunophilin FKBP52 modulates telomerase activity by promoting the cytoplasmic retrotransport of hTERT. Biochem. J. 2016;473:3517–3532. doi: 10.1042/BCJ20160344. PubMed DOI

Fitzgerald M.S., Riha K., Gao F., Ren S., McKnight T.D., Shippen D.E. Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc. Natl. Acad. Sci. USA. 1999;96:14813–14818. doi: 10.1073/pnas.96.26.14813. PubMed DOI PMC

Fajkus P., Peska V., Zavodnik M., Fojtova M., Fulneckova J., Dobias S., Kilar A., Dvorackova M., Zachova D., Necasova I., et al. Telomerase RNAs in land plants. Nucleic Acids Res. 2019;47:9842–9856. doi: 10.1093/nar/gkz695. PubMed DOI PMC

Greider C.W. Regulating telomere length from the inside out: The replication fork model. Genes Dev. 2016;30:1483–1491. doi: 10.1101/gad.280578.116. PubMed DOI PMC

Pennock E., Buckley K., Lundblad V. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell. 2001;104:387–396. doi: 10.1016/S0092-8674(01)00226-4. PubMed DOI

Nandakumar J., Bell C.F., Weidenfeld I., Zaug A.J., Leinwand L.A., Cech T.R. The TEL patch of telomere protein TPP1 mediates telomerase recruitment and processivity. Nature. 2012;492:285–289. doi: 10.1038/nature11648. PubMed DOI PMC

De Lange T. How telomeres solve the end-protection problem. Science. 2009;326:948–952. doi: 10.1126/science.1170633. PubMed DOI PMC

Majerska J., Schrumpfova P.P., Dokladal L., Schorova S., Stejskal K., Oboril M., Honys D., Kozakova L., Polanska P.S., Sykorova E. Tandem affinity purification of AtTERT reveals putative interaction partners of plant telomerase in vivo. Protoplasma. 2017;254:1547–1562. doi: 10.1007/s00709-016-1042-3. PubMed DOI

Rossignol P., Collier S., Bush M., Shaw P., Doonan J.H. Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase. J. Cell Sci. 2007;120:3678–3687. doi: 10.1242/jcs.004119. PubMed DOI

Surovtseva Y.V., Shakirov E.V., Vespa L., Osbun N., Song X., Shippen D.E. Arabidopsis POT1 associates with the telomerase RNP and is required for telomere maintenance. EMBO J. 2007;26:3653–3661. doi: 10.1038/sj.emboj.7601792. PubMed DOI PMC

Schrumpfova P.P., Vychodilova I., Dvorackova M., Majerska J., Dokladal L., Schorova S., Fajkus J. Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase. Plant J. 2014;77:770–781. doi: 10.1111/tpj.12428. PubMed DOI PMC

Romaniuk A., Paszel-Jaworska A., Toton E., Lisiak N., Holysz H., Krolak A., Grodecka-Gazdecka S., Rubis B. The non-canonical functions of telomerase: To turn off or not to turn off. Mol. Biol. Rep. 2019;46:1401–1411. doi: 10.1007/s11033-018-4496-x. PubMed DOI

Blackburn E.H., Epel E.S., Lin J. Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science. 2015;350:1193–1198. doi: 10.1126/science.aab3389. PubMed DOI

Saretzki G. Extra-telomeric functions of human telomerase: Cancer, mitochondria and oxidative stress. Curr. Pharm. Des. 2014;20:6386–6403. doi: 10.2174/1381612820666140630095606. PubMed DOI

Lin K.W., McDonald K.R., Guise A.J., Chan A., Cristea I.M., Zakian V.A. Proteomics of yeast telomerase identified Cdc48-Npl4-Ufd1 and Ufd4 as regulators of Est1 and telomere length. Nat. Commun. 2015;6:8290. doi: 10.1038/ncomms9290. PubMed DOI PMC

Fu D., Collins K. Purification of human telomerase complexes identifies factors involved in telomerase biogenesis and telomere length regulation. Mol. Cell. 2007;28:773–785. doi: 10.1016/j.molcel.2007.09.023. PubMed DOI PMC

Ungar L., Yosef N., Sela Y., Sharan R., Ruppin E., Kupiec M. A genome-wide screen for essential yeast genes that affect telomere length maintenance. Nucleic Acids Res. 2009;37:3840–3849. doi: 10.1093/nar/gkp259. PubMed DOI PMC

Zachova D., Fojtova M., Dvorackova M., Mozgova I., Lermontova I., Peska V., Schubert I., Fajkus J., Sykorova E. Structure-function relationships during transgenic telomerase expression in Arabidopsis. Physiol. Plant. 2013;149:114–126. doi: 10.1111/ppl.12021. PubMed DOI

Dokladal L., Benkova E., Honys D., Duplakova N., Lee L.Y., Gelvin S.B., Sykorova E. An armadillo-domain protein participates in a telomerase interaction network. Plant Mol. Biol. 2018;97:407–420. doi: 10.1007/s11103-018-0747-4. PubMed DOI

Schrumpfova P.P., Fajkus J. Composition and Function of Telomerase-A Polymerase Associated with the Origin of Eukaryotes. Biomolecules. 2020;10:1425. doi: 10.3390/biom10101425. PubMed DOI PMC

Gao J., Zhu Y., Zhou W., Molinier J., Dong A., Shen W.H. NAP1 family histone chaperones are required for somatic homologous recombination in Arabidopsis. Plant Cell. 2012;24:1437–1447. doi: 10.1105/tpc.112.096792. PubMed DOI PMC

Kolarova K., Nespor Dadejova M., Loja T., Lochmanova G., Sykorova E., Dvorackova M. Disruption of NAP1 genes in Arabidopsis thaliana suppresses the fas1 mutant phenotype, enhances genome stability and changes chromatin compaction. Plant J. 2021;106:56–73. doi: 10.1111/tpj.15145. PubMed DOI

Zhou W., Gao J., Ma J., Cao L., Zhang C., Zhu Y., Dong A., Shen W.H. Distinct roles of the histone chaperones NAP1 and NRP and the chromatin-remodeling factor INO80 in somatic homologous recombination in Arabidopsis thaliana. Plant J. 2016;88:397–410. doi: 10.1111/tpj.13256. PubMed DOI

Charbonnel C., Rymarenko O., Da Ines O., Benyahya F., White C.I., Butter F., Amiard S. The Linker Histone GH1-HMGA1 Is Involved in Telomere Stability and DNA Damage Repair. Plant Physiol. 2018;177:311–327. doi: 10.1104/pp.17.01789. PubMed DOI PMC

Bieluszewski T., Galganski L., Sura W., Bieluszewska A., Abram M., Ludwikow A., Ziolkowski P.A., Sadowski J. AtEAF1 is a potential platform protein for Arabidopsis NuA4 acetyltransferase complex. BMC Plant Biol. 2015;15:75. doi: 10.1186/s12870-015-0461-1. PubMed DOI PMC

Sacharowski S.P., Gratkowska D.M., Sarnowska E.A., Kondrak P., Jancewicz I., Porri A., Bucior E., Rolicka A.T., Franzen R., Kowalczyk J., et al. SWP73 Subunits of Arabidopsis SWI/SNF Chromatin Remodeling Complexes Play Distinct Roles in Leaf and Flower Development. Plant Cell. 2015;27:1889–1906. doi: 10.1105/tpc.15.00233. PubMed DOI PMC

Liu Z., Zhu Y., Gao J., Yu F., Dong A., Shen W.H. Molecular and reverse genetic characterization of NUCLEOSOME ASSEMBLY PROTEIN1 (NAP1) genes unravels their function in transcription and nucleotide excision repair in Arabidopsis thaliana. Plant J. 2009;59:27–38. doi: 10.1111/j.1365-313X.2009.03844.x. PubMed DOI

Liu Z.Q., Gao J., Dong A.W., Shen W.H. A truncated Arabidopsis NUCLEOSOME ASSEMBLY PROTEIN 1, AtNAP1;3T, alters plant growth responses to abscisic acid and salt in the Atnap1;3-2 mutant. Mol. Plant. 2009;2:688–699. doi: 10.1093/mp/ssp026. PubMed DOI

Schorova S., Fajkus J., Zaveska Drabkova L., Honys D., Schrumpfova P.P. The plant Pontin and Reptin homologues, RuvBL1 and RuvBL2a, colocalize with TERT and TRB proteins in vivo, and participate in telomerase biogenesis. Plant J. 2019;98:195–212. doi: 10.1111/tpj.14306. PubMed DOI

Mozgova I., Mokros P., Fajkus J. Dysfunction of chromatin assembly factor 1 induces shortening of telomeres and loss of 45S rDNA in Arabidopsis thaliana. Plant Cell. 2010;22:2768–2780. doi: 10.1105/tpc.110.076182. PubMed DOI PMC

Jaske K., Mokros P., Mozgova I., Fojtova M., Fajkus J. A telomerase-independent component of telomere loss in chromatin assembly factor 1 mutants of Arabidopsis thaliana. Chromosoma. 2013;122:285–293. doi: 10.1007/s00412-013-0400-6. PubMed DOI

Van Leene J., Hollunder J., Eeckhout D., Persiau G., Van De Slijke E., Stals H., Van Isterdael G., Verkest A., Neirynck S., Buffel Y., et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010;6:397. doi: 10.1038/msb.2010.53. PubMed DOI PMC

Takahashi N., Quimbaya M., Schubert V., Lammens T., Vandepoele K., Schubert I., Matsui M., Inze D., Berx G., De Veylder L. The MCM-binding protein ETG1 aids sister chromatid cohesion required for postreplicative homologous recombination repair. PLoS Genet. 2010;6:e1000817. doi: 10.1371/journal.pgen.1000817. PubMed DOI PMC

Tuteja N., Tran N.Q., Dang H.Q., Tuteja R. Plant MCM proteins: Role in DNA replication and beyond. Plant Mol. Biol. 2011;77:537–545. doi: 10.1007/s11103-011-9836-3. PubMed DOI

Froelich C.A., Kang S., Epling L.B., Bell S.P., Enemark E.J. A conserved MCM single-stranded DNA binding element is essential for replication initiation. eLife. 2014;3:e01993. doi: 10.7554/eLife.01993. PubMed DOI PMC

Li N., Zhai Y., Zhang Y., Li W., Yang M., Lei J., Tye B.K., Gao N. Structure of the eukaryotic MCM complex at 3.8 A. Nature. 2015;524:186–191. doi: 10.1038/nature14685. PubMed DOI

Lycka M., Peska V., Demko M., Spyroglou I., Kilar A., Fajkus J., Fojtova M. WALTER: An easy way to online evaluate telomere lengths from terminal restriction fragment analysis. BMC Bioinform. 2021;22:145. doi: 10.1186/s12859-021-04064-0. PubMed DOI PMC

Forsburg S.L. Eukaryotic MCM proteins: Beyond replication initiation. Microbiol. Mol. Biol. Rev. 2004;68:109–131. doi: 10.1128/MMBR.68.1.109-131.2004. PubMed DOI PMC

Drissi R., Dubois M.L., Douziech M., Boisvert F.M. Quantitative Proteomics Reveals Dynamic Interactions of the Minichromosome Maintenance Complex (MCM) in the Cellular Response to Etoposide Induced DNA Damage. Mol. Cell. Proteom. 2015;14:2002–2013. doi: 10.1074/mcp.M115.048991. PubMed DOI PMC

Dubois M.L., Bastin C., Levesque D., Boisvert F.M. Comprehensive Characterization of Minichromosome Maintenance Complex (MCM) Protein Interactions Using Affinity and Proximity Purifications Coupled to Mass Spectrometry. J. Proteome Res. 2016;15:2924–2934. doi: 10.1021/acs.jproteome.5b01081. PubMed DOI

Osman K., Yang J., Roitinger E., Lambing C., Heckmann S., Howell E., Cuacos M., Imre R., Durnberger G., Mechtler K., et al. Affinity proteomics reveals extensive phosphorylation of the Brassica chromosome axis protein ASY1 and a network of associated proteins at prophase I of meiosis. Plant J. 2018;93:17–33. doi: 10.1111/tpj.13752. PubMed DOI PMC

Takashi Y., Kobayashi Y., Tanaka K., Tamura K. Arabidopsis replication protein A 70a is required for DNA damage response and telomere length homeostasis. Plant Cell Physiol. 2009;50:1965–1976. doi: 10.1093/pcp/pcp140. PubMed DOI

Aklilu B.B., Peurois F., Saintome C., Culligan K.M., Kobbe D., Leasure C., Chung M., Cattoor M., Lynch R., Sampson L., et al. Functional Diversification of Replication Protein A Paralogs and Telomere Length Maintenance in Arabidopsis. Genetics. 2020;215:989–1002. doi: 10.1534/genetics.120.303222. PubMed DOI PMC

Huang H., Stromme C.B., Saredi G., Hodl M., Strandsby A., Gonzalez-Aguilera C., Chen S., Groth A., Patel D.J. A unique binding mode enables MCM2 to chaperone histones H3-H4 at replication forks. Nat. Struct. Mol. Biol. 2015;22:618–626. doi: 10.1038/nsmb.3055. PubMed DOI PMC

Carrie C., Whelan J. Widespread dual targeting of proteins in land plants: When, where, how and why. Plant Signal. Behav. 2013;8:644–662. doi: 10.4161/psb.25034. PubMed DOI PMC

Edmondson A.C., Song D., Alvarez L.A., Wall M.K., Almond D., McClellan D.A., Maxwell A., Nielsen B.L. Characterization of a mitochondrially targeted single-stranded DNA-binding protein in Arabidopsis thaliana. Mol. Genet. Genom. 2005;273:115–122. doi: 10.1007/s00438-004-1106-5. PubMed DOI

Nelson B.K., Cai X., Nebenfuhr A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007;51:1126–1136. doi: 10.1111/j.1365-313X.2007.03212.x. PubMed DOI

Yoo H.H., Kwon C., Lee M.M., Chung I.K. Single-stranded DNA binding factor AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J. 2007;49:442–451. doi: 10.1111/j.1365-313X.2006.02974.x. PubMed DOI

Palm D., Simm S., Darm K., Weis B.L., Ruprecht M., Schleiff E., Scharf C. Proteome distribution between nucleoplasm and nucleolus and its relation to ribosome biogenesis in Arabidopsis thaliana. RNA Biol. 2016;13:441–454. doi: 10.1080/15476286.2016.1154252. PubMed DOI PMC

Farmer L.M., Book A.J., Lee K.H., Lin Y.L., Fu H., Vierstra R.D. The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis. Plant Cell. 2010;22:124–142. doi: 10.1105/tpc.109.072660. PubMed DOI PMC

Qi Y., Tsuda K., Nguyen le V., Wang X., Lin J., Murphy A.S., Glazebrook J., Thordal-Christensen H., Katagiri F. Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J. Biol. Chem. 2011;286:31297–31307. doi: 10.1074/jbc.M110.211615. PubMed DOI PMC

Koroleva O.A., Calder G., Pendle A.F., Kim S.H., Lewandowska D., Simpson C.G., Jones I.M., Brown J.W., Shaw P.J. Dynamic behavior of Arabidopsis eIF4A-III, putative core protein of exon junction complex: Fast relocation to nucleolus and splicing speckles under hypoxia. Plant Cell. 2009;21:1592–1606. doi: 10.1105/tpc.108.060434. PubMed DOI PMC

Gong Z., Dong C.H., Lee H., Zhu J., Xiong L., Gong D., Stevenson B., Zhu J.K. A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell. 2005;17:256–267. doi: 10.1105/tpc.104.027557. PubMed DOI PMC

Palm D., Streit D., Shanmugam T., Weis B.L., Ruprecht M., Simm S., Schleiff E. Plant-specific ribosome biogenesis factors in Arabidopsis thaliana with essential function in rRNA processing. Nucleic Acids Res. 2019;47:1880–1895. doi: 10.1093/nar/gky1261. PubMed DOI PMC

Reichel M., Liao Y., Rettel M., Ragan C., Evers M., Alleaume A.M., Horos R., Hentze M.W., Preiss T., Millar A.A. In Planta Determination of the mRNA-Binding Proteome of Arabidopsis Etiolated Seedlings. Plant Cell. 2016;28:2435–2452. doi: 10.1105/tpc.16.00562. PubMed DOI PMC

Naprstkova A., Malinska K., Zaveska Drabkova L., Billey E., Naprstkova D., Sykorova E., Bousquet-Antonelli C., Honys D. Characterization of ALBA Family Expression and Localization in Arabidopsis thaliana Generative Organs. Int. J. Mol. Sci. 2021;22:1652. doi: 10.3390/ijms22041652. PubMed DOI PMC

Lahmy S., Guilleminot J., Cheng C.M., Bechtold N., Albert S., Pelletier G., Delseny M., Devic M. DOMINO1, a member of a small plant-specific gene family, encodes a protein essential for nuclear and nucleolar functions. Plant J. 2004;39:809–820. doi: 10.1111/j.1365-313X.2004.02166.x. PubMed DOI

Witkin K.L., Collins K. Holoenzyme proteins required for the physiological assembly and activity of telomerase. Genes Dev. 2004;18:1107–1118. doi: 10.1101/gad.1201704. PubMed DOI PMC

Dona M., Mittelsten Scheid O. DNA Damage Repair in the Context of Plant Chromatin. Plant Physiol. 2015;168:1206–1218. doi: 10.1104/pp.15.00538. PubMed DOI PMC

Fleurdepine S., Deragon J.M., Devic M., Guilleminot J., Bousquet-Antonelli C. A bona fide La protein is required for embryogenesis in Arabidopsis thaliana. Nucleic Acids Res. 2007;35:3306–3321. doi: 10.1093/nar/gkm200. PubMed DOI PMC

Fojtova M., Peska V., Dobsakova Z., Mozgova I., Fajkus J., Sykorova E. Molecular analysis of T-DNA insertion mutants identified putative regulatory elements in the AtTERT gene. J. Exp. Bot. 2011;62:5531–5545. doi: 10.1093/jxb/err235. PubMed DOI PMC

Perea-Resa C., Hernandez-Verdeja T., Lopez-Cobollo R., del Mar Castellano M., Salinas J. LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell. 2012;24:4930–4947. doi: 10.1105/tpc.112.103697. PubMed DOI PMC

Kandasamy M.K., Deal R.B., McKinney E.C., Meagher R.B. Silencing the nuclear actin-related protein AtARP4 in Arabidopsis has multiple effects on plant development, including early flowering and delayed floral senescence. Plant J. 2005;41:845–858. doi: 10.1111/j.1365-313X.2005.02345.x. PubMed DOI

Renfrew K.B., Song X., Lee J.R., Arora A., Shippen D.E. POT1a and components of CST engage telomerase and regulate its activity in Arabidopsis. PLoS Genet. 2014;10:e1004738. doi: 10.1371/journal.pgen.1004738. PubMed DOI PMC

Galati A., Micheli E., Cacchione S. Chromatin structure in telomere dynamics. Front. Oncol. 2013;3:46. doi: 10.3389/fonc.2013.00046. PubMed DOI PMC

Gentry M., Hennig L. Remodelling chromatin to shape development of plants. Exp. Cell Res. 2014;321:40–46. doi: 10.1016/j.yexcr.2013.11.010. PubMed DOI

Ghanim G.E., Fountain A.J., van Roon A.M., Rangan R., Das R., Collins K., Nguyen T.H.D. Structure of human telomerase holoenzyme with bound telomeric DNA. Nature. 2021;593:449–453. doi: 10.1038/s41586-021-03415-4. PubMed DOI PMC

Chuang H.W., Feng J.H., Feng Y.L., Wei M.J. An Arabidopsis WDR protein coordinates cellular networks involved in light, stress response and hormone signals. Plant Sci. 2015;241:23–31. doi: 10.1016/j.plantsci.2015.09.024. PubMed DOI

Trigg S.A., Garza R.M., MacWilliams A., Nery J.R., Bartlett A., Castanon R., Goubil A., Feeney J., O’Malley R., Huang S.C., et al. CrY2H-seq: A massively multiplexed assay for deep-coverage interactome mapping. Nat. Methods. 2017;14:819–825. doi: 10.1038/nmeth.4343. PubMed DOI PMC

Efroni I., Han S.K., Kim H.J., Wu M.F., Steiner E., Birnbaum K.D., Hong J.C., Eshed Y., Wagner D. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev. Cell. 2013;24:438–445. doi: 10.1016/j.devcel.2013.01.019. PubMed DOI PMC

Kummari D., Palakolanu S.R., Kishor P.B.K., Bhatnagar-Mathur P., Singam P., Vadez V., Sharma K.K. An update and perspectives on the use of promoters in plant genetic engineering. J. Biosci. 2020;45:119. doi: 10.1007/s12038-020-00087-6. PubMed DOI

Lee L.Y., Wu F.H., Hsu C.T., Shen S.C., Yeh H.Y., Liao D.C., Fang M.J., Liu N.T., Yen Y.C., Dokladal L., et al. Screening a cDNA library for protein-protein interactions directly in planta. Plant Cell. 2012;24:1746–1759. doi: 10.1105/tpc.112.097998. PubMed DOI PMC

Citovsky V., Lee L.Y., Vyas S., Glick E., Chen M.H., Vainstein A., Gafni Y., Gelvin S.B., Tzfira T. Subcellular localization of interacting proteins by bimolecular fluorescence complementation in planta. J. Mol. Biol. 2006;362:1120–1131. doi: 10.1016/j.jmb.2006.08.017. PubMed DOI

Heinekamp T., Kuhlmann M., Lenk A., Strathmann A., Droge-Laser W. The tobacco bZIP transcription factor BZI-1 binds to G-box elements in the promoters of phenylpropanoid pathway genes in vitro, but it is not involved in their regulation in vivo. Mol. Genet. Genom. 2002;267:16–26. doi: 10.1007/s00438-001-0636-3. PubMed DOI

Curtis M.D., Grossniklaus U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 2003;133:462–469. doi: 10.1104/pp.103.027979. PubMed DOI PMC

Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003;301:653–657. doi: 10.1126/science.1086391. PubMed DOI

Sessions A., Burke E., Presting G., Aux G., McElver J., Patton D., Dietrich B., Ho P., Bacwaden J., Ko C., et al. A high-throughput Arabidopsis reverse genetics system. Plant Cell. 2002;14:2985–2994. doi: 10.1105/tpc.004630. PubMed DOI PMC

Rosso M.G., Li Y., Strizhov N., Reiss B., Dekker K., Weisshaar B. An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 2003;53:247–259. doi: 10.1023/B:PLAN.0000009297.37235.4a. PubMed DOI

Brunaud V., Balzergue S., Dubreucq B., Aubourg S., Samson F., Chauvin S., Bechtold N., Cruaud C., DeRose R., Pelletier G., et al. T-DNA integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep. 2002;3:1152–1157. doi: 10.1093/embo-reports/kvf237. PubMed DOI PMC

Liu Q., Wang J., Miki D., Xia R., Yu W., He J., Zheng Z., Zhu J.K., Gong Z. DNA replication factor C1 mediates genomic stability and transcriptional gene silencing in Arabidopsis. Plant Cell. 2010;22:2336–2352. doi: 10.1105/tpc.110.076349. PubMed DOI PMC

Ni D.A., Sozzani R., Blanchet S., Domenichini S., Reuzeau C., Cella R., Bergounioux C., Raynaud C. The Arabidopsis MCM2 gene is essential to embryo development and its over-expression alters root meristem function. New Phytol. 2009;184:311–322. doi: 10.1111/j.1469-8137.2009.02961.x. PubMed DOI

Herridge R.P., Day R.C., Macknight R.C. The role of the MCM2-7 helicase complex during Arabidopsis seed development. Plant Mol. Biol. 2014;86:69–84. doi: 10.1007/s11103-014-0213-x. PubMed DOI

Andreuzza S., Li J., Guitton A.E., Faure J.E., Casanova S., Park J.S., Choi Y., Chen Z., Berger F. DNA LIGASE I exerts a maternal effect on seed development in Arabidopsis thaliana. Development. 2010;137:73–81. doi: 10.1242/dev.041020. PubMed DOI

Griffith M.E., Mayer U., Capron A., Ngo Q.A., Surendrarao A., McClinton R., Jurgens G., Sundaresan V. The TORMOZ gene encodes a nucleolar protein required for regulated division planes and embryo development in Arabidopsis. Plant Cell. 2007;19:2246–2263. doi: 10.1105/tpc.106.042697. PubMed DOI PMC

Fojtova M., Fajkus P., Polanska P., Fajkus J. Terminal Restriction Fragments (TRF) Method to Analyze Telomere Lengths. Bio-protocols. 2015;5:e1671. doi: 10.21769/BioProtoc.1671. DOI

Wan X., Wang W., Liu J., Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med. Res. Methodol. 2014;14:135. doi: 10.1186/1471-2288-14-135. PubMed DOI PMC

Higgins J.P.T., Thomas J., Chandler J., Cumpston M., Li T., Page M.J., Welch W.A., editors. Cochrane Handbook for Systematic Reviews of Interventions. 2nd ed. John Wiley & Sons; Chichester, UK: 2019.

Histone Chaperone Deficiency in Arabidopsis Plants Triggers Adaptive Epigenetic Changes in Histone Variants and Modifications