Cytokinins (CKs) are known to regulate the biogenesis of chloroplasts under changing environmental conditions and at different stages of plant ontogenesis. However, the underlying mechanisms are still poorly understood. Apparently, the mechanisms can be duplicated in several ways, including the influence of nuclear genes that determine the expression of plastome through the two-component CK regulatory circuit. In this study, we evaluated the role of cytokinins and CK signaling pathway on the expression of nuclear genes for plastid RNA polymerase-associated proteins (PAPs). Cytokinin induced the expression of all twelve Arabidopsis thalianaPAP genes irrespective of their functions via canonical CK signaling pathway but this regulation might be indirect taking into consideration their different functions and versatile structure of promoter regions. The disruption of PAP genes contributed to the abolishment of positive CK effect on the accumulation of the chloroplast gene transcripts and transcripts of the nuclear genes for plastid transcription machinery as can be judged from the analysis of pap1 and pap6 mutants. However, the CK regulatory circuit in the mutants remained practically unperturbed. Knock-out of PAP genes resulted in cytokinin overproduction as a consequence of the strong up-regulation of the genes for CK synthesis.

Institute of Experimental Botany Czech Academy of Sciences Rozvojova 263 165 02 Prague Czech Republic

Timiryazev Institute of Plant Physiology Russian Academy of Sciences Botanicheskaya 35 127276 Moscow Russia

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Brenner W.G., Ramireddy E., Heyl A., Schmülling T. Gene regulation by cytokinin in Arabidopsis. Front. Plant Sci. 2012;3:8. doi: 10.3389/fpls.2012.00008. PubMed DOI PMC

Bhargava A., Clabaugh I., To J.P., Maxwell B.B., Chiang Y.H., Schaller G.E., Kieber J.J. Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 2013;162:272–294. doi: 10.1104/pp.113.217026. PubMed DOI PMC

Brenner W.G., Schmülling T. Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Front. Plant Sci. 2015;6:29. doi: 10.3389/fpls.2015.00029. PubMed DOI PMC

Rashotte A.M., Mason M.G., Hutchison C.E., Ferreira F.J., Schaller G.E., Kieber J.J. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl. Acad. Sci. USA. 2006;103:11081–11085. doi: 10.1073/pnas.0602038103. PubMed DOI PMC

Cortleven A., Schmülling T. Regulation of chloroplast development and function by cytokinin. J. Exp. Bot. 2015;66:4999–5013. doi: 10.1093/jxb/erv132. PubMed DOI

Zubo Y.O., Blakley I.C., Franco-Zorrilla J.M., Yamburenko M.V., Solano R., Kieber J.J., Schaller G.E. Coordination of chloroplast development through the action of the GNC and GLK transcription factor families. Plant Physiol. 2018;178:130–147. doi: 10.1104/pp.18.00414. PubMed DOI PMC

Chiang Y.H., Zubo Y.O., Tapken W., Kim H.J., Lavanway A.M., Howard L., Schaller G.E. Functional characterization of the GATA transcription factors GNC and CGA1 reveals their key role in chloroplast development, growth, and division in Arabidopsis. Plant Physiol. 2012;160:332–348. doi: 10.1104/pp.112.198705. PubMed DOI PMC

Zhelyazkova P., Sharma C.M., Förstner K.U., Liere K., Vogel J., Börner T. The primary transcriptome of barley chloroplasts: Numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell. 2012;24:123–136. doi: 10.1105/tpc.111.089441. PubMed DOI PMC

Pfannschmidt T., Blanvillain R., Merendino L., Courtois F., Chevalier F., Liebers M., Lerbs-Mache S. Plastid RNA polymerases: Orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. J. Exp. Bot. 2015;66:6957–6973. doi: 10.1093/jxb/erv415. PubMed DOI

Grübler B., Merendino L., Twardziok S.O., Mininno M., Allorent G., Chevalier F., Ravanel S. Light and plastid signals regulate different sets of genes in the albino mutant pap7-1. Plant Physiol. 2017;175:1203–1219. doi: 10.1104/pp.17.00982. PubMed DOI PMC

Yagi Y., Shiina T. Recent advances in the study of chloroplast gene expression and its evolution. Front. Plant Sci. 2014;5:61. doi: 10.3389/fpls.2014.00061. PubMed DOI PMC

Danilova M.N., Kudryakova N.V., Doroshenko A.S., Zabrodin D.A., Rakhmankulova Z.F., Oelmüller R., Kusnetsov V.V. Opposite roles of the Arabidopsis cytokinin receptors AHK2 and AHK3 in the expression of plastid genes and genes for the plastid transcriptional machinery during senescence. Plant Mol. Biol. 2017;93:533–546. doi: 10.1007/s11103-016-0580-6. PubMed DOI

Bastakis E., Hedtke B., Klermund C., Grimm B., Schwechheimer C. LLM-domain B-GATA transcription factors play multifaceted roles in controlling greening in Arabidopsis. Plant Cell. 2018;30:582–599. doi: 10.1105/tpc.17.00947. PubMed DOI PMC

Borsellino L. Ph.D. Thesis. Humbolt Universität zu Berlin; Berlin, Germany: 2012. Influence of Light and Cytokinin on Organellar Phage-Type RNA Polymerase Transcript Levels and Transcription of Organellar Genes in Arabidopsis thaliana.

Liebers M., Chevalier F., Blanvillain R., Pfannschmidt T. PAP genes are tissue-and cell-specific markers of chloroplast development. Planta. 2018;248:629–646. doi: 10.1007/s00425-018-2924-8. PubMed DOI

Dobrev P.I., Kamınek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J. Chromatogr. A. 2002;950:21–29. doi: 10.1016/S0021-9673(02)00024-9. PubMed DOI

Dobrev P.I., Vankova R. Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol. Biol. 2012;913:251–261. PubMed

Steffens N.O., Galuschka C., Schindler M., Bülow L., Hehl R. AthaMap web tools for database-assisted identification of combinatorial cis-regulatory elements and the display of highly conserved transcription factor binding sites in Arabidopsis thaliana. Nucleic Acids Res. 2005;33:397–402. doi: 10.1093/nar/gki395. PubMed DOI PMC

Yagi Y., Ishizaki Y., Nakahira Y., Tozawa Y., Shiina T. Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase. Proc. Natl. Acad. Sci. USA. 2012;109:7541–7546. doi: 10.1073/pnas.1119403109. PubMed DOI PMC

Gilkerson J., Perez-Ruiz J.M., Chory J., Callis J. The plastid-localized pfkB-type carbohydrate kinases fructokinase-like 1 and 2 are essential for growth and development of Arabidopsis thaliana. BMC Plant Biol. 2012;12:1–17. doi: 10.1186/1471-2229-12-102. PubMed DOI PMC

Danilova M.N., Kudryakova N.V., Andreeva A.A., Doroshenko A.S., Pojidaeva E.S., Kusnetsov V.V. Differential impact of heat stress on the expression of chloroplast-encoded genes. Plant Physiol. Biochem. 2018;129:90–100. doi: 10.1016/j.plaphy.2018.05.023. PubMed DOI

He L., Zhang S., Qiu Z., Zhao J., Nie W., Lin H., Zhu L. FRUCTOKINASE-LIKE PROTEIN 1 interacts with TRXz to regulate chloroplast development in rice. J. Integr. Plant Biol. 2018;60:94–111. doi: 10.1111/jipb.12631. PubMed DOI

Werner T., Schmuülling T. Cytokinin action in plant development. Curr. Opin. Plant Biol. 2009;12:527–538. doi: 10.1016/j.pbi.2009.07.002. PubMed DOI

Aloni R., Langhans M., Aloni E., Dreieicher E., Ullrich C.I. Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J. Exp. Bot. 2005;56:1535–1544. doi: 10.1093/jxb/eri148. PubMed DOI

Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowska D., Kakimoto T. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. USA. 2006;103:16598–16603. doi: 10.1073/pnas.0603522103. PubMed DOI PMC

Werner T., Motyka V., Laucou V., Smets R., Van Onckelen H., Schmülling T. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 2003;15:2532–2550. doi: 10.1105/tpc.014928. PubMed DOI PMC

Ha S., Vankova R., Yamaguchi-Shinozaki K., Shinozaki K., Tran L.S.P. Cytokinins: Metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 2012;17:172–179. doi: 10.1016/j.tplants.2011.12.005. PubMed DOI

Chang S.H., Lee S., Um T.Y., Kim J.K., Do Choi Y., Jang G. pTAC10, a key subunit of plastid-encoded RNA polymerase, promotes chloroplast development. Plant Physiol. 2017;174:435–449. doi: 10.1104/pp.17.00248. PubMed DOI PMC

Arsova B., Hoja U., Wimmelbacher M., Greiner E., Üstün Ş., Melzer M., Börnke F. Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: Evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell. 2010;22:1498–1515. doi: 10.1105/tpc.109.071001. PubMed DOI PMC

Kusnetsov V.V., Oelmüller R., Sarwat M.I., Porfirova S.A., Cherepneva G.N., Herrmann R.G., Kulaeva O.N. Cytokinins, abscisic acid and light affect accumulation of chloroplast proteins in Lupinus luteus cotyledons without notable effect on steady-state mRNA levels. Planta. 1994;194:318–327. doi: 10.1007/BF00197531. DOI

Shevtsov S., Nevo-Dinur K., Faigon L., Sultan L.D., Zmudjak M., Markovits M., Ostersetzer-Biran O. Control of organelle gene expression by the mitochondrial transcription termination factor mTERF22 in Arabidopsis thaliana plants. PLoS ONE. 2018;13:e0201631. doi: 10.1371/journal.pone.0201631. PubMed DOI PMC

Yamburenko M.V., Zubo Y.O., Vanková R., Kusnetsov V.V., Kulaeva O.N., Börner Th. Abscisic acid represses the transcription of chloroplast genes. J. Exp. Bot. 2013;64:4491–4502. doi: 10.1093/jxb/ert258. PubMed DOI PMC

Xie M., Chen H., Huang L., O’Neil R.C., Shokhirev M.N., Ecker J.R. A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development. Nat. Commun. 2018;9:1604. doi: 10.1038/s41467-018-03921-6. PubMed DOI PMC

MacQuarrie K.L., Fong A.P., Morse R.H., Tapscott S.J. Genome-wide transcription factor binding: Beyond direct target regulation. Trends Genet. 2011;27:141–148. doi: 10.1016/j.tig.2011.01.001. PubMed DOI PMC

Zhang H., He H., Wang X., Wang X., Yang X., Li L., Deng X.W. Genome-wide mapping of the HY5-mediated genenetworks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J. 2011;65:346–358. doi: 10.1111/j.1365-313X.2010.04426.x. PubMed DOI

Doroshenko A.S., Danilova M.N., Andreeva A.A., Kudryakova N.V., Kuznetsov V.V., Kusnetsov V.V. The Transcription Factor HY5 Is Involved in the Cytokinin-Dependent Regulation of the Expression of Genes Encoding Proteins Associated with Bacterial Plastid RNA-Polymerase during De-Etiolation of Arabidopsis thaliana. Dokl. Biochem. Biophys. 2020;492:124–129. doi: 10.1134/S1607672920020076. PubMed DOI

Kulaeva O.N., Burkhanova E.A., Karavaiko N.N., Selivankina S.Y., Porfirova S.A., Maslova G.G., Börner T. Chloroplasts affect the leaf response to cytokinin. J. Plant. Physiol. 2002;159:1309–1316. doi: 10.1078/0176-1617-00761. DOI

Chory J., Reinecke D., Sim S., Washburn T., Brenner M. A role for cytokinins in de-etiolation in Arabidopsis (det mutants have an altered response to cytokinins) Plant. Physiol. 1994;104:339–347. doi: 10.1104/pp.104.2.339. PubMed DOI PMC

Burman N., Khurana J.P. Plastid Development in Leaves during Growth and Senescence. Springer; Dordrecht, The Netherlands: 2013. Photoregulation of Chloroplast Development: Retrograde Signaling; pp. 569–588.

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