Cytokinin-Regulated Expression of Genes and Its Implication for the Expression of Chloroplast-Encoded Genes

Overview

Journal Biomolecules

Publisher MDPI

Specialties Biochemistry
Molecular Biology

Date 2020 Dec 16

PMID 33322466

Citations 7

Authors

Aleksandra A Andreeva

Radomira Vankova

Ivan A Bychkov

Natalia V Kudryakova

Maria N Danilova

Jozef Lacek

Elena S Pojidaeva

Victor V Kusnetsov

Affiliations

Soon will be listed here.

Abstract

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 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 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 and 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.

Citing Articles

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Cytokinin biosynthesis in cyanobacteria: Insights for crop improvement.

Uniyal S, Bhandari M, Singh P, Singh R, Tiwari S Front Genet. 2022; 13:933226.

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References

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(2):339-347. PMC: 159204. DOI: 10.1104/pp.104.2.339. View

Yagi Y, Shiina T . Recent advances in the study of chloroplast gene expression and its evolution. Front Plant Sci. 2014; 5:61. PMC: 3933795. DOI: 10.3389/fpls.2014.00061. View

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 U S A. 2012; 109(19):7541-6. PMC: 3358912. DOI: 10.1073/pnas.1119403109. View

Xie M, Chen H, Huang L, ONeil R, Shokhirev M, Ecker J . A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development. Nat Commun. 2018; 9(1):1604. PMC: 5913131. DOI: 10.1038/s41467-018-03921-6. View

Shevtsov S, Nevo-Dinur K, Faigon L, Sultan L, Zmudjak M, Markovits M . Control of organelle gene expression by the mitochondrial transcription termination factor mTERF22 in Arabidopsis thaliana plants. PLoS One. 2018; 13(7):e0201631. PMC: 6066234. DOI: 10.1371/journal.pone.0201631. View

Zhelyazkova P, Sharma C, Forstner K, Liere K, Vogel J, Borner T . The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell. 2012; 24(1):123-36. PMC: 3289561. DOI: 10.1105/tpc.111.089441. View

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(3):582-599. PMC: 5894840. DOI: 10.1105/tpc.17.00947. View

Yamburenko M, Zubo Y, Vankova R, Kusnetsov V, Kulaeva O, Borner T . Abscisic acid represses the transcription of chloroplast genes. J Exp Bot. 2013; 64(14):4491-502. PMC: 3808324. DOI: 10.1093/jxb/ert258. View

Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich C . Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot. 2005; 56(416):1535-44. DOI: 10.1093/jxb/eri148. View

10.

Bhargava A, Clabaugh I, To J, Maxwell B, Chiang Y, Schaller G . Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 2013; 162(1):272-94. PMC: 3641208. DOI: 10.1104/pp.113.217026. View

11.

Steffens N, Galuschka C, Schindler M, Bulow 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(Web Server issue):W397-402. PMC: 1160156. DOI: 10.1093/nar/gki395. View

12.

Cortleven A, Schmulling T . Regulation of chloroplast development and function by cytokinin. J Exp Bot. 2015; 66(16):4999-5013. DOI: 10.1093/jxb/erv132. View

13.

Danilova M, Kudryakova N, Andreeva A, Doroshenko A, Pojidaeva E, Kusnetsov 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. View

14.

MacQuarrie K, Fong A, Morse R, Tapscott S . Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet. 2011; 27(4):141-8. PMC: 3068217. DOI: 10.1016/j.tig.2011.01.001. View

15.

Dobrev P, Vankova R . Quantification of abscisic Acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol Biol. 2012; 913:251-61. DOI: 10.1007/978-1-61779-986-0_17. View

16.

Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M . 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(5):1498-515. PMC: 2899873. DOI: 10.1105/tpc.109.071001. View

17.

He L, Zhang S, Qiu Z, Zhao J, Nie W, Lin H . FRUCTOKINASE-LIKE PROTEIN 1 interacts with TRXz to regulate chloroplast development in rice. J Integr Plant Biol. 2018; 60(2):94-111. DOI: 10.1111/jipb.12631. View

18.

Zubo Y, Blakley I, Franco-Zorrilla J, Yamburenko M, Solano R, Kieber J . Coordination of Chloroplast Development through the Action of the GNC and GLK Transcription Factor Families. Plant Physiol. 2018; 178(1):130-147. PMC: 6130010. DOI: 10.1104/pp.18.00414. View

19.

Brenner W, Schmulling T . Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Front Plant Sci. 2015; 6:29. PMC: 4330702. DOI: 10.3389/fpls.2015.00029. View

20.

Werner T, Schmulling T . Cytokinin action in plant development. Curr Opin Plant Biol. 2009; 12(5):527-38. DOI: 10.1016/j.pbi.2009.07.002. View