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pTAC10, an S1-domain-containing component of the transcriptionally active chromosome complex, is essential for plastid gene expression in Arabidopsis thaliana and is phosphorylated by chloroplast-targeted casein kinase II

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Abstract

In higher plant chloroplasts, the plastid-encoded RNA polymerase (PEP) consists of four catalytic subunits and numerous nuclear-encoded accessory proteins, including pTAC10, an S1-domain-containing protein. In this study, pTAC10 knockout lines were characterized. Two ptac10 mutants had an albino phenotype and severely impaired chloroplast development. The pTAC10 genomic sequence fused to a four-tandem MYC tag driven by its own promoter functionally complemented the ptac10-1 mutant phenotype. pTAC10 was present in both the chloroplast stroma and thylakoids. Two-dimensional blue native polyacrylamide gel electrophoresis (BN-PAGE), and immunoblotting assays showed that pTAC10:MYC co-migrates with one of the PEP core subunits, RpoB. A comprehensive investigation of the plastid gene expression profiles by quantitative RT-PCR revealed that, compared with wild-type plants, the abundance of PEP-dependent plastid transcripts is severely decreased in the ptac10-1 mutant, while the amount of plastid transcripts exclusively transcribed by NEP either barely changes or even increases. RNA blot analysis confirmed that PEP-dependent chloroplast transcripts, including psaB, psbA and rbcL, substantially decrease in the ptac10-1 mutant. Immunoblotting showed reduced accumulation of most chloroplast proteins in the ptac10 mutants. These data indicate the essential role of pTAC10 in plastid gene expression and plastid development. pTAC10 interacts with chloroplast-targeted casein kinase 2 (cpCK2) in vitro and in vivo and can be phosphorylated by Arabidopsis cpCK2 in vitro at sites Ser95, Ser396 and Ser434. RNA-EMSA assays showed that pTAC10 is able to bind to the psbA, atpE and accD transcripts, suggesting a non-specific RNA-binding activity of pTAC10. The RNA affinity of pTAC10 was enhanced by phosphorylation and decreased by the amino acid substitution Ser434-Ala of pTAC10. These data show that pTAC10 is essential for plastid gene expression in Arabidopsis and that it can be phosphorylated by cpCK2.

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Acknowledgements

We thank ABRC Bioresources, which kindly provided the transgenic Arabidopsis lines (CS16115 and CS16140). We would like to thank Prof. CM Lu from IBCAS for the kind donation of RpoB antibody. We appreciate that Prof. XW Sun from SHNU for his help in western blotting. We also thank Prof. Jean-David Rochaix for his help in the language editing of this manuscript. This work was supported by grants from the National Natural Science Foundation of China (31570232 and 31370271) and by the Innovation Program of Shanghai Municipal Education Commission (14YZ066).

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    1. College of Life and Environmental Sciences, Shanghai Normal University, Shanghai, 200234, China

      Qing-Bo Yu, Tuan-Tuan Zhao, Lin-Shan Ye, Ling Cheng, Ying-Qian Wu, Chao Huang & Zhong-Nan Yang

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    Qing-Bo Yu and Tuan-Tuan Zhao have contributed equally to this work.

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    Supplementary Figure 1. Alignment of the amino acid sequences of the pTAC10 orthologs

    . The alignment was generated using ClustalW (Thompson et al., 1994) with default parameters and BoxShade 3.21 (http://www.ch.embnet.org/software/BOX_form.html). The positions of identical and similar sequences are indicated in black and grey boxes, respectively. All the sequences used to build the alignment were obtained from NCBI (http://www.ncbi.nlm.nih.gov/). (PDF 581 KB)

    Supplementary Figure 2. Identification of phosphorylation sites of pTAC10 by CK2 in vitro

    . (A) Phosphorylation sites determined by mass spectrometry are shown. (B) The amino acid sequence around the phosphorylation sites in pTAC10. The phosphoacceptors are indicated by “*”, and the acidic residues at n + 3 are highlighted in grey; (C) An independent phosphorylation analysis of pTAC10. Immunoblot analysis of pTAC10 phosphorylation by cpCK2 in vitro using anti-phospho-Ser, Thr and Tyr antibodies. CK2 was used as positive control. “+” indicates the presence of reagent in the reaction system, and “-” indicates the absence of reagent in the reaction system. “*” indicates the band corresponding to pTAC10. (D) SDS–PAGE analysis of total proteins from unpurified (1) and purified (2) E. coli containing MBP:cpCK2 protein (M) with molecular markers (PageRuler Prestained Protein Ladder, Fermentas) indicated. (JPG 2750 KB)Supplementary material 2 (JPG 843 KB)

    Supplementary Figure 3. Mass spectrometric analyses of phosphorylated peptides from of pTAC10 bycpCK2 in vitro

    . (A) to (C) LC–MS extracted ion chromatograms showing intensities of the phosphorylated peptide signals from the phosphorylated peptide corresponding to the pTAC10 protein. The phosphorylated Ser residue in the peptide sequence is marked with "ph" on the top of the corresponding amino acid. (JPG 1135 KB)Supplementary material 2 (JPG 843 KB)

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    Supplementary material 5 (DOC 113 KB)

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    Yu, QB., Zhao, TT., Ye, LS. et al. pTAC10, an S1-domain-containing component of the transcriptionally active chromosome complex, is essential for plastid gene expression in Arabidopsis thaliana and is phosphorylated by chloroplast-targeted casein kinase II. Photosynth Res 137, 69–83 (2018). https://doi.org/10.1007/s11120-018-0479-y

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