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Heterologous expression of Chrysanthemum nankingense TCP13 suppresses leaf development in Arabidopsis thaliana

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Abstract

TCP genes encode plant-specific transcription factors in various species that they play important roles in plant growth and development. In the present study, we cloned the TCP transcription factor, TCP13, from Chrysanthemum nankingense (CnTCP13). CnTCP13 belongs to the class II CIN subfamily of the TCP family and harbors an atypical basic-helix-loop-helix motif, that was preferentially expressed in the leaf. CnTCP13 transcription was significantly inhibited 24 h after exogenous application of 6-BA. The CnTCP13 protein was localized in the nuclei of transformed onion epidermal cells and did not exhibit transcriptional activation. Heterologous expression of CnTCP13 in Arabidopsis thaliana reduced leaf size. qRT-PCR analysis revealed that the transcription levels of cell division-related genes were altered in transgenic A. thaliana containing CnTCP13. CnTCP2 and CnF-box were identified as putative interaction proteins of CnTCP13 by a yeast two-hybrid assay and bimolecular fluorescence complementation. CnF-box belongs to the F-box family and is abundantly expressed in roots. The CnF-box protein was localized in the nucleus and had no transcriptional activation. In A. thaliana, CnF-box overexpression led to strong crinkling of leaves. Taken together, CnTCP13 is involved in leaf development through the regulation of cell division-related genes, and likely by its interaction with CnTCP2 and CnF-box.

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Acknowledgements

This research was supported by the National Key Research and Development Program of China (2018YFD1000401), the National Natural Science Foundation of China (31,872,149), the Natural Science Fund of Qinghai Province, China (2018-HZ-819), A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.

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  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Landscaping, Ministry of Agriculture and Rural Affairs. Key Laboratory of Biology of Ornamental Plants in East China, National Forestry and Grassland Administration, College of Horticulture, Nanjing Agricultural University, Weigang No. 1, Nanjing, 210095, Jiangsu, China

    Xiangyu Qi, Yixin Qu, Jiafu Jiang, Yunxiao Guan, Aiping Song, Peipei Cao, Zhiyong Guan, Weimin Fang, Sumei Chen, Fadi Chen & Haibin Wang

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  1. Xiangyu Qi
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  2. Yixin Qu
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Contributions

XYQ, HBW and FDC designed the experiment. XYQ, YXQ, APS and PPC performed the experiment. XYQ, ZYG and WMF analyzed the data and wrote the manuscript. XYQ, JFJ, YXG and SMC revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Haibin Wang.

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Supplementary Information

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Fig. S1. PCR-based identification of interaction proteins of CnTCP13. Supplementary material 1 (TIF 1585.6 kb)

10725_2021_743_MOESM2_ESM.tif

Fig. S2. Characterization of the CnF-box. (a) Amino-acid comparison of CnF-box and F-box homologues from other species. (b) Phylogenetic relationship of CnF-box and other F-box family proteins. The bar (0.02) indicated branch length. The GenBank accession numbers of the amino acid sequences used were: HaF-box (Helianthus annuus, XP_022020705.1), CcF-box (Cynara cardunculus var. Scolymus, KVH89818.1), SiSKIP31(Sesamum indicum, XP_011082189.1), HuSKIP31(Herrania umbratica, XP_021273565.1), NnSKIP31-like (Nelumbo nucifera, XP_010275142.1), MnSKIP31 (Morus notabilis, XP_010111779.1), McSKIP31(Momordica charantia, XP_022140264.1), PpSKIP31 (Prunus persica, XP_007222722.1), PaSKIP31(Prunus avium, XP_021810235.1), CfSKIP31(Cephalotus follicularis, GAV80251.1), GmSKIP31-like (Glycine max, XP_003517102.1), MtSKIP31(Medicago truncatula, XP_003612486.1), AiSKIP31(Arachis ipaensis, XP_016201304.1), AdSKIP31(Arachis duranensis, XP_015963458.1), CqSKIP31(Chenopodium quinoa, XP_021744740.1), SoSKIP31(Spinacia oleracea, XP_021848668.1), HbSKIP31(Hevea brasiliensis, XP_021685246.1), JcSKIP31(Jatropha curcas, XP_012079765.1). Supplementary material 2 (TIF 3352.0 kb)

10725_2021_743_MOESM3_ESM.tif

Fig. S3. Differential expression patterns of CnF-box in various tissues of C. nankingense. Supplementary material 3 (TIF 1100.8 kb)

10725_2021_743_MOESM4_ESM.tif

Fig. S4. Subcellular localization of the CnF-box protein in onion epidermal cells and the transcriptional activation of CnF-box. (a) GFP activity generated by the p35S::GFP-CnCnF-box transgene introduced into onion epidermal peels. Fluorescence: images obtained in the green fluorescence channel; DIC: images obtained in bright light; Merge: overlay plots. Bar: 50 μm. (b) Yeast one-hybrid assay was used to detect transcriptional activation of CnF-box.. Supplementary material 4 (TIF 3504.1 kb)

Table S1. Primer sequences used in this study. Supplementary material 5 (DOCX 22.5 kb)

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Qi, X., Qu, Y., Jiang, J. et al. Heterologous expression of Chrysanthemum nankingense TCP13 suppresses leaf development in Arabidopsis thaliana. Plant Growth Regul 95, 331–341 (2021). https://doi.org/10.1007/s10725-021-00743-3

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