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. 2024 Aug;33(4):195-210.
doi: 10.1007/s11248-024-00383-z. Epub 2024 Aug 6.

A novel AP2/ERF transcription factor, NtERF10, positively regulates plant height in tobacco

Li Xu  1 , Yong Xu  1 , Jia-Rui Jiang  1 , Chang-Xin Cheng  2 , Wen-Wu Yang  1 , Le-le Deng  1 , Qi-Li Mi  1 , Wan-Li Zeng  1 , Jing Li  1 , Qian Gao  1 , Hai-Ying Xiang  1 , Xue-Mei Li  3
Affiliations

A novel AP2/ERF transcription factor, NtERF10, positively regulates plant height in tobacco

Li Xu et al. Transgenic Res. 2024 Aug.

Abstract

Ethylene response factors have been shown to be involved in the effects of plant developmental processes and to regulate stress tolerance. The aim of this study was to recognize the regulatory mechanisms of ethylene response factors on tobacco plant height. In this study, a gene-edited mutant (ERF10-KO) and wild type (WT) were utilized as experimental materials. Transcriptome and metabolome analyses were used to investigate the regulatory mechanism of NtERF10 gene editing on plant height in tobacco. Here, through the analysis of differentially expressed genes (DEGs), 2051 genes were upregulated and 1965 genes were downregulated. We characterized the different ERF10-KO and WT plant heights and identified key genes for photosynthesis, the plant hormone signal transduction pathway and the terpene biosynthesis pathway. NtERF10 was found to affect the growth and development of tobacco by regulating the expression levels of the PSAA, PSBA, GLY17 and GGP3 genes. Amino acid metabolism was analyzed by combining analyses of differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs). In addition, we found that members of the bHLH, NAC, MYB, and WRKY transcription factor families have vital roles in regulating plant height. This study not only provides important insights into the positive regulation of the ethylene response factor NtERF10 on plant height during plant growth and development but also provides new research ideas for tobacco molecular breeding.

Keywords: NtERF10; Metabolome; Plant height; Tobacco; Transcriptome.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
NtERF10 gene mutant lines and phenotypic analysis. A CRISPR/Cas9-mediated NtERF10 gene mutation in Nicotiana tobacum (red words indicate sgRNA sequences; position of editing is indicated by red arrow); B phenotype of WT and ERF10-KO mutant plants under normal conditions; C plant height of WT and ERF10-KO mutant plants. * and ** indicate significant differences between the results at p ≤ 0.05 and p ≤ 0.01, respectively. Bars represent the mean ± SE. (Color figure online)
Fig. 2
Fig. 2
Transcriptome changes and functional analysis of tobacco dwarf mutant (ERF10-KO) and wild-type samples (WT). A PCA analysis of ERF10-KO and WT expression. B 50 genes with significant changes in ERF10-KO and WT. C Volcano diagram of up- and down-regulation of differential genes (DEGs). D GSEA enrichment analysis of five pathways that up-regulated differential gene enrichment. E GSEA enrichment analysis of five pathways that down-regulated differential gene enrichment
Fig. 3
Fig. 3
Functional study of genes that differ between ERF10-KO and WT. A–D GESA analyzed genes related to photosynthesis, glutathione-metabolism, glyceropholipid-metabolism, glycerolipid-metabolism. E–I DEGs for cell membranes lipids metabolism, photosynthesis and glutathione metabolism in ERF10-KO and WT
Fig. 4
Fig. 4
Differential genes in plant hormone-related genes. A GSEA analysis of plant hormone signal transduction related genes. B–D ethylene response, gibberellins, and Brassinosteroids production are all represented by genes
Fig. 5
Fig. 5
Expression patterns of terpene synthesis-related genes in ERF10-KO and WT
Fig. 6
Fig. 6
Overview of metabolome analysis between ERF10-KO and WT. A PLSDA analysis of metabolomic data between ERF10-KO and WT. B Volcano plot for metabolite differential analysis between ERF10-KO and WT. Among them, yellow represents up-regulation and purple represents down-regulation, and the differential metabolites with the most obvious changes are marked with names. C Pathways of major enrichment of differential metabolites. D Expression heatmap of top 26 differential metabolites. (Color figure online)
Fig. 7
Fig. 7
Combined functional analysis of amino acids biosynthesis genes and amino acids contents
Fig. 8
Fig. 8
Splicing and translation-related differential gene changes in ERF10-KO and WT. A and B GSEA analysis of splicing and translation related genes. C and D Specific differential gene changes in ribosome and spliceosome
Fig. 9
Fig. 9
Identification and expression of transcription factors linked to dwarfism in ERF10-KO and WT. The transcription factor families bHLH, NAC, MYB, and WRKY are included. bHLH, basic helix-loop-helix; NAC, Nac protein; MYB, MYB proteins; WRKY, WRKY proteins
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