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. 2023 Jan 31:14:1107550.
doi: 10.3389/fpls.2023.1107550. eCollection 2023.

Overdominant expression of genes plays a key role in root growth of tobacco hybrids

Kai Pi  1   2 , Ying Huang  1   2 , Wen Luo  1   2 , Shuaibo Zeng  1   2 , Zejun Mo  3 , Lili Duan  3 , Renxiang Liu  1   2
Affiliations

Overdominant expression of genes plays a key role in root growth of tobacco hybrids

Kai Pi et al. Front Plant Sci. .

Abstract

Heterosis has greatly improved the yield and quality of crops. However, previous studies often focused on improving the yield and quality of the shoot system, while research on the root system was neglected. We determined the root numbers of 12 F1 hybrids, all of which showed strong heterosis, indicating that tobacco F1 hybrids have general heterosis. To understand its molecular mechanism, we selected two hybrids with strong heterosis, GJ (G70 × Jiucaiping No.2) and KJ (K326 × Jiucaiping No.2), and their parents for transcriptome analysis. There were 84.22% and 90.25% of the differentially expressed genes were overdominantly expressed. The enrichment analysis of these overdominantly expressed genes showed that "Plant hormone signal transduction", "Phenylpropanoid biosynthesis", "MAPK signaling pathway - plant", and "Starch and sucrose metabolism" pathways were associated with root development. We focused on the analysis of the biosynthetic pathways of auxin(AUX), cytokinins(CTK), abscisic acid(ABA), ethylene(ET), and salicylic acid(SA), suggesting that overdominant expression of these hormone signaling pathway genes may enhance root development in hybrids. In addition, Nitab4.5_0011528g0020、Nitab4.5_0003282g0020、Nitab4.5_0004384g0070 may be the genes involved in root growth. Genome-wide comparative transcriptome analysis enhanced our understanding of the regulatory network of tobacco root development and provided new ideas for studying the molecular mechanisms of tobacco root development.

Keywords: WGCNA; heterosis; overdominant expression; root system; transcriptomics.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Phenotypic parameters and Heterosis of two tobacco F1 hybrids and their parents. (A) Photographs of the two hybrids and their parents used in this study. (B) Root number of F1 hybrid and its parents(G = G70, J = Jiucaiping No.2, GJ = G70 × Jiucaiping No.2, K = K326, KJ =K326 × Jiucaiping No.2). (C) Heterosis of two tobacco F1 hybrids (GJ and KJ). Error bars indicate standard error. Different small letters showed significant differences (P<0.05).
Figure 2
Figure 2
Global gene expression profiling during root development. (A) Pearson correlation analysis of the two hybrids and their parents, and the color code on the right represents Pearson correlation coefficient. (B) Principal component analysis (PCA) of RNA-Seq data. Each point shows the average of three repeats.
Figure 3
Figure 3
Distribution of differentially expressed genes (DEGs) between hybrids and parents. MP represents the average value of parents. (A) The number of different expressed genes between GJ and its parents during root development. (B) Venn shows the distribution of GJ and parental DEGs. (C) The number of different expressed genes between KJ and its parents during root development. (D) Venn shows the distribution of KJ and parental DEGs.
Figure 4
Figure 4
12 gene expression patterns of DEGs between hybrids and parents. (A) Classification of 12 gene expression patterns (♂: paternal; H: hybrid; ♀: maternal). (B) The number of genes of GJ and KJ hybrids in each model. (C) The number and proportion of the five total expression patterns after classification in DEGs.
Figure 5
Figure 5
Enrichment analysis of KEGG pathway of GJ and KJ overdominant expression genes. (A) KEGG analysis of overdominant up-regulated and down-regulated genes in GJ hybrids. (B) KEGG analysis of overdominant up-regulated and down-regulated genes in KJ hybrids.
Figure 6
Figure 6
Overdominant expression genes of hormone signal transduction related to AUX, CTK, ABA, ET and SA biosynthesis. These genes showed overdominant expression in both hybrids.
Figure 7
Figure 7
Overdominant expression genes related to cell population promotion, cell differentiation, multiple cell growth and primary commodity issue development. These genes were overdominant expression in both hybrids.
Figure 8
Figure 8
Weighted gene co-expression network analysis (WGCNA). (A) Hierarchical cluster tree shows 10 modules of co-expressed genes. The lower heatmap shows modules in designated colors. The module grey is for unassigned genes. (B) Heat maps showing the correlation of module-trait, the Pearson correlation coefficient and P values of significant modules are given. (C) Connectivity between 6 genes.
Figure 9
Figure 9
(A) Phylogenetic trees of root development genes in tobacco. (B) Comparison of RNA-seq and RT-qPCR gene expression levels of root related genes in two hybrids and their parents.
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