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Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum - PubMed

️Mon Jan 01 2024

Review

Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum

Jiangshuo Su et al. BMC Plant Biol. 2024.

Abstract

Background: Heterosis breeding is one of the most important breeding methods for chrysanthemum. To date, the genetic mechanisms of heterosis for waterlogging tolerance in chrysanthemum are still unclear. This study aims to analyze the expression profiles and potential heterosis-related genes of two hybrid lines and their parents with extreme differences in waterlogging tolerance under control and waterlogging stress conditions by RNA-seq.

Results: A population of 140 F₁ progeny derived from Chrysanthemum indicum (Nanchang) (waterlogging-tolerant) and Chrysanthemum indicum (Nanjing) (waterlogging-sensitive) was used to characterize the extent of genetic variation in terms of seven waterlogging tolerance-related traits across two years. Lines 98 and 95, respectively displaying positive and negative overdominance heterosis for the waterlogging tolerance traits together with their parents under control and waterlogging stress conditions, were used for RNA-seq. In consequence, the maximal number of differentially expressed genes (DEGs) occurred in line 98. Gene ontology (GO) enrichment analysis revealed multiple stress-related biological processes for the common up-regulated genes. Line 98 had a significant increase in non-additive genes under waterlogging stress, with transgressive up-regulation and paternal-expression dominant patterns being the major gene expression profiles. Further, GO analysis identified 55 and 95 transgressive up-regulation genes that overlapped with the up-regulated genes shared by two parents in terms of responses to stress and stimulus, respectively. 6,640 genes in total displaying maternal-expression dominance patterns were observed in line 95. In addition, 16 key candidate genes, including SAP12, DOX1, and ERF017 which might be of significant importance for the formation of waterlogging tolerance heterosis in line 98, were highlighted.

Conclusion: The current study provides a comprehensive overview of the root transcriptomes among F₁ hybrids and their parents under waterlogging stress. These findings lay the foundation for further studies on molecular mechanisms underlying chrysanthemum heterosis on waterlogging tolerance.

Keywords: Chrysanthemum; Heterosis; Overdominant expression; RNA-seq; Waterlogging tolerance.

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Conflict of interest statement

The authors declare no competing interests.

Figures

**Fig. 1**
Frequency distribution of seven waterlogging tolerance traits and box plot of MFVW in the F₁ population derived from *C. indicum* (Nanchang) and *C. indicum* (Nanjing). a Shoot height. b Root length. c Shoot fresh weight. d Root fresh weight. e Shoot dry weight. f Root dry weight. g Score. The green and orange arrowheads in panel a-g indicate the two parents: NC, *C. indicum* (Nanchang); NJ, *C. indicum* (Nanjing). h Box plot showing the variation of MFVWs among the five waterlogging tolerance levels in F₁ lines

**Fig. 2**
Phenotypic characteristics of F₁ hybrids 95 and 98 and their parents. a plant phenotype of hybrids and parents after 9 days of waterlogging stress. Scale bar = 2 cm. **b-g** Statistical analysis of shoot height (SH), root length (RL), shoot fresh weight (SFW), root fresh weight (RFW), shoot dry weight (SDW), and root dry weight (RDW) of F₁ hybrid 95 and 98 and their parents. Different letters indicate significant difference at P < 0.05 between individuals. Data represent mean values ± SE. The control group is prefixed with C; The 9-day waterlogging stress treatment group is prefixed with W; NC indicates female parent *C. indicum* (Nanchang), and NJ indicates male parent *C. indicum* (Nanjing)

**Fig. 3**
Basic analysis of differentially expressed genes. **a, b** Histogram and venn diagrams showing the number of up-regulated and down-regulated differentially expressed genes among hybrids 95 and 98 and their parents under waterlogging stress and control conditions. **c-e** Histogram and venn diagrams of up-regulated and down-regulated differentially expressed genes in paired comparison between hybrids and parents under control condition. **f-h** Histogram and venn diagrams of up-regulated and down-regulated differentially expressed genes in paired comparison between hybrids and parents under waterlogging stress condition. The control group is prefixed with a capital letter C; The 9-day waterlogging stress treatment group is prefixed with a capital letter W; NC, *C. indicum* (Nanchang); NJ, *C. indicum* (Nanjing)

**Fig. 4**
Basic analysis of differentially expressed genes and KEGG enrichment analysis of line 98 and its parents under waterlogging stress and control conditions. **a, b** Venn diagram of up-regulated and down-regulated differentially expressed genes. c KEGG enrichment map of 3,931 common DEGs of line 98. The numbers on the right side of the bar graph represent the number of genes contained in the corresponding KEGG pathway; The numbers in parentheses represent the significance level of the corresponding KEGG pathway (-Log₁₀(Q value)). The KEGG enrichment map mentioned in the figure has been granted copyright permission by Kanehisa Laboratories

**Fig. 5**
Analysis of gene expression trends in hybrids compared to parents under control and waterlogging stress conditions. **a, b** The gene expression genetic patterns of line 98. **c, d** The gene expression genetic patterns of line 95. The corresponding P-value is marked in the expression pattern diagram, and the significant expression patterns (P < 0.05) are marked in gray. e Statistical analysis of the number of genes contained in each expression pattern. The control group is prefixed with a capital letter C; The 9days waterlogging stress treatment group is prefixed with a capital letter W; the numbers after C and W represent biological repeated numbers; NC, *C. indicum* (Nanchang); NJ, *C. indicum* (Nanjing)

**Fig. 6**
Enrichment analysis of 5,069 unique transgressive up–regulation genes and expression heat map of 16 candidate genes. a Enrichment of GO biological process terms for 5,069 unique transgressive up–regulation genes of line 98. Only the top 20 GO terms with the lowest Q value are shown. b KEGG enrichment of 5,069 unique transgressive up–regulation expression genes in line 98. Only the top 20 pathways with the lowest Q value are shown. The numbers on the right side of the bar graph represent the number of genes contained in the corresponding GO terms. The numbers in parentheses represent the significance level of the corresponding GO terms (-Log₁₀(Q value)). The KEGG enrichment map mentioned in the figure has been granted copyright permission by Kanehisa Laboratories. c Expression heatmaps of 9 hormone response-related genes enriched in GO terms in response to the hormone. d Expression heatmaps of 7 plant stress resistance-related genes enriched in GO terms in response to stress. The legend at the right of the figure indicates the gene expression levels transformed by log₁₀ (FPKM)

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Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum - PubMed