Physiological, transcriptomic, and metabolomic analyses of the chilling stress response in two melon (Cucumis melo L.) genotypes

Abstract

Background: Chilling stress is a key abiotic stress that severely restricts the growth and quality of melon (Cucumis melo L.). Few studies have investigated the mechanism of response to chilling stress in melon.

Results: We characterized the physiological, transcriptomic, and metabolomic response of melon to chilling stress using two genotypes with different chilling sensitivity ("162" and "13-5A"). "162" showed higher osmotic regulation ability and antioxidant capacity to withstand chilling stress. Transcriptome analysis identified 4395 and 4957 differentially expressed genes (DEGs) in "162" and "13-5A" under chilling stress, respectively. Metabolome analysis identified 615 and 489 differential enriched metabolites (DEMs) were identified in "162" and "13-5A" under chilling stress condition, respectively. Integrated transcriptomic and metabolomic analysis showed enrichment of glutathione metabolism, and arginine (Arg) and proline (Pro) metabolism, with differential expression patterns in the two genotypes. Under chilling stress, glutathione metabolism-related DEGs, 6-phosphogluconate dehydrogenase (G6PDH), glutathione peroxidase (GPX), and glutathione s-transferase (GST) were upregulated in "162," and GSH conjugates (L-gamma-glutamyl-L-amino acid and L-glutamate) were accumulated. Additionally, "162" showed upregulation of DEGs encoding ornithine decarboxylase, Pro dehydrogenase, aspartate aminotransferase, pyrroline-5-carboxylate reductase, and spermidine synthase and increased Arg, ornithine, and Pro. Furthermore, the transcription factors (TFs), MYB, ERF, MADS-box, and bZIP were significantly upregulated, suggesting their crucial role in chilling tolerance of melon.

Conclusions: These findings elucidate the molecular response mechanism to chilling stress in melon and provide insights for breeding chilling-tolerant melon.

Keywords: Chilling stress; Melon; Metabolome; Transcriptome.

Fig. 1

Morphological and physiological characteristics of melon seedlings (genotypes 162 and 13-5 A) under chilling stress. Melon seedlings exposed to low temperature 6 °C for 12 h. A Morphological traits; B Fv/Fm; C H₂O₂ staining; D soluble sugar, soluble protein content, MDA, O₂⁻ and H₂O₂ contents; and (E) SOD, POD, CAT and APX activity of the 162 and 13-5 A genotypes in the control group (0 h exposure) and treatment group (12 h exposure). Asterisks indicate significant differences at P < 0.05

Fig. 2

Transcriptome analysis of melon genotypes 162 and 13-5 A under chilling stress (6 ℃) for 0 h and 12 h. A Correlation analysis (n = 12); B PCA; n = 12; C Venn diagram of the number of DEGs in various comparisons (5–12 h vs. 5 A–0 h, 162–12 h vs. 162–0 h, 162–0 h vs. 5 A–0 h and 162–12 h vs. 5–12 h); D Numbers of DEGs in each comparison; E GO analysis of DEGs shown in (D); F KEGG analysis of DEGs shown in (D)

Fig. 3

Analysis of TFs in two melon genotypes exposed to chilling stress. A Number of TFs with differential expression; B Venn diagram showing the differentially expressed TF genes common between the comparisons 5–12 h vs. 5 A–0 h and 162–12 h vs. 162–0 h; C Expression profiles of the MYB, AP2/ERF, WRKY, TCP, and bZIP genes in the two genotypes

Fig. 4

Analysis of DEMs in melon leaves under chilling stress. A The number of DEMs in 5–12 h vs. 5 A–0 h, 162–12 h vs. 162–0 h, 162–0 h vs. 5 A–0 h, and 162–12 h vs. 5–12 h. B Venn diagram showing the overlap of DEMs in 162–12 h vs. 162–0 h and 13–5 A-12 h vs. 13–5 A-0 h

Fig. 5

KEGG analysis of DEGs and DEMs in the 5–12 h vs. 5–12 h and 162–12 h vs. 162–12 h comparisons

Fig. 6

Changes in DEGs and DEMs involved in glutathione metabolism in the melon genotypes 162 and 13-5 A under chilling stress conditions. The color of the rectangles represents significance

Fig. 7

Changes in DEGs and DEMs in Arg and Pro metabolism