Transcriptomic and metabolomic profiling provide novel insights into fruit development and flesh coloration in Prunus mira Koehne, a special wild peach species

Abstract

Background: Flesh color is one of the most important traits for the commercial value of peach fruit. To unravel the underlying regulatory network in Prunus mira, we performed an integrated analysis of the transcriptome and metabolome of 3 fruit types with various flesh pigmentations (milk-white, yellow and blood) at 3 developmental stages (pit-hardening, cell enlargement and fruit ripening).

Results: Transcriptome analysis showed that an intense transcriptional adjustment is required for the transition from the pit-hardening to the cell enlargement stage. In contrast, few genes were differentially expressed (DEGs) from the cell enlargement to the fruit ripening stage and importantly, the 3 fruits displayed diverse transcriptional activities, indicating that difference in fruit flesh pigmentations mainly occurred during the ripening stage. We further investigated the DEGs between pairs of fruit types during the ripening stage and identified 563 DEGs representing the 'core transcriptome' associated with major differentiations between the 3 fruit types, including flesh pigmentation. Meanwhile, we analyzed the metabolome, particularly, at the ripening stage and uncovered 40 differential metabolites ('core metabolome') between the 3 fruit types including 5 anthocyanins, which may be the key molecules associated with flesh coloration. Finally, we constructed the regulatory network depicting the interactions between anthocyanins and important transcripts involved in fruit flesh coloration.

Conclusions: The major metabolites and transcripts involved in fruit flesh coloration in P. mira were unraveled in this study providing valuable information which will undoubtedly assist in breeding towards improved fruit quality in peach.

Keywords: Flesh pigmentation; Gene regulatory network; Metabolites; Prunus mira.

Fig. 1

The phenotypes of the fruit flesh of Prunus mira cv. “PMHR”, “PMHF” and “PMHY”. Bar = 1 cm

Fig. 2

Heatmap clustering showing correlation among Prunus mira different samples based on global expression profiles

Fig. 3

Differential expressed genes (DEG) during fruit developmental stages in Prunus mira. a. Venn diagram showing the shared and unique DEGs between pit-hardening (A) and cell enlargement (B) stages in PMHF, PMHR and PMHY; b. Venn diagram showing the shared and unique DEGs between cell enlargement (B) and fruit ripening (C) stages in PMHF, PMHR and PMHY; c. Venn diagram showing the shared and unique DEGs between the transitions from A to B and B to C

Fig. 4

Identification of the shared and unique differential expressed genes between pairs of fruit types (PMHFvsPMHR, PMHFvsPMHR, PMHRvsPMHY) at the fruit ripening stage (C) in Prunus mira

Fig. 5

Phenylpropanoid-flavonoid biosynthetic pathway-related genes differentially expressed in PMHF, PMHR and PMHY during the fruit ripening stage (C). Phenylalanine ammonia-lyase (PAL), cinnamic acid 4-hydroxylase (C4H), 4 coumarate CoA ligase (4CL), chalcone synthase (CHS), chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), UDP-flavonoid glucosyl transferase (UFGT) and peroxidase (POD). The line chart displays the expression levels of the genes (FPKM value)

Fig. 6

Principal component analysis of the metabolite quantification in 3 Prunus mira fruit types (PMHF, PMHR and PMHY) at 3 fruit developmental stages (pit-hardening (A), cell enlargement (B) and fruit ripening (C))

Fig. 7

Identification of the differentially accumulated metabolites (DAM) between pairs of fruit types during the fruit ripening stage. a. PMHFvsPMHR, b. PMHFvsPMHY, c. PMHRvsPMHY, d. Venn diagram depicting the shared and unique DAMs between group comparisons

Fig. 8

Overview of the phenylpropanid-flavonoid biosynthetic pathway during the fruit ripening stage in 3 Prunus mira fruit types (PMHF, PMHR and PMHY). Color scale from dark green to dark red for the heatmap represents the log2 value of the metabolite content. The boxplots based on 3 biological replicates show the variation of the metabolite contents in the 3 fruit types

Fig. 9

Regulatory networks connecting transcripts and 5 anthocyanin-related metabolites. The networks in a. PMHF, b. PMHR, c. PMHY were visualized with the Cytoscape software (version 3.6.1)