Inter-Species Comparative Analysis of Components of Soluble Sugar Concentration in Fleshy Fruits

Abstract

The soluble sugar concentration of fleshy fruit is a key determinant of fleshy fruit quality. It affects directly the sweetness of fresh fruits and indirectly the properties of processed products (e.g., alcohol content in wine). Despite considerable divergence among species, soluble sugar accumulation in a fruit results from the complex interplay of three main processes, namely sugar import, sugar metabolism, and water dilution. Therefore, inter-species comparison would help to identify common and/or species-specific modes of regulation in sugar accumulation. For this purpose, a process-based mathematical framework was used to compare soluble sugar accumulation in three fruits: grape, tomato, and peach. Representative datasets covering the time course of sugar accumulation during fruit development were collected. They encompassed 104 combinations of species (3), genotypes (30), and growing conditions (19 years and 16 nutrient and environmental treatments). At maturity, grape showed the highest soluble sugar concentrations (16.5-26.3 g/100 g FW), followed by peach (2.2 to 20 g/100 g FW) and tomato (1.4 to 5 g/100 g FW). Main processes determining soluble sugar concentration were decomposed into sugar importation, metabolism, and water dilution with the process-based analysis. Different regulation modes of soluble sugar concentration were then identified, showing either import-based, dilution-based, or import and dilution dual-based. Firstly, the higher soluble sugar concentration in grape than in tomato is a result of higher sugar importation. Secondly, the higher soluble sugar concentration in grape than in peach is due to a lower water dilution. The third mode of regulation is more complicated than the first two, with differences both in sugar importation and water dilution (grape vs. cherry tomato; cherry tomato vs. peach; peach vs. tomato). On the other hand, carbon utilization for synthesis of non-soluble sugar compounds (namely metabolism) was conserved among the three fruit species. These distinct modes appear to be quite species-specific, but the intensity of the effect may significantly vary depending on the genotype and management practices. These results provide novel insights into the drivers of differences in soluble sugar concentration among fleshy fruits.

Keywords: dilution; fruit metabolism; grape; peach; sugar importation; tomato.

FIGURE 1

Distribution of fruit fresh weight (FW; A) and soluble sugar concentration (B) in grape, cherry tomato, tomato, and peach at maturity. White points represent median of FW and soluble sugar concentration of a given fruit species in the dataset. The violin shape represents the distribution of the variables in each fruit species.

FIGURE 2

Developmental profiles of FW (A–D), dry weight (DW; E–H), and soluble sugar concentration (I–L) in grape (A,E,I), cherry tomato (B,F,J), tomato (C,G,K), and peach (D,H,L) fruits. All curves are smoothed fits of the observed data points using the “loess” function in R software (R Development Core Team, 2010).

FIGURE 3

The dynamic (A–D) and the absolute value of mean cumulative (E–H) contributions of sugar importation, sugar metabolism, and water dilution on sugar accumulation in grape, cherry tomato, tomato, and peach during the late fruit development stages. Sugar represents the mean increment of sugar concentration during the targeted period (E–H). To make the developmental profiles comparable among fruits, development stages were normalized with flowering to be 0 and maturity to be 1. The absolute value of cumulative contributions were calculated over the period from 40% maturity to 100% maturity (blue dashed lines), and then divided by the duration (days) of the chosen period for each condition. Different letters for a given component in different fruits (E–H) indicate a significant difference, based on non-parametric multiple comparison for unbalanced one-way factorial designs in R.

FIGURE 4

Summary of the differences among fruit species regarding soluble sugar concentration and of its components, sugar importation, sugar metabolism, and water dilution. Different colors indicate the difference of each criterion between the fruit at row and the fruit at column, with red for higher, green for lower, and gray for no difference. Sugar represents the mean increment of sugar concentration during the targeted period.

FIGURE 5

Principal component analysis (PCA) analysis of genotypes and growing conditions of the three fruit species. The three components (importation, metabolism, dilution) were used to make the PCA discriminate the three fruit species (A). Soluble sugar concentration, FW, and DW were projected as non-active variables on the first two PCs (B). To have a better view of the genotypes and growing conditions, a zooming of the general scatter plot (A) was conducted for each fruit (C for grape, D for cherry tomato and tomato, and E for peach). The genotype, year, and truss (for tomato) of the fruits were labeled as “genotype-year-truss.” Mt = Merlot, CS = Cabernet-Sauvignon, CF = Cabernet franc, GW643 = Gewurztraminer, Ri49 = Riesling in (C). Green and yellow dots represent white grape genotypes and pink, violet and brown dots represent red grape genotypes (C). HC, MC, and LC represent high, mean and low crop loads, respectively (D,E).