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. 2023 Feb 1;71(4):1873-1885.
doi: 10.1021/acs.jafc.2c07207. Epub 2023 Jan 18.

Biosynthesis of Chlorophyll and Other Isoprenoids in the Plastid of Red Grape Berry Skins

António Teixeira  1 , Henrique Noronha  1 , Sarah Frusciante  2 , Gianfranco Diretto  2 , Hernâni Gerós  1
Affiliations

Biosynthesis of Chlorophyll and Other Isoprenoids in the Plastid of Red Grape Berry Skins

António Teixeira et al. J Agric Food Chem. .

Abstract

Despite current knowledge showing that fruits like tomato and grape berries accumulate different components of the light reactions and Calvin cycle, the role of green tissues in fruits is not yet fully understood. In mature tomato fruits, chlorophylls are degraded and replaced by carotenoids through the conversion of chloroplasts in chromoplasts, while in red grape berries, chloroplasts persist at maturity and chlorophylls are masked by anthocyanins. To study isoprenoid and lipid metabolism in grape skin chloroplasts, metabolites of enriched organelle fractions were analyzed by high-performance liquid chromatography-high-resolution mass spectrometry (HPLC-HRMS) and the expression of key genes was evaluated by real-time polymerase chain reaction (PCR) in berry skins and leaves. Overall, the results indicated that chloroplasts of the grape berry skins, as with leaf chloroplasts, share conserved mechanisms of synthesis (and degradation) of important components of the photosynthetic machinery. Some of these components, such as chlorophylls and their precursors, and catabolites, carotenoids, quinones, and lipids have important roles in grape and wine sensory characteristics.

Keywords: HPLC-MS analysis; freeze dry; grape berry skins; plastid isolation.

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Conflict of interest statement

The authors declare no competing financial interest.

Figures

Figure 1
Figure 1
Plastid purification from leaves and grape berry skins of Vitis vinifera cv. “Vinhão” at green and mature developmental stages. Chloroplast samples were observed under an epifluorescence microscope.
Figure 2
Figure 2
Changes in targeted isoprenoids from purified plastids from green leaf and berry skin of red grapes cv. “Vinhão”: supervised partial least squares-discriminant analysis (PLS-DA) of (A) green berry vs mature berry, (B) green leaf vs mature leaf, and (C) heatmap of the observed changes. Variables in the PLS-DA score plot were colored according to the tissue and developmental stage. Data represent, for each metabolite, the fold on the internal standard (IS, a-tocopherol acetate) level/gm DW. Asterisks indicate statistical significance between mature (E-L 38) and green (E-L 34) conditions following the Student’s t-test: *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001; and ****P ≤ 0.0001.
Figure 3
Figure 3
Relative content of isoprenoids from purified plastids and transcripts expression of key genes of green and mature berry skin of red grape berry cv. “Vinhão”, involved in the biosynthesis of isoprenoids. (A) Chlorophyll biosynthesis pathway. (B) Relative expression of key genes involved in the biosynthesis of chlorophylls. (C) Isoprenoid biosynthesis pathway with the ratio of metabolites (log2 green/mature) identified in purified plastids from the skin of grape berries and leaves at green (E-L 34) and mature (E-L 38) stages of development. (D) Relative expression of key genes involved in isoprenoid biosynthesis. Gray metabolite and blue gene names indicate measurements from the present study. Asterisks indicate statistical significance between mature (E-L 38) and green (E-L 34) stages following the Student’s t-test: *P ≤ 0.05; **P ≤ 0.01; and ***P ≤ 0.001.
Figure 4
Figure 4
Modifications observed in targeted lipids present in plastids purified from green leaf and berry skin of red grapes cv. “Vinhão”: Supervised Partial Least Squares-Discriminant Analysis (PLS-DA) of (A) green berry vs mature berry, (B) green leaf vs mature leaf, and (C) heatmap of the observed modifications. Variables in PLS-DA score plot were colored according to the tissue and developmental stage. Asterisks indicate statistical significance between mature (E-L 38) and green (E-L 34) conditions following the Student’s t-test: *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001; and ****P ≤ 0.0001.
Figure 5
Figure 5
Lipids and targeted key genes from grape berries and leaves. (A) Simplified schematic of lipid biosynthesis in plastid and (B) endoplasmic reticulum, and (C) expression of key genes involved in lipid biosynthesis. Asterisks indicate statistical significance between mature (E-L 38) and green (E-L 34) conditions following the Student’s t-test: **P ≤ 0.01.
Figure 6
Figure 6
Correlation network of transcripts and metabolites from plastids purified from grapevine berry skins of red grapes and leaves of cv. “Vinhão” at mature stages of grape berry development normalized to green stages. Network is visualized with lines joining the nodes (edges) representing correlations: direct (positive) correlations are shown in red, while inverse (negative) correlations are shown in blue. Edge thickness is proportional to the respective correlation value (ρ). Node shapes represent a gene transcript (diamonds) or a metabolite (circles—isoprenoids; hexagons—lipids) from different biosynthetic pathways. For more details, see Materials and Methods and Supplementary Table 5.
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