Exploring the diversity in Citrus fruit colouration to decipher the relationship between plastid ultrastructure and carotenoid composition

Abstract

Differentiation of new and characteristic plastid ultrastructures during ripening of citrus fruits in both peel and pulp appears to be strongly correlated with the content and complement of carotenoids. Most of the species of the Citrus genus display a wide range in fruit colouration due to differences in carotenoids; however, how this diversity is related and may contribute to plastid differentiation and ultrastructure is currently unknown. To that end, carotenoid profile and plastid ultrastructure were compared in peel and pulp of three sweet oranges: the ordinary orange-coloured Navel, rich in β,β-xanthophylls, the yellow Pinalate mutant with an elevated content of colourless carotenes and reduced β,β-xanthophylls, and the red-fleshed Cara Cara with high concentration of colourless carotenes and lycopene in the pulp; and two grapefruits: the white Marsh, with low carotenoid content, and the red Star Ruby, accumulating upstream carotenes and lycopene. The most remarkable differences in plastid ultrastructure among varieties were detected in the pulp at full colour, coinciding with major differences in carotenoid composition. Accumulation of lycopene in Cara Cara and Star Ruby pulp was associated with the presence of needle-like crystals in the plastids, while high content of upstream carotenes in Pinalate pulp was related to the development of a novel plastid type with numerous even and round vesicles. The presence of plastoglobuli was linked to phytoene and xanthophyll accumulation, suggesting these structures as the main sites for the accumulation of these pigments. Peel chromoplasts were richer in membranes compared to pulp chromoplasts, reflecting their different biogenesis. In summary, differences in carotenoid composition and accumulation of unusual carotenoids are mirrored by the development of diverse and novel chromoplast types, revealing the plasticity of these organelles to rearrange carotenoids inside different structures to allow massive accumulation and thus contributing to the chemical stability of the carotenoids.

Distinct Mechanisms of the ORANGE Protein in Controlling Carotenoid Flux

“…A comparative transcriptional study of carotenoid biosynthesis genes suggests that low expression of b-LCY causes the high lycopene accumulation in the red-fruited cultivar (Alquezar et al, 2013). Microscopic analysis indicates that the white grapefruit pulp exhibited fewer chromoplasts per cell and that carotenoid crystalloid structures were absent, while in the red grapefruit pulp, chromoplasts were more abundant and frequently contained crystals (Lado et al, 2015). In this example, the differences in carotenoid composition and accumulation were reflected by the development of specific chromoplast types.…”

“…Plastid development in white-and red-fleshed grapefruit (Citrus paradisi) indicates that the differentiation of distinctive plastids could be correlated with a characteristic carotenoid content (Lado et al, 2015). While the red-fruited cv Star Ruby accumulates high carotenoid levels in the ripe fruit (predominantly phytoene, phytofluene, and lycopene), the white-fruited cv Marsh accumulates very low carotenoid levels (phytoene and violaxanthin).…”

A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health

“…This diversity reflects the wide variety of carotenoid profiles found in chromoplasts from different plant species, tissues, organs, or developmental stages. Interestingly, different chromoplast types and substructures can coexist in the same tissue [101,104]. A strong relationship between carotenoid deposition form and their bioavailability has been established, making this an attractive area of development for food research specialists [103] (see Section 4.3 below).…”

Regulation of Banana Phytoene Synthase (MaPSY) Expression, Characterization and Their Modulation under Various Abiotic Stress Conditions

“…They are predominantly synthesized through plastid localized 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway in chloroplasts and chromoplasts (Flores-Perez et al, 2008; Rodriguez-Concepcion, 2010; Jarvis and López-Juez, 2013; Kaur et al, 2016) (Supplementary Figure S1). Chromoplasts can differentiate from the pre-existing chloroplasts during fruit ripening or directly from proplastids, leucoplasts and amyloplasts in non-green tissues to facilitate carotenoid storage (Sandmann et al, 2006; Maass et al, 2009; Jarvis and López-Juez, 2013; Lado et al, 2015). …”