Physical barriers to carotenoid bioaccessibility. Ultrastructure survey of chromoplast and cell wall morphology in nine carotenoid‐containing fruits and vegetables

Jeffery, Jennifer; Holzenburg, Andreas; King, Stephen R.

doi:10.1002/jsfa.5767

Cited by 110 publications

(68 citation statements)

References 26 publications

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“…Another distinctive feature of C orange and SR grapefruit pulp chromoplasts was the presence of needle-like crystals (Figs. 5f,l,6c,d,g,h), coinciding with the presence of lycopene in this tissue and resembling those previously described in other lycopeneaccumulating fruits (Simkin et al 2007;Schweiggert et al 2011;Jeffery et al 2012;Nogueira et al 2013) and in the pulp and peel of red grapefruit (Cao et al 2012;Jeffery et al 2012;Lado et al 2015). By contrast, at breaker stage in MSH pulp, the low content of carotenoids was related to a lack of any defined sink structures (Fig.…”

Section: Discussionsupporting

confidence: 87%

“…7a, b). These crystals could facilitate lycopene accumulation and limit isomerization reactions, as has been proposed for (all-E)-isomers of b-carotene in carrot roots (Kim et al 2010), mango (Vasquez-Caicedo et al 2006;Jeffery et al 2012) and (all-E)-lycopene in tomato (Simkin et al 2007;Nogueira et al 2013). Carotenoid-containing crystals were firstly described to occur inside the lumina of some thylakoids, exhibiting an external membrane even in mature chromoplasts (Ljubesic et al 1991).…”

Section: Discussionmentioning

confidence: 94%

“…Other structures have been described to coexist with plastoglobuli in the chromoplasts, and the relative abundance of each type of structure leads to the classification as globular, tubular, membranous and crystalloid chromoplasts (Sitte et al 1980;Egea et al 2010). Moreover, the development of sub-chromoplast structures seems to be related to the type of carotenoids that are sequestered (Ljubesic et al 1991;Nogueira et al 2013), and these structures may act also as a physical barrier influencing the bioaccessibility of carotenoids from fruits and vegetables (Jeffery et al 2012).…”

Section: Introductionmentioning

confidence: 99%

“…Plastoglobuli were also reported to be present in flavedo chromoplasts of Satsuma mandarin (Shimokawa et al 1978), grapefruit (Gross 1987) and lemon (Ljubesic 1984). The chromoplasts from the pulp of the red Star Ruby grapefruit were described as sparse and exclusive to the outer cells of the juice sacs and seemed to be dominated by electron-transparent vesicles and electron-dense background material (Jeffery et al 2012). Cao et al (2012) have classified the chromoplasts of the peel of Marsh grapefruit, Cara Cara orange and Sunburst mandarin as globular, due to the presence of large numbers of plastoglobuli.…”

Section: Introductionmentioning

confidence: 99%

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

Lado

Zacarı́as

Gurrea

et al. 2015

Planta

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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.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Lado

Zacarı́as

Gurrea

et al. 2015

Planta

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“…7). The existence of organized internal membranes in tomato chromoplasts was previously reported (Harries and Spurr, 1969;Jeffery et al, 2012) and it is possible that the chromorespiratory pathway may be located in these structures. This hypothesis is in agreement with the lack of effect of CCCP in the respiratory activity of sonicated chromoplasts (Fig.…”

Section: Chromoplast Respiratory Activity Is Linked To Atp Synthesismentioning

confidence: 74%

Tomato Fruit Chromoplasts Behave as Respiratory Bioenergetic Organelles during Ripening

et al. 2014

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During tomato (Solanum lycopersicum) fruit ripening, chloroplasts differentiate into photosynthetically inactive chromoplasts. It was recently reported that tomato chromoplasts can synthesize ATP through a respiratory process called chromorespiration. Here we show that chromoplast oxygen consumption is stimulated by the electron donors NADH and NADPH and is sensitive to octyl gallate (Ogal), a plastidial terminal oxidase inhibitor. The ATP synthesis rate of isolated chromoplasts was dependent on the supply of NAD(P)H and was fully inhibited by Ogal. It was also inhibited by the proton uncoupler carbonylcyanide m-chlorophenylhydrazone, suggesting the involvement of a chemiosmotic gradient. In addition, ATP synthesis was sensitive to 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, a cytochrome b 6 f complex inhibitor. The possible participation of this complex in chromorespiration was supported by the detection of one of its components (cytochrome f) in chromoplasts using immunoblot and immunocytochemical techniques. The observed increased expression of cytochrome c 6 during ripening suggests that it could act as electron acceptor of the cytochrome b 6 f complex in chromorespiration. The effects of Ogal on respiration and ATP levels were also studied in tissue samples. Oxygen uptake of mature green fruit and leaf tissues was not affected by Ogal, but was inhibited increasingly in fruit pericarp throughout ripening (up to 26% in red fruit). Similarly, Ogal caused a significant decrease in ATP content of red fruit pericarp. The number of energized mitochondria, as determined by confocal microscopy, strongly decreased in fruit tissue during ripening. Therefore, the contribution of chromoplasts to total fruit respiration appears to increase in late ripening stages.

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Bioaccessibility and bioavailability

Rodriguez–Amaya

2015

Food Carotenoids

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Physical barriers to carotenoid bioaccessibility. Ultrastructure survey of chromoplast and cell wall morphology in nine carotenoid‐containing fruits and vegetables

Abstract: A more precise description of the physical characteristics of foods that stand as barriers to bioaccessibility can help in understanding which are more or less inhibitory for particular foods.

Cited by 110 publications

References 26 publications

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

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

Tomato Fruit Chromoplasts Behave as Respiratory Bioenergetic Organelles during Ripening

Bioaccessibility and bioavailability

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