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Side-effects of domestication: cultivated legume seeds contain similar tocopherols and fatty acids but less carotenoids than their wild counterparts.

Fernández-Marín B, Milla R, Martín-Robles N, Arc E, Kranner I, Becerril JM, García-Plazaola JI - BMC Plant Biol. (2014)

Bottom Line: Unexpectedly, we found that following domestication, the contents of carotenoids, including lutein and zeaxanthin, decreased in all ten species (total carotenoid content decreased 48% in average).An undirected change in the contents of tocopherols and fatty acids was found, with contents increasing in some species and decreasing in others, independently of the changes in carotenoids.In some species, polyunsaturated fatty acids (linolenic acid especially), α-tocopherol and γ-tocopherol decreased following domestication.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Apdo. 644, 48080, Bilbao, Spain. beatriz.fernandezm@ehu.es.

ABSTRACT

Background: Lipophilic antioxidants play dual key roles in edible seeds (i) as preservatives of cell integrity and seed viability by preventing the oxidation of fats, and (ii) as essential nutrients for human and animal life stock. It has been well documented that plant domestication and post-domestication evolution frequently resulted in increased seed size and palatability, and reduced seed dormancy. Nevertheless, and surprisingly, it is poorly understood how agricultural selection and cultivation affected the physiological fitness and the nutritional quality of seeds. Fabaceae have the greatest number of crop species of all plant families, and most of them are cultivated for their highly nutritious edible seeds. Here, we evaluate whether evolution of plants under cultivation has altered the integrated system formed by membranes (fatty acids) and lipophilic antioxidants (carotenoids and tocopherols), in the ten most economically important grain legumes and their closest wild relatives, i.e.: Arachis (peanut), Cicer (chickpea), Glycine (soybean), Lathyrus(vetch), Lens (lentil), Lupinus (lupin), Phaseolus (bean), Pisum (pea), Vicia (faba bean) and Vigna (cowpea).

Results: Unexpectedly, we found that following domestication, the contents of carotenoids, including lutein and zeaxanthin, decreased in all ten species (total carotenoid content decreased 48% in average). Furthermore, the composition of carotenoids changed, whereby some carotenoids were lost in most of the crops. An undirected change in the contents of tocopherols and fatty acids was found, with contents increasing in some species and decreasing in others, independently of the changes in carotenoids. In some species, polyunsaturated fatty acids (linolenic acid especially), α-tocopherol and γ-tocopherol decreased following domestication.

Conclusions: The changes in carotenoids, tocopherols and fatty acids are likely side-effects of the selection for other desired traits such as the loss of seed dormancy and dispersal mechanisms, and selection for seed storability and taste. This work may serve as baseline to broaden our knowledge on the integrated changes on crop fitness and nutritional quality following domestication.

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Composition of carotenoids and tocopherols in seeds of grain legumes and their closest wild relatives. (A) Individual carotenoids and tocopherols are expressed as proportions of total contents. Data are means (n = 5). (B) Bisector plots representing the absolute contents of carotenoids and tocopherols in grain legumes plotted against their closest wild relatives (only compounds shared among most species are shown). Data points below the dotted line (y = x) indicate that grain legumes contained less seed carotenoids or tocopherols than their wild relatives.
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Fig2: Composition of carotenoids and tocopherols in seeds of grain legumes and their closest wild relatives. (A) Individual carotenoids and tocopherols are expressed as proportions of total contents. Data are means (n = 5). (B) Bisector plots representing the absolute contents of carotenoids and tocopherols in grain legumes plotted against their closest wild relatives (only compounds shared among most species are shown). Data points below the dotted line (y = x) indicate that grain legumes contained less seed carotenoids or tocopherols than their wild relatives.

Mentions: The composition of individual carotenoids and tocopherols in grain legumes also differed from that of their wild relatives (Figure 2). Lutein was the predominant carotenoid in all the species, followed by zeaxanthin and β-carotene (Figure 2A), except for the Vigna wild relative. Of all tocopherols, γ-tocopherol was the most abundant isoform in all species, except for Vigna and Arachis monticola, where δ − tocopherol and α-tocopherol were the main isoforms, respectively. No tocotrienols were detected in any seed lot. As a proportion of total seed carotenoids, lutein was higher in the grain legumes than in their wild relatives, except for Arachis. When present, lutein epoxide, neoxanthin, violaxanthin, and antheraxanthin as a proportion of total carotenoids were lower in domesticated legume seeds (Figure 2A). As a proportion of total tocopherols, α-tocopherol was lower whereas γ-tocopherol was higher in domesticated plants (Figure 2A). The absolute content of lutein was lower in grain legumes than in their wild relatives, accounting for the lower amount of total carotenoids, whereas no consistent difference between grain legumes and their wild counterparts was found for the individual tocopherols (Figure 2B, Additional file 2, Additional file 3).Figure 2


Side-effects of domestication: cultivated legume seeds contain similar tocopherols and fatty acids but less carotenoids than their wild counterparts.

Fernández-Marín B, Milla R, Martín-Robles N, Arc E, Kranner I, Becerril JM, García-Plazaola JI - BMC Plant Biol. (2014)

Composition of carotenoids and tocopherols in seeds of grain legumes and their closest wild relatives. (A) Individual carotenoids and tocopherols are expressed as proportions of total contents. Data are means (n = 5). (B) Bisector plots representing the absolute contents of carotenoids and tocopherols in grain legumes plotted against their closest wild relatives (only compounds shared among most species are shown). Data points below the dotted line (y = x) indicate that grain legumes contained less seed carotenoids or tocopherols than their wild relatives.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4302433&req=5

Fig2: Composition of carotenoids and tocopherols in seeds of grain legumes and their closest wild relatives. (A) Individual carotenoids and tocopherols are expressed as proportions of total contents. Data are means (n = 5). (B) Bisector plots representing the absolute contents of carotenoids and tocopherols in grain legumes plotted against their closest wild relatives (only compounds shared among most species are shown). Data points below the dotted line (y = x) indicate that grain legumes contained less seed carotenoids or tocopherols than their wild relatives.
Mentions: The composition of individual carotenoids and tocopherols in grain legumes also differed from that of their wild relatives (Figure 2). Lutein was the predominant carotenoid in all the species, followed by zeaxanthin and β-carotene (Figure 2A), except for the Vigna wild relative. Of all tocopherols, γ-tocopherol was the most abundant isoform in all species, except for Vigna and Arachis monticola, where δ − tocopherol and α-tocopherol were the main isoforms, respectively. No tocotrienols were detected in any seed lot. As a proportion of total seed carotenoids, lutein was higher in the grain legumes than in their wild relatives, except for Arachis. When present, lutein epoxide, neoxanthin, violaxanthin, and antheraxanthin as a proportion of total carotenoids were lower in domesticated legume seeds (Figure 2A). As a proportion of total tocopherols, α-tocopherol was lower whereas γ-tocopherol was higher in domesticated plants (Figure 2A). The absolute content of lutein was lower in grain legumes than in their wild relatives, accounting for the lower amount of total carotenoids, whereas no consistent difference between grain legumes and their wild counterparts was found for the individual tocopherols (Figure 2B, Additional file 2, Additional file 3).Figure 2

Bottom Line: Unexpectedly, we found that following domestication, the contents of carotenoids, including lutein and zeaxanthin, decreased in all ten species (total carotenoid content decreased 48% in average).An undirected change in the contents of tocopherols and fatty acids was found, with contents increasing in some species and decreasing in others, independently of the changes in carotenoids.In some species, polyunsaturated fatty acids (linolenic acid especially), α-tocopherol and γ-tocopherol decreased following domestication.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Apdo. 644, 48080, Bilbao, Spain. beatriz.fernandezm@ehu.es.

ABSTRACT

Background: Lipophilic antioxidants play dual key roles in edible seeds (i) as preservatives of cell integrity and seed viability by preventing the oxidation of fats, and (ii) as essential nutrients for human and animal life stock. It has been well documented that plant domestication and post-domestication evolution frequently resulted in increased seed size and palatability, and reduced seed dormancy. Nevertheless, and surprisingly, it is poorly understood how agricultural selection and cultivation affected the physiological fitness and the nutritional quality of seeds. Fabaceae have the greatest number of crop species of all plant families, and most of them are cultivated for their highly nutritious edible seeds. Here, we evaluate whether evolution of plants under cultivation has altered the integrated system formed by membranes (fatty acids) and lipophilic antioxidants (carotenoids and tocopherols), in the ten most economically important grain legumes and their closest wild relatives, i.e.: Arachis (peanut), Cicer (chickpea), Glycine (soybean), Lathyrus(vetch), Lens (lentil), Lupinus (lupin), Phaseolus (bean), Pisum (pea), Vicia (faba bean) and Vigna (cowpea).

Results: Unexpectedly, we found that following domestication, the contents of carotenoids, including lutein and zeaxanthin, decreased in all ten species (total carotenoid content decreased 48% in average). Furthermore, the composition of carotenoids changed, whereby some carotenoids were lost in most of the crops. An undirected change in the contents of tocopherols and fatty acids was found, with contents increasing in some species and decreasing in others, independently of the changes in carotenoids. In some species, polyunsaturated fatty acids (linolenic acid especially), α-tocopherol and γ-tocopherol decreased following domestication.

Conclusions: The changes in carotenoids, tocopherols and fatty acids are likely side-effects of the selection for other desired traits such as the loss of seed dormancy and dispersal mechanisms, and selection for seed storability and taste. This work may serve as baseline to broaden our knowledge on the integrated changes on crop fitness and nutritional quality following domestication.

Show MeSH