The effect of temperature and radiation on flavonol aglycones and flavonol glycosides of kale (Brassica oleracea var. sabellica)
Highlights
► Temperature and radiation influence flavonol glycosides in kale structure-dependent. ► Establishment of compound–climate relationship for flavonol aglycones and glycosides for the first time. ► Low temperature induce antioxidant relevant quercetin glycosides.
Introduction
Climate simulations for central and northern Europe indicated in various scenario runs that, as a result of greenhouse gases in the atmosphere, warming in these regions will be most noticeable in late autumn and winter, whereas radiation is still being degraded in this season (Räisänen & Ruokolainen, 2008). In calculations, eight to nine months per year were expected to be warmer than the median for 1971–2000 worldwide (Räisänen & Ruokolainen, 2008). Even though it has been predicted that warmer temperatures will affect biochemical processes in plants (Chmura et al., 2011), there is a lack of information about the influence of increasing temperatures in winter on secondary plant compounds, such as flavonoids. Flavonols belong to the flavonoids and were associated with protective effects against several types of cancer (Knekt et al., 2002) and cardiovascular diseases (Lin et al., 2007) due to their antioxidant potential, especially quercetin (Williams, Spencer, & Rice-Evans, 2004). In human beings the absorption of quercetin glycosides, except the rhamnoglucoside rutin, is higher than that of the quercetin aglycone (Manach, Williamson, Morand, Scalbert, & Rémésym, 2005). Zietz et al., 2010 found that quercetin glycosides had a higher antioxidant potential than their corresponding kaempferol glycosides in kale.
Flavonoids could be influenced by climate conditions such as temperature and radiation. Low temperature enhanced phenolic compounds and total flavonoids as a result of enzymatic repair inhibition, combined with higher quantities of reactive oxygen species (ROS) (Bilger et al., 2007, Klimov et al., 2008), e.g. Harbaum-Piayda et al. (2010) found that the concentration of kaempferol glycosides was higher at 9 °C than at 22 °C in pak choi (Brassica rapa var. chinensis) in a greenhouse experiment. Additionally, flavonoids protect plants from radiation damage, acting as shielding components and strong scavengers of reactive oxygen species (ROS) (Edreva, 2005). Most studies investigated the impact of UV-B on flavonoids (Jansen, Hectors, O’Brien, Guisez, & Potters, 2008). In soybean leaves the quercetin glycosides were lower when UV-B was excluded (Winter & Rostás, 2008). The reduction of radiation was associated with lower concentrations of flavonoids for the perennial woody species Ligustrum vulgare and Phillyrea latifoilia (Agati & Tattini, 2010), as well as for the annual leafy species Brassica rapa and Brassica juncea (Fallovo, Schreiner, Schwarz, Colla, & Krumbein, 2011).
As a leafy vegetable, kale (Brassica oleracea var. sabellica), rich in health-promoting flavonols (Hertog, Hollman, & Katan, 1992), is commonly cultivated in central and northern Europe, as well as in North America. Together with broccoli, brussel sprouts and cabbage, it belongs to the Brassicaceae family. As a winter crop, kale is exposed to low temperature but also grows at low radiation. Kale has high concentrations of the flavonol aglycones kaempferol and quercetin, followed by isorhamnetin (Fig. 1) (Huang, Wang, Eaves, Shikany, & Pace, 2007). The total concentration of these flavonol aglycones ranged between 6.0 and 14.8 mg g−1 dry matter, which relates to 97.4–298.5 mg 100 g−1 fresh matter (Schmidt et al., 2010a). In particular the traditional, old cvs Altmärker Braunkohl, Halbhoher grüner Krauser and Lerchenzunge provide a high total concentration of flavonols (Schmidt et al., 2010a). In addition, detailed identification has revealed that kale has a naturally occurring complex profile of flavonol glycosides (Ferreres et al., 2009, Lin and Harnly, 2009, Olsen et al., 2009, Schmidt et al., 2010b). A total of 71 flavonol glycosides have been identified by HPLC–DAD–ESI–MSn in different kale cultivars, including 27 non-acylated, 30 monoacylated and 14 diacylated glycosides (Schmidt et al., 2010b). Flavonol glycosides were acylated with p-coumaroyl, caffeoyl, feruloyl, hydroxyferuloyl and sinapoyl residues (Fig. 1).
While temperature and radiation treatments are often focused on flavonol aglycones or total flavonols (Fallovo et al., 2011, Olsen et al., 2010, Schmidt et al., 2010a) our investigations were additionally extended on structurally different flavonol glycosides. The aim of the present study was to investigate whether and how the climate factors of temperature and radiation in European winter influence the formation of flavonol glycosides, as they differ distinctly in their chemical structure by various glycosylation and acylation patterns. To the best of our knowledge, we established a compound–climate relationship for temperature and photosynthetic active radiation (PAR) to quantify plant response to synthesising climate-dependent flavonol aglycones and flavonol glycosides for the first time.
Section snippets
Plant material and experimental design
Eight kale cultivars were set in a randomised block design, with three replicates, on the experimental fields at the Leibniz-Institute of Vegetable and Ornamental Crops Grossbeeren/Erfurt e.V. (Grossbeeren, Germany) for two years (experiments I and II): F1 hybrids: ‘Winterbor’ (by Bruno Nebelung, Norken, Germany), ‘Redbor’ (by Chrestensen, Erfurt, Germany), ‘Winnetou’ (by Bruno Nebelung, Norken, Germany) and ‘Arsis’ (by Gärtner Pötschke, Kaarst, Germany); traditional old cultivars: ‘Altmärker
Results and discussion
The leafy Brassica vegetable kale has structurally different flavonol glycosides and is therefore a suitable model plant for investigating the structure-specific formation of flavonol glycosides with respect to climate effects. The following major flavonol glycosides were considered: the non-acylated triglucoside quercetin-3-O-sophoroside-7-O-d-glucoside and the corresponding kaempferol-3-O-sophoroside-7-O-d-glucoside, the monoacylated triglucoside quercetin-3-O-sinapoyl-sophoroside-7-O-d
Conclusion
Since kale is characterised by various glycosylated and acylated flavonol glycosides, it is a suitable model plant to quantify the plant’s response to climate change by flavonol formation. In our experiment, it was demonstrated that not only the cultivar but also the year and harvest time, both characterised by temperature and radiation, influenced the flavonol profile in kale. The flavonol concentration and the major flavonol aglycones quercetin and kaempferol responded virtually identically
Acknowledgements
We sincerely thank Elke Büsch and Ursula Zentner for conducting the growth experiments and technical assistance. This study was funded by the DFG (Projects: KR-2066/3-1 and KR-1452/12-1).
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