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. 2024 Mar 26;25(7):3677.
doi: 10.3390/ijms25073677.

Adjustments of the Phytochemical Profile of Broccoli to Low and High Growing Temperatures: Implications for the Bioactivity of Its Extracts

Ivana Šola  1 , Daria Gmižić  1 , Marija Pinterić  2 , Ana Tot  3 , Jutta Ludwig-Müller  4
Affiliations

Adjustments of the Phytochemical Profile of Broccoli to Low and High Growing Temperatures: Implications for the Bioactivity of Its Extracts

Ivana Šola et al. Int J Mol Sci. .

Abstract

Climate change causes shifts in temperature patterns, and plants adapt their chemical content in order to survive. We compared the effect of low (LT) and high (HT) growing temperatures on the phytochemical content of broccoli (Brassica oleracea L. convar. botrytis (L.) Alef. var. cymosa Duch.) microgreens and the bioactivity of their extracts. Using different spectrophotometric, LC-MS/MS, GC-MS, and statistical methods, we found that LT increased the total phenolics and tannins in broccoli. The total glucosinolates were also increased by LT; however, they were decreased by HT. Soluble sugars, known osmoprotectants, were increased by both types of stress, considerably more by HT than LT, suggesting that HT causes a more intense osmotic imbalance. Both temperatures were detrimental for chlorophyll, with HT being more impactful than LT. HT increased hormone indole-3-acetic acid, implying an important role in broccoli's defense. Ferulic and sinapic acid showed a trade-off scheme: HT increased ferulic while LT increased sinapic acid. Both stresses decreased the potential of broccoli to act against H2O2 damage in mouse embryonal fibroblasts (MEF), human keratinocytes, and liver cancer cells. Among the tested cell types treated by H2O2, the most significant reduction in ROS (36.61%) was recorded in MEF cells treated with RT extracts. The potential of broccoli extracts to inhibit α-amylase increased following both temperature stresses; however, the inhibition of pancreatic lipase was increased by LT only. From the perspective of nutritional value, and based on the obtained results, we conclude that LT conditions result in more nutritious broccoli microgreens than HT.

Keywords: Brassicaceae; ROS; auxins; climate change; metabolic response; microgreens; photosynthetic pigments; polyphenolics; temperature stress; vitamin C.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
The impact of different concentrations of extracts from broccoli cultivated under room (RT), high (HT), and low (LT) temperature on the levels of ROS within (a) mouse embryonal fibroblasts (MEF), (b) normal human keratinocytes (HaCaT), (c) hepatocellular carcinoma (HepG2), (d) colorectal carcinoma (HCT116), and (e) lung carcinoma (H460) cell cultures. Values represent mean ± standard deviation of three biological replicates. Different letters indicate a significant difference between the RT, HT, and LT broccoli microgreens, separately for each extract concentration (ANOVA, Duncan test, p ≤ 0.05). An asterisk (*) indicates a significant difference between each group of cells treated with broccoli microgreen extracts and control cells (Student’s t-test, p ≤ 0.05). A double asterisk (**) indicates a significant difference between cells treated with H2O2 only and cells treated simultaneously with H2O2 and broccoli extract at a 0.05 mg/mL concentration (Student’s t-test, p ≤ 0.05). AU = arbitrary units; Con = control cells; DCF = dichlorodihydrofluorescein; FI = fluorescence intensity.
Figure 2
Figure 2
The principal component analysis showing (a) the relation between broccoli microgreens grown under room (RT), high (HT), and low (LT) temperatures based on the analyzed variables, whose grouping is shown in the (b) part of the figure. ABA = abscisic acid; Car = carotenoids; cc = conjugated compound; Chl = chlorophyll; fc = free compound; FerA= ferulic acid; GLS = total intact glucosinolates; H2O2 = hydrogen peroxide; H460 = lung carcinoma; HaCaT = normal human keratinocytes; HCT116 = colorectal carcinoma; HepG2 = hepatocellular carcinoma; IAA = indole-3-acetic acid; K = kaempferol; L-asc = L-ascorbic acid, MEF = mouse embryonal fibroblasts; Porf = porphyrins; PROT = total proteins; Q = quercetin; SinA = sinapic acid; SS = total soluble sugars; TA = total monomeric anthocyanins; TF = total flavonoids; TFlo = total flavonols; THCA = total hydroxycinnamic acids; TP = total phenolics; TPA = total phenolic acids; TPAN = total proanthocyanidins; TT = total tannins.
Figure 3
Figure 3
Hierarchical clustering of broccoli microgreens grown at room (RT), high (HT), and low (LT) temperature expressed as Euclidean distance, based on the measured total and individual bioactive compounds, their pigments, their hormones, the ability to inhibit lipase, the antioxidant capacity, and their effect on the intracellular levels of ROS in different cell types.
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