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. 2023 Feb 14:14:1124750.
doi: 10.3389/fpls.2023.1124750. eCollection 2023.

Regulation of carotenoid and flavonoid biosynthetic pathways in Lactuca sativa var capitate L. in protected cultivation

Vanessa Harbart  1   2 , Katja Frede  1 , Maria Fitzner  1   2 , Susanne Baldermann  1   3
Affiliations

Regulation of carotenoid and flavonoid biosynthetic pathways in Lactuca sativa var capitate L. in protected cultivation

Vanessa Harbart et al. Front Plant Sci. .

Abstract

In the face of a growing world population and limited land, there is an urgent demand for higher productivity of food crops, and cultivation systems must be adapted to future needs. Sustainable crop production should aim for not only high yields, but also high nutritional values. In particular, the consumption of bioactive compounds such as carotenoids and flavonoids is associated with a reduced incidence of non-transmissible diseases. Modulating environmental conditions by improving cultivation systems can lead to the adaption of plant metabolisms and the accumulation of bioactive compounds. The present study investigates the regulation of carotenoid and flavonoid metabolisms in lettuce (Lactuca sativa var capitate L.) grown in a protected environment (polytunnels) compared to plants grown without polytunnels. Carotenoid, flavonoid and phytohormone (ABA) contents were determined using HPLC-MS and transcript levels of key metabolic genes were analyzed by RT-qPCR. In this study, we observed inverse contents of flavonoids and carotenoids in lettuce grown without or under polytunnels. Flavonoid contents on a total and individual level were significantly lower, while total carotenoid content was higher in lettuce plants grown under polytunnels compared to without. However, the adaptation was specific to the level of individual carotenoids. For instance, the accumulation of the main carotenoids lutein and neoxanthin was induced while the β-carotene content remained unchanged. In addition, our findings suggest that the flavonoid content of lettuce depends on transcript levels of the key biosynthetic enzyme, which is modulated by UV light. A regulatory influence can be assumed based on the relation between the concentration of the phytohormone ABA and the flavonoid content in lettuce. In contrast, the carotenoid content is not reflected in transcript levels of the key enzyme of either the biosynthetic or the degradation pathway. Nevertheless, the carotenoid metabolic flux determined using norflurazon was higher in lettuce grown under polytunnels, suggesting posttranscriptional regulation of carotenoid accumulation, which should be an integral part of future studies. Therefore, a balance needs to be found between the individual environmental factors, including light and temperature, in order to optimize the carotenoid or flavonoid contents and to obtain nutritionally highly valuable crops in protected cultivation.

Keywords: UV; bioactive compounds; carotenoid; crop cultivation; flavonoid; greenhouse; lettuce; metabolism.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Impact on carotenoid and flavonoid biosynthetic pathways in plants. Arrows with dashed lines indicate more than one reaction, arrows with continuous lines indicate one reaction; key enzymes of flavonoid and carotenoid pathways are highlighted by colored boxes; black squares indicate metabolites identified in lettuce in this study. CHS, Chalcone synthase; PSY, Phytoene synthase; CCD4, Carotenoid cleavage dioxygenase4; OR, Orange protein; UVR8, Ultraviolet resistance locus8; HY5, Elongated hypocotyl5; PIF1, Phytochrome interacting factor1; DMAPP, dimethylallyl diphosphate; IPP, isopentenyl diphosphate; GGPP, geranylgeranyl diphosphate; MEP/DOXP, mevalonate/non-mevalonate pathway.
Figure 2
Figure 2
Differences in light intensity and light quality without and under polytunnels. (A, B) UV, and (C) PAR transmittance (%) of polytunnel materials with and without antifogging additives compared to without polytunnels, (D) UVA/B ratio, and (E) UV/PAR ratio. Measurements were conducted within the second experimental repetition (in May). Data represent mean ± SD (n = 4). Different letters indicate significant differences (p ≤ 0.05); no letters indicate no significance. UV, ultraviolet; PAR, photosynthetic active radiation.
Figure 3
Figure 3
Flavonoids in lettuce cultivated without or under polytunnels. (A) Individual, and (B) total content of flavonoid glycosides (μg mg-1 DM) in lettuce grown without or under polytunnels with and without antifogging additives. The first experimental repetition in April is shown. The data are expressed as mean ± SE (n = 4). Significant differences (p ≤ 0.05) between treatment of individual compounds and total content are indicated by different letters. Gc, glucuronide; MG, malonyl glucoside.
Figure 4
Figure 4
Total carotenoid content affected by polytunnel cultivation. Carotenoid content (ng mg-1 DM) in lettuce grown without or under polytunnels with and without antifogging additives. (A) Individual carotenoids β-/ϵ-branch and downstream, (B) upper pathway metabolite phytoene, and (C) total carotenoids. First experimental repetition in April is shown. The data are expressed as mean ± SE (n = 4). Significant differences (p ≤ 0.05) between treatment of individual compounds and total content are indicated by different letters; no letters indicate absence of significance.
Figure 5
Figure 5
Gene transcripts for key enzymes of the core carotenoid and flavonoid biosynthesis pathways. Transcript levels of (A) HY5, (B) PIF1, (C) UVR8, (D) PSY, (E) CCD4, (F) CHS, (G) OR, and (H) OR-like in lettuce grown without or under polytunnels with and without antifogging additives. The first experimental repetition in April is shown. The data are expressed as Box-Whisker-Plots (n = 4); Whiskers show maximal and minimal values. Data was normalized to lettuce grown without polytunnels. Different letters indicate significant differences (p ≤ 0.05) of transcripts under different cultivation conditions; no letters indicate absence of significance. HY5, Elongated hypocotyl5; PIF1, Phytochrome interacting factor1; UVR8, Ultraviolet resistance locus8; PSY, Phytoene synthase; CCD4, Carotenoid cleavage dioxygenase4; CHS, Chalcone synthase; OR, Orange protein; OR-like, Orange-like protein.
Figure 6
Figure 6
Phytohormone ABA content in lettuce. Abscisic acid content (ng mg-1 DM) in lettuce grown without or under polytunnels with and without antifogging additives. The first experimental repetition in April is shown. The data are expressed as mean ± SE (n = 4). Different letters indicate significant differences (p ≤ 0.05).
Figure 7
Figure 7
Metabolic flux of the carotenoid pathway determined with norflurazon. Relative phytoene accumulation in lettuce grown without or under polytunnels with and without antifogging additives. Lettuce was treated with the bleaching herbicide norflurazone (NFZ) or with water as a control (C). The data are expressed as mean ± SE of two independent experimental repetitions (each with n = 4). Data were normalized to NFZ lettuce cultivation without polytunnels (indicated by the black line). Asterisks indicate significant differences of NFZ treatment to control (p ≤ 0.05), whereas different letters indicate significant differences due to cultivation condition (p ≤ 0.05).
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Grants and funding

This work was supported by the Landwirtschaftliche Rentenbank “Research for innovations in the agricultural sector” (grant number 854 798) as part of the PermAFog project.

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