Role of sucrose in modulating the low-nitrogen-induced accumulation of phenolic compounds in lettuce (Lactuca sativa L.).
carbon resource
nitrogen
nitrogen assimilation
phenolic metabolism
sucrose
Journal
Journal of the science of food and agriculture
ISSN: 1097-0010
Titre abrégé: J Sci Food Agric
Pays: England
ID NLM: 0376334
Informations de publication
Date de publication:
Dec 2020
Dec 2020
Historique:
received:
17
04
2020
revised:
11
06
2020
accepted:
19
06
2020
pubmed:
21
6
2020
medline:
23
4
2021
entrez:
21
6
2020
Statut:
ppublish
Résumé
Phenolic compounds are phytochemicals present in vegetables which contribute to human health. Although nitrogen deficiency and sucrose (Suc) are linked to phenolic production in vegetables, the relationship between them in the regulation of phenolic biosynthesis remains unknown. This study investigated the potential role of Suc in regulating phenolic biosynthesis of lettuce under low-nitrogen (LN) conditions. Our results showed that LN treatment significantly increased Suc content in lettuce by inducing rapid increases in activities of sucrose synthesis-related enzymes. Exogenous Suc further stimulated LN-induced phenolic accumulation in lettuce by upregulating the expression of genes (PAL, CHS, F3H, DFR, F35H and UFGT) involved in phenolic biosynthesis. The opposite effects were true for exogenous 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) application. No changes were observed in chlorophyll content in LN-treated lettuce, in either the presence or absence of Suc application. Notably, exogenous DCMU resulted in decreases of maximum quantum efficiency of photosystem II (PSII) photochemistry, actual efficiency of PSII and electron transport rate in PSII and increase of quantum yield of non-regulated energy dissipation in PSII in lettuce under LN conditions, whereas these effects were reversed on Suc application. Exogenous Suc also increased glutamine synthetase and glutamate synthase activities in LN-treated lettuce. These results suggest that Suc is involved in LN-induced phenolic production in lettuce by enhancing photosynthetic and nitrogen assimilation efficiency to increase the supply of carbon resources and precursors for phenolic biosynthesis. © 2020 Society of Chemical Industry.
Sections du résumé
BACKGROUND
BACKGROUND
Phenolic compounds are phytochemicals present in vegetables which contribute to human health. Although nitrogen deficiency and sucrose (Suc) are linked to phenolic production in vegetables, the relationship between them in the regulation of phenolic biosynthesis remains unknown. This study investigated the potential role of Suc in regulating phenolic biosynthesis of lettuce under low-nitrogen (LN) conditions.
RESULTS
RESULTS
Our results showed that LN treatment significantly increased Suc content in lettuce by inducing rapid increases in activities of sucrose synthesis-related enzymes. Exogenous Suc further stimulated LN-induced phenolic accumulation in lettuce by upregulating the expression of genes (PAL, CHS, F3H, DFR, F35H and UFGT) involved in phenolic biosynthesis. The opposite effects were true for exogenous 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) application. No changes were observed in chlorophyll content in LN-treated lettuce, in either the presence or absence of Suc application. Notably, exogenous DCMU resulted in decreases of maximum quantum efficiency of photosystem II (PSII) photochemistry, actual efficiency of PSII and electron transport rate in PSII and increase of quantum yield of non-regulated energy dissipation in PSII in lettuce under LN conditions, whereas these effects were reversed on Suc application. Exogenous Suc also increased glutamine synthetase and glutamate synthase activities in LN-treated lettuce.
CONCLUSIONS
CONCLUSIONS
These results suggest that Suc is involved in LN-induced phenolic production in lettuce by enhancing photosynthetic and nitrogen assimilation efficiency to increase the supply of carbon resources and precursors for phenolic biosynthesis. © 2020 Society of Chemical Industry.
Substances chimiques
Phenols
0
Chlorophyll
1406-65-1
Sucrose
57-50-1
Nitrogen
N762921K75
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5412-5421Subventions
Organisme : National Natural Science Foundation of China
ID : 31872167
Organisme : Zhejiang University
Informations de copyright
© 2020 Society of Chemical Industry.
Références
Deng GF, Lin X, Xu XR, Gao LL, Xie JF and Li HB, Antioxidant capacities and total phenolic contents of 56 vegetables. J Funct Foods 5:260-266 (2013).
Tsao R, Chemistry and biochemistry of dietary polyphenols. Nutrients 2:1231-1246 (2010).
Zhang H and Tsao R, Dietary polyphenols, oxidative stress and antioxidant and anti-inflammatory effects. Curr Opin Food Sci 8:33-42 (2016).
Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S and Tattini M, Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35-45 (2013).
Sarkar D and Shetty K, Metabolic stimulation of plant phenolics for food preservation and health. Annu Rev Food Sci Technol 5:395-413 (2014).
Wang R, Wang GL and Ning Y, PALs: emerging key players in broad-spectrum disease resistance. Trends Plant Sci 24:785-787 (2019).
Yuan Q and Zhao L, The mulberry (Morus alba L.) fruit: a review of characteristic components and health benefits. J Agric Food Chem 65:10383-10394 (2017).
Lillo C, Lea US and Ruoff P, Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 31:587-601 (2008).
Carbone F, Preuss A, De Vos RC, D'Amico E, Perrotta G, Bovy AG et al., Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ 32:1117-1131 (2009).
Wang Y and Frei M, Stressed food: the impact of abiotic environmental stresses on crop quality. Agric Ecosyst Environ 141:271-286 (2011).
Marin A, Ferreres F, Barbera GG and Gil MI, Weather variability influences color and phenolic content of pigmented baby leaf lettuces throughout the season. J Agric Food Chem 63:1673-1681 (2015).
Su N, Wu Q and Cui J, Increased sucrose in the hypocotyls of radish sprouts contributes to nitrogen deficiency-induced anthocyanin accumulation. Front Plant Sci 7:1976 (2016).
Qadir O, Siervo M, Seal CJ and Brandt K, Manipulation of contents of nitrate, phenolic acids, chlorophylls, and carotenoids in lettuce (Lactuca sativa L.) via contrasting responses to nitrogen fertilizer when grown in a controlled environment. J Agric Food Chem 65:10003-10010 (2017).
Zhou W, Chen Y, Xu H, Liang X, Hu Y, Jin C et al., Short-term nitrate limitation prior to harvest improves phenolic compound accumulation in hydroponic-cultivated lettuce (Lactuca sativa L.) without reducing shoot fresh weight. J Agric Food Chem 66:10353-10361 (2018).
Zhou W, Liang X, Zhang Y, Li K, Jin B, Lu L et al., Reduced nitrogen supply enhances the cellular antioxidant potential of phenolic extracts through alteration of the phenolic composition in lettuce (Lactuca sativa L.). J Sci Food Agric 99:4761-4771 (2019).
Zhou W, Liang X, Dai P, Chen Y, Zhang Y, Zhang M et al., Alteration of phenolic composition in lettuce (Lactuca sativa L.) by reducing nitrogen supply enhances its anti-proliferative effects on colorectal cancer cells. Int J Mol Sci 20:4205 (2019).
Keunen E, Peshev D, Vangronsveld J, Van Den Ende W and Cuypers A, Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242-1255 (2013).
Ruan YL, Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33-67 (2014).
Ljung K, Nemhauser JL and Perata P, New mechanistic links between sugar and hormone signalling networks. Curr Opin Plant Biol 25:130-137 (2015).
Solfanelli C, Poggi A, Loreti E, Alpi A and Perata P, Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637-646 (2006).
Jia H, Wang Y, Sun M, Li B, Han Y, Zhao Y et al., Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol 198:453-465 (2013).
Jeong H, Sung J, Yang J, Kim Y, Jeong HS and Lee J, Effect of sucrose on the functional composition and antioxidant capacity of buckwheat (Fagopyrum esculentum M.) sprouts. J Funct Foods 43:70-76 (2018).
Harding SA, Jarvie MM, Lindroth RL and Tsai CJ, A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones. J Exp Bot 60:3443-3452 (2009).
Boussadia O, Steppe K, Zgallai H, Ben El Hadj S, Braham M, Lemeur R et al., Effects of nitrogen deficiency on leaf photosynthesis, carbohydrate status and biomass production in two olive cultivars ‘Meski’ and ‘Koroneiki’. Sci Hortic 123:336-342 (2010).
Becker C, Urlić B, Jukić Špika M, Kläring H, Krumbein A, Baldermann S et al., Nitrogen limited red and green leaf lettuce accumulate flavonoid glycosides, caffeic acid derivatives, and sucrose while losing chlorophylls, β-carotene and xanthophylls. PLoS One 10:e0142867 (2015).
Kim MJ, Moon Y, Tou JC, Mou B and Waterland NL, Nutritional value, bioactive compounds and health benefits of lettuce (Lactuca sativa L.). J Food Compos Anal 49:19-34 (2016).
Zlotek U, Swieca M and Jakubczyk A, Effect of abiotic elicitation on main health-promoting compounds, antioxidant activity and commercial quality of butter lettuce (Lactuca sativa L.). Food Chem 148:253-260 (2014).
Jia ZS, Tang MC and Wu J, The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555-559 (1999).
Mphahlele RR, Stander MA, Fawole OA and Opara UL, Effect of fruit maturity and growing location on the postharvest contents of flavonoids, phenolic acids, vitamin C and antioxidant activity of pomegranate juice (cv. Wonderful). Sci Hortic 179:36-45 (2014).
Filip M, Vlassa M, Coman V and Halmagyi A, Simultaneous determination of glucose, fructose, sucrose and sorbitol in the leaf and fruit peel of different apple cultivars by the HPLC-RI optimized method. Food Chem 199:653-659 (2016).
Klann EM, Chetelat RT and Bennett BA, Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol 103:863-870 (1993).
Ranwala AP, Shun-Suke I and Hiroshi M, Acid and neutral invertases in the mesocarp of developing muskmelon (Cucumis melo L. cv Prince) fruit. Plant Physiol 96:881-886 (1991).
Arnon DI, Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1-10 (1949).
Tang QY and Zhang CX, Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci 20:254-260 (2013).
Caretto S, Linsalata V, Colella G, Mita G and Lattanzio V, Carbon fluxes between primary metabolism and phenolic pathway in plant tissues under stress. Int J Mol Sci 16:26378-26394 (2015).
Canton FR, Suarez FM and Canovas MF, Molecular aspects of nitrogen mobilization and recycling in trees. Photosynth Res 83:265-278 (2005).
Rosa M, Prado C, Podazza G, Interdonato R, Gonzalez JA, Hilal M et al., Soluble sugars-metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388-393 (2009).
Teng S, Keurentjes J, Bentsink L, Koornneef M and Smeekens S, Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139:1840-1852 (2005).
Lin XY, Ye YQ, Fan SK, Jin CW and Zheng SJ, Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant Physiol 170:907-920 (2016).
Takahashi S and Badger MR, Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53-60 (2011).
Singh S, Lewis NG and Neil Towers GH, Nitrogen recycling during phenylpropanoid metabolism in sweet potato tubers. J Plant Physiol 153:316-323 (1998).
Bittsanszky A, Pilinszky K, Gyulai G and Komives T, Overcoming ammonium toxicity. Plant Sci 231:184-190 (2015).