Broccoli: Comparison
Please note this is a comparison between Version 4 by Nicole Yin and Version 3 by Rocio González Barrio.

Broccoli is one of the jewels of the horticultural crops worldwide, belonging to the cruciferous family and very rich in key nutrients (vitamins, minerals, fibre, etc.) as well as a great group of bioactive compounds including carotenoids, phenolic compounds and glucosinolates. Among these phytochemicals, the most-studied in crucifers associated with disease prevention and wellbeing are glucosinolates [See also https://encyclopedia.pub/808]. The content of carotenoids, phenolic compounds and glucosinolates naturally present in broccoli, can be increased through the management and control of the agronomic and environmental conditions used for broccoli cultivation. In this sense, the study of the effects of pre-harvest factors in the concentration of health-promoting compounds in broccoli, as a new strategy to be implemented in the field, can be considered of great interest. This would help to determine the best agronomic practices and cultivation conditions to improve the content of the compounds of interest in broccoli, without compromising its overall quality.

  • carotenoids
  • phenolic compounds
  • glucosinolates
  • bioactive compounds
  • pre-harvest factors
  • quality composition
  • methyl jasmonate
  • seasonal variations

1. Introduction

The Brassica family is a group of vegetables widely consumed around the world, including cabbages, cauliflower, Brussels sprouts, radishes and broccoli (Brassica oleracea L. var. italica) among others [1][1]. In the last few years, the consumption of cruciferous foods in Spain has increased. Specifically, the consumption of broccoli has undergone a significant rise, with a positive effect on the agricultural economy, particularly in the Murcia region (southeastern Spain), which is the region with the greatest production of broccoli in Europe [2,3][2][3]. This rise in consumption is related to increased adherence to healthier diets by European consumers, since this family of vegetables, and particularly broccoli, has high contents of fiber, minerals and vitamins, and is an important source of bioactive compounds with high antioxidant activity (carotenoids, phenolic compounds and glucosinolates) [4][4].

2. Bioactive compounds contents and influencing factors

Although a single serving of broccoli provides a wide range of phytochemicals with beneficial effects for human health [1][1], the contents of these compounds vary depending on physiological, genetic and agronomic factors (including the cultivar, soil composition, agronomic treatments, climatic conditions and pre- and post-harvest treatments [5,6][5][6]). Carotenoids, one of the characteristic groups of compounds in broccoli, are natural pigments derived from the isoprenoid pathway, and are formed of a C40 backbone that differs according to the specific carotenoid being considered [7][7]. Carotenoid content can vary in broccoli plants as a result of environmental conditions—mainly temperature and sunlight [8,9][8][9]—while genetic factors and treatment applications can also affect the content [10][10]. Moreover, the content varies among the distinct parts of the plant, being higher in florets than in stalks [11][11]. The major carotenoids found in broccoli are β-carotene and lutein [12][12]. Phenolic compounds comprise one or more aromatic rings attached to hydroxyl groups [13][13]. Quercetin and kaempferol are the main flavonol glycosides, whereas chlorogenic and sinapic derivatives are the main hydroxycinnamic acid derivatives found in broccoli [14,15][14][15]. Glucosinolates (GLSs) are constituted by a thioglucose group, a sulphonated oxime group and a side chain derived from methionine, phenylalanine, tryptophan or a branched-chain amino acid [16][16]. Glucoraphanin (GRA), glucoiberin (GIB) and glucobrassicin (GBS) are the major GLSs in broccoli [17[17][18],18], and their breakdown products  the isothiocyanates (ITC) and indoles  are important due to their health-promoting activities, being strong inducers of phase II detoxification enzymes by regulation of the Nrf2–Keap1–ARE cellular system,  with a wide role in the  development and progression of  chronic diseases (e.g., cancers, respiratory problems and type 2 diabetes mellitus, and  their anti-inflammatory properties [19][19]. 

Long-term clinical studies, as well as in vivo and in vitro studies, have associated the consumption of broccoli and its phytochemicals, mainly GRA and its related ITC sulforaphane, with a reduction in the risk of suffering non-communicable-diseases (NCDs), such as metabolic syndrome (obesity, diabetes and dyslipidaemia) and some types of cancer (lung, stomach, colon and rectal) [19–21][19][20][21]. However, the amount of glucosinolatos ingested, the inter-individual variability among subjects, the bioaccessibility and bioavailability of these compounds, as well as the factors that affect phytochemical composition in the natural matrix( namely the production practices, handling, cooking procedures, among others), must be taken into account to provide scientific evidences of the health effects of bioactive compounds from broccoli [19][19]

For this reason, there is increased industrial interest in the improvement of the synthesis and accumulation of their bioactive compounds in plants, which naturally varies due to physiological, genetic and agronomic factors [6,22,23][6][22][23]. Additionally,  cooking practices also affect the content of GLSs and degree of conversion to their bioactive ITC [19][19]. With regard to improving the quality of the vegetables or the content of bioactive compounds, an increase in plant stress[6][24] [6,24] can lead to a higher synthesis of these secondary metabolites.

The management of agronomic and environmental conditions is very important to the content of phytochemicals. Broccoli shows little tolerance to cold and windy climates, preferring mild and bright environments with neutral soil pH [5][5]. Low temperatures can change the color of the florets from green to purple (anthocyanins), affecting the overall market acceptability. Elicitation is the main tool used to increase the content of secondary metabolites in vegetables, as it induces stress responses in plants. There are several types and classifications of elicitors; depending on their origin, we can differentiate among biotic, abiotic (chemical or physical) and phytohormones [23][23]. Another important classification is the time when the elicitor is applied; there are pre-harvest and post-harvest treatments, which can sometimes be combined. Several studies have involved the application of elicitors to broccoli plants in order to improve their nutritional properties (although this application is more common for seeds and sprouts). For instance, methionine, glucose, sucrose and mannitol applied as biotic elicitors during germination can increase the total contents of GLSs, anthocyanins and phenolics [25,26][25][26]. Ethanol and UV-C radiation have been used as abiotic, chemical and physical elicitors, respectively, and post-harvest treatments have led to an increase in GLSs and phenolic compounds [27,28][27][28]. Finally, for broccoli, phytohormones are probably the most-studied elicitor, while jasmonic acid (JA), methyl-jasmonate (MeJA) and salicylic acid are the most widely used, and have yielded increases in bioactive compounds in broccoli sprouts and adult plants [26][26]. Most of these studies have been performed under controlled conditions based on laboratory experiments or greenhouse control. However, in the scientific literature very few studies can be found under field conditions.

In this sense, a recent study has reported the results of a field-based experiment where three crop trials were carried out to evaluate the effects of seasonal and dosage application of methyl-jasmonate on ‘Parthenon’ broccoli, cultivated under real producing conditions in South-Eastern Spain [29][29]. Different quality parameters and the content of individual bioactive compounds (carotenoids, glucosinolates and phenolic compounds) were measured as authors hypothesed that the application of methyl-jasmonate treatments as elicitor in aerial parts of the plants would improve its content and accordingly its beneficial properties on health. The results showed that the use of methyl-jasmonate as preharvest treatment could be a new field strategy to improve the health-promoting compounds of ‘Parthenon’ broccoli, without compromising its overall quality. The results can be considered to be of great interest to grower and processor industries that sell broccoli and look for the best agronomic practices and conditions to offer healthier products to consumers.

References

  1. Fahey, J. Brassica: Characteristics and Properties. Encycl. Food Health 2016, 469–477.
  2. Food and Agriculture Organization Corporate Statistical Database (FAOSTAT). New Food Balances. Available online: http://www.fao.org/faostat/en/#data/FBS (accessed on 2 December 2019).
  3. Ministry of Agriculture, Fisheries and Food. Available online: https://www.mapa.gob.es/es/estadistica/temas/publicaciones/anuario-de-estadistica/2019/default.aspx?parte=3&capitulo=07&grupo=6&seccion=32 (accessed on 18 September 2020).
  4. Shi, J.; Gao, L.; Zuo, J.;Wang, Q.;Wang, Q.; Fan, L. Exogenous sodium nitroprusside treatment of broccoli florets extends shelf life, enhances antioxidant enzyme activity, and inhibits chlorophyll-degradation. Postharvest Boil. Technol. 2016, 116, 98–104.
  5. Branca, F. Cauliflower and Broccoli. In Handbook of Plant Breeding; Springer Science and Business Media LLC:Berlin, Germany, 2007; Volume 1, pp. 151–186.
  6. Ciancaleoni, S.; Onofri, A.; Torricelli, R.; Negri, V. Broccoli yield response to environmental factors in sustainable agriculture. Eur. J. Agron. 2016, 72, 1–9.
  7. Mijts, B.N.; Lee, P.C.; Schmidt-Dannert, C. Engineering Carotenoid Biosynthetic Pathways. Enzyme Eng.Evolut. Gen. Methods 2004, 388, 315–329.
  8. Schonhof, I.; Kläring, H.-P.; Krumbein, A.; Clausen,W.; Schreiner, M. Effect of temperature increase under low radiation conditions on phytochemicals and ascorbic acid in greenhouse grown broccoli. Agric. Ecosyst. Environ. 2007, 119, 103–111.
  9. Moreira-Rodríguez, M.; Nair, V.; Benavides, J.; Cisneros-Zevallos, L.; Jacobo-Velázquez, D.A. UVA, UVB Light, and Methyl Jasmonate, Alone or Combined, Redirect the Biosynthesis of Glucosinolates, Phenolics, Carotenoids, and Chlorophylls in Broccoli Sprouts. Int. J. Mol. Sci. 2017, 18, 2330.
  10. Neugart, S.; Baldermann, S.; Hanschen, F.S.; Klopsch, R.;Wiesner-Reinhold, M.; Schreiner, M. The intrinsic quality of brassicaceous vegetables: How secondary plant metabolites are a_ected by genetic, environmental, and agronomic factors. Sci. Hortic. 2018, 233, 460–478.
  11. Liu, M.; Zhang, L.; Ser, S.L.; Cumming, J.; Ku, K.-M. Comparative Phytonutrient Analysis of Broccoli By-Products: The Potentials for Broccoli By-Product Utilization. Molecules 2018, 23, 900.
  12. Dos Reis, L.C.R.; De Oliveira, V.R.; Hagenn, M.; Jablonski, A.; Flôres, S.H.; Rios, A.D.O. Carotenoids, flavonoids, chlorophylls, phenolic compounds and antioxidant activity in fresh and cooked broccoli (Brassica oleracea var. Avenger) and cauliflower (Brassica oleracea var. Alphina F1). LWT 2015, 63, 177–183.
  13. Minatel, I.O.; Borges, C.V.; Ferreira, M.I.; Gomez, H.A.; Chen, C.Y.; Lima, G.P. Phenolic Compounds: Functional Properties, Impact of Processing and Bioavailability. Phenolic Compd. Biol. Act. 2017, 1–24.
  14. Cartea, M.E.; Francisco, M.; Soengas, P.; Velasco, P. Phenolic Compounds in Brassica Vegetables. Molecules 2010, 16, 251–280.
  15. Vallejo, F.; Tomás-Barberán, F.A.; García-Viguera, C. Phenolic compound contents in edible parts of broccoli inflorescences after domestic cooking. J. Sci. Food Agric. 2003, 83, 1511–1516.
  16. Moreno, D.A.; Carvajal, M.; Lopez-Berenguer, C.; García-Viguera, C. Chemical and biological characterisation of nutraceutical compounds of broccoli. J. Pharm. Biomed. Anal. 2006, 41, 1508–1522.
  17. Je_ery, E.; E Stewart, K. Upregulation of Quinone Reductase by Glucosinolate Hydrolysis Products from Dietary Broccoli. Enzyme Eng. Evolut. Gen. Methods 2004, 382, 457–469.
  18. Chiu, Y.-C.; Matak, K.; Ku, K.-M. Methyl jasmonate treated broccoli: Impact on the production of glucosinolates and consumer preferences. Food Chem. 2019, 299, 125099.
  19. Quirante-Moya, S.; García-Ibañez, P.; Quirante-Moya, F.; Villaño, D.; Moreno, DA. The Role of Brassica Bioactives on Human Health: Are We Studying It the RightWay. Molecules, 2020, 25, 1591.
  20. Raiola, A.; Errico, A.; Petruk, G.; Monti, D.M.; Barone, A.; Rigano, M.M. Bioactive Compounds in Brassicaceae Vegetables with a Role in the Prevention of Chronic Diseases. Molecules 2017, 23, 15.
  21. Latté, K.P.; Appel, K.-E.; Lampen, A. Health benefits and possible risks of broccoli—An overview. Food Chem. Toxicol. 2011, 49, 3287–3309.
  22. Charron, C.S.; Saxton, A.M.; Sams, C.E. Relationship of climate and genotype to seasonal variation in the glucosinolate-myrosinase system. I. Glucosinolate content in ten cultivars of Brassica oleracea grown in fall and spring seasons. J. Sci. Food Agric. 2005, 85, 671–681.
  23. Baenas, N.; García-Viguera, C.; Moreno, D.A. Elicitation: A Tool for Enriching the Bioactive Composition of Foods. Molecules 2014, 19, 13541–13563.
  24. Asensio, E.; Sanvicente, I.; Mallor, C.; Menal-Puey, S. Spanish traditional tomato. E_ects of genotype, location and agronomic conditions on the nutritional quality and evaluation of consumer preferences. Food Chem. 2019, 270, 452–458.
  25. Guo, R.; Yuan, G.; Wang, Q. E_ect of sucrose and mannitol on the accumulation of health-promoting compounds and the activity of metabolic enzymes in broccoli sprouts. Sci. Hortic. 2011, 128, 159–165.
  26. Baenas, N.; García-Viguera, C.; Moreno, D.A. Biotic Elicitors E_ectively Increase the Glucosinolates Content in Brassicaceae Sprouts. J. Agric. Food Chem. 2014, 62, 1881–1889.
  27. Xu, F.; Chen, X.; Jin, P.;Wang, X.;Wang, J.; Zheng, Y. E_ect of ethanol treatment on quality and antioxidant activity in postharvest broccoli florets. Eur. Food Res. Technol. 2012, 235, 793–800.
  28. Duarte-Sierra, A.; Nadeau, F.; Angers, P.; Michaud, M.; Arul, J. UV-C hormesis in broccoli florets: Preservation, phyto-compounds and gene expression. Postharvest Boil. Technol. 2019, 157, 110965.
  29. Nuñez-Gómez, V.; Baenas, N.; Navarro-González, I.; García-Alonso, J.; Moreno, DA.; González-Barrio, R.; Periago, MJ. Seasonal Variation of Health-Promoting Bioactives in Broccoli and Methyl-Jasmonate Pre-Harvest Treatments to Enhance Their Contents. Foods. 2020. 9, 1971.

 

References

  1. J.W. Fahey; Brassica: Characteristics and Properties. Encyclopedia of Food and Health 2016, null, 469-477, 10.1016/b978-0-12-384947-2.00083-0.
  2. Food and Agriculture Organization Corporate Statistical Database (FAOSTAT). New Food Balances. Available online: http://www.fao.org/faostat/en/#data/FBS (accessed on 2 December 2019).
  3. Ministry of Agriculture, Fisheries and Food. Available online: https://www.mapa.gob.es/es/estadistica/temas/publicaciones/anuario-de-estadistica/2019/default.aspx?parte=3&capitulo=07&grupo=6&seccion=32 (accessed on 18 September 2020).
  4. Junyan Shi; Lipu Gao; Jinhua Zuo; Qing Wang; Qian Wang; Linlin Fan; Exogenous sodium nitroprusside treatment of broccoli florets extends shelf life, enhances antioxidant enzyme activity, and inhibits chlorophyll-degradation. Postharvest Biology and Technology 2016, 116, 98-104, 10.1016/j.postharvbio.2016.01.007.
  5. Branca, F. Cauliflower and Broccoli. In Handbook of Plant Breeding; Springer Science and Business Media LLC: Berlin, Germany, 2007; Volume 1, pp. 151–186.
  6. Ciancaleoni, S.; Onofri, A.; Torricelli, R.; Negri, V. Broccoli yield response to environmental factors in sustainable agriculture. Eur. J. Agron. 2016, 72, 1–9.
  7. Benjamin N Mijts; Pyung C Lee; Claudia Schmidt-Dannert; Engineering Carotenoid Biosynthetic Pathways. Methods in Enzymology 2004, 388, 315-329, 10.1016/s0076-6879(04)88025-x.
  8. Schonhof, I.; Kläring, H.-P.; Krumbein, A.; Clausen, W.; Schreiner, M. Effect of temperature increase under low radiation conditions on phytochemicals and ascorbic acid in greenhouse grown broccoli. Agric. Ecosyst. Environ. 2007, 119, 103–111.
  9. Moreira-Rodríguez, M.; Nair, V.; Benavides, J.; Cisneros-Zevallos, L.; Jacobo-Velázquez, D.A. UVA, UVB Light, and Methyl Jasmonate, Alone or Combined, Redirect the Biosynthesis of Glucosinolates, Phenolics, Carotenoids, and Chlorophylls in Broccoli Sprouts. Int. J. Mol. Sci. 2017, 18, 2330.
  10. Susanne Neugart; Susanne Baldermann; Franziska S. Hanschen; Rebecca Klopsch; Melanie Wiesner-Reinhold; Monika Schreiner; The intrinsic quality of brassicaceous vegetables: How secondary plant metabolites are affected by genetic, environmental, and agronomic factors. Scientia Horticulturae 2018, 233, 460-478, 10.1016/j.scienta.2017.12.038.
  11. Mengpei Liu; Lihua Zhang; Suk Lan Ser; Jonathan R Cumming; Kang-Mo Ku; Comparative Phytonutrient Analysis of Broccoli By-Products: The Potentials for Broccoli By-Product Utilization. Molecules 2018, 23, 900, 10.3390/molecules23040900.
  12. Luzia Caroline Ramos Dos Reis; Viviani Ruffo De Oliveira; Martine Elisabeth Kienzle Hagen; André Jablonski; Eliseu Rodrigues; Alessandro De Oliveira Rios; Carotenoids, flavonoids, chlorophylls, phenolic compounds and antioxidant activity in fresh and cooked broccoli (Brassica oleracea var. Avenger) and cauliflower (Brassica oleracea var. Alphina F1). LWT - Food Science and Technology 2015, 63, 177-183, 10.1016/j.lwt.2015.03.089.
  13. Igor Otavio Minatel; Cristine Vanz Borges; Hector Alonzo Gomez Gomez Maria Izabela Ferreira; Hector Alonzo Gomez Gomez; Chung-Yen Oliver Chen; Chung-Yen Oliver Chen And Giuseppina Pace Pereira Lima; Phenolic Compounds: Functional Properties, Impact of Processing and Bioavailability. Phenolic Compounds - Biological Activity 2017, null, 1–24, 10.5772/66368.
  14. Cartea, M.E.; Francisco, M.; Soengas, P.; Velasco, P. Phenolic Compounds in Brassica Vegetables. Molecules 2010, 16, 251–280.
  15. Vallejo, F.; Tomás-Barberán, F.A.; García-Viguera, C. Phenolic compound contents in edible parts of broccoli inflorescences after domestic cooking. J. Sci. Food Agric. 2003, 83, 1511–1516.
  16. D.A. Moreno; M. Carvajal; C. López-Berenguer; Cristina García-Viguera; Chemical and biological characterisation of nutraceutical compounds of broccoli. Journal of Pharmaceutical and Biomedical Analysis 2006, 41, 1508-1522, 10.1016/j.jpba.2006.04.003.
  17. Jeffery, E.; E Stewart, K. Upregulation of Quinone Reductase by Glucosinolate Hydrolysis Products from Dietary Broccoli. Enzyme Eng. Evolut. Gen. Methods 2004, 382, 457–469.
  18. Chiu, Y.-C.; Matak, K.; Ku, K.-M. Methyl jasmonate treated broccoli: Impact on the production of glucosinolates and consumer preferences. Food Chem. 2019, 299, 125099.
  19. Sarai Quirante-Moya; Paula García-Ibañez; Francisco Quirante-Moya; Débora Villaño; Diego A. Moreno; The Role of Brassica Bioactives on Human Health: Are We Studying It the Right Way?. Molecules 2020, 25, 1591, 10.3390/molecules25071591.
  20. Assunta Raiola; Angela Errico; Ganna Petruk; Daria Maria Monti; Amalia Barone; Maria Manuela Rigano; Bioactive Compounds in Brassicaceae Vegetables with a Role in the Prevention of Chronic Diseases. Molecules 2017, 23, 15, 10.3390/molecules23010015.
  21. Klaus Peter Latté; Klaus-Erich Appel; Alfonso Lampen; Health benefits and possible risks of broccoli – An overview. Food and Chemical Toxicology 2011, 49, 3287-3309, 10.1016/j.fct.2011.08.019.
  22. Charron, C.S.; Saxton, A.M.; Sams, C.E. Relationship of climate and genotype to seasonal variation in the glucosinolate-myrosinase system. I. Glucosinolate content in ten cultivars of Brassica oleracea grown in fall and spring seasons. J. Sci. Food Agric. 2005, 85, 671–681.
  23. Baenas, N.; García-Viguera, C.; Moreno, D.A. Elicitation: A Tool for Enriching the Bioactive Composition of Foods. Molecules 2014, 19, 13541–13563.
  24. Asensio, E.; Sanvicente, I.; Mallor, C.; Menal-Puey, S.; Spanish traditional tomato. E_ects of genotype, location and agronomic conditions on the nutritional quality and evaluation of consumer preferences. Food Chem. 2019, 270, 452–458.
  25. Guo, R.; Yuan, G.; Wang, Q. E_ect of sucrose and mannitol on the accumulation of health-promoting compounds and the activity of metabolic enzymes in broccoli sprouts. Sci. Hortic. 2011, 128, 159–165.
  26. Baenas, N.; García-Viguera, C.; Moreno, D.A. Biotic Elicitors E_ectively Increase the Glucosinolates Content in Brassicaceae Sprouts. J. Agric. Food Chem. 2014, 62, 1881–1889.
  27. Xu, F.; Chen, X.; Jin, P.;Wang, X.;Wang, J.; Zheng, Y. E_ect of ethanol treatment on quality and antioxidant activity in postharvest broccoli florets. Eur. Food Res. Technol. 2012, 235, 793–800.
  28. Duarte-Sierra, A.; Nadeau, F.; Angers, P.; Michaud, M.; Arul, J. UV-C hormesis in broccoli florets: Preservation, phyto-compounds and gene expression. Postharvest Boil. Technol. 2019, 157, 110965.
  29. Vanesa Nuñez-Gómez; Nieves Baenas; Inmaculada Navarro-González; Javier García-Alonso; Diego A. Moreno; Rocío González-Barrio; M. J. Periago; Seasonal Variation of Health-Promoting Bioactives in Broccoli and Methyl-Jasmonate Pre-harvest Treatments to Enhance Their Contents. Foods 2020, 9, 1371, 10.3390/foods9101371.
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