Variation in Broccoli Cultivar Phytochemical Content under Organic and Conventional Management Systems: Implications in Breeding for Nutrition

Organic agriculture requires cultivars that can adapt to organic crop management systems without the use of synthetic pesticides as well as genotypes with improved nutritional value. The aim of this study encompassing 16 experiments was to compare 23 broccoli cultivars for the content of phytochemicals associated with health promotion grown under organic and conventional management in spring and fall plantings in two broccoli growing regions in the US (Oregon and Maine). The phytochemicals quantified included: glucosinolates (glucoraphanin, glucobrassicin, neoglucobrassin), tocopherols (δ-, γ-, α-tocopherol) and carotenoids (lutein, zeaxanthin, β-carotene). For glucoraphanin (17.5%) and lutein (13%), genotype was the major source of total variation; for glucobrassicin, region (36%) and the interaction of location and season (27.5%); and for neoglucobrassicin, both genotype (36.8%) and its interactions (34.4%) with season were important. For δ- and γ- tocopherols, season played the largest role in the total variation followed by location and genotype; for total carotenoids, genotype (8.41–13.03%) was the largest source of variation and its interactions with location and season. Overall, phytochemicals were not significantly influenced by management system. We observed that the cultivars with the highest concentrations of glucoraphanin had the lowest for glucobrassicin and neoglucobrassicin. The genotypes with high concentrations of glucobrassicin and neoglucobrassicin were the same cultivars and were early maturing F1 hybrids. Cultivars highest in tocopherols and carotenoids were open pollinated or early maturing F1 hybrids. We identified distinct locations and seasons where phytochemical performance was higher for each compound. Correlations among horticulture traits and phytochemicals demonstrated that glucoraphanin was negatively correlated with the carotenoids and the carotenoids were correlated with one another. Little or no association between phytochemical concentration and date of cultivar release was observed, suggesting that modern breeding has not negatively influenced the level of tested compounds. We found no significant differences among cultivars from different seed companies.

[1]  Erica N. C. Renaud,et al.  Broccoli Cultivar Performance under Organic and Conventional Management Systems and Implications for Crop Improvement , 2014 .

[2]  S. Boddupalli,et al.  Genetic regulation of glucoraphanin accumulation in Beneforté® broccoli , 2013, The New phytologist.

[3]  E. Vogtmann,et al.  Cruciferous vegetables intake and the risk of colorectal cancer: a meta-analysis of observational studies. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[4]  Enda Cummins,et al.  Factors influencing levels of phytochemicals in selected fruit and vegetables during pre- and post-harvest food processing operations , 2013 .

[5]  S. Fox,et al.  Comparison of organic and conventional selection environments for spring wheat , 2012 .

[6]  L. Helyes,et al.  Yield and phytochemical compounds of broccoli as affected by temperature, irrigation, and foliar sulfur supplementation , 2012 .

[7]  D. Bravata,et al.  Are Organic Foods Safer or Healthier Than Conventional Alternatives? , 2012, Annals of Internal Medicine.

[8]  Huifang Yu,et al.  Genotypic variation of glucosinolates in broccoli (Brassica oleracea var. italica) florets from China , 2012 .

[9]  C. la Vecchia,et al.  Cruciferous vegetables and cancer risk in a network of case-control studies. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[10]  F. El-Baz,et al.  Enhancement of phenolics, flavonoids and glucosinolates of Broccoli (Brassica olaracea, var. Italica) as antioxidants in response to organic and bio-organic fertilizers , 2012 .

[11]  M. Ittersum,et al.  The crop yield gap between organic and conventional agriculture , 2012 .

[12]  Suthawan Charoenprasert,et al.  Effect of organic and conventional cropping systems on ascorbic acid, vitamin C, flavonoids, nitrate, and oxalate in 27 varieties of spinach (Spinacia oleracea L.). , 2012, Journal of agricultural and food chemistry.

[13]  V. Picchi,et al.  Phytochemical content in organic and conventionally grown Italian cauliflower , 2012 .

[14]  L. Pollak,et al.  Maize: Breeding and Field Testing for Organic Farmers , 2011 .

[15]  U. Hamm,et al.  Consumer attitudes towards organic versus conventional food with specific quality attributes , 2011 .

[16]  M. Grusak,et al.  Mineral Concentration of Broccoli Florets in Relation to Year of Cultivar Release , 2011 .

[17]  M. Bunning,et al.  Environmental Temperatures Influence Antioxidant Properties and Mineral Content in Broccoli Cultivars Grown Organically and Conventionally , 2011 .

[18]  R. Bennett,et al.  Seasonal Effects on Bioactive Compounds and Antioxidant Capacity of Six Economically Important Brassica Vegetables , 2011, Molecules.

[19]  J. Juvik,et al.  Effect of Selenium Fertilization and Methyl Jasmonate Treatment on Glucosinolate Accumulation in Broccoli Florets , 2011 .

[20]  P. Petocz,et al.  Evaluation of the Micronutrient Composition of Plant Foods Produced by Organic and Conventional Agricultural Methods , 2011, Critical reviews in food science and nutrition.

[21]  A. Birch,et al.  Phytochemicals of Brassicaceae in plant protection and human health--influences of climate, environment and agronomic practice. , 2011, Phytochemistry.

[22]  A. Ismail,et al.  Carotenoids and Their Isomers: Color Pigments in Fruits and Vegetables , 2011, Molecules.

[23]  C. Seal,et al.  Agroecosystem Management and Nutritional Quality of Plant Foods: The Case of Organic Fruits and Vegetables , 2011 .

[24]  Karen Salandanan,et al.  Cultivar choice provides options for local production of organic and conventionally produced tomatoes with higher quality and antioxidant content. , 2010, Journal of the science of food and agriculture.

[25]  T. Lam,et al.  Cruciferous Vegetable Intake and Lung Cancer Risk: A Nested Case-Control Study Matched on Cigarette Smoking , 2010, Cancer Epidemiology, Biomarkers & Prevention.

[26]  A. Hussain,et al.  Mineral Composition of Organically Grown Wheat Genotypes: Contribution to Daily Minerals Intake , 2010, International journal of environmental research and public health.

[27]  M. Büchler,et al.  Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. , 2010, Cancer treatment reviews.

[28]  M. Wolfe,et al.  The effect of the year of wheat variety release on productivity and stability of performance on two organic and two non-organic farms , 2010, The Journal of Agricultural Science.

[29]  A. Mitchell,et al.  Content of ascorbic acid, quercetin, kaempferol and total phenolics in commercial broccoli , 2009 .

[30]  D. Kopsell,et al.  Importance of Genotype on Carotenoid and Chlorophyll Levels in Broccoli Heads , 2009 .

[31]  J. Juvik,et al.  Feasibility for improving phytonutrient content in vegetable crops using conventional breeding strategies: case study with carotenoids and tocopherols in sweet corn and broccoli. , 2009, Journal of Agricultural and Food Chemistry.

[32]  C. Benbrook.  The Impacts of Yield on Nutritional Quality: Lessons from Organic Farming , 2009 .

[33]  N. Fernández-García,et al.  Agricultural practices for enhanced human health , 2008, Phytochemistry Reviews.

[34]  H. Piepho,et al.  Comparing the performance of cereal varieties in organic and non-organic cropping systems in different European countries , 2008, Euphytica.

[35]  Andreas Fleck,et al.  Breeding for organic agriculture: the example of winter wheat in Austria , 2008, Euphytica.

[36]  H. Reents,et al.  Effects of genotype and environment on N uptake and N partition in organically grown winter wheat (Triticum aestivum L.) in Germany , 2008, Euphytica.

[37]  P. Struik,et al.  Can conventional breeding programmes provide onion varieties that are suitable for organic farming in the Netherlands? , 2008, Euphytica.

[38]  D. Roupakias,et al.  Response to conventional and organic environment of thirty-six lentil (Lens culinaris Medik.) varieties , 2008, Euphytica.

[39]  Robenzon E. Lorenzana,et al.  Genetic Correlation between Corn Performance in Organic and Conventional Production Systems , 2008 .

[40]  P. G. Reeves,et al.  Relationship between yield and mineral nutrient concentrations in historical and modern spring wheat cultivars , 2008, Euphytica.

[41]  S. Adam,et al.  Comparison of glucosinolate levels in commercial broccoli and red cabbage from conventional and ecological farming , 2008 .

[42]  C. Feldman,et al.  Nutritional quality of organic, conventional, and seasonally grown broccoli using vitamin C as a marker , 2008, International journal of food sciences and nutrition.

[43]  R. Hayes,et al.  Prospective study of fruit and vegetable intake and risk of prostate cancer. , 2007, Journal of the National Cancer Institute.

[44]  W. Chow,et al.  Dietary risk factors for kidney cancer in Eastern and Central Europe. , 2007, American journal of epidemiology.

[45]  S. Lyon,et al.  Evidence of varietal adaptation to organic farming systems , 2007 .

[46]  N. Juge,et al.  Molecular basis for chemoprevention by sulforaphane: a comprehensive review , 2007, Cellular and Molecular Life Sciences.

[47]  David E. Williams,et al.  Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. , 2007, Pharmacological research.

[48]  A. Krumbein,et al.  Sulfur and nitrogen supply influence growth, product appearance, and glucosinolate concentration of broccoli , 2007 .

[49]  M. Clifford,et al.  Plant Secondary Metabolites , 2006 .

[50]  D. Kopsell,et al.  Accumulation and bioavailability of dietary carotenoids in vegetable crops. , 2006, Trends in plant science.

[51]  Erica N. C. Renaud,et al.  Three-year comparison of the content of antioxidant microconstituents and several quality characteristics in organic and conventionally managed tomatoes and bell peppers. , 2006, Journal of agricultural and food chemistry.

[52]  C. Kimbeng,et al.  Heterosis for horticultural traits in Broccoli , 2006, Theoretical and Applied Genetics.

[53]  E. Carey,et al.  Does Organic Production Enhance Phytochemical Content of Fruit and Vegetables? Current Knowledge and Prospects for Research , 2006 .

[54]  J. Finley,et al.  Cultivation conditions and selenium fertilization alter the phenolic profile, glucosinolate, and sulforaphane content of broccoli. , 2005, Journal of medicinal food.

[55]  A. Saxton,et al.  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 , 2005 .

[56]  J. Fahey,et al.  Glucoraphanin level in broccoli seed is largely determined by genotype , 2005 .

[57]  D. Neuberg,et al.  Dietary intake of Cruciferous vegetables, Glutathione S-transferase (GST) polymorphisms and lung cancer risk in a Caucasian population , 2004, Cancer Causes & Control.

[58]  Donald R. Davis,et al.  Changes in USDA Food Composition Data for 43 Garden Crops, 1950 to 1999 , 2004, Journal of the American College of Nutrition.

[59]  M. Lefsrud,et al.  Variation in Lutein, β-carotene, and Chlorophyll Concentrations among Brassica oleracea Cultigens and Seasons , 2004 .

[60]  J. Finley,et al.  Cruciferous Vegetables: Cancer Protective Mechanisms of Glucosinolate Hydrolysis Products and Selenium , 2004, Integrative cancer therapies.

[61]  F. Harker.  Organic food claims cannot be substantiated through testing of samples intercepted in the marketplace: a horticulturalist's opinion , 2004 .

[62]  Ross M. Welch,et al.  Breeding for micronutrients in staple food crops from a human nutrition perspective. , 2004, Journal of experimental botany.

[63]  J. Fahey,et al.  Genetic and environmental effects on glucosinolate content and chemoprotective potency of broccoli , 2004 .

[64]  Anna Saba,et al.  Attitudes towards organic foods and risk/benefit perception associated with pesticides , 2003 .

[65]  R. Bone,et al.  Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. , 2003, Annual review of nutrition.

[66]  F. Tomás-Barberán,et al.  Effect of climatic and sulphur fertilisation conditions, on phenolic compounds and vitamin C, in the inflorescences of eight broccoli cultivars , 2003 .

[67]  F. Tomás-Barberán,et al.  Total and individual glucosinolate contents in inflorescences of eight broccoli cultivars grown under various climatic and fertilisation conditions , 2003 .

[68]  G. Williamson,et al.  Development of isothiocyanate-enriched broccoli, and its enhanced ability to induce phase 2 detoxification enzymes in mammalian cells , 2003, Theoretical and Applied Genetics.

[69]  D. Barrett,et al.  Comparison of the total phenolic and ascorbic acid content of freeze-dried and air-dried marionberry, strawberry, and corn grown using conventional, organic, and sustainable agricultural practices. , 2003, Journal of agricultural and food chemistry.

[70]  B. P. Klein,et al.  Glucosinolate profiles in Broccoli: Variation in levels and implications in breeding for cancer chemoprotection , 2002 .

[71]  D. Dubois,et al.  Soil Fertility and Biodiversity in Organic Farming , 2002, Science.

[72]  J. Prescott,et al.  A Comparison of the Nutritional Value, Sensory Qualities, and Food Safety of Organically and Conventionally Produced Foods , 2002, Critical reviews in food science and nutrition.

[73]  E. Rosa,et al.  Total and Individual Glucosinolate Content in 11 Broccoli Cultivars Grown in Early and Late Seasons , 2001 .

[74]  S. Rabot,et al.  The nutritional significance, biosynthesis and bioavailability of glucosinolates in human foods , 2000 .

[75]  Ke,et al.  Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects , 1999, The Plant journal : for cell and molecular biology.

[76]  J. Juvik,et al.  Quantification of carotenoid and tocopherol antioxidants in Zea mays. , 1999, Journal of agricultural and food chemistry.

[77]  B. P. Klein,et al.  Carotene, tocopherol, and ascorbate contents in subspecies of Brassica oleracea. , 1999, Journal of agricultural and food chemistry.

[78]  B. P. Klein,et al.  Variation of glucosinolates in vegetable crops of Brassica oleracea. , 1999, Journal of agricultural and food chemistry.

[79]  G. Williamson,et al.  Selective increase of the potential anticarcinogen 4-methylsulphinylbutyl glucosinolate in broccoli. , 1998, Carcinogenesis.

[80]  R. Goldbohm,et al.  Epidemiological studies on brassica vegetables and cancer risk. , 1996, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[81]  S. Mayne,et al.  Beta‐carotene, carotenoids, and disease prevention in humans , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[82]  Hilmer Sørensen,et al.  Glucosinolates in Broccoli Stored under Controlled Atmosphere , 1995 .

[83]  R. Dixon,et al.  Stress-Induced Phenylpropanoid Metabolism. , 1995, The Plant cell.

[84]  S. Ceccarelli.  Specific adaptation and breeding for marginal conditions , 1994, Euphytica.

[85]  A. Mozafar.  Nitrogen fertilizers and the amount of vitamins in plants: a review , 1993 .

[86]  W. Kwolek,et al.  Glucosinolates in Crucifer Vegetables: Broccoli, Brussels Sprouts, Cauliflower, Collards, Kale, Mustard Greens, and Kohlrabi , 1987, Journal of the American Society for Horticultural Science.

[87]  H. Munger.  The Potential of Breeding Fruits and Vegetables for Human Nutrition , 1979, HortScience.

[88]  M. Clifford,et al.  Plant Secondary Metabolites: Occurrence, Structure And Role In The Human Diet , 2014 .

[89]  E. V. Bueren,et al.  Organic crop breeding , 2012 .

[90]  Jing Yuan,et al.  Effect of nitrogen fertilization on ascorbic acid, glucoraphanin content and quinone reductase activity in broccoli floret and stem. , 2010 .

[91]  A. Krumbein,et al.  Genotypic effects on glucosinolates and sensory properties of broccoli and cauliflower. , 2004, Die Nahrung.

[92]  S. Ceccarelli.  Adaptation to low/high input cultivation , 2004, Euphytica.

[93]  S. Kritchevsky.  β-Carotene, Carotenoids and the Prevention of Coronary Heart Disease , 1999 .

[94]  R. Heaney,et al.  Glucosinolates and their breakdown products in food and food plants. , 1983, Critical reviews in food science and nutrition.