Kale is a leaf vegetable and includes cultivars mainly belong to B. oleracea and some cultivars of B. napus. Traditionally, kale has been used as a garnish, but is gaining popularity as a primary ingredient due to public perception that kale is one of the healthiest foods (Migliozzi et al., 2015). Kale placed 15th for nutrient content in a study conducted by the Centers for Disease Control ranking 47 “powerhouse” fruits and vegetables (Di Noia, 2014). However, the only dietary mineral included in the assessment of nutrient density was Fe.
Minerals play vital roles in various biological processes during different stages of growth and development in plants. Plants provide up to 17 essential minerals for normal plant growth and development as well as for human nutrition (Ohkama-Ohtsu and Wasaki, 2010; Singh et al., 2013). These essential minerals for plant growth and development can be classified into two groups depending on the concentration required for plant growth and development: macronutrients and micronutrients. Macronutrients include carbon, hydrogen, oxygen, nitrogen, P, K, sulfur, Ca, and Mg, whereas Mn, Fe, Zn, Cu, molybdenum, boron, nickel, and chlorine belong to the micronutrient group (Singh et al., 2013). In addition, silicon and Na can be included among the macronutrients and micronutrients, respectively (Marschner, 2012; Santos et al., 2014; Taiz et al., 2015).
Potassium is present in abundance in most plant cells/tissues (Bindraban et al., 2015; Britto and Kronzucker, 2008; Maathuis, 2009). The concentration of K tends to be high in young tissues, because of K’s active involvement in photosynthesis, respiration, and water homeostasis (Kopsell et al., 2013; Singh et al., 2013), as well as its relatively high mobility within the plant (Maathuis, 2009). Similar to K, Ca is abundant in tissues (Maathuis, 2009). Calcium plays an important role in plant growth and development, coordinating cell responses to various internal and external stimuli, and to environmental stresses (Kopsell et al., 2013; McAinsh and Pittman, 2009; Maathuis, 2009; White and Broadley, 2003). Calcium tends to be present at low abundance within plant cells (Bindraban et al., 2015; Maathuis and Diatloff, 2013) and concentrations of cytosolic Ca2+ are submicromolar, likely due to the difficulty in Ca transport to plant tissues (Karley and White, 2009). However, significant amounts of Ca are found in mature and senescing organs (White and Broadley, 2003). Another divalent cation, Mg, is associated with chlorophyll and protein synthesis, and plays an important role as an enzyme cofactor (Maathuis, 2009; McAinsh and Pittman, 2009; Singh et al., 2013).
One of the nutrients important in energy storage is P. Phosphorous is required for the synthesis of nucleic acids, phospholipids, and adenosine triphosphate (Bindraban et al., 2015; Singh et al., 2013). More than 90% of P in the soil cannot be used by plants (Maathuis and Diatloff, 2013). A large amount of P is usually stored in seeds and later used for embryo development, germination, and seedling growth (Marschner, 2012). Among the less required nutrients; Fe, Mn, and Cu are involved in photosynthesis, chlorophyll synthesis, and redox reactions, whereas Zn is associated with the formation of chlorophyll and N metabolism, and plays a role as a metal cofactor in various transcription factors and activates a large number of enzymes in plants (Maathuis and Diatloff, 2013; Singh et al., 2013; Taiz et al., 2015). Another micronutrient, Na, can substitute K in some metabolic functions (Taiz et al., 2015).
Essential nutrients are not only important for plant growth and development, but are also required in the human diet (Santos et al., 2014). Mineral deficiency is a global issue, with over 60% of the world’s population being Fe deficient and over 30% being Zn deficient (White and Broadly, 2009), whereas Ca, Mg, and Cu deficiencies are prevalent in both developed and developing countries (White and Broadly, 2009). Iron, Zn, Mn, and Cu are important cofactors for endogenous antioxidant vitamins, which protect the human body against diseases due to free radical damage (Matés et al., 1999). Although Mn deficiency is rare in humans, Mn plays an important role as a cofactor for enzymes involved in antioxidant functions, bone development, and neurotransmitter production (Pope et al., 2016). Calcium deficiency results in bone loss, which increases risk of osteoporosis. Adequate P intake is also important for bone health. In human health, high Na and low K consumption increases the risk of hypertension (Binia et al., 2015). Plant foods are low in Na, whereas K is present in abundance in most plant cells (Bindraban et al., 2015; Britto and Kronzucker, 2008; Maathuis, 2009).
Studies evaluating the nutrient composition of kale have been limited to either old varieties (Migliozzi et al., 2015) or the adult stage tissues (Ayaz et al., 2006). Kawashima and Soares (2003) analyzed the mineral profile of eight leafy vegetables popularly consumed in Brazil and reported that kale offered the highest concentrations of K and Ca. Currently, popular kale market classes include curly (‘Dwarf Blue Curled’ and ‘Scarlet’), lacinato, Siberian (‘Red Russian’), and ornamental (Migliozzi et al., 2015). These cultivars exhibit differences in leaf pigmentation. ‘Dwarf Blue Curled’ has green leaves, ‘Red Russian’ has green leaf blades with purple midveins, and ‘Scarlet’ has red leaves. In some plant cultivars, pigmentation has been related to mineral content. Previously, we demonstrated that romaine and crisphead lettuces grown under greenhouse conditions showed significantly higher K and P concentrations in red leaf cultivars than green leaf cultivars (Kim et al., 2016).
Besides choice of cultivar, kale is also marketed by stage of maturity (Migliozzi et al., 2015). Kale leaves lose palatability with maturation due to increased toughness, causing microgreen (young seedlings with cotyledons with or without a couple of true leaves) to be preferred due to the tender texture. However, growth stage may also impact nutrient content. Generally, higher nutritional value was reported in younger leaves than mature lettuce leaves (Pinto et al., 2014). A recent comprehensive review of microgreens by Mir et al. (2016) reported that consumption of mustard, cabbage, radish, buckwheat, lettuce, and spinach microgreens has increased due to suggestions of higher concentrations of bioactive phytochemicals important for human health, such as dietary minerals, compared with mature greens. However, to our knowledge, there has been no published comparative study investigating mineral content among microgreen, baby green, and adult kale.
Our hypothesis was that genetic differences (cultivars with differing leaf pigmentation) and developmental stages (from cotyledon to adult stage) influence the mineral content of kale. Therefore, the objective of this study was to determine whether harvesting kale at different growth stages affected mineral composition in three kale cultivars with differing leaf color.
Ayaz, F.A., Glew, R.H., Millson, M., Huang, H.S., Chuang, L.T., Sanz, C. & Hayirlioglu-Ayaz, S. 2006 Nutrient contents of kale (Brassica oleracease L. var. acephala DC.) Food Chem. 96 572 579
Bindraban, P.S., Dimkpa, C., Nagarajan, L., Roy, A. & Rabbings, R. 2015 Revisiting fertilizers and fertilization strategies for improved nutrient uptake by plants Biol. Fertil. Soils 51 897 911
Binia, A., Jaeger, J., Hu, Y., Singh, A. & Zimmermann, D. 2015 Daily potassium intake and sodium-to-potassium ratio in the reduction of blood pressure: A meta-analysis of randomized controlled trials J. Hypertens. 33 8 1509 1520
Karley, A.J. & White, P.J. 2009 Moving cationic minerals to edible tissues: Potassium, magnesium, calcium Curr. Opin. Plant Biol. 12 291 298
Kawashima, L.M. & Soares, L.M.V. 2003 Mineral profile of raw and cooked leafy vegetables consumed in southern Brazil J. Food Compos. Anal. 16 605 611
Kim, M.J., Moon, Y., Kopsell, D.A., Park, S., Tou, J.C. & Waterland, N.L. 2016 Nutritional value of crisphead ‘Iceberg’ and romaine lettuces (Lactuca sativa L.) J. Agr. Sci. 8 11 19 34
Kopsell, D.E., Kopsell, D.A., Sams, C.E. & Barickman, T.C. 2013 Ratio of calcium to magnesium influences biomass, elemental accumulations, and pigment concentrations in kale J. Plant Nutr. 36 2154 2165
Maathuis, F.J.M. & Diatloff, E. 2013 Roles and functions of plant mineral nutrients, p. 1–21. In: F.J.M. Maathuis (ed.). Methods in molecular biology. Springer Science Business Media, LLC, New York, NY
Marschner, H. 2012 Mineral nutrition of higher plants. 3rd ed. Academic, London, UK
Migliozzi, M., Thavarajah, D., Thavarajah, P. & Smith, P. 2015 Lentil and kale: Complementary nutrient-rich whole food sources to combat micronutrient and calorie malnutrition Nutrients 7 11 9285 9298
Mir, S.A., Shah, M.A. & Mir, M.M. 2016 Microgreens: Production, shelf life and bioactive components. Crit. Rev. Food Sci. Nutr. 2016 Feb. 8:0 [Epub ahead of print]
Ohkama-Ohtsu, N. & Wasaki, J. 2010 Recent progress in plant nutrition research: Cross-talk between nutrients, plant physiology and soil microorganisms Plant Cell Physiol. 51 8 1255 1264
Pinto, E., Almeida, A.A., Aguiar, A.A. & Ferreira, I.M. 2014 Changes in macrominerals, trace elements and pigments content during lettuce (Lactuca sativa L.) growth: Influence of soil composition Food Chem. 152 603 611
Pope, J., Nizielski, S. & McCook, A. 2016 Ch. 14. Trace minerals, p. 310–330. In: Nutrition for a changing world. McMillan, New York, NY
Rosa, E. & Heaney, R. 1996 Seasonal variation in protein, mineral and glucosinolate composition of Portuguese cabbages and kale Anim. Feed Sci. Technol. 57 111 127
Santos, J., Oliva-Teles, M.T., Delerue-Matos, C. & Liverira, M.B 2014 Muto-elemental analysis of ready-to-eat “baby leaf” vegetables using microwave digestion and high-resolution continuum source atomic absorption spectrometry Food Chem. 151 311 316
Singh, U.M., Sareen, P., Sengar, R.S. & Kumar, A. 2013 Plant ionomics: A newer approach to study mineral transport and its regulation Acta Physiol. Plant. 35 2641 2653
Taiz, L., Zeiger, E., Möller, I.M. & Murphy, A. 2015 Mineral nutrition, p. 119–142. In: A.D. Sinauer (ed.). Plant physiology and development. Sinauer Associates, Inc., Sunderland, MA
USDA 2016 National Nutrient Database for Standard Reference Release 28. USDA, Washington, DC
White, P.J. & Broadly, R. 2009 Biofortification of crops with seven mineral elements often lacking in human diets-iron, zinc, copper, calcium, magnesium, selenium and iodine New Physiol. 182 49 84