1. Introduction
For the increasing world population, sustainable and adequate food production to meet human needs, while producing food of adequate human nutritional value, is of highest importance [
1,
2,
3,
4,
5,
6,
7]. Therefore, a complementary metric of nutritional yield was suggested for agricultural production [
2]. Also, the impact of nutrient-dense food on human health has been stressed [
8], in line with the need for increased nutrition production per hectare to sustain the world’s population with nutritious food. Nutritional yield and nutrient density in staple crops has been taken into consideration in plant breeding [
5,
7,
9,
10,
11,
12], although the main focus has been higher yield. It is well known that breeding for the traditional metric of yield might imply a reduction in the nutritional value of these staple crops [
13,
14].
In the present changing environment, with increased fluctuations in weather due to climate change and extreme events such as droughts, floods, hailstorms, and cyclones [
15], stability in yield and quality parameters (e.g., nutritional yield) are increasingly important in crops. Therefore, stability analyses of crops will become of higher importance in breeding for future cultivars. Such parameters are especially important in staple crops expected to make up the main part of the daily intake of humans. Locally adapted genotypes are especially important when highly nutritious and organic food is to be produced by cultivation; i.e., local adaptation becomes more important when chemical inputs cannot be used [
16,
17]. Organic production of cereals constituted 4% of those grown in Sweden in 2009 and the trend has been constantly increasing in recent years [
18]. Also, the stability (stable performance of genotypes over production years) of the genotypes as well as adaptability to diverse conditions is of relevance for organic production due to the lack of chemical-based inputs to secure stable yield [
16].
High nutrition content in crops adapted to organic agriculture has been identified as one major goal [
4,
16,
19]. Several wheat genotypes have previously been identified as highly nutritious and adapted to the organic production practices prevalent in Sweden [
3,
20,
21]. Nevertheless, the issues of nutritional yield, nutrient density, local adaptation, stability, and adaptability to diverse conditions remain to be evaluated and better understood in organically produced staple crops.
Specifically, two minerals, iron (Fe) and zinc (Zn), have been pointed out as being deficit in the human diet [
22]. The World Health Organization has identified these two minerals as the two major minerals contributing to human nutritional deficiency [
5]. Over 60% of the world’s population is estimated as Fe-deficient and over 30% as Zn-deficient [
11,
12,
23]. Furthermore, these deficiencies are not limited to the developing world but are also present in the developed world [
24]. As summarized from literature in the Nordic Nutrition Recommendations 2012, Fe deficiency was found in 18%–26% of Swedish females between the ages of 15 and 21. In general, 10%–22% of Nordic women of childbearing age are Fe-deficient [
25]. Therefore, the target to increase the content of the two micronutrients has been prioritized in wheat breeding [
5,
7,
9,
26,
27,
28].
Two other minerals, copper (Cu) and magnesium (Mg), are considered as essential trace elements for human health and lower intake than recommended has been reported in populations both from developing and developed countries [
7,
9,
11,
12,
29,
30]. Mg is one predominant mineral of cereal grains [
30], and in fact whole grain cereals are considered one of the main sources of dietary Mg [
25]. The intake of Cu and Mg is above the recommended levels in Nordic countries [
25]. However, decreasing content of both minerals has been reported in higher-yielding modern wheat cultivars [
3,
12,
13,
14].
The present study aimed to increase the understanding of how high nutritional yield and nutrient density can be obtained in organically grown wheat. Therefore, yield and concentration of the four mentioned minerals (Fe, Zn, Cu, and Mg) were evaluated in organic wheat grown over three years in Sweden. The wheat was evaluated for nutritional yield and nutrient density of these four minerals. Another aim was to better understand the presence of local adaptation among wheat genotypes. Thus, the stability and adaptability of yield and nutritional yields, as well as the nutritional value of the genotypes, were evaluated and genotypes were ranked according to their performance in terms of nutritional yield.
4. Discussion
Rankings of the genotypes in the present study resulted in determination of genotypes with high nutritional yields for the four minerals under study that were at stable for that nutritional yield (“balanced” genotypes) across the three years of study (
Table 4 and
Table 6). The importance of breeding for stability has been stressed earlier [
40,
53,
54] as it is economically essential both for farmers and end-users to have reliable production every year. From the AMMI stability analysis it can be inferred that, in spite of a significant Genotype × Environment interaction effect for nutritional yield, there were genotypes that could confidently be selected combining both stability and high nutritional yield. The BLUP procedure allowed for the identification of genotypes with high genotypic value and high stability/adaptability. Some genotypes appeared at the top of the rankings independent of the applied methods, increasing the confidence that these genotypes should be selected for breeding highly nutritional populations. In fact, stability across environments is a requirement for breeding for high nutrient content to be possible [
1]. Thus, “balanced” genotypes with local adaptation, stability, good yields, and high mineral contents can be an option for production in low-input agricultural systems, prevalent in both developed and developing countries.
The present study was able to identify winter wheat genotypes locally adapted to organic agriculture and with notable nutritional concentrations and high nutritional yields for the minerals Fe, Zn, Cu, and Mg (
Table 1 and
Table 8). The newly introduced metrics of nutritional yield [
2] opens up options to compare the usefulness of different production systems for food production to feed the growing population of the world. Therefore, we made a comparison of the nutritional yields obtained from the highest nutritional yielding genotypes in this study with nutritional yields calculated from reports [
30,
55] on yield and concentration of Fe, Zn, Cu, and Mg in conventional or intensive wheat trials (
Table 8). The modern conventional Swedish bread wheat varieties had a yield 1.7 times higher [
56] than the genotypes evaluated in the present study. Furthermore, the nutritional yields of the conventional Swedish wheat varieties [
56] were 1.46, 1.37, 1.44, and 1.66 times higher for Fe, Zn, Cu, and Mg, respectively, as compared to the wheat from the present study (
Table 8). Intensively grown French elite wheat genotypes [
30], with a substantially higher yield than the wheat in the present study, resulted in higher nutritional yields despite a low concentration of minerals in the grain. Differences in relationships between yield and mineral content in cereal grains might be related to variations in nitrogen uptake in the cereals. However, nitrogen uptake was not recorded in the present study and is therefore an issue to be evaluated in future studies. If a breeding program could develop novel high yielding genotypes with high concentration of minerals in the grains, this would of course lead to high nutritional yields of such genotypes. However, recent studies have indicated a decrease in nutritional compounds e.g., Fe and Zn in modern varieties, indicating that genetic improvements have resulted in the dilution of nutrition [
51]. One breeding program targeting high grain mineral concentration is headed by the Consultative Group for International Agricultural Research (CGIAR). This organization has a specific program (HarvestPlus) with a mission to develop and promote biofortified food crops from staple crops rich in vitamins and minerals (
www.harvestplus.org). However, the CGIAR research programs are mainly targeting the poor in developing countries, although knowledge coming from such research programs might also influence the breeding of high-yielding varieties for developed countries. One important aspect to solve with improved biofortification of crops is the increase in phytate, which reduces the bioavailability of Fe and Zn and often goes hand in hand with an increase in these trace elements [
51]. A previous study on mineral content in organically grown wheat in Sweden did not show obvious correlations between Fe, Zn, and P (phytate) [
3]. The bioavailability of the Fe and Zn was not evaluated in the present investigation and is a matter for future investigations.
The nutrient density was higher in the wheat in the present study as compared to both the conventional Swedish bread wheat varieties and the French elite wheat genotypes. This is clearly seen in the fact that around 270 g of wheat (i.e., of Svale and Walde) are needed in order to achieve 100% of the daily recommended intake (DRI;
Table 8). For conventional and elite wheat, more than 300 g, or even more than 350 g, in some cases (
Table 8), is needed for the same achievement. Average wheat consumption varies in different countries, but to secure adequate intake of minerals from wheat consumption a nutrient-dense food is desired. Nutrient-dense food [
57] has obvious implications for the caloric intake of consumers, which in many occasions is intended to be reduced, particularly in places where obesity and overweight are health issues [
25,
58]. Thus, taking both nutritional yields and nutrient density into consideration, some of the genotypes evaluated here are clearly alternatives to conventionally produced wheat.
In Nordic countries, cereals are known to contribute a significant part, approx. 90% of Fe, of the daily mineral requirement in the diet [
25]. Thus, with the present consumption of whole grain products, only around 15% of the daily requirements of the four evaluated minerals are consumed by the average consumer in Sweden, while the consumption of flour-based products contributes almost 90% of the daily requirement (
Table S1). However, these shares of the daily requirements of the four minerals evaluated are reached at consumption of the genotypes in the present study. Less nutrient-dense wheat genotypes than the highest ones evaluated in the present study would contribute even less to fulfilling daily requirements than the genotypes evaluated here. If less nutrient-dense genotypes are to be used (e.g., conventional wheat varieties), recommendations for intake of cereal products need to be increased to reach adequate intake levels of the four evaluated minerals, especially Fe and Zn. As whole grain products are also known as an important source of other bioactive compounds besides the evaluated minerals, it might be desirable to increase the average consumption of whole-grain-based cereal products [
3,
21,
59].
It was noted in the present study that the genotype with the highest yield (Starke) was not the genotype with the highest concentration (expressed in mg·kg
−1) of the four minerals studied. Conversely, the genotypes with the highest mineral concentrations, such as primitives
T. monococcum and Svart emmer, did not show high yields. This inverse relationship between yield and mineral concentration has been described in the past [
13,
14], and in fact low-yielding primitive genotypes produced in organic conditions have been shown to have a higher concentration of many nutritionally important minerals, while high-yielding cultivars have been shown to have lower mineral concentrations [
3,
14]. What this study has shown is that evaluating genotypes by nutritional yield allows for the selection of more “balanced” genotypes that do not have the maximum yields (
Table 4,
Table 5 and
Table 6) but compensate for that with their mineral concentrations, and this is reflected in their nutritional yield. This approach has been recommended in the face of scarce land resources [
2], also taking into consideration that more nutritious crops must also be acceptable to farmers in terms of yield [
7,
8,
9,
10]. Furthermore, such “balanced” genotypes with high nutritional yield and high nutrient density are of great relevance both for the developing world in order to obtain sufficient mineral concentrations in their food but also in the developed world to increase mineral intake per calorie.
Given the number of nutrients that are of importance to human health and derived from whole grain cereals [
60], it is difficult to evaluate genotypes (for breeding and/or selection) in terms of overall nutritional quality. There are also genetic correlations among these nutrients and other economically important traits making it impossible to consider any of these traits separately [
46,
61]. Thus, selection indexes have been implemented in order to evaluate genotypes for several traits [
46,
61]. In this study, we calculated selection indexes to summarize the nutritional yields for which the genotypes in this study were evaluated. Even though the two indexes we employed are conceptually very different [
46,
49,
50], the same genotypes were located in top positions of their respective rankings, i.e., Svale, Starke, Jacoby, and Walde. These same also genotypes appear very stable and adaptable, so the selection indexes support and add value to the selection of these genotypes for the continuation of the breeding process.
The necessity of breeding varieties specifically adapted to organic agriculture has been stated previously [
4,
10,
16,
19]. Additionally, the necessity that these varieties include among their characteristics a high nutritional value has also been stated [
4,
20,
60,
62,
63]. Breeding organic wheat for nutritional value will add to the benefits perceived by consumers regarding the consumption of organic foods [
56]. The yields obtained by some old varieties in the present study suggest that these perform well under the conditions of organic agriculture. It may be said that when dealing with breeding for organic agriculture, it is important to select varieties with high nutritional value, high performance against weeds, and high yield, but this kind of comprehensive breeding for organic agriculture is still scarce [
4,
10]. The present study is part of a bigger project aimed at generating cereal populations adapted to organic production conditions prevalent in Sweden, and with desirable health-promoting, nutritional, and baking characteristics.