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. 2021 Oct 7;27(10):2297–2313. doi: 10.1007/s12298-021-01081-4

Potato biofortification: an effective way to fight global hidden hunger

Baljeet Singh 1,2, Umesh Goutam 2, Sarvjeet Kukreja 3, Jagdev Sharma 4, Salej Sood 1, Vinay Bhardwaj 1,✉
PMCID: PMC8526655  PMID: 34744367

Abstract

Hidden hunger is leading to extensive health problems in the developing world. Several strategies could be used to reduce the micronutrient deficiencies by increasing the dietary uptake of essential micronutrients. These include diet diversification, pharmaceutical supplementation, food fortification and crop biofortification. Among all, crop biofortification is the most sustainable and acceptable strategy to overcome the global issue of hidden hunger. Since most of the people suffering from micronutrient deficiencies, have monetary issues and are dependent on staple crops to fulfil their recommended daily requirements of various essential micronutrients. Therefore, increasing the micronutrient concentrations in cost effective staple crops seems to be an effective solution. Potato being the world’s most consumed non-grain staple crop with enormous industrial demand appears to be an ideal candidate for biofortification. It can be grown in different climatic conditions, provide high yield, nutrition and dry matter in lesser time. In addition, huge potato germplasm have natural variations related to micronutrient concentrations, which can be utilized for its biofortification. This review discuss the current scenario of micronutrient malnutrition and various strategies that could be used to overcome it. The review also shed a light on the genetic variations present in potato germplasm and suggest effective ways to incorporate them into modern high yielding potato varieties.

Keywords: Micronutrients, Potato, QTL, GWAS, Transgenics

Introduction

Feeding the world is a massive challenge because the global population is increasing at alarming rates. It is estimated that world population will increase to 9.6 billion by 2050 (Mishra et al. 2018). At present, nearly 800 million people are undernourished (FAO 2017) and around 2 billion people are suffering from micronutrient malnutrition, which is called as hidden hunger (IFPRI 2016; UN General Assembly 2016). Among all the micronutrients, the deficiencies of Zinc (Zn) and Iron (Fe) are widespread. Worldwide 1.6 billion people are Fe deficient (McLean et al. 2009) and about 17% of the global population is Zn deficient (Wessells and Brown 2012; Hefferon 2019). This situation becomes even worse in developing countries like India (Talsma et al. 2017; Harding et al. 2018). Approximately, 50% of the global micronutrient deficient population live in India (Ritchie et al. 2018). During the last decade, a lot of progress has been made to reduce this hidden hunger by various ways such as food fortification, dietary supplements and biofortification (Obersteiner et al. 2016; FAO 2017; Allen and de Brauw 2018).

Crop biofortification has emerged as a powerful tool to combat micronutrient malnutrition. It is a cost-effective approach, which paves its way towards sustainable micronutrient supply to the poor. Since the twenty-first century, a number of biofortified crops have been released worldwide (Garg et al. 2018; Meena et al. 2018). However, being the staple food a large portion of world’s population depends upon cereals, which however provides insufficient amounts of micronutrients (Pérez-Massot et al. 2013; Garcia-Oliveira et al. 2018). Therefore, to reduce the micronutrient malnutrition globally, there is an urgent need to improve the world’s most consumed non-grain food crop ‘Potato’. It is already a rich source of micronutrients (Navarre et al. 2016, 2019; Zaheer and Akhtar 2016; Furrer et al. 2018), especially when consumed along with skin (Subramanian et al. 2011). Its biofortification could be a boon for people suffering from hidden hunger. More than 50% potatoes are produced by developing countries (FAO 2009), where the micronutrient malnutrition is highly prevalent (Perez-Escamilla et al. 2018; Wakeel et al. 2018). Thus, importance of micronutrient biofortification in potato becomes high from the human health perspective as it is consumed in high amounts by a larger portion of world population.

Hidden hunger: a silent epidemic

Micronutrients play vital roles in both humans and plants. Their deficiencies may lead to serious health issues in humans and it may cause yield or quality losses in plants (Quintaes and Diez-Garcia 2015; Dimkpa and Bindraban 2016). Insufficient intake of micronutrients by humans is called as hidden hunger (Ritchie et al. 2018). Worldwide, micronutrient malnutrition is somehow associated with more than 50% deaths (Lyons 2018). About 150 million children below the age of five show stunted growth and about 50 million are under weighed (UNICEF 2018). Nearly, 52 million children below five years suffer malnutrition globally, including ~ 36 million children in Asia and 2 million in India (Singh et al. 2015). Hidden hunger is widespread in developing countries and become an abysmal for the poor (Harding et al. 2018). The major reasons exacerbating the hidden hunger are; low monetary resources, lack of diversity in diet, dependence upon high yielding cereals which are often less micronutrient dense (Von Grebmer 2018; Zikankuba et al. 2019). The micronutrient malnutrition due to Fe and Zn deficiencies is most prevalent and have most devastating effects (Bailey et al. 2015). The recommended levels of Fe, Zn, Cu and I required for the ideal functioning of the human body has been compiled in Table 1.

Table 1.

Recommended Daily Allowance (RDA) of Iron (Fe), Zinc (Zn), Copper (Cu) and Iodine (I) for different age groups and genders.

Source The data for table is obtained from National Institutes of Health (NIH), Office of Dietary Supplements, https://ods.od.nih.gov/ (Accessed on 08/05/2021)

Age Iron Zinc Copper Iodine
Male Female Pregnancy Male Female Pregnancy Male Female Pregnancy Male Female Pregnancy
0–6 months 0.27 mg* 0.27 mg* 2 mg* 2 mg* 200 mcg * 200 mcg* 110 mcg* 110 mcg*
7–12 months 11 mg 11 mg 3 mg 3 mg 220 mcg * 220 mcg* 130 mcg* 130 mcg*
1–3 years 7 mg 7 mg 3 mg 3 mg 340 mcg 340 mcg 90 mcg 90 mcg
4–8 years 10 mg 10 mg 5 mg 5 mg 440 mcg 440 mcg 90 mcg 90 mcg
9–13 years 8 mg 8 mg 8 mg 8 mg 700 mcg 700 mcg 120 mcg 120 mcg
14–18 years 11 mg 15 mg 27 mg 11 mg 9 mg 12 mg 890 mcg 890 mcg 1000 mcg 150 mcg 150 mcg 220 mcg
19–50 years 8 mg 18 mg 27 mg 11 mg 8 mg 11 mg 900 mcg 900 mcg 1000 mcg 150 mcg 150 mcg 220 mcg
51 + years 8 mg 8 mg 11 mg 8 mg 900 mcg 900 mcg 150 mcg* 150 mcg*
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*Adequate intake

Current strategies to overcome hidden hunger

There are several ways to reduce the hidden hunger, which could be implicated to increase dietary intake of essential micronutrients such as dietary diversification, medical supplementation, food fortification and crop biofortification (Fig. 1) (Wakeel et al. 2018). The choice of strategies for reducing hidden huger depends upon several factors such as availability of resources, financial status of target population, sustainability, accessibility and acceptability of consumers. Dependence upon one type of food on regular basis may lead to a specific type of micronutrient malnutrition. Therefore, diet diversification is a simple, effective and natural way to increase micronutrient bioavailability (Gibson and Hotz 2001). For example, adequately diversified dietary intake helps to reduce serious health issues during pregnancy (Agrawal et al. 2015). Diet diversification can be achieved via different strategies; (1) agriculture based (use of diverse vegetables, fruits and other plant based products), (2) animal based (incorporation of different animal based food and/or seafood products into diet) and (3) integration of processed food products (Maqbool and Beshir 2019). However, changing the regional food habits of people is a challenging task. Worldwide, the dietary supplements are used to reduce the effects of malnutrition. Previous studies have shown that diet supplements are not just to reduce the hidden hunger but these are also used to enhance the performance of athletes (Maughan et al. 2018). A number of physiological disorders related to micronutrient malnutrition can be eradicated by dietary supplementation (Stewart et al. 2015; Petry et al. 2016). However, most of the times dietary supplements cause some adverse side effects too (Wu and Tsai 2016). Moreover, the hidden hunger is highly prevalent in poor, who cannot afford diversified diet and dietary supplements. Thus, government’s financial support is required to make this intervention effective for the poor (Meenakshi et al. 2010).

Fig. 1.

Fig. 1

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Different strategies to reduce the burden of global hidden hunger

Food fortification is another way to enhance nutritional value of food by adding vital trace elements and vitamins to it with minimal risk to health (Garrett 2018). Food fortification can be done at industrial level (Mannar and Hurrell 2018) and/or directly at consumer’s plate (Somassè et al. 2018). The foods that are economical, easily available and consumed in high amounts in a region can be targeted for industrial fortification. Studies have revealed that, micronutrient powders (MNP) are effective to reduce anaemia and gain weight in children under 2 years of age (Lazzerini 2013; Somassè et al. 2018). This method of food fortification also has some shortcomings. Food fortification with micronutrients may change its quality, flavour, shelf life, colour, appearance and consequently lead to poor consumers acceptance (Habeych et al. 2016; Blanco-Rojo and Vaquero 2019). However, this approach is more economical than the use of pharmaceutical supplements but still the population suffering from micronutrient malnutrition cannot afford it (Bouis 2003).

Improving micronutrient concentrations through biofortification is a cost effective, reliable and sustainable method that could supply micronutrients to the poor in long terms. It is an upcoming approach with tremendous potential to increase the nutritional value of food crops in the fields, rather than adding nutrients artificially into them while processing. Plenty of nutrient rich food crops have been developed successfully through biofortification (Garg et al. 2018; Meena et al. 2018). However, the eradication of micronutrient malnutrition in developing countries where staple crops lack micronutrients is still a big challenge (Pérez-Massot et al. 2013).

Potato an ideal crop for biofortification

Potato is a versatile crop and its biofortification can reduce the micronutrient malnutrition significantly (Fig. 2). It is a staple crop of many countries because it is easy to grow, requires less land than other major crops and provides more nutrients per unit area, time and money (Mullins et al. 2006). It is cultivated under different climates such as temperate, tropical and subtropical regions and its production and consumption has increased tremendously in the developing countries (Zaheer and Akhtar 2016). It is consumed as fresh vegetable and also has massive industrial demand (Furrer et al. 2018). It is naturally a nutrient rich crop (Table 2). Due to its nutritional value potato, became the staple food of many countries. It provides more nutrients in lesser price than most of the other vegetables and fruits (Drewnowski and Rehm 2013). It is a good source of carbohydrate, protein, minerals, vitamins and dietary fibres. As per the nutritional profile, potatoes provide a good quantity of vitamin C, vitamin B6, K, Fe and folate (Robertson et al. 2018). If cooked without peeling off potatoes can provide more nutrients and dietary fibres (Singh et al. 2020a, b; Sampaio et al. 2020). However, the nutritional value may vary slightly from variety to variety. For example, coloured potatoes are a rich source of antioxidants such as polyphenols, β-carotene, carotenoids, anthocyanins and flavonoids (Soare et al. 2020). Some of these compounds remain in significant amounts even after cooking such as anthocyanin (Ercoli et al. 2021).

Fig. 2.

Fig. 2

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Major reasons for proposing potato an ideal candidate for biofortification

Table 2.

Nutritional profile of raw potatoes with skin (

Source: United States Department of Agriculture (USDA), Agricultural Research Service (ARS), 2018)

Name Value per 100 g 38 g skin
Proximates
Water 83.29 g 31.65 g
Energy 58 kcal 22 kcal
Protein 2.57 g 0.98 g
Total lipid (fat) 0.10 g 0.04 g
Carbohydrate, by difference 12.44 g 4.73 g
Fiber, total dietary 2.5 g 0.9 g
Minerals
Calcium, Ca 30 mg 11 mg
Iron, Fe 3.24 mg 1.23 mg
Magnesium, Mg 23 mg 9 mg
Phosphorus, P 38 mg 14 mg
Potassium, K 413 mg 157 mg
Sodium, Na 10 mg 4 mg
Zinc, Zn 0.35 mg 0.13 mg
Vitamins
Vitamin C, total ascorbic acid 11.4 mg 4.3 mg
Thiamin 0.021 mg 0.008 mg
Riboflavin 0.038 mg 0.014 mg
Niacin 1.033 mg 0.393 mg
Vitamin B-6 0.239 mg 0.091 mg
Folate 17 µg 6 µg
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Recently Jongstra et al. (2020) reported that iron bioavailability in potatoes is very high as compared to the cereals. Andre et al. (2015) used an in vitro gastrointestinal digestion and a CaCO2 lines based model of human intestine and showed that around 70% of iron released from the potatoes remains available at the intestinal level. Further, only a small amount of Zn from different agricultural foods is bioavailable to humans at gastrointestinal level. The food crops contain various organic compounds some of them favours Zn absorption and some can reduce its bioavailability such as phytic acid (PA). The molar ratio of PA:Zn is widely used to measure the Zn bioavailability in foods. The Zn bioavailability in potato tubers is high because of the presence of high concentrations of organic compounds, which promote absorption of Zn in potatoes and low concentrations of compounds, which restrain Zn absorption. Therefore, a significant amount of the recommended dietary allowance (RDA) for iron and zinc can be obtained from potatoes. Vergara et al. (2019) successfully increased the Zn bioavailability in potato tubers by priming the tubers in zinc solution.

Moreover, an extensive amount of natural variations for micronutrient content exists in vast potato germplasm (Burgos et al. 2007; Ritter et al. 2008; Haynes et al. 2012; Paget et al. 2014; Subramanian et al. 2017; Singh et al. 2020a, b). These variations can be utilized to develop biofortified potatoes (Fig. 3). The potato germplasm collections are maintained at different locations throughout the world (Table 3). The potato germplasm has a great variation in terms of tuber size, shape, flesh color, skin color, distribution of pigments, skin type, nutrient concentrations and tolerance to biotic and abiotic stresses (Jiménez et al. 2009; Berdugo-Cely et al. 2017; Furrer et al. 2017; de Haan et al. 2019; Singh et al. 2020a, b). Therefore, diverse potato gene pool must have some unidentified genes that might be utilized in the potato biofortification programs. Identification of genes controlling tuber mineral concentration in diverse potato populations will permit the scientists to expand the range of variations in present potato cultivars (Bradshaw et al. 2006; Subramanian et al. 2017). Moreover, potato genome sequence is available publically, which can catalyse the process of biofortification with the help of advance biotechnological tools. Potato biofortification can be done via three different methods viz., agronomical, transgenic and breeding (Garg et al. 2018; Shukla and Mishra 2018).

Fig. 3.

Fig. 3

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A systematic flow chart proposing an effective way for the development of micronutrient rich potato varieties

Table 3.

Different institutes having collection and maintenance of potato germplasm

Name Location Reference
International Potato Centre CIP, Lima, Peru https://cipotato.org/genebankcip/
Dutch-German Potato Collection CGN, Wageningen, The Netherlands https://www.wur.nl/en/Research-Results/Statutory-research-tasks/Centre-for-Genetic-Resources-the-Netherlands-1/Expertise-areas/Plant-Genetic-Resources/CGN-crop-collections/CGN-potato-collection.htm
The Gross Luesewitz Potato Collections GLKS, IPK, Groß Lusewitz, Germany https://www.ipk-gatersleben.de/en/genebank/satellite-collections-north/gross-luesewitz-potato-collections/
The Potato Collection of the Vavilov Institute VIR, St Petersburg, Russia Dzyubenko (2018)
US Potato Genebank NRSP-6, Sturgeon Bay, USA https://www.ars-grin.gov/nr6/
Commonwealth Potato Collection The James Hutton Institute (JHI), Dundee, Scotland https://ics.hutton.ac.uk/germinate-cpc/#home
The Indian Council of Agricultural Research-Central Potato Research Institute ICAR-CPRI, Shimla, India https://www.cpri.in/
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Agronomical biofortification

Agronomical biofortification involves the seed tuber priming and application of mineral fertilizers to enhance the micronutrient concentrations in the edible portion of food crops (Cakmak and Kutman 2018). Vergara et al. (2019) reported successful zinc biofortification by priming the potato tubers in 10 mg/ml Zn for 12 h. The micronutrient containing mineral fertilizers can be applied to plants via foliar application or through soil application (Poblaciones and Rengel 2016; de Valença et al. 2017). Both soil and foliar application of trace elements have been employed to biofortify the major food crops including potato (Cakmak and Kutman 2018; Lyons 2018). However, foliar application of micronutrient fertilizers is a more efficient approach to improve the mineral content in the edible parts of a crop than the soil application (Zhao et al. 2014; Lawson et al. 2015; Kromann et al. 2017). Previous studies showed that micronutrient spraying on potato plants enhance the micronutrient concentrations in tubers and also increase the tuber yield and dry matter content (Al-Jobori and Al-Hadithy 2014; Kromann et al. 2017; Zhang et al. 2019).

The agronomic biofortification has tremendous potential to increase the nutrient content in potato (Table 4) but on the downside, it has some limitations too. The efficiency of agronomic biofortification depends upon various factors such as soil composition, soil pH, mineral mobility, mineral accumulation, environmental conditions and plant growth stage when the fertilizers are applied (Dimkpa and Bindraban 2016; Garg et al. 2018). It is not an efficient method to increase the bioavailability of nutrients, which are synthesized via plant metabolism. Further in case of Fe, this method is not much effective because Fe is immobilized in soil in ferric form but plants absorb Fe in ferrous form (Pérez-Massot et al. 2013). Moreover, it is a temporary and an expensive way of biofortification, one has to perform the same agronomic practices repeatedly.

Table 4.

List of different agronomic practices for biofortification of potato

Method Type of biofortification Country References
Foliar application Se Italy Poggi et al. (2000), Cuderman et al. (2008)
Foliar application Se Slovenia Zhang et al. (2019)
Foliar application Mg, S, Zn, B India Ramesh et al. (2019)
Foliar application cobalamin, folic acid and ascorbic acid Egypt Youssif et al. (2017)
Foliar application Zn, B, Fe, Mn India Moinuddin et al. (2017)
Foliar application Fe, Zn, Mn, Ti Poland Wadas and Kalinowski (2019)
Foliar application urea, humic acid (HA), Zn, B Pakistan Shah et al. (2016)
Foliar application Nanaofertilizer, Seaweed and Hypertonic Iraq Al-Juthery et al. (2018)
Foliar application Fe, Mn, Cu, Zn Iraq Al-Jobori and Al-Hadithy (2014)
Foliar application Zn United Kingdom White et al. (2017)
Both Foliar and Soil application Zn, Fe United States Kromann et al. (2017)
Both Foliar and Soil application Zn, Fe Bolivia Gabriel et al. (2015)
Tuber priming Zn Brazil Vergara et al. (2019)
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Transgenic approach

The biofortification of micronutrients using transgenic approach provides sustainability because transgenics produce self-fortifying seeds (Blancquaert et al. 2015). The development of nutrient rich crops using transgenic approach is an efficient and cost-effective method. This approach allows using a broad range of genes associated with different micronutrients from even entirely unrelated species (Xu et al. 2017; Muñiz García et al. 2018) and can be used to reduce the content of anti-nutrients (Pérez-Massot et al. 2013). Thus, it permits the biofortification of a nutrient, which does not exist in the whole germplasm of a crop. Moreover, tissue specific biofortification can be done using transgenic approach (De Lepeleire et al. 2018). Therefore, the concentrations of micronutrients in the edible part of targeted crop can be enhanced. To maximize the uptake, mobilization and storage of micronutrients in plants many transgenic studies have been performed in major food crops (Saalbach et al. 2014; Takenaka et al. 2019; Wu et al. 2019). Recently, various attempts have been made by scientists to enhance the potato tuber quality with respect to micronutrients via transgenic approach (Mitchell et al. 2017; Xu et al. 2017; Bagri et al. 2018; Muñiz García et al. 2018). The overexpression of PDXII gene from Arabidopsis thaliana in potato under the control of CaMV35S promoter increased the accumulation of vitamin B6 and enhanced abiotic stress tolerance (Bagri et al. 2018). Likewise, incorporation of Arabidopsis ABF4 in potato improved the tuber yield, quality and abiotic stress tolerance (Muñiz García et al. 2018). Furthermore, AtMYB12 gene from Arabidopsis has increased the content of caffeoylquinic acids and flavonols in potato tubers (Li et al. 2016). Many genes associated with micronutrient acquisition, transportation, accumulation and tolerance have been reported previously (Blancquaert et al. 2017; Kumar et al. 2018; Moreira et al. 2018; Papierniak et al. 2018; Migocka et al. 2019). Legay et al. (2012) reported the elevated expression of several genes including the well-known iron regulators FRO1, FRO2, IRTI, FRD3, NRAMP, VIT1, FIT/FER in in-vitro potato plantlets grown in iron deficient media. As the functions of these genes are known in other non-graminaceous plants, thus their overexpressor transgenic potato lines could be developed to enhance the tuber Fe content in Fe deficient soils. Beside these, manually curated nutrient use efficiency (NtUE)-related genes and quantitative trait loci (QTLs) are available at (Kumar et al. 2018). By using transgenic techniques, nutrient rich crops can be developed. However, despite of numerous successful transgenic studies (Table 5), only few nutrient rich transgenic varieties have been released (Garg et al. 2018). This is because of legal and ethical issues associated with transgenics.

Table 5.

Transgenic studies conducted for potato biofortification

Micro-nutrient Gene(s) References
Beta-carotene StLCYb Song et al. (2016)
Beta-carotene lycopene epsilon cyclase (LCY-e) Diretto et al. (2006)
Amino acid composition AmA1 Chakraborty et al. (2010)
Anthocyanins, phenolic acids chalcone synthase (CHS), chalcone isomerase (CHI), and dihydroflavonol reductase (DFR) Lukaszewicz et al. (2004)
Vitamin B9 HPPK/DHPS, FPGS De Lepeleire et al. (2018)
Vitamin B6 PDX-II gene Bagri et al. (2018)
Vitamin C GalUR gene Hemavathi et al. (2009)
Vitamin C StVTC2A Bulley et al. (2012)
Vitamin C StDHAR Qin et al. (2011)
Vitamin A EuCrtB, EuCrtI, EuCrtY Diretto et al. (2007)
Vitamin A BoOr Lopez et al. (2008)
Vitamin A PaCrtB Ducreux et al. (2005)
Calcium Scax1 Park (2005)
Calcium Cax2b chimeric Kim et al. (2006)
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Breeding

The micronutrient concentrations in various staple crops has been increased by conventional breeding experiments without affecting the other agronomic traits. Various attempts have been made to increase micronutrient content in potato through plant breeding approaches (Table 6). However, in potato the traditional breeding programs were primarily focused to increase the crop yield and disease resistance (Kikuchi et al. 2015). Moreover, most of the modern potato cultivars were developed from a limited germplasm brought from Andeans of South America by repeated breeding. Hence, most of the modern potato cultivars have less genetic variability (Fig. 4) (Barrell et al. 2013; Hameed et al. 2018). However, Berdugo-Cely et al. (2017), reported that the potato germplasm present at ‘the colombian central collection’ have great phenotypic and genotypic diversity. By using 4666 SNPs, they find out 23 significant and robust marker-trait associations with different phenotypic traits. Haynes et al. 2012 investigated genetic variations associated with micronutrient concentrations in 18 potato clones and reported significant variations for Fe, Zn, Cu and Mn concentrations in potato. Further, Haan et al. (2019), reported high nutritional diversity for dry matter, energy, protein, iron and zinc content in Andean diverse landraces and modern potato varieties. As the huge pool of ‘potato germplasm’ itself have genetic variations for micronutrient content (de Haan et al. 2019; Haynes et al. 2012), so it can be biofortified using conventional breeding.

Table 6.

List of studies conducted for potato biofortification by plant breeding

Micro-nutrient(s) Country Reference(s)
Zn, Fe Peru (Burgos et al. 2007)
Fe United states (Brown et al. 2010)
Cu, Fe, Mn, Zn United states (Haynes et al. 2012)
Fe, Zn, Mg, Mn, Ca Colombia (Peña et al. 2015)
Antioxidants Peru (Lachman and Hamouz 2005; Andre et al. 2007)
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Fig. 4.

Fig. 4

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Pyramid chart depicts the decreased genetic diversity in modern potato varieties due to potato domestication, repeated breeding and transgenic studies performed for better agronomic traits

Breeding approaches to increase micronutrient content in potato tubers depends upon environmental conditions and soil composition (Trawczyński 2016; Martins et al. 2018). The genotype x environment interactions (GEI) have significant effect on tuber’s nutritional quality (Mohammed 2017; Haynes et al. 2019). Burgos et al. (2007), reported notable variations in the tuber Fe and Zn concentrations due to GEI when grown at two different locations. Therefore, multi-environmental trials are required to choose potential parents for potato breeding programs and to reduce the effect of GEI (Kelly et al. 2007).

Genetic approaches to speed up potato biofortification

Different strategies can be used in potato biofortification programme to speed up the process such as association mapping, QTL mapping to identify potential candidate genes and reverse genetic approaches to validate their functionality (Fig. 3).

Association mapping and QTL analysis

Exploration of desirable genetic variations and their introgression into the modern potato varieties is a big challenge due to high heterozygosity and polyploid nature of potato genome (PGSC 2011). Association mapping (AM) or genome-wide association studies (GWAS) are efficient techniques to screen the fruitful genes and genomic regions associated with a complex phenotypic trait (Ma et al. 2016; Rojas et al. 2019). It provides higher mapping resolution in comparison to linkage mapping population (Huang and Han 2014). So far, these techniques have been employed to screen the genes/markers/QTLs associated with micronutrient contents in various food crops (Table 7). In potato, these have been performed successfully to identify the marker-trait associations for tuber bruising (Urbany et al. 2011; D’hoop et al. 2014), starch content (Schönhals et al. 2016), and glycoalkaloid content (Manrique-Carpintero et al. 2014; Vos et al. 2016). Genotyping by sequencing (GBS) based GWAS experiment was performed on a panel of 170 potato landraces with genetic variations for Fe and Zn content. They found four genetic markers significantly associated with Fe content and seven with zinc content (CGIAR 2016). However, the genetic basis of micronutrient content in potato is still poorly known and demands further investigation of genetic variations linked to micronutrient content (Haynes et al. 2012).

Table 7.

List of various studies conducted successfully to identify marker-trait associations for mineral nutrient concentrations in different crops by exploiting the germplasm diversity using association mapping (AM) and genome-wide association mapping (GWAS)

Crop Nutrient for AM Population size No of significant associations Country References
Common bean (Phaseolus vulgaris L.) N, P, K, Ca, Mg, Fe, Zn, and Mn 174 accessions 31 quantitative trait nucleotides Croatia Gunjača et al. (2021)
Common bean (Phaseolus vulgaris L.) Fe, Zn, C, K, Ca, P, and Mg 109 genotypes NA India Jan et al. (2021)
Vigna radiata L Ca, Fe, K, Mn, P, S, and Zn 95 genotypes 43 MTAs United States Wu et al. (2020)
Phaseolus Vulgaris L Fe, Zn Vitamin A 206 genotypes 10 SNP marker trait associations Mexico Binagwa et al. (2020)
Rice (Oryza sativa L.) Fe and Zn concentrations 152 7 QTLs (2 for Fe and 5 for Zn) Philippines Descalsota-Empleo et al. (2019)
Wheat (Aegilops tauschii) Micronutrients (Fe, Zn, Cu, and Mn) 167 accessions 19 SNP marker trait associations India Arora et al. (2019)
Rice (Oryza sativa) Ionomic Variation (N, P, K, Ca, Mg, Fe, Mn, Mo, B, Cu, Zn, Co, Na, Cd, As, Pb, Cr) 529 accessions 72 loci associated China Yang et al. (2018)
Maize (Zea mays L.) Fe and Zn concentration 923 inbred lines 46 SNP marker trait associations (26 for Fe and 20 for Zn) Mexico Hindu et al. (2018)
Wheat (Triticum aestivum L.) Zn concentration 369 wheat genotypes 40 SNP marker-trait associations Germany Alomari et al. (2018)
Lentil (Lens culinaris subsp. culinaris) Fe and Zn concentration 96 germplasm lines 7 SSR marker trait associations India Singh et al. (2017)
Spinach (Spinacia oleracea L.) Mineral element concentrations (B, Ca, Co, Cu, Fe, K, Mg, Mn, Mo, Na, Ni, P, S, Zn) 292 accessions 45 SNP marker trait associations United States Qin et al. (2017)
Common bean (Phaseolus vulgaris L.) Micronutrients (Fe, Zn and protein) 96 genotypes 13 SSR marker trait associations India Mahajan et al. (2017)
Rice (Oryza sativa L.) Fe and Zn concentration 222 accessions 60 QTLs (29 for Fe and 30 for Zn) China Zhang et al. (2017)
Barley (Hordeum vulgare L.) Mn concentration 248 barley varieties 54 SNP marker trait associations Denmark Leplat et al. (2016)
Potato (Solanum tuberosum L.) Fe and Zn concentrations 170 11 marker trait associations (4 for Fe and 7 for Zn) Peru CGIAR (2016)
Chickpea (Cicer arietinum L.) Fe and Zn concentrations 92 accessions (39 desi and 53 kabuli) 16 genomic loci (gene-based SNPs) India Upadhyaya et al. (2016)
Rice (Oryza sativa) Mineral Element Contents (Fe, Zn, Se, Cd, Pb) 416 accessions (planted) but only 378 were finally used 20 QTLs China Huang et al. (2015)
Rice (Oryza sativa L.) Mineral Element Contents Zn, Fe, Cu, Mn, P, Ca, K, Mg 219 accessions planted but only 175 were used 60 SSR marker trait associations China Nawaz et al. (2015)
Maize (Zea mays L.) Fe concentration 302 maize inbred lines planted but 267 35 SNP marker trait associations Germany Benke et al. (2015)
Rice (Oryza sativa L.) As, Cu, Mo and Zn concentrations 312 accessions 17 SNP marker-trait associations Several countries Norton et al. (2014)
Chickpea (Cicer arietinum L.) Fe and Zn concentrations 94 accessions 8 marker trait associations Canada Diapari et al. (2014)
Barley (Hordeum vulgare L.) landraces Fe and Zn concentration 298 accessions 14 SNP marker trait associations United States Mamo et al. (2014)
Sorghum (Sorghum bicolor (L.) Moench) Grain quality traits including Ca and P 300 accessions 8 SNP marker trait associations United States Sukumaran et al. (2012)
Arabidopsis Thaliana Mineral Element Contents (B, Na, Mg, P, S, K, Ca, Mn, Fe, Co, Ni, Cu, Zn, As, Se, Rb, Mo, Cd) 96 accessions Many different associations for different traits Belgium Baxter et al. (2012)
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Reverse genetic approaches

GWAS, QTL mapping and by utilizing different bioinformatics approaches potential candidate genes/markers/QTLs associated with micronutrient content can be identified. However, functional validation of these potential candidates is important before their incorporation into any potato cultivars, which can done by reverse genetic approaches. For an instance, virus induced gene silencing (VIGS) is a simple, rapid and efficient method to study the gene function by suppressing its expression (Bekele et al. 2019). The role of ferric reductase oxidase (FRO1) gene has been verified in Nicotiana benthamiana using tobacco rattle virus (TRV) based VIGS (Gama et al. 2017). This technique has been successfully applied to validate the functionality of various candidate genes in potato (Cui et al. 2009; Zhong et al. 2018). Generation of transfer (T)-DNA mutants is also a fast and effective way to study the candidate gene’s function (Radhamony et al. 2005; Duangpan et al. 2013). This technique can also be employed in potato to develop T-DNA mutant lines for any specific gene (An et al. 2005; Duangpan et al. 2013). In addition, other reverse genetic techniques such as RNA interference (RNAi) (Aggarwal et al. 2018), clustered regularly interspaced short palindromic repeats (CRISPR) (Klimek-Chodacka et al. 2018; Martín-Pizarro et al. 2019), zinc finger nucleases (ZFNs) (Petolino 2015) and targeting induced local lesions in genomes (TILLING) (Chen et al. 2014; Sánchez et al. 2018) can also be employed for the same reason. In the last decade, CRISPR-Cas9 based genome editing has been extensively used for crop improvement (Yin et al. 2017; Langner et al. 2018; Singh et al. 2018). It involves a guide RNA (gRNA) of about 20 nucleotides (spacer sequence) complementary to the target gene and a Cas9 endonuclease enzyme that has the ability to generate double stranded breaks (DSB) 3–4 bases after the protospacer adjacent motif (PAM). These DSB later on gets repaired either by error prone non-homologous end-joining pathway (NHEJ) or by homology directed repair pathway (HDR) (Zhao et al. 2016; Jiang and Doudna 2017).

Conclusion

Overcoming the hidden hunger is very crucial for a large portion of world population. Although several approaches are available but biofortification seems to be a highly sustainable approach. Dietary diversification, pharmaceutical supplementation and food fortification are not affordable for poor. Thus, these are less sustainable methods than crop biofortification. Potato crop gives significant response to agronomic practices such as tuber priming, use of soil and foliar fertilizers but farmers should be aware of dose and time of fertilizer application to get the best benefit of it. Moreover, understanding of genetic basis of micronutrient concentrations in potato tubers can facilitate potato biofortification. Wide range of genetic diversity for mineral concentration exists in potato germplasm that can be utilized via genetic engineering and plant breeding to develop nutrient rich potato varieties. However, due to ethical and biosafety issues the development of biofortified transgenic potatoes is less efficient approach to reduce hidden hunger in comparison to plant breeding. Although, traditional breeding experiments are time consuming, but nowadays with the help of advance biotechnological tools more precise and accurate breeding programs can be designed to improve micronutrient concentration in potato.

Future perspective

During the last decade, genetic engineering and genome-editing techniques, advance biotechnological, bioinformatics tools, and new breeding technologies have been mushroomed up because of their application potential. Earlier, these technologies were focused to improve the quantitative traits in potato (Hameed et al. 2018). However, to reduce the hidden hunger these techniques individually or in combination should be applied to improve the tuber micronutrients concentrations. Various attempts have been performed successfully to improve the mineral concentrations, vitamin and protein content, beta-carotene, and antioxidants levels. To catalyse the potato biofortification programs a better understanding of various pathways associated with the mineral elements uptake, accumulation and assimilation is required, which can be achieved by using advanced tools. Many genes associated with micronutrient concentrations are validated in model plants and in major food crops including potato. The potential genes from other species can be introduced to potato cultivars via genetic engineering. The expression of positive regulatory genes can be enhanced in potato and the genes that promote biosynthesis of anti-nutritional compounds can be knocked down via genome editing techniques or gene silencing approaches. The techniques namely ZFNs, transcription activator-like effector nucleases (TALENs) and CRISPR offer precise genome editing. These techniques provide a potential alternative of transgenic approaches, as these do not involve the permanent insertion foreign genes. CRISPR-Cas9 technique can be successfully applied to potato with the help of geminivirus replicons (GVRs) (Butler et al. 2016; Nadakuduti et al. 2019). Potato is responsive to plant tissue culture based propagation (Bamberg et al. 2016), thus it is comparatively easy to develop nutrient rich superior non-GMO potato plants for future with these approaches.

However, vast potato germplasm itself have many unknown genes that can increase the content of mineral elements in it. With the advent of next generation sequencing (NGS) techniques and availability of potato genome sequence, the genetic variations underlying the mineral composition can be investigated through GBS based GWAS technique. This technique provide potential candidate genes/markers associated with an observable trait that can be later validated by reverse genetic approaches. After validation, breeders can use them to speed up the development of biofortified potato varieties through marker-assisted selection (MAS) breeding and precision breeding. Previously most of the breeding experiments in potato were based upon phenotypic characters but now with the help of GWAS, these can be planned on the basis of genotypic variations. However, for the development of stable phenotypes understanding of GEI is also important. Ultimately, all these advanced biotechnological tools and high-throughput sequencing methods will lead to the development of nutrient rich potato varieties and help to diminish the grave problem of hidden hunger especially in the developing world.

Acknowledgements

This study was financed by Department of Science and Technology-Science and Engineering Research Board (DST-SERB) in the form of an externally funded project to Indian Council of Agricultural Research—Central Potato Research Institute (ICAR-CPRI), Shimla, India.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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