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Current knowledge on genetic biofortification in lentil Jitendra Kumar, Debjyoti Sen Gupta, Shiv Kumar, Sanjeev Gupta, and Narendra Pratap Singh J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.6b02171 • Publication Date (Web): 09 Aug 2016 Downloaded from http://pubs.acs.org on August 10, 2016

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Journal of Agricultural and Food Chemistry

Current knowledge on genetic biofortification in lentil Jitendra Kumar †, Debjyoti Sen Gupta †, Shiv Kumar §, Sanjeev Gupta △, Narendra Pratap Singh ▽ †

Division of Crop Improvement, ICAR-Indian Institute of Pulses Research, Kanpur, Uttar

Pradesh, 208024, India §

International Center for Agricultural Research in the Dry Areas (ICARDA), B.P. 6299,

Rabat-Institutes, Rabat, Morocco. △

AICRP on MULLaRP, ICAR- Indian Institute of Pulses Research, Kanpur, Uttar

Pradesh, 208024, India. ▽

Division of Biotechnology, ICAR- Indian Institute of Pulses Research, Kanpur, Uttar Pradesh, 208024, India.

*Corresponding author. E-mail: [email protected]; [email protected]

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ACS Paragon Plus Environment


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ABSTRACT

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Micronutrient deficiency in human body, popularly known as “hidden hunger”, causes many

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health problems. It presently affects more than two billion people worldwide especially in

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south Asia and sub-Saharan Africa. Biofortification of food crop varieties is one of the ways

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to combat the problem of hidden hunger using conventional plant breeding and transgenic

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methods. Lentils are rich source of protein, micronutrients and vitamins including iron, zinc,

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selenium, folates, and carotenoids. Lentil genetic resources including germplasm and wild

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species showed genetic variability for these traits. Studies revealed that single serving of

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lentils could provide a significant amount of the recommended daily allowance of

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micronutrients and vitamins for adults. Therefore, lentils have been identified as a food

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legume for biofortification, which could provide whole food solution to the global

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micronutrient malnutrition. The present review discusses the current ongoing efforts towards

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the genetic biofortification in lentils using classical breeding and molecular marker-assisted

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approaches.

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Keywords

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Biofortification, Breeding, Pre-breeding, Genomics, Molecular markers, Micronutrients,

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Lentils

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INTRODUCTION

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Malnutrition is a worldwide problem that occurs due to insufficient availability of proteins,

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carbohydrates, vitamins, micronutrients and presence of anti-nutritional compounds in the

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daily human diet. However, deficiency of micronutrients is increasingly becoming more

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serious now because globally people consume more carbohydrate rich cereals based diet,

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which is low in micronutrients and vitamins.1-3 More than 2 billion people are affected with

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micronutrient malnutrition in the developing world 4,5 while all over the world >3 billion

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population suffers with micronutrient deficiencies.6-8 Though in few parts, calorie intake is

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sufficient, people suffer from hidden hunger due to deficiency of micronutrients in their diet.

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As a result several health problems occur including low birth weight, anaemia, learning

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disabilities, increased morbidity and mortality rates, low work productivity, and high

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healthcare costs.9,10 Deficiencies of iron (Fe), zinc (Zn), selenium (Se), and iodine (I) are

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commonly found worldwide especially in the rural population of developing countries.

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Deficiencies of vitamin A, Zn, Fe, and/or I together cause about 20% deaths in children under

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the age of five years.11 The problem of Zn and Fe deficiency has been observed more in pre-

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school children, and pregnant women.9,12,13 The World Health Organization (WHO) estimates

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that approximately 25% of the world’s population suffers from anaemia,14 while 17.3% of

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people are at health risk due to inadequate Zn intake.15 This Zn deficiency leads to estimated

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annual deaths of 433,000 children under the age of five years.16 Globally, Se deficiency

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causes two important diseases Keshan disease (cardiomyopathy) and Kashin–Beck disease

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(osteoarthropathy) and more than one billion people are suffered with these diseases.17 It is

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especially prevalent in those countries where bioavailable Se is low in soils (100 to 2000 µg

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kg−1).18,19,20 It is an important micronutrient because it prevents cytotoxic effect of arsenic21

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due to mutual detoxification.22 Deficiency of folate or vitamin B9 causes several other health

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problems and it occurs worldwide among millions of people in both developed and

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developing countries.23 In the past, efforts were made to overcome the problems of

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malnutrition by adopting the different approaches like nutrient supplementation, food

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fortification and biofortification. However, among various approaches, genetic biofortification

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has been identified as a sustainable and cost-effective approach to provide essential

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micronutrients and vitamins to poor population through daily diet.12,24

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Previously a number of reviews have been published either on general aspects of

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biofortification25,26 or on biofortification of specific crop species such as wheat (Triticum

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aestivum) 27-29 and common bean (Phaseolus vulgaris).30,31 In few other articles, genetic

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potential for increasing the concentrations of Fe and Zn and reducing concentration of anti-

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nutrients such as phytic acid (PA) of various food crops such as maize (Zea mays), rice (Oryza

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sativa), wheat (T. aestivum) and common bean (P. vulgaris) and field pea (Pisum sativum)

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have been reviewed in detail.32-36 Based on beneficial nutritional properties, lentils have been

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identified as one of the five healthiest foods in the world.37 These are rich in starch and

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proteins and have high concentration of micronutrients.38 Also lentils are free in cholesterol,

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low in saturated fat, very low in sugar, and a rich source of dietary fibers, iron, phosphorous,

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thiamine, vitamins B and C, folates, and several antioxidant components.39 Thus use of lentils

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in diet can have beneficial impact on health by reducing the risk of several chronic diseases

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including coronary heart disease, type II diabetes, cardiovascular diseases, cancer and aging as

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a disease.40-42 In many developing countries particularly Bangladesh, India and Nepal, Sri

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Lanka, Syria, Lebanon, Turkey, Iran millions of people do consume lentil in form of soup or

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“dal”. Lentils are becoming increasingly popular among the people of developed countries

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due to its nutritional value and therefore, many processing industries are developing the

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biofortified packed food products such as ‘Plentils’, ‘Crunchy Lentil Chips’, ‘Amy’s Organic

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Soups’, ‘Lentil Crakers’, ‘Red Lentil Veggie Soup’, ‘Barley –Lentils-Risotto with Avocado

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Mousse’, and gluten free crackers, pasta, pizza crusts and snacks. This clearly indicates that

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any degree of increase in micronutrient concentrations in lentils is surely going to impact

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human health by increasing the availability of required micronutrient in diet. Therefore, in

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recent years, focus has been made on genetic biofortfication of lentils in order to develop

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more nutritionally rich cultivars in lentils and to popularize the cultivation of these biofortified

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varieties for overcoming the nutritional deficiencies of poor people who consume lentils in

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their daily diet. In the present article, efforts have been made to present the current progress

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made in lentil genetic biofortification research.

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NUTRITIONAL VALUE OF LENTILS

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Lentil (Lens culinaris Medik.) is an important cool-season food legume grown worldwide in

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52 countries. However, four major countries including India (36%), western Canada (18%),

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south-eastern Turkey (15%), and Australia (4%) contribute >70% of total world production of

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lentil.43 Its global annual production is around 4 million tons from 3.6m ha areas.43 Naturally,

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lentils are an excellent source of macronutrients, micronutrients and phytochemicals.44,45 The

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composition of these components in lentil seeds have been determined by several workers and

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nutritional value of lentils has been described in different studies.23,46,47 Studies show that

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intake of 100 g lentil grain can provide 41 to 113% of the recommended daily allowance

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(RDA) of Fe, 40-68% of Zn and 77-122% of Se. Besides lentil is rich in β-carotene

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concentration (2 to 12 µg/g).48 A study conducted on North America grown lentils showed that

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naturally lentils are low in PA-phosphorus (0.7–1.2 mg/ g). This PA level is comparatively

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lower than low PA containing mutants identified in other crops such as rice (1.22-2.23 mg/g),

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soybean (1.77-4.86 mg/g), wheat (1.24-2.51 mg/g), maize (3.3-3.7 mg/g) and common bean

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(0.52-1.38 mg/g). Lentils are also associated with a lower incidence of breast cancer due to the

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presence of dietary flavonol.49 Also its cooking saves time and energy due to faster cooking

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ability of lentils (37%, and palmitic acid, which has a content of about

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12%.55 6


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Phytochemicals, which have been into phenolic acids, flavanols, flavonols,

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soyasaponins, phytic acid and condensed tannins,56 are beneficial to health as they reduce the

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risk of several chronic diseases. These diseases are cardiovascular diseases, neural disorders

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such as Alzheimer’s and Parkinson’s disease, diabetes and cancer.57 The concentration of

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various phytochemicals has been studied in lentil flour. Phytic acid concentration has been

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observed in Canadian lentil from 6.2 to 8.8 mg/g.58 The concentration of trypsin inhibitors

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varies from 29.37 TIU/mg protein- 33.86 TIU/mg protein.53,59 Tocopherols and carotenoids

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are strong antioxidants. Lutein, which is a non-provitamin A oxygen-containing carotenoid,

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reduces incidence of age related macular degeneration, cataracts, cancer, and cardiovascular

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disease 60,61 and also helps to promote the eye and skin health.62 Many research groups studied

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antioxidant activities of hydrophilic phytochemicals such as phenolics and lipophilic

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compounds in lentils.44,63 Naturally, raw legume flour has high resistant starch value, ranging

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from 16 % (lentils) to 21% (white bean). Resistant starch are products of starch degradation,

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which are not absorbed in the small intestine of healthy individuals.64 In case of lentil, starch

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not only of high value, but also absorbed starch slowly releases glucose into the blood as

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lentils have lowest glycaemic index (GI) among major staple foods.65 Lentils consumption is

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beneficial to manage Type 2 diabetes and helps to reduce body weight.66 The glycaemic index

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has been reported 42-50 in lentils, 49-55 in chickpeas, 52-60 in beans and 100 in wheat,

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which is comparatively much lower than other pulses and cereals.67 This chemical

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composition of lentil seeds indicates that lentil is suitable for use as a whole food that can help

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to overcome the problem of global malnutrition among poor populations.48 Therefore, among

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legumes, lentils have been gaining increasing attention for health benefits as human diet, and

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are considered to be an excellent source of dietary antioxidants largely due to their high level

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of bioactive phytochemicals.68 Also in developed western countries, where lentils are

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consumed less, it has been highly recommended to diversify food by incorporating lentils in

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diet.69,70

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Red and green lentils are consumed worldwide, but ~ 80% of the world’s lentils are

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red cotyledon. The red lentils are eaten in dehulled splitted or whole form.71 Studies have also

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been conducted to estimate the nutritional value of green and red lentils by comparing the

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various nutritional components in seeds. For example, highest concentration (290 mg/g) of

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total phenolic compounds was found in red lentils compared to green lentils (68 mg/g).72,73

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Although no significant differences have been observed for antioxidant capacities of green

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and red lentil seeds, total phenolic compounds’ concentration and antioxidant capacity of red

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lentil proteins has been identified higher than the green lentil proteins.74 The range of total

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phenolic compounds’ concentration has been observed comparatively higher in green

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cultivars (4.46 to 8.34 mg CAE/g dry weight) than red lentils (5.04 to 7.02 mg CAE/g dry

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weight).75 The differences have also been observed for protein concentration between red and

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green lentils and it was found that red lentils has comparatively higher protein concentration

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(25.88%) than green lentils (23.03 %).51, 76 In cooked lentils, red lentils have higher amount of

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total dietary fibers (9.23%) than green lentils (5.24 %).77

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GENETIC BIOFORTIFICATION

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In agronomic biofortification, concentration of micronutrients is increased by utilizing

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inorganic fertilizers and improving solubilization and mobilization of micronutrients in the

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soil using intercropping and crop rotations, as well as by increasing the activities of soil

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microorganisms.12 Several reports indicated that agronomic biofortification increases the

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concentration of micronutrients in seeds. For example, selenium (Se) fertilizer application

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increased Se concentration in lentil seeds78 as observed in other crops such as potato tubers,

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tea leaves, and field pea seeds.79-81 Though it is a rapid method to develop the micronutrient

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dense staple food crop, it is not always a successful and sustainable approach because it

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increases the production cost, especially in developing countries82 and also the fertilizer

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availability is reducing throughout the world. Moreover, there is a need to take care of the rate

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of application of inorganic fertilizer because of the narrow window between toxic and

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beneficial levels especially in case of Se fertilizers.83 In contrast, genetic biofortification using

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conventional breeding for improved nutritional traits by plants may be an effective and a long-

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term sustainable solution for increasing the micronutrient status in deficient human

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populations.84, 85 In genetic biofortification, classical breeding and modern genomic

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approaches are used to characterize and exploit genetic variation for increasing micronutrient

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concentration in seed or any other plant part. The current genomic approaches help to identify

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the gene/QTLs controlling concentration of micronutrients which are used through marker

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assisted breeding.86,87 Thus, these approaches could exploit genetic variation to develop

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micronutrient dense crop varieties.88 Plant breeders screen existing genotypes in a large set of

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germplasm collection to determine the extent of genetic variation available for a particular

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trait. Breeding of nutritious cultivars rich in Fe, Zn and other nutrients as well as those

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substances that promote their bioavailability has been widely accepted as a cost-effective way

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to minimize the extent of micronutrient deficiencies.28 Presently, different strategies are either

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being utilized or can be utilized for developing the biofortified lentil cultivars through genetic

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biofortification (Figure 1).

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POTENTIAL TRAITS FOR GENETIC BIOFORTIFICATION IN LENTIL

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Lentils are rich sources of proteins, micronutrients, vitamins and many other phytochemicals.

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These compounds are required for our normal body function and deficiency of any one of

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these cause severe health problems. Therefore genetic biofortification has been concentrated

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mainly on those nutritional deficiencies which are affecting a large population worldwide

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especially among the people of developing countries. Also there are some phytochemicals

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present in lentil, which are toxic to human body and are targeted for reduction of their

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concentration by introgressing the genes that produce particular anti-nutritional phytochemical

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in less concentration in plant. These potential traits have been summarized in Table 1 and

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discussed in detail in the following section.

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Protein

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Proteins are building blocks of human body and hence its inclusion in our daily diet has

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significant role for maintaining the normal metabolic activity of the body. Protein rich pulses

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are major source of protein in vegetarian diet. Like other pulses lentils have a significant

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amount of proteins in their seeds, however protein concentration depends on environmental

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conditions and genetic potential of a particular genotype. Studies showed that protein

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concentration ranges from 22 to 31 % in lentil seeds.90 Also protein concentration in green

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(23.03%) and red (25.88%) lentils has also been observed within this range.76 Therefore, there

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is still scope to develop cultivars dense with proteins and it is one of the important traits for

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genetic biofortification. However, a rigorous genetic analysis is required for improvement in

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this trait. Also, significant variation has been found in the individual amino acids’

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concentration in different genotypes of lentils. For example, a study showed genotypic

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differences in isoleucine concentration and it varied from 3.9 to 4.4 g/16 g N, while

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concentration of cystine varied in different genotypes from 0.5- 0.9 g/16 g N.76,90 In lentils,

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methionine and cystine amino acids were found deficient in their amino acid profiles.76,90

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Micronutrients

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Deficiencies of micronutrients especially Fe, Zn and Se are the most prevalent among the

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world’s population and commonly occurred in those areas where either cereals based foods

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are used in daily diet 35 or soils are poor for these micronutrients.100-102 In lentil, a range of

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genetic variability has been observed among the available genetic resources for these

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micronutrients and has a lot of scope to increase concentration of these micronutrients in the

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biofortified cultivars through breeding.

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Prebiotic carbohydrates

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A prebiotic is a selectively fermented ingredient that allows specific changes, both in the

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composition and/or activity in the gastrointestinal microbiota that confers benefits upon host

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well-being and health.103 The changes among microbial population in the human gut can

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produce a wide range of positive effects on health.104 The obesity and related non

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communicable diseases are a major concern worldwide because more than one in every ten

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adults is affected by it.13 Prebiotics enriched diet may be a solution to reduce obesity.105,106

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Lentils contain a number of prebiotic carbohydrates. Some of them are raffinose family

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oligosaccharides (RFO)107 and resistant starch.53,108 Other prebiotic carbohydrates derivatives

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or sugar alcohols are sorbitol, mannitol, kestose, and nystose. These carbohydrates were not

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detected in lentils grown in Australia.109 However, among these, sorbitol has been identified

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in varying concentrations in germinated seeds of lentil varieties.110 The concentration of

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raffinose-family oligosaccharides (RFO), sugar alcohols, fructooligosaccharides (FOS),

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resistant starch carbohydrates were 4071 mg, 1423 mg, 62 mg and 7.5 g/100 g dry matter,

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respectively, in lentil.104 These reports indicated that prebiotic carbohydrates are potential

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traits for genetic biofortification and their genetic potential can be explored by analyzing large

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collections of genetic resources including accessions of wild relatives in order to find out

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potential donors for these traits. However, concentration of RFOs should be increased to an

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optimal level because their higher concentration can cause digestion related problem due to

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their fermentation.

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Folates or Vitamin B9

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Folates are involved in single carbon metabolism and are vital for the physiology.

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Tetrahydrofolate and its derivatives, collectively called folates, are water-soluble B-

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vitamins.23 These convert carbohydrate into glucose in human body. The deficiency of folates

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causes neural tube defects and other birth related defects in infants. Humans and animals

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cannot synthesize folates, and therefore folates are supplied through plant- and animal-based

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foods. Few studies showed that genetic variability exists for folates in lentils.23,111,112 and

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hence it is another important nutritional trait for genetic biofortification for developing the

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lentil cultivars dense with folates.

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Phytic acid

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Phytic Acid (PA) or 1,2,3,4,5,6-hexakis myo-inositol phosphate is the main phosphorous (P)

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storage form in staple food crops.113 It limits the bioavailability of micronutrients (e.g. Fe, Zn,

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Ca and Mg) by binding them. However, its role has also been identified as an antioxidant and

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its anticarcinogenic/antineoplastic properties can reduce or prevent kidney stone formation

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besides playing important roles in many physiological processes in both humans and

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animals.114 Therefore, manipulation of PA concentration can be attempted in genetic

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biofortification of lentils. The PA threshold level, which is beneficial for plant as well as

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nutrient bioavailability, needs further studies for genetic biofortification of lentils.

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Dietary Fibers

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Dietary fiber is the edible nondigestible carbohydrates and lignins found in plant food. The

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dietary fiber is a healthy food component with hypoglycemic effect.115 Like other food

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legumes lentil seeds are typically high in fiber and of this, approximately one-third to three-

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quarter is insoluble fiber and the remaining is soluble fiber.116-118 Evaluation to identify lentil

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genotypes for high concentration of dietary fiber could be a biofortification objective.

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Fatty acids

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The knowledge about the fatty acids composition in lentil and the extent of variability for each

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type is important to better understand the health benefits of lentils. Zhang et al.68 reported that

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78-82% of total lipids (2-3%) were essential fatty acids in lentil genotypes. Gamma-

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tocopherol was the major tocopherol (96-98%) and lutein was the major carotenoid (64-78%)

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in lentils.68 These workers also observed strong antioxidant activity of carotenoids in lentils.

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Evaluation of a larger set of lentil genotypes is necessary to find out the existing variations for

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these traits, if any.

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Phenolics

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Lentils are not only an excellent source of macronutrients such as protein, fatty acids,

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fibers, and carbohydrates, but also contains phytochemicals45 which can be categorized

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into phenolic acids, flavonols, soyasaponins, phytic acid, and condensed tannins.56 The

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phenolic compounds of lentil possess high level of antioxidant activity.70,73,119-123 In

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lentils, bound phytochemicals form about 82-85% of total antioxidant activity. However,

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in other legumes including chickpeas, yellow and green beans, and soybeans this

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percentage ranges between 25 and 39%.70This antioxidant activity inhibits or delays the

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oxidation of lipids, proteins, and DNA, thereby preventing the onset of oxidative diseases

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in the body.124 Few studies showed that people who consume the phenolic compound rich

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foods such as lentils have less possibility of onset of several chronic non-communicable

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diseases.125,126 Apart from antioxidant activity, phenolic compounds may also play a key

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role in the inhibition of α-glucosidase and lipase activities.127,128 The inhibition of α-

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glucosidase reduces intestinal glucose digestion and absorption, consequently controlling

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the post-prandial glycaemic response, which is key to manage of Type 2 diabetes.129

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Therefore, phenolic compounds are important potential traits for biofortification in lentil. 14


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Zou et al.130 determined phenolic composition of different fraction of lentil extract and

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reported that lentil is high in antioxidant phenolics concentration. Further, cooking does

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not impair the phytochemical antioxidants.131 Similar studies should be conducted in a

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larger set of genotypes to find out the inherent variation for phenolic compounds in

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lentils.126,132

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CURRENT STATUS OF GENETIC BIOFORTIFICATION FOR TARGET TRAITS

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Initially, screening for determination of existing natural variation for favorable alleles

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controlling enhanced concentration for target nutritional traits has been used in lentils. This

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helped to identify available genetic variability that can be exploited as donor for transferring

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the useful genes in the background of cultivated genotypes and also to use it directly as

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biofortified variety, if identified variant is already a high yielding variety.

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In the past, significant genetic variability has been observed for concentration of

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different nutrients among lentil land races from different countries including Turkey, Syria,

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Canada, and Pakistan (Table 2). These land races were adaptive to some specific nutritional

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traits due to their preference over a long period of time in particular growing regions. Hence,

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these studies have targeted nutritional traits such as folates, macro- and micro-nutrients.

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A screening of >1600 accessions of lentils including local land races, breeding lines,

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released cultivars and wild relatives for iron and zinc concentration showed significant genetic

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variability ranging from 42–132 ppm for Fe and 23–78 ppm for Zn.133,137 Another study

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observed genetic variability for folate concentration (216 to 290 µg/100 g) when 10 lentil

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cultivars of USA were evaluated over multi-year and multi-location in a field trial. The focus

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has been made in these studies on precise screening of genetic resources for different

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micronutrients, by developing the area homogenized with targeted nutrient or identifying

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areas that are naturally homogeneous. It leads to the development of maps using geo-statistics

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that show variability for targeted micronutrient.138

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Naturally, lentil is a rich source of organic Se, selenomethionine.135,139 Cooking lentil

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in boiling water does not change total Se concentration.136 Therefore, it has been targeted for

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genetic biofortification and a study of seven breeding lines showed significant genotypic

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differences for Se concentration.140,141 Genotypic differences for Se have also been found

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among the lentil genotypes grown in USA.78 It has been observed that cultivar CDC

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Greenland has higher Se concentration, but low in Fe and Zn concentration compared to

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Merrit. On other hand, Red Chief has been identified as low in Se, but high in Fe, Zn, Ca, and

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K compared to the other cultivars. Similarly Spanish brown cultivar Pardina had richness with

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Fe and Zn concentration but low in Se concentration. In general, green lentils have been

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poorer in Fe and Zn concentration and rich with Se concentration.142 Lentils are rich source of

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β‐carotene and significant variability for this compound (2 to 12 µg/g) has also been reported

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among genotypes grown in USA.48

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Interestingly, folate concentration in lentil was observed significantly higher than the

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other pulse crops such as chickpea (42−125 µg/100 g), yellow field pea (41−55 µg/100 g), and

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green field pea (50−202 µg/100 g). A serving of 100 g lentils provides 54−73% of

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recommended daily allowance of dietary folates for adult.23 Significant genotypic differences

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had also been observed in the lentil genotypes for folate concentration (114 ± 3 to 330

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±7µg/100g) as well as for total dietary fibers. It has been observed that high concentration of

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both of these compounds existed in Mediterranean landraces as compared to the breeding

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lines and released varieties of lentil.112 Recently, Jha et al.111 evaluated a set of four popular

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lentil cultivars from replicated field trials over two locations for folate concentration along

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with other food legumes. Folate concentration ranged between 137-182µg/100 g in lentils.111

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Significant environment effect on folate concentrations was also detected.111 Turkish land

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races also showed a range of diversity not only for micronutrients but also for

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macronutrients.136 Breeding lines, varieties and parental lines along with exotic lines of lentil

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grown under Indian conditions had also revealed a range of variability for macro and micro

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nutrients. Concentrations of Ca and Mg in Indian germplasms are much lower than Turkish

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germplasm.136 In contrast to this, variability for P (3907 – 7262 mg/kg) and K (4771-9634

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mg/kg) has been identified to be much higher than Turkish land races (P: 2860-5330 mg/kg;

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K: 6380-9500 mg/kg). Higher amount of Fe, Zn and Se was also observed in Indian genotypes

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and breeding lines compared to exotic lines (unpublished results of Kumar J.). Similarly,

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significant genotypic effects were identified on Fe and Zn concentration among 41 elite lines

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of lentils when grown over three locations in India.143

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Prebiotic carbohydrates are important components of healthy diets supporting

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healthful hindgut microbiota. Some prebiotic carbohydrates show significant variation among

361

lentil genotypes, suggesting potential for increasing their amounts through conventional plant

362

breeding.53,108,144 In a recent study, significant genetic variability had been observed among 10

363

commercial lentil varieties for several prebiotic carbohydrates including raffinose-family

364

oligosaccharides (RFO), sugar alcohols, fructooligosaccharides (FOS), and resistant starch

365

(RS).104 However, this study showed that RFO concentration varies from genotype to

366

genotype and RS varies from location to location. While sorbitol and mannitol both vary by

17



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367

variety and location. Thus lentils possess nutritionally significant amounts of prebiotic

368

carbohydrates that may be possible to be increased through breeding and location sourcing.104

369

Antioxidant and enzyme inhibitory activities of the phenolics may differ in different

370

popular lentil cultivars as well as in available lentil genetic resources. Many studies have

371

investigated presence of the phenolic compounds and antioxidants in traditional lentil

372

cultivars.44,145 Recently inhibitory capability of phenolics against α-glucosidase and lipase

373

activities, which are required for controlling the blood glucose levels and obesity in human

374

body, have been assessed among 20 most popular lentil cultivars grown in Canada.78 In this

375

study, total phenolic content has varied from 4.46 to 8.34 mg CAE/g dry weight among 20

376

lentil cultivars. This study also showed genotypic differences for total flavonoid and

377

condensed tannin content.78 Also significant variability was observed for antioxidant and

378

enzyme inhibitory effects of phenolic compounds in lentil cultivars.78 Thus identification of

379

genetic potential of genotype for targeted nutritional traits helps to provide supporting

380

information for selecting phenolic compound enriched lentil cultivars and also for developing

381

lentil-based functional foods through genetic biofortification.78

382

As compared to other pulse crops, limited efforts have been made for determination of

383

protein content among lentil genotypes. Studies showed that protein concentration ranged

384

between 22 to 31 % in all type of lentils. 76,89,90 A study showed no significant genetic

385

variability for this trait among six genotypes of lentils.89 However, in lentil a large collection

386

of lentil germplasm is still unscreened for protein concentration. Therefore, systematic efforts

387

are required to screen these genetic resources so that useful donors could be identified for

388

improving the protein content through genetic manipulation. An inheritance study in chickpea

389

exhibited a continuous variation for protein content indicating that this trait is inherited

18


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390

quantitatively.146 In this study, blue flower individuals of F2 population produced higher mean

391

protein content (21.81%) probably due to their reduced seed size and it was observed that grey

392

seed coat color group had highest mean protein content (21.8%) compared to other color

393

groups.146 This study also showed a significant negative correlation of protein concentration

394

with seed size (-0.40), harvest index (-0.58) and seed yield (-0.18) and positive correlation

395

with days to maturity (0.14), plant height (0.30), secondary branches (0.14), biomass (0.15).146

396

Similar studies in lentils could increase understanding on genetic manipulation of protein

397

content through breeding approaches.

398 399

EFFORTS TOWARDS THE USE OF WILD GENETIC RESOURCES FOR

400

IMPROVING NUTRITIONAL VALUE THROUGH PRE-BREEDING APPROACHES

401 402

Wild species are the rich reservoir of useful alien genes, which are no longer available within

403

the cultivated gene-pool.147 Continuous efforts have been underway to collect and conserve

404

wild relatives of various food legume crops in national and international gene banks.148,149

405

Over the years, International Center for Agricultural Research in the Dry Areas (ICARDA)

406

has collected and conserved 587 accessions representing all wild Lens species (L. culinaris

407

ssp. orientalis, L. odemensis , L. nigricans, L. ervoides, L. lamottii, ) from 26 countries. Many

408

species have shown cross compatibility with cultivated species in a number of studies carried

409

out in the past. For instance, wild species L. culinaris ssp. orientalis and L. odemensis had

410

been found crossable with cultivated lentils,150-152 although the fertility of the hybrids depends

411

on the chromosome arrangement of the wild parent.153 Most accessions of L. culinaris ssp.

412

orientalis cross readily with L. culinaris, and both are genetically isolated from the other

19



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413

species. Lens nigricans and L. ervoides are not readily crossable with the cultivated lentil

414

using conventional crossing methods due to hybrid embryo breakdown.154 Crosses are

415

possible between L. culinaris and the remaining species, but they are characterized by a high

416

frequency of hybrid embryo abortion, albino seedlings and chromosomal rearrangements that

417

result in hybrid sterility, if these seedlings reach maturity.154,155 This cross compatibility

418

resulted in successful introgression of alien genes from wild relatives; however traits have

419

been limited to a few diseases and insect pests, which are controlled by major gene(s).156

420

However, advances in tissue culture techniques could now help in embryo rescue, which

421

facilitated alien gene introgression from wild species of secondary gene pool.157 Moreover,

422

evolutionary forces make changes in accessions of wild species towards the possible cross-

423

compatibility with cultivated species. As a result, earlier cross-incompatible wild species may

424

now cross with cultivated species. Revisiting the crossability relationships of recent lentil

425

cultivars and wild species is necessary. Therefore, pre-breeding efforts are urgently required

426

particularly involving those wild species, which carry useful alien genes for biofortification

427

traits.

428

The wild relatives are important sources for generation of new variability through

429

recombination breeding approaches. In other legume crop, such as common bean, wild species

430

have been identified as donors for high concentration of micronutrients.158 In wheat, wild

431

relatives have substantial variation for nutritional traits such as Zn and Fe. 159-161 In lentil,

432

however, limited efforts have been used to identify the wild relatives with high micronutrients

433

and vitamins concentrations. The study conducted at ICAR-Indian Institute of Pulses

434

Research, Kanpur using 10 accessions of lentil wild species on average 29.7% protein, phenol

435

concentration of 8.9 mg/100g and total antioxidant activity (16.17 µmole TE/g) were

20


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436

observed, which were higher values than those of cultivated Lens species (unpublished data).

437

More recently, a wild accession of L. orientalis, ILWL 118 having Fe concentration of 150

438

ppm has been identified and this accession is being extensively utilized in pre-breeding

439

program.162 This indicates potential of wild relatives for using them in breeding program.

440

However, for this purpose, concerted efforts are required to screen more wild resources of

441

lentils for micronutrients and other nutritional traits and these identified resources could be

442

utilized to transfer alien genes from wild species through wide hybridization in lentils.

443 444

MOLECULAR MARKER -ASSISTED BIOFORTIFICATION: A LESSON FROM

445

OTHER CROPS

446 447

In lentil, significant progress has been made in development of genomic resources.163, 164

448

Recent development in the next generation sequencing techniques has facilitated sequencing

449

of lentil genome (23x coverage). It covered half the genome i.e. 2.7 Gb of the expected 4.3Gb

450

and additional 125x coverage is currently being assembled.165 Gene sequences for several

451

traits of interest were identified using the initial 23x draft assembly and derived SNP markers

452

are now available for mapping the genes/QTLs for important agronomic traits in the lentil

453

breeding program.165 In lentil, genes/QTLs have already been identified for several traits of

454

agronomic importance (see reference 165 for more details). In lentil, those genes controlling Fe

455

uptake have been mapped in a biparental RIL population [ILL 8006–BM (Barimasur-4) x

456

CDC Milestone] through QTL analysis. In this case, phenotyping data of RILs in three

457

different locations in Turkey was recorded for Fe concentration (37-149 mg/kg) and

458

population was genotyped using164 molecular markers, including 150 AFLPs, 27 SSRs and

21



Page 22 of 62

459

four SNPs. QTL analysis resulted in identification of 4 QTLs for Fe uptake that can be used in

460

molecular breeding towards the development of biofortified cultivars.166 A study has identified

461

at least 6 and 15 lentil genotypes stable for Fe and Zn concentration over three locations,

462

respectively.143 These genotypes have been characterized with 32 polymorphic SSR markers.

463

As a result, diverse parents have been identified for Fe and Zn concentration in their grains

464

in order to use them in hybridization program for obtaining the transgressive segregants of the

465

traits.143 Recently QTL mapping has been conducted for selenium concentration in RIL

466

mapping population developed from the cross PI 320937 (119 µg/kg) × Eston (883 µg/kg). In

467

this study, four QTL regions and 36 putative QTL markers, with LOD scores ranging from

468

3.00 to 4.97, distributed across two linkage groups (LG2 and LG5) have been identified to be

469

associated with seed Se concentration. These QTLs have explained 6.3–16.9% of the

470

phenotypic variation.167 Further efforts are underway to characterize more diverse natural

471

genetic variation in lentil with more number of molecular markers in Molecular Breeding

472

Laboratory of ICAR-Indian Institute of Pulses Research in order to map the genes for

473

nutritional traits using association mapping. Significant progress has been made in other

474

legume crops with regard to mapping and tagging of the gene(s)/QTL controlling

475

micronutrients concentrations.168 For example, in case of mungbean and soybean, QTL

476

identified for phytic acid concentration had explained only low to moderate amount of

477

phenotypic variation.169, 170 Similarly QTL for Fe and Zn concentration in common bean has

478

also explained moderate phenotypic variation.30,171-175 In chickpea, Diapari et al.176 identified

479

eight SNPs controlling iron and zinc concentrations in chickpea (Cicer arietinum), among

480

them one SNP was associated with both iron and zinc concentrations. On the other hand in

481

cereals such as rice, maize, and barley, significant progress has been made to the

22


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482

understanding of the distinct routes for Fe and Zn uptake in the seed. Moreover, pathways for

483

biofortified traits have been extensively studied in model crops.177-180 Therefore, knowledge of

484

these pathways could be utilized in identification of gene(s)/QTL responsible for controlling

485

the variation for biofortification related traits in lentil using the comparative genomic

486

approaches and would facilitate the development of functional markers for MAS.164 In rice,

487

QTL has also been identified for Zn biofortification and functional markers associated with

488

QTL controlling Zn concentration showed significant variation within a RIL population.181

489

For example, in maize, genetic markers associated with higher concentration of provitamin A

490

were identified. These PCR based DNA markers distinguish alleles of three key genes of

491

maize endosperm carotenoid biosynthesis (PSY1, lcyE and crtRB1) and hence help to assess

492

the provitamin A concentration in maize kernels easily. Therefore, efforts have been made to

493

develop maize varieties with increased pro-vitamin A concentration through marker assisted

494

breeding in order to combat vitamin A deficiencies.182

495 496

HARVESTPLUS CHALLENGE PROGRAM TOWARDS THE DEVELOPMENT OF

497

BIOFORTIFIED LENTIL CULTIVARS

498 499

In 2004, the HarvestPlus Challenge Program was officially founded by the Bill and Melinda

500

Gates Foundation and other donors. In 2012, HarvestPlus became component of the CGIAR

501

Research Program on Agriculture for Nutrition and Health (A4NH). Initiative has been taken

502

by the Consultative Group on International Agricultural Research (CGIAR) through

503

HarvestPlus Challenge Program on development of biofortified lentils that are rich with iron,

504

zinc, and provitamin A.183 During second phase of HarvestPlus program, International Center

23



Page 24 of 62

505

for Agricultural Research in the Dry Areas (ICARDA) took lead for developing the

506

biofortified lentils. This program has focused to develop the high yielding lentil cultivars with

507

high concentration of Fe and Zn. Initially, efforts had been made to identify the biofortified

508

varieties in lentil through screening of existing released varieties. In this direction, released

509

varieties of different countries (i.e. Bangladesh, Ethiopia, Nepal, Morocco, Turkey, Syria,

510

Lesotho and Portugal) were screened for Fe and Zn concentration under this program. As a

511

result, a number of released varieties have been found to possess high iron and zinc

512

concentrations along with good agronomic performance (Table 3). These varieties or cultivars

513

were fast tracked and are being used as biofortified varieties of lentils for economically poor

514

regions of the world. For example, in Bangladesh, the Government has taken a massive

515

dissemination program to promote promising lentil varieties (Barimasur 5 and Barimasur 6)

516

having high Fe and Zn. Similarly in Nepal, lentil varieties such as Khajurah1, Khajurah 2,

517

Sishir and Shital are spreading fast in the Terai region of Nepal. In India, the variety Pusa

518

Vaibhav rich in Fe is being grown by farmers in its north-west plain agro-climatic zone.184 In

519

future, more biofortified varieties of lentils would be released for general cultivation in

520

different countries. For example, in Nepal, variety ILL 7723 has been recommended by the

521

National Variety Release Committee for cultivation.137

522 523

LIMITATIONS OF GENETIC BIOFORTIFICATION IN LENTIL

524 525

Impact of Environmental conditions

526

24


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527

The soil and environmental conditions such as pH, temperature, radiation, precipitation,

528

organic matter, and soil texture affect the concentration and solubility of micronutrients to

529

plant roots.185-187 Breeding for nutritional traits may also be complicated by environmental

530

conditions, particularly growing locations. Therefore, it is required to have knowledge of

531

environment and genotype × environment interactions in order to develop stable biofortified

532

cultivars or to design location specific breeding of traits in any particular biofortification

533

program. In lentil, accumulation of PA, Fe, and Zn in the seeds are known to vary with

534

weather (rainfall and temperature), location and soil conditions.78,93,188 A few numbers of

535

studies were conducted to know effects of genotypes, years, locations and their interactions on

536

different nutritional traits in lentil.23, 78,93,111,188 It has been shown that concentration of

537

micronutrients varies from one geographical region to other region when global lentil samples

538

were studied (see reference 46). For example, high concentrations of Fe observed in seed

539

sample of Syria (63 mg/kg), Turkey (60 mg/kg), USA (56 mg/kg), and Nepal (50 mg/kg),

540

while it was low in seed samples of Australia (46 mg/kg) and Morocco (42 mg/kg). Similarly

541

higher Zn was found in lentils grown in Syria (36 mg/kg), Turkey (32 mg/kg), and USA (28

542

mg/kg) and lowest in Australia (18 mg/kg) and Morocco (27 mg/kg). In case of Se, a survey

543

showed that genotypes belonging to Nepal and Australia samples have higher Se

544

concentrations (180 and 148 µg/kg, respectively) compared to genotypes from Syria,

545

Morocco, and Turkey (22, 28, and 47 µg/kg, respectively).46 In another study, Turkish land

546

races showed higher concentration of Ca in their seeds (0.48- 1.28g/kg), while lentil samples

547

grown in Indian conditions showed richness in Fe (37-156 mg/kg) and Zn (26-65 mg/kg)

548

concentration (Kumar J. unpublished data).136

25



549

Page 26 of 62

The multi-location testing of varieties/advanced lines of lentil in Bangladesh, Ethiopia,

550

India, Nepal, and Syria showed significant genotype by environment (G×E) interaction for Fe

551

and Zn.137 It has been observed that Fe concentration is more sensitive to environmental

552

fluctuations compared to seed Zn concentration. These studies identified few genotypes with

553

stable high-iron and zinc concentrations such as IPL 320 and L4704 in India.137 Kumar et

554

al.143 have also reported that Fe concentration is more sensitive to environmental conditions

555

compared to Zn in a multi-location study. The evaluation of seven lentil genotypes over four

556

locations along with a farmers’ field survey conducted in Bangladesh revealed significant

557

genotype and location differences for seed Se concentration but genotype × location

558

interaction was non-significant.141 In Australia, similar results were obtained when 12 lentil

559

genotypes were evaluated over seven locations.141,189 Recently, genotype (G) × environmental

560

(E) interactions for folate concentration in 10 lentil cultivars of USA have been studied over

561

two years, which showed a significant year × location interaction effect on lentil folate

562

concentration.23 Similarly the significant G × E interaction was also reported by Jha et al.111 In

563

another study, the impact of temperature has been shown on PA, Fe and Zn concentration

564

among mature seeds of 11 lentil genotypes. This study was conducted under simulated long

565

term temperature regimes representative of Saskatoon, Canada (decreasing temperatures) and

566

Lucknow, India (increasing temperatures). In this study, PA and Zn concentrations in lentil

567

seeds have been observed significantly higher in the rising temperature regime (8.8 mg/g and

568

69 mg/kg, respectively) than in the decreasing temperature regime (6.7 mg/g and 61 mg/kg,

569

respectively). Fe concentrations followed the same trend (116 vs. 113 mg/kg). Therefore, if

570

the lentil cultivars with lower concentration of PA needed to be developed, the cooler

571

temperatures of temperate summers might be an important factor. In other crop, like wheat,

26


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572

breeding for high Zn concentration is complicated by environmental conditions, particularly

573

soil composition.190 Overall, most of the studies suggested that micronutrient concentrations

574

of the grain or seed are largely influenced by the genetic and environmental factors. Hence

575

further studies should be conducted under different environmental conditions for validating

576

the results. Moreover, nutritional traits such as folate, Se and Zn, which are highly influenced

577

by conditions of local environments, location specific biofortified cultivars can be developed

578

by utilizing the genetic variability for these traits.23 This becomes more important under the

579

changing climatic conditions where increase in winter temperature patterns can facilitate the

580

increase of concentration of anti-nutrients such as PA. Therefore , success in global hidden

581

hunger will depend upon the genetic biofortification to develop cultivars having high

582

concentration of Fe and Zn and low level of anti-nutrients.

583 584

Heritability of nutritional traits

585 586

Heritability of a trait is important to plant breeders for making genetic improvement

587

particularly in quantitatively inherited traits through selection. Use of trait heritability

588

estimates distinguish the proportion of total phenotypic variances caused by genotype and

589

environmental factors and tell us that what extent we can get response to selection in selected

590

population over the initial breeding pool.191 Thus poor trait heritability has a limitation in

591

improvement of nutritional traits as large proportion of phenotypic variation is under the

592

control of environments (see above). However, broad sense heritability has been estimated

593

from 64 to 68% for nutritional traits such as Fe and Zn concentration (Kumar J. unpublished

594

results). This moderate level of heritability estimates of Fe and Zn concentrations showed the

27



Page 28 of 62

595

possibility of breeding for high Fe and Zn containing lentil genotypes (Kumar J. unpublished

596

results). In other crops like wheat, similarly, G × E effect was not identified a serious issue for

597

breeding of high Zn because studies showed high heritability and high genetic correlation

598

between locations for seed Zn concentration.192

599 600

Pros and cons of a target nutritional trait: Level optimization

601 602

A nutritional trait in lentil may be beneficial or harmful depending upon the objective to

603

increase or decrease the concentration of that trait. Therefore, optimum concentration of

604

respective trait is essentially required to consider in genetic biofortification. For example

605

phytic acid is an anti-nutritional phytochemical in lentil seeds because its presence limits

606

bioavailability of micronutrients (e.g. Fe, Zn, Ca and Mg) to human body by binding them. A

607

study showed that Fe concentration is positively correlated with PA and also relative Fe

608

bioavailability negatively correlated with PA concentration in lentil.193 On the other hand,

609

studies showed that low level of PA in seeds had adverse effect on seeding germination

610

because PA is the main phosphorous (P) storage form in staple food crops.194 Therefore,

611

genetic biofortification has been suggested to develop lentil cultivars with optimal level of

612

phytic acid. These limitations have restricted the nutritional improvement of such traits

613

through genetic means. However in recent years, efforts have been made to identify the lower

614

concentration PA mutant lines that have 50% reduction in PA concentration but no negative

615

effect on seedling germination in legumes.195 Also it has been shown that Fe and PA are

616

controlled by separate genes and hence there is a possibility to breed Fe dense crops with low

617

concentration of PA.12 Another strategy has been suggested to develop the cultivars having

28


Page 29 of 62


618

high concentration of minerals as a result of which negative impact of PA will be minimal and

619

sufficient micronutrients will be available in the diet.196 Genetic biofortification programs for

620

improving quality of lentils require stringent and cumbersome screening of traits over time in

621

order to assess the potential nutritional value of a particular lentil genotype. Moreover,

622

methods assessing iron bioavailability, for example, Caco-2 cell culture method or measuring

623

concentration of phytic acid or any mineral require a lots of expenditure, technical expertise

624

and instrument facilities, which limits routine screening of such traits.

625 626

FUTURE PERSPECTIVES

627 628

The genetic variability exists among the cultivated germplasm for nutritional traits that can be

629

exploited in breeding programs. Genetic variability has also been identified for the

630

concentration of a particular essential amino acid in the protein composition of lentils. Hence

631

concerted efforts are required to improve the essential amino acids particularly methionine

632

and cystine for which lentil proteins are to be found deficient. Further many nutritional traits

633

in lentil were highly influenced with environmental conditions and, genetic makeup of a

634

particular genotype and in many instances maximum expression of the concerned trait could

635

be found in specific location only. Therefore, efforts should be concentrated on location

636

specific breeding of such nutritional traits. The wild relatives have been identified as potential

637

donors for nutritional traits in many crops. However, such variations have not been explored

638

in lentils so far, although wild relatives have been identified as useful genetic resources for

639

other agronomical traits. Therefore, in future emphasis would be given on wild relatives for

640

generating the useful pre-breeding materials for biofortification related traits. Now genomics

29



Page 30 of 62

641

has become an integral part of breeding programs. In lentils, excellent progress has already

642

been made in development of genomic resources. However, these genomic resources have not

643

been fully exploited in genetic biofortification of lentil crops. Molecular markers can be used

644

in tagging and mapping of genomic regions that control the expression of nutritional traits

645

through association analysis. These developments can facilitate to dissect complex genetics

646

regulating the nutritional traits. The markers associated with favorable genes/QTL affecting

647

the biofortification traits can be used in marker assisted breeding that would accelerate the

648

development of biofortified lentil cultivars rapidly and cost effectively in near future.

649 650

ACKNOWLEDGEMENTS

651 652

Authors are thankful to Indian Council of Agricultural Research (ICAR), New Delhi and

653

Consultative Group for International Agricultural Research (CGIAR) for providing financial

654

support under HarvestPlus Challenge Program for carrying out the research work on

655

biofortfication in lentil.

656 657

REFERENCES

658 659 660 661

(1) Stewart, C. P.; Dewey, K. G.; Ashoran, P. The under nutrition epidemic: an urgent health priority. Lancet 2010, 375, 282. (2) Cakmak, I.; Kalayci, M.; Kaya, Y.; Torun, A. A.; Aydin, N.; Wang, Y.; Arisoy, Z.;

662

Erdem, H.; Yazici, A.; Gokmen, O.; Ozturk, L.; Horst, W. J. Biofortification and

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localization of zinc in wheat grain. J. Agric. Food Chem. 2010, 58, 9092-9102.

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(3) Bouis, H.; Low, J.; McEwan, M.; Tanumihardjo, S. Biofortification: Evidence and lessons

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learned linking agriculture and nutrition. 2013. Available at

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http://www.fao.org/fileadmin/user_upload/agn/pdf/Biofortification_paper.pdf. (accessed

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on July 25, 2015).

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(4) Cakmak, I.; Pfeiffer, W.; McClafferty, B. Biofortification of durum wheat with Zn and Fe. Cereal Chem. 2010, 87, 10-20. (5) Depar, N.; Rajpar, I.; Memon, M. Y.; Imtiaz, M.; Hassan, Z. Micronutrient nutrient

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densities in some domestic and exotic rice genotypes. Pak. J. Agri. Agril. Engg. Vet. Sc.

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2011, 27, 134–142.

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(6) Welch, R. M. 1–24 in Farming for nutritious foods: agricultural technologies for

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improved human health. IFAFAO Agriculture Conference on Global food security and

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the role of sustainable fertilization. 26- 28 March, Rome, Italy. 2003.

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(7) Sramkova, Z.; Gregova, E.; Sturdik, E. Chemical composition and nutritional quality of wheat grain. Acta. Chim. Slovaca, 2009, 2, 115- 138.

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(8) Nagy, R.; Grob, H.; Weder, B.; Brearley, C.; Martinoia, E. ABC transporters: key players

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healthy food and feed. Food and Agriculture Cost Action FA0905. 4-5 June, 2012.

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J. I. New challenges in studying nutrition disease interactions in the developing world. J.

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(12) White, P. J.; Broadley, M. R. Biofortification of crops with seven micronutrient elements

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often lacking in human diets -iron, zinc, copper, calcium, magnesium, selenium and

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iodine. New Phytology 2009, 182, 49-84.

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(13) World Health Organization (WHO). The World Health Report. World Health Organization, Geneva, Switzerland. 2012.

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(14) World Health Organization WHO. Worldwide Prevalence of Anaemia 1993–2005: WHO

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Global Database on Anaemia. B. de Benoist, E. McLean, I. Egli, M. Cogswell (Eds).

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World Health Organization Press, Geneva, Switzerland. 2008.

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(15) Wessells, K. R., Brown, K. H. Estimating the global prevalence of zinc deficiency:

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stunting. PLoS One 2012, 7, e50568.

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(16) World Health Organization WHO. Global Health Risks. Mortality and Burden of Disease

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1199


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1200

phosphate composition in soybean lines with independent ipk1 mutations. The Plant

1201

Genome 2015, 8, 1-10.

1202 1203 1204

(196) Savage, G. P.; Deo, S. The nutritional value of peas (Pisums ativum). A literature review. Nutr. Abstr. Rev. 1989, 59, 65–88. (197) Johnson, C. R.; Thavarajah, D.; Thavarajah, P.; Fenlason, A.; McGee, R.; Kumar, S.;

1205

Combs, Jr, G. F. A global survey of low-molecular weight carbohydrates in lentils. J.

1206

Food Comp. Anal. 2015, 44, 178–185.

1207 1208 1209 1210 1211 1212 1213 1214 1215

Figure Caption

1216 1217

Figure 1. Schematic diagram of multidisciplinary biofortification research. In this flow

1218

diagram the entire process of development of biofortified lentil varieties are shown. The

1219

process is initiated with selection of lines with high micronutrient or vitamin concentration

1220

with optimum food matrix profile. The donor gene or quantitative trait loci is then transferred

1221

to the desired line through crossing or marker assisted selection (MAS) or transgenesis. After

55



Page 56 of 62

1222

going through multiple cycles of selections through different filial generations the stabilized

1223

advanced breeding line fulfilling the breeding objectives is released and notified for mass

1224

cultivation. The impact analysis of released biofortified varieties can be done by clinical trials

1225

(adopted from Gupta, D.S.; Ekanayake, L. J.; Johnson, C.; Amarakoon, D.; Kumar, S. Rice,

1226

Wheat and Maize Biofortification. In Sustainable Agriculture Reviews. 2015. pp. 123-140.

1227

Springer International Publishing.; it will be reproduced with permission from Springer

1228

International Publishing Switzerland).

1229 1230 1231 1232 1233 1234 1235 1236 1237 1238 1239 1240 1241 1242 1243 1244 1245 1246 1247 1248 1249 1250 1251 1252 1253 1254 1255 1256 1257 1258 1259 1260

56


Page 57 of 62


1261 1262 1263 1264 1265 1266 1267 1268 1269

Table 1. Concentartion of nutritional and anti-nutritional compounds and targeted

1270

objectives for genetic biofortification in lentil

1271

traits

concentration range

target for

reference

improvement nutritional compounds protein

15.9 -32 %

increase

76, 89-91

starch

34.7- 65.0 %

increase

91,50-52

dietary Fibers

5.1-26.6 %

increase

92

fatty Acids

0.3- 3.5 g/100 g

increase

92

iron

73-90 mg/kg

increase the

93

zinc

44-54 mg/kg

increase

93

6.24-27.73 mg GAE/g

decrease

76

decrease

75

decrease

75

micronutrients

anti-nutritional compounds total phenolics

defatted sample total flavonoids

1.15-4.94 mg CE/g defatted sample

condensed tanin content

3.14-12.97 mg CE/g

57



Page 58 of 62

defatted sample phyto-oestrogens

8.9-12.3 µg/100g dry

decrease

94

matter phytate

3.9-11.9 mg/g

decrease

47

saponins

0.07-0.13 g/ 100 g

decrease

95

25-55 TIA/mg of

decrease

96

-

decrease

97

lectins

-

reduce

98

vicilin protein

-

decrease

99

enzyme inhibitors protease inhibitor

protein α-amylase inhibitor toxins

low molecular weight carbohydrates

1272 1273 1274 1275 1276 1277 1278

sorbitol

1250–1824 mg/100 g

increase

197

mannitol

57–132 mg/ 100 g

increase

197

galactinol

46–89 mg/100 g

increase

197

sucrose

1750–2355 mg/100 g

increase

197

raffinose + stachyose

3314– 4802 mg/100 g

increase

197

verbascose

1907–2453 mg/100 g

increase

197

nystose,

8–450 mg/100 g

increase

197

GAE=Gallic Acid Equivalent, CE= Chinan Equivalent, TIA= Tripsin Inhibitor Activity

58


Page 59 of 62


1279 1280 1281 1282 1283

Table 2. Genetic variability studied for Fe, Zn, and Se concentration among gemplasm

1284

lines of lentil

type of screening

number of

range of variability

material

genotypes

Fe

Zn (mg/kg)

(mg/kg) land races, wild

1600

43-132

country

reference

ICARDA,

133

Se (µg/g)

22-78

types and

Syria

breeding lines lentil germplasm

-

41-109

22-78

-

do

134

breeding lines,

900

73-90

44-54

425-673

Canada

93, 135

46

49- 81

42- 73

-

Turkey

136

96

37 - 157

26-65

240-

India

Kumar J.

germplasm and modern high yielding genotypes land races, cultivars land races, breeding material,

630

exotic lines

(unpublished data)

1285 59



Page 60 of 62

1286 1287 1288 1289 1290

Table 3. Lentil variety rich in Fe and Zn identified through analysis of released cultivars

1291

under the HarvestPlus Challenge Program of CGIAR country

Bangladesh

Nepal

India

Syria/Lebanon

Ethiopia

name of variety

content (ppm) Fe

Zn

Barimasur -4

86.2

-

Barimasur-5

86

59

Barimasur-6

86

63

Barimasur-7

81

-

Sisir

98

64

Khajurah-2

100.7

59

Khajurah-1

-

58

Sital

-

59

Shekhar

83.4

-

Simal

81.6

-

PusaVaibhav

102

-

L 4704

125

74

Idlib-2

73

-

Idlib-3

72

-

Alemaya

82

66

1292 60


Page 61 of 62


1293 1294 1295

1296 1297 1298 1299 1300 1301 1302 1303 1304 1305 1306 1307 1308 1309 1310

Figure 1.

61



1311 1312 1313 1314 1315 1316 1317 1318 1319

Graphic for table of contents

1320

62


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Current Knowledge on Genetic Biofortification in Lentil - Journal of

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