Artocarpus Lakoocha Roxb. and Artocarpus Heterophyllus Lam
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plants Article Artocarpus lakoocha Roxb. and Artocarpus heterophyllus Lam. Flowers: New Sources of Bioactive Compounds Arun Kumar Gupta 1 , Muzamil Ahmad Rather 2, Avinash Kumar Jha 1, Abhinay Shashank 3, Somya Singhal 1, Maanas Sharma 1, Urbi Pathak 4, Dipti Sharma 5 and Andrea Mastinu 6,* 1 Department of Food Engineering and Technology, Tezpur University, Assam 784028, India; [email protected] (A.K.G.); [email protected] (A.K.J.); [email protected] (S.S.); [email protected] (M.S.) 2 Department of Molecular Biology and Biotechnology, Tezpur University, Assam 784028, India; [email protected] 3 Department of Dairy Science and Food Technology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221005, India; [email protected] 4 Department of Food Science, ISA Lille, 59800 Lille, France; [email protected] 5 Department of Food Technology, Shyama Prasad Mukherji College for Women, University of Delhi, Delhi 110026, India; [email protected] 6 Department of Molecular and Translational Medicine, Division of Pharmacology, University of Brescia, 25123 Brescia, Italy * Correspondence: [email protected]; Tel.: +39-030-371-7653 Received: 21 September 2020; Accepted: 3 October 2020; Published: 9 October 2020 Abstract: Artocarpus heterophyllus Lam. (AH) and Artocarpus lakoocha Roxb. (AL) are two endemic plants that grow on the Asian continent. To date, their applications have been aimed at using their fruit as a food source or for some of their therapeutic virtues. In this study, attention was given to the flowers of AH and AL. Initially, the cytotoxicity of the phytoextracts was assessed, and the content of minerals, phenols, and flavonoids was determined. Furthermore, some antioxidant components were identified by HPLC. Furthermore, the ability of AH and AL extracts to modulate the gene expression of some targets involved in the antioxidant response was studied. The results obtained highlighted the nutritional and antioxidant value of the AH and AL flower extracts. This study will contribute to enhancing the use of AH and AL flowers as potential supplements in human nutrition. Keywords: Artocarpus lakoocha Roxb.; Artocarpus heterophyllus Lam.; antioxidant properties; DMPD radical; antimicrobial properties 1. Introduction The genus Artocarpus consists of tropical plants of the Moraceae family that are mainly cultivated in Asian countries such as India, Bhutan, Sri Lanka, Thailand, Bangladesh, and Malaysia [1,2]. Artocarpus includes almost 60 genera and more than 1000 species. This genus is believed to produce a high yield along with an ample number of nutritional components. Its species are used as a source of food and also in traditional medicinal practices [3]. Artocarpus heterophyllus Lam. (AH), popularly known as Ceylon jack tree or jackfruit, is considered to be “poor man’s food”, as it is widely available in summer at an economical price when there is a shortage of agricultural produce in India [4,5]. In India, it is also called “Panasa”, “Atibruhatphala”, “Kantaphal”, and “Kanthal” due to its physical characteristics. The AH tree is also considered to be a source of flavonoids, sterols, volatile acids, carotenoids, and tannins, which vary depending on the Plants 2020, 9, 1329; doi:10.3390/plants9101329 www.mdpi.com/journal/plants Plants 2020, 9, x FOR PEER REVIEW 2 of 16 Plants 2020, 9, 1329 2 of 16 considered to be a source of flavonoids, sterols, volatile acids, carotenoids, and tannins, which vary depending on the stage of maturity [6–10]. Moreover, it also has a unique combination of iron, stage of maturity [6–10]. Moreover, it also has a unique combination of iron, vitamin C, vitamin B vitamin C, vitamin B complex (especially vitamin B6, niacin, folic acid, and riboflavin), and minerals complex(mainly calcium (especially and potassium) vitamin B6 ,[11,12]. niacin, The folic fruit acid, of AH and has riboflavin), been employed and minerals in value (mainly‐added products calcium andsuch potassium) as fruit juice, [11 dried,12]. chips, The fruit jam, of candies,AH has jelly, been marmalades, employed in leather, value-added and ice products cream, depending such as fruit on juice,the sensorial dried chips, characteristics jam, candies, at different jelly, marmalades, stages [11]. leather, AH bears and flowers ice cream, after depending 6–8 years of on planting, the sensorial and characteristicsflowers start to at bloom different from stages November [11]. AH tobears March. flowers It is reported after 6–8 yearsthat, being of planting, a monoecious and flowers tree, start the toflowers bloom are from covered November by two tospathes March. of 5–10 It is reportedcm in length that, [13] being (Figure a monoecious 1A). The central tree, theand flowers peripheral are coveredregions bear by two male spathes flowers, of 5–10while cm footstalks in length from [13] the (Figure main1 A).trunk The bear central female and flowers peripheral (generally regions round bear malein shape). flowers, The whiledistinction footstalks between from the the flowers main trunk can be bear made female based flowers on surface (generally characteristics: round in shape).female Theflowers distinction are generally between large the flowerswith a rough can be surface, made based whereas on surface male characteristics:flowers are small female with flowers a smooth are generallysurface (Figure large with 1A). a rough surface, whereas male flowers are small with a smooth surface (Figure1A). Figure 1. ((A)) Artocarpus heterophyllus Lam. flowers; flowers; ( B)) tree tree of Artocarpus lakoocha Roxb. with with flowers; flowers; (C) upside view of Artocarpus lakoocha Roxb. flower;flower; (D) cut-outcut‐out section of Artocarpus lakoocha flower.flower. Artocarpus lakoocha Roxb. ( AL) is another important species of Artocarpus. It is commonly known as “lakuchi” in India, “lokhat” in Thailand, and “tampang” in Malaysia. The The tree tree of AL is mostly known for itsits woodwood and and edible edible fruits fruits due due to to its its excellent excellent nutraceutical nutraceutical properties properties [14 [14].]. In In the the foothills foothills of theof the Himalayas Himalayas in Nepal, in Nepal, the leavesthe leaves and flowersand flowers of this of tree this also tree act also as freshact as fodder fresh forfodder lactating for lactating animals dueanimals to its due excellent to its excellent source of source bioactive of bioactive compounds compounds [15–17]. Traditionally,[15–17]. Traditionally, it is also taken it is also as medicine taken as formedicine people for su ffpeopleering fromsuffering liver-related from liver diseases‐related [18 diseases]. The edible [18]. The fruits edible and flowersfruits and of ALflowersare consumed of AL are asconsumed vegetables, as vegetables, pickles, and pickles, chutney and duechutney to its due astringent to its astringent and acidic and flavoracidic flavor [14]. The[14]. extractThe extract and bioactiveand bioactive compounds compounds from from the bark, the leaves,bark, leaves, seeds, seeds, and pericarp and pericarp of AL fruit of AL have fruit been have shown been toshown possess to exceptionalpossess exceptional phytochemical, phytochemical, nutritional, nutritional, and valuable and valuable pharmacological pharmacological properties properties [16,19 [16,19–21].–21]. This fruitThis isfruit capable is capable of offering of offering numerous numerous inhibitory inhibitory factors suchfactors as antibacterial,such as antibacterial, antitubercular, antitubercular, antiviral, antifungal,antiviral, antifungal, antiplatelet, antiplatelet, antiarthritic, tyrosinaseantiarthritic, inhibitory, tyrosinase cytotoxicity, inhibitory, and Hcytotoxicity,2O2 scavenging and activity, H2O2 asscavenging well as exceptional activity, as activities well as exceptional against herpes activities simplex against virus herpes (HSV) simplex and human virus immunodeficiency(HSV) and human virusimmunodeficiency (HIV) [1,22–27 virus]. The (HIV) flowering [1,22–27]. pattern The flowering of AL is similar pattern to ofAH AL, whereis similar both to male AH, where and female both flowersmale and appear female on flowers the same appear tree. on The the flowers same tree. are generallyThe flowers irregularly are generally round irregularly with a yellow round velvety with a surface.yellow velvety The male surface. flowers The are male orange-yellow, flowers are while orange female‐yellow, flowers while are female reddish flowers [28] (Figure are reddish1B–D). [28] (FigureIn general,1B–D). in both the studied species, the male flowers appear first, and the female flowers come out afterIn general, and are in immediately both the studied fertilized. species, In order the male not toflowers have the appear interference first, and of the pollination, female flowers in this work,come out it was after decided and are to immediately use only male fertilized. flowers. In order not to have the interference of pollination, in this work,Most ofit was the studiesdecided on to thisuse subjectonly male have flowers. explored the ripe fruit of both Artocarpus lakoocha Roxb. and ArtocarpusMost of the heterophyllus studies on Lam.this subject [1,19]. have However, explored scant the attention ripe fruit has of been both paid Artocarpus to the flowers lakoocha of Roxb. these plants.and Artocarpus As is known, heterophyllus the flowers Lam. can [1,19]. contain However, many secondary scant attention metabolites has been with paid high to antioxidant the flowers and of antimicrobialthese plants. As activities is known, [29