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Recent Insights Into Anthocyanin Pigmentation, Synthesis, Trafficking biomolecules Review Recent Insights into Anthocyanin Pigmentation, Synthesis, Trafficking, and Regulatory Mechanisms in Rice (Oryza sativa L.) Caryopsis Enerand Mackon 1, Guibeline Charlie Jeazet Dongho Epse Mackon 1, Yafei Ma 1, Muhammad Haneef Kashif 2, Niyaz Ali 3, Babar Usman 1 and Piqing Liu 1,* 1 State Key Laboratory of Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, Guangxi University, Nanning 530005, China; [email protected] (E.M.); [email protected] (G.C.J.D.E.M.); [email protected] (Y.M.); [email protected] (B.U.) 2 Key Laboratory of Plant Genetics and Breeding, College of Agriculture, Guangxi University, Nanning 530005, China; [email protected] 3 State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bio-Resources, College of Life Science and Technology, Guangxi University, Nanning 530004, China; [email protected] * Correspondence: [email protected]; Tel.: +86-133-9770-0471 Abstract: Anthocyanins are antioxidants used as natural colorants and are beneficial to human health. Anthocyanins contribute to reactive oxygen species detoxification and sustain plant growth and development under different environmental stresses. They are phenolic compounds that are broadly distributed in nature and are responsible for a wide range of attractive coloration in many plant Citation: Mackon, E.; Jeazet Dongho organs. Anthocyanins are found in various parts of plants such as flowers, leaves, stems, shoots, and Epse Mackon, G.C.; Ma, Y.; Haneef grains. Considering their nutritional and health attributes, anthocyanin-enriched rice or pigmented Kashif, M.; Ali, N.; Usman, B.; Liu, P. rice cultivars are a possible alternative to reduce malnutrition around the globe. Anthocyanin Recent Insights into Anthocyanin biosynthesis and storage in rice are complex processes in which several structural and regulatory Pigmentation, Synthesis, Trafficking, genes are involved. In recent years, significant progress has been achieved in the molecular and and Regulatory Mechanisms in Rice (Oryza sativa L.) Caryopsis. genetic mechanism of anthocyanins, and their synthesis is of great interest to researchers and the Biomolecules 2021, 11, 394. https:// scientific community. However, limited studies have reported anthocyanin synthesis, transportation, doi.org/10.3390/biom11030394 and environmental conditions that can hinder anthocyanin production in rice. Rice is a staple food around the globe, and further research on anthocyanin in rice warrants more attention. In this Academic Editors: review, metabolic and pre-biotic activities, the underlying transportation, and storage mechanisms of Roque Bru-Martinez and anthocyanins in rice are discussed in detail. This review provides potential information for the food Carmen Socaciu industry and clues for rice breeding and genetic engineering of rice. Received: 20 December 2020 Keywords: antioxidant; anthocyanin; cyanidin-3-glucoside; black rice; transcription factor; antho- Accepted: 1 March 2021 cyanin vacuolar intrusion; transporters; MBW complex Published: 7 March 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- iations. Anthocyanins are water-soluble plant pigments, responsible for a wide range of at- tractive colors in leaves, fruits, grains, and flowers [1], with most colors being red, blue, purple, and dark purple [2]. They belong to the group of phenolic compounds derived from flavonoids which play an important biological role in plants [3]. The pigments are glycosylated (aglycone), methylated or acylated forms of anthocyanidin [4,5]. Thus far, four Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. putative functions of anthocyanins have been reported: (1) reactive oxygen species (ROS) This article is an open access article mediators, (2) strong antioxidants, (3) chelating agents for metalloids and metals, and distributed under the terms and (4) sunscreen and promoter of leaf turgor, mainly during nutrient shortage [6]. Some scien- conditions of the Creative Commons tific studies such as animal models and human clinical trials revealed that anthocyanins Attribution (CC BY) license (https:// have potential antioxidant and antimicrobial properties, improve visual and neurological creativecommons.org/licenses/by/ health, and protect against various non-communicable diseases [5]. Consequently, they 4.0/). are considered health-promoting compounds [7] and may play a fundamental role in Biomolecules 2021, 11, 394. https://doi.org/10.3390/biom11030394 https://www.mdpi.com/journal/biomolecules Biomolecules 2021, 11, x FOR PEER REVIEW 2 of 26 (http://creativecommons.org/li- anins have potential antioxidant and antimicrobial properties, improve visual and neuro- censes/by/4.0/). logical health, and protect against various non-communicable diseases [5]. Consequently, Biomolecules 2021, 11, 394 2 of 25 they are considered health-promoting compounds [7] and may play a fundamental role in preventing several human diseases. Other supporting studies elucidated that anthocy- anins are effective in supporting glucose homeostasis [8] in the treatment of cardiovascu- preventing several human diseases. Other supporting studies elucidated that anthocyanins lar diseases and diabetes [9,10], hyperlipidemia and insulin resistance in fructose-fed rats are effective in supporting glucose homeostasis [8] in the treatment of cardiovascular dis- [11],eases and and cancer diabetes and [9, 10tumors], hyperlipidemia [2,12–14]. Further and insulin studies resistance reported in fructose-fed that anthocyanins rats [11], can re- duceand cancerthe levels and tumorsof serum [2,12 creatinine,–14]. Further blood studies urea reported nitrogen that (BUN), anthocyanins renal canxanthine reduce oxidase (XOD),the levels malondialdehyde of serum creatinine, (MDA), blood ureaand nitrogennitric oxide (BUN), (NO) renal [15], xanthine Additionally, oxidase (XOD), they have a positivemalondialdehyde effect in anti-carcinogenic (MDA), and nitric oxideand anti-inflammation (NO) [15], Additionally, responses they have [7,16]. a positive Having these medicinaleffect in anti-carcinogenic properties, anthocyanins and anti-inflammation are often used responses as alternatives [7,16]. Having for thesefood medicinalcolorants as well asproperties, bioactive anthocyanins components are in often nutraceutical used as alternatives and traditional for food medicine colorants [17]. as well Under as bioac- biotic and abiotictive components stress exposure, in nutraceutical anthocyanins and traditional sustain plant medicine growth [17]. and Under development biotic and abiotic as they indi- rectlystress protect exposure, leaves anthocyanins from damage sustain and plant main growthtain normal and development photosynthetic as they activity indirectly [18–20]. protect leaves from damage and maintain normal photosynthetic activity [18–20]. Anthocyanins have been found in different rice plant parts and most interestingly in Anthocyanins have been found in different rice plant parts and most interestingly in thethe rice rice caryopsis, which which leads leads to attractiveto attractive coloration coloration [21]. [21]. The colors The colors of the riceof the caryopsis rice caryopsis rangerange between brown, brown, red, red, purple, purple, and and black black due to due the to varying the varying composition composition and concentra- and concen- trationtion of pigmentsof pigments [22– 24[22–24].]. The different The different combinations combinations of anthocyanin of anthocyanin and proanthocyanidin and proanthocya- nidinare responsible are responsible for the for color the differentiation color differentiat (Tableion1). (Table The higher 1). The the higher total anthocyanin the total anthocya- nincontent content (TAC) (TAC) in the in ricethe bran,rice bran, the blacker the blacker the rice the bran riceappears; bran appears; on the on contrary, the contrary, the the higherhigher the the amount amount of total proanthocyanidin (TPC), (TPC), the the redder redder the the rice rice bran bran appears. appears. The pigmentationThe pigmentation increases increases as the as therice ricecaryopsis caryopsis develops, develops, and and changes changes are are observed observed at at different different developmental stages, either in the rice caryopsis or in the extracted pigment developmental stages, either in the rice caryopsis or in the extracted pigment between plants between plants accumulating anthocyanin and proanthocyanin and in non-pigmented rice accumulating(Figure1). anthocyanin and proanthocyanin and in non-pigmented rice (Figure 1). Figure 1. The pigment gradient in black rice compared to brown and red rice caryopses during Figuredevelopmental 1. The pigment stages. Note: gradient This figure in black was rice drawn compared and adapted to brown based onand the red experiment rice caryopses conducted during developmentalby Jiamyangyuen stages. et al., 2017.Note: This figure was drawn and adapted based on the experiment con- ducted by Jiamyangyuen et al., 2017. The type of anthocyanin detected in black rice caryopses varies depending on the cultivarThe and type the of extraction anthocyanin method detected (Table2 in). Someblack methodsrice caryopses can detect varies both depending major and on the cultivarminor anthocyanins. and the extraction High-performance method (Table liquid 2). chromatography Some methods (HPLC) can detect with ultraviolet- both major and visible
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