Improve Anthocyanin and Zinc Concentration in Purple Rice by Nitrogen and Zinc Fertilizer Application

doi:10.1016/j.rsci.2022.07.004

Abstract

Abstract:

Zinc (Zn) is an essential micronutrient for plant growth and development, and anthocyanin is a secondary metabolite compound generally produced under stress conditions; both have benefits to human health. Rice is a staple food crop for most of the world’s population, and purple rice is well known as a natural source of Zn and anthocyanins, but their stability depends upon many factors. This review focuses on the opportunity to increase Zn and anthocyanin compounds in purple rice grains via Zn and nitrogen (N) management during cultivation. Variation in grain Zn concentration and anthocyanin compounds is found among purple rice varieties, thus presenting a challenge for breeding programs aiming at high grain Zn and anthocyanin contents. Genetic engineering has successfully achieved a high-efficiency vector system comprising two regulatory genes and six structural anthocyanin-related genes driven by endosperm-specific promoters to engineer purple endosperm rice that can provide new high-anthocyanin varieties. Grain Zn and anthocyanin concentrations in rice can also be affected by environmental factors during cultivation, e.g., light, temperature, soil salinity and nutrient (fertilizer) management. Applying N and Zn fertilizer is found to influence the physiological mechanisms of Zn absorption, uptake, transport and remobilization to promote grain Zn accumulation in rice, while N application can improve anthocyanin synthesis by promoting its biosynthesis pathway via the use of phenylalanine as a precursor. In summary, there is an opportunity to improve both grain Zn and anthocyanin in purple rice by appropriate management of Zn and N fertilizers during cultivation for specific varieties.

Key words: purple rice, anthocyanin, secondary metabolite, zinc deficiency, fertilizer

Suchila Utasee, Sansanee Jamjod, Sittisavet Lordkaew, Chanakan Prom-U-Thai. Improve Anthocyanin and Zinc Concentration in Purple Rice by Nitrogen and Zinc Fertilizer Application[J]. Rice Science, 2022, 29(5): 435-450.

Figures/Tables 5

Table 1. Range of zinc (Zn) concentration in non-colored rice grains from different germplasms.

Germplasm source	No. of rice varieties	Zn concentration (mg/kg)	Reference
IRRI	939	13.5-58.4	Welch and Graham, 1999
Thailand	127	17.0-59.0	Saenchai et al, 2012; Jaksomsak et al, 2015; Jamjod et al, 2017; Jaksomsak et al, 2021; Fongfon et al, 2021b
Lao, PDR	49	15.2-24.1	Xiongsiyee et al, 2018
India	159	14.5-35.3	Maganti et al, 2020

Fig. 1. Flavonoid biosynthesis in plant. PAL, Phenylalanine ammonia lyase; C4H, Cinnamic acid 4-hydroxylase; 4CL, 4-Coumaric acid:coenzyme A ligase; CHS, Chalcone synthase; CHI, Chalcone isomerase; FNS, Flavone synthase; F3H, Flavanone 3- hydroxylase; FLS, Flavonol synthesis; DFR, Dihydroflavonol 4-reductase; ANS, Anthocyanin synthase; UFGT, UDP-glucose:flavonoid-3-O- glucosyltransferase.

Fig. 2. Characteristics of rice plants and grains of color rice and non-pericarp color rice. A, Grains of color rice and non-pericarp color rice. From left to right are purple color (Kum Doi Saket), red color (Hom Mali Deang), unpolished and polished rice (Khao Dowk Mali 105). B, Plants of color rice (left) and non-pericarp color rice (right). C, Grains of two purple rice varieties.

Table 2. Anthocyanin (cyanidin-3-O-glucoside) concentration in bran fraction and unpolished rice among purple rice varieties from different germplasms.

Germplasm	No. of varieties		Reference
Bran fraction ^a (mg/g)
USA	25	0.7-17.3	Chen et al, 2017
Thailand	11	0-6.5	Wisetkomolmat et al, 2022
Unpolished rice ^b (mg/g)
Thailand, China and Sri Lanka	12	0.194-1.408	Yodmanee et al, 2011
China	15	0-6.500	Chen et al, 2012; Xia et al, 2021
Thailand	25	0.025-4.000	Yodmanee et al, 2011; Somsana et al, 2013; Jaksomsak et al, 2021
Lao, PDR	9	0-2.200	Xiongsiyee et al, 2018
Indonesia	18	0.112-1.032	Fitri et al, 2021
Korea	6	0-6.456	Islam et al, 2022

Fig. 3. Diagram of purple rice with high grain Zn and anthocyanin concentrations.

References 147

[1]	Aboutalebian M A, Ekbatani G Z, Sepehri A. 2012. Effects of on-farm seed priming with zinc sulfate and urea solutions on emergence properties, yield and yield components of three rainfed wheat cultivars. Ann Biolog Res, 3(10): 4790-4796.
[2]	Ahuja U, Ahuja S, Chaudhary N, Thakrar R. 2007. Red rices: Past, present and future. Asian Agri-History, 11(4): 291-304.
[3]	Akhter D, Qin R, Nath U K, Eshag J, Jin X L, Shi C H. 2019. A rice gene, OsPL, encoding a MYB family transcription factor confers anthocyanin synthesis, heat stress response and hormonal signaling. Gene, 699: 62-72.
[4]	Alloway B J. 2008. Micronutrients and crop production: An introduction. In: Alloway B J. Micronutrient Deficiencies in Global Crop Production. Springer: 1-39.
[5]	Amarowicz R, Cwalina-Ambroziak B, Janiak M A, Bogucka B. 2020. Effect of N fertilization on the content of phenolic compounds in Jerusalem artichoke (Helianthus tuberosus L.) tubers and their antioxidant capacity. Agronomy, 10(8): 1215.
[6]	Anami B S, Malvade N N, Palaiah S. 2020. Classification of yield affecting biotic and abiotic paddy crop stresses using field images. Inf Process Agric, 7(2): 272-285.
[7]	Andreini C, Banci L, Bertini I, Rosato A. 2006. Counting the zinc- proteins encoded in the human genome. J Proteome Res, 5(1): 196-201. PMID
[8]	Appa Rao S, Schiller J, Bounphanousay C, Jackson M. 2006. Diversity within the traditional rice varieties of Laos. In: Schiller J M, Chanphengxay M B, Linguist B, Appa Rao S. Rice in Laos. In: Schiller J M, Chanphengxay M B, Linguist B, Appa Rao S. Rice in Laos. Los Banos, the Philippine: International Rice Research Institute: 123-140.
[9]	Asadi E, Ghehsareh A M, Moghadam E G, Hoodaji M, Zabihi H R. 2019. Improvement of pomegranate colorless arils using iron and zinc fertilization. J Clean Prod, 234: 392-399.
[10]	Azuma A. 2018. Genetic and environmental impacts on the biosynthesis of anthocyanins in grapes. Horticult J, 87(1): 1-17.
[11]	Bana R C, Gupta A K, Bana R S, Shivay Y S, Bamboriya S D, Thakur N P, Puniya R, Gupta M, Jakhar S R, Kailash, Choudhary R S, Bochalya R S, Bajaya T, Kumar V, Kumar P, Choudhary A K. 2022. Zinc-coated urea for enhanced zinc biofortification, nitrogen use efficiency and yield of basmati rice under typic fluvents. Sustainability, 14(1): 104.
[12]	Bhat F M, Sommano S R, Riar C S, Seesuriyachan P, Chaiyaso T, Prom-U-Thai C. 2020. Status of bioactive compounds from bran of pigmented traditional rice varieties and their scope in production of medicinal food with nutraceutical importance. Agronomy, 10(11): 1817.
[13]	Boonchuay P, Cakmak I, Rerkasem B, Prom-U-Thai C. 2013. Effect of different foliar zinc application at different growth stages on seed zinc concentration and its impact on seedling vigor in rice. Soil Sci Plant Nutr, 59(2): 180-188.
[14]	Bouis H E, Saltzman A. 2017. Improving nutrition through biofortification: A review of evidence from HarvestPlus, 2003 through 2016. Glob Food Secur, 12: 49-58.
[15]	Broadley M R, White P J, Hammond J P, Zelko I, Lux A. 2007. Zinc in plants. New Phytol, 173(4): 677-702. PMID
[16]	Cakmak I, Pfeiffer W H, McClafferty B. 2010. REVIEW: Biofortification of durum wheat with zinc and iron. Cereal Chem J, 87(1): 10-20.
[17]	Castillo-González J, Ojeda-Barrios D, Hernández-Rodríguez A, González-Franco A C, Robles-Hernández L, López-Ochoa G R. 2018. Zinc metalloenzymes in plants. Interciencia, 43(4): 242-248.
[18]	Chan L K, Koay S S, Boey P L, Bhatt A. 2010. Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Biol Res, 43(1): 127-135. PMID
[19]	Chariyakornkul A, Inboot N, Taya S, Wongpoomchai R. 2021. Low-polar extract from seed of Cleistocalyx nervosum var. paniala modulates initiation and promotion stages of chemically- induced carcinogenesis in rats. Biomed Pharmacother, 133: 110963.
[20]	Chasapis C T, Ntoupa P S A, Spiliopoulou C A, Stefanidou M E. 2020. Recent aspects of the effects of zinc on human health. Arch Toxicol, 94(5): 1443-1460. PMID
[21]	Chattha M U, Hassan M U, Khan I, Chattha M B, Mahmood A, Chattha M U, Nawaz M, Subhani M N, Kharal M, Khan S. 2017. Biofortification of wheat cultivars to combat zinc deficiency. Front Plant Sci, 8: 281. PMID
[22]	Chen M D, Song Y M, Lin P Y. 2000. Zinc effects on hyperglycemia and hypoleptinemia in streptozotocin-induced diabetic mice. Horm Metab Res, 32(3): 107-109. PMID
[23]	Chen X L, Xue X Z, Guo W Z, Wang L C, Qiao X J. 2016. Growth and nutritional properties of lettuce affected by mixed irradiation of white and supplemental light provided by light-emitting diode. Sci Hortic, 200: 111-118.
[24]	Chen X L, Yang Q C, Song W P, Wang L C, Guo W Z, Xue X Z. 2017. Growth and nutritional properties of lettuce affected by different alternating intervals of red and blue LED irradiation. Sci Hortic, 223: 44-52.
[25]	Chen X Q, Nagao N, Itani T, Irifune K. 2012. Anti-oxidative analysis, and identification and quantification of anthocyanin pigments in different coloured rice. Food Chem, 135(4): 2783-2788. PMID
[26]	Choi S, Liu X, Pan Z. 2018. Zinc deficiency and cellular oxidative stress: Prognostic implications in cardiovascular diseases. Acta Pharmacol Sin, 39(7): 1120-1132. PMID
[27]	Chunthaburee S, Sakuanrungsirikul S, Wongwarat T, Sanitchon J, Pattanagul W, Theerakulpisut P. 2016. Changes in anthocyanin content and expression of anthocyanin synthesis genes in seedlings of black glutinous rice in response to salt stress. Asian J Plant Sci, 15: 56-65.
[28]	Coni P, Pichiri G, Lachowicz J I, Ravarino A, Ledda F, Fanni D, Gerosa C, Piras M, Coghe F, Gibo Y, Cau F, Castagnola M, van Eyken P, Saba L, Piludu M, Faa G. 2021. Zinc as a drug for Wilson’s disease, non-alcoholic liver disease and COVID-19-related liver injury. Molecules, 26(21): 6614.
[29]	Daiponmak W, Theerakulpisut P, Thanonkao P, Vanavichit A, Prathepha P. 2010. Changes of anthocyanin cyanidin-3-glucoside content and antioxidant activity in Thai rice varieties under salinity stress. ScienceAsia, 36(4): 286-291.
[30]	Das S, Jahiruddin M, Islam M R, Mahmud A A, Hossain A, Laing A M. 2020. Zinc biofortiﬁcation in the grains of two wheat (Triticum aestivum L.) varieties through fertilization. Acta Agrobot, 73(1): 7312.
[31]	Bake A, Brouwer I D, Giller K E. 2017. Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa. Glob Food Secur, 12: 8-14.
[32]	Deng G F, Xu X R, Zhang Y, Li D, Gan R Y, Li H B. 2013. Phenolic compounds and bioactivities of pigmented rice. Crit Rev Food Sci Nutr, 53(3): 296-306.
[33]	Duncan E G, O’Sullivan C A, Roper M M, Palta J, Whisson K, Peoples M B. 2018. Yield and nitrogen use efficiency of wheat increased with root length and biomass due to nitrogen, phosphorus, and potassium interactions. J Plant Nutr Soil Sci, 181(3): 364-373.
[34]	Enaru B, Drețcanu G, Pop T D, Stǎnilǎ A, Diaconeasa Z. 2021. Anthocyanins: Factors affecting their stability and degradation. Antioxidants, 10(12): 1967.
[35]	Erenoglu E B, Kutman U B, Ceylan Y, Yildiz B, Cakmak I. 2011. Improved nitrogen nutrition enhances root uptake, root-to-shoot translocation and remobilization of zinc (⁶⁵Zn) in wheat. New Phytol, 189(2): 438-448. PMID
[36]	Farooq M, Ullah A, Rehman A, Nawaz A, Nadeem A, Wakeel A, Nadeem F, Siddique K H M. 2018. Application of zinc improves the productivity and biofortification of fine grain aromatic rice grown in dry seeded and puddled transplanted production systems. Field Crops Res, 216: 53-62.
[37]	Feng L J, Ou W W, Yang Y B, Qi Y, Qi Z, Zhang J L. 2022. Black rice anthocyanins alleviate hyperuricemia in mice: Possible inhibitory effects on xanthine oxidase activity by cyanidin 3-O-glucoside. J Cereal Sci, 104: 103406.
[38]	Fitri I G S, Nurhasanah , Handoyo T. 2021. Genetic and phytochemical analysis of Indonesian black rice cultivars. J Crop Sci Biotechnol, 24(5): 567-578.
[39]	Fongfon S, Prom-U-Thai C, Pusadee T, Jamjod S. 2021a. Responses of purple rice genotypes to nitrogen and zinc fertilizer application on grain yield, nitrogen, zinc, and anthocyanin concentration. Plants, 10(8): 1717.
[40]	Fongfon S, Pusadee T, Prom-U-Thai C, Rerkasem B, Jamjod S. 2021b. Diversity of purple rice (Oryza sativa L.) landraces in northern Thailand. Agronomy, 11(10): 2029.
[41]	Frías-Moreno M N, Espino-Díaz M, Dávila-Aviña J, Gonzalez- Aguilar G A, Ayala-Zavala J F, Molina-Corral F J, Parra-Quezada R A, Orozco G I O. 2020. Preharvest nitrogen application affects quality and antioxidant status of two tomato cultivars. Bragantia, 79(1): 134-144.
[42]	Gammoh N Z, Rink L. 2017. Zinc in infection and inflammation. Nutrients, 9(6): 624.
[43]	Giorgi A, Mingozzi M, Madeo M, Speranza G, Cocucci M. 2009. Effect of nitrogen starvation on the phenolic metabolism and antioxidant properties of yarrow (Achillea collina Becker ex Rchb.). Food Chem, 114(1): 204-211.
[44]	Gould K S. 2004. Nature’s Swiss army knife: The diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol, 2004(5): 314-320.
[45]	Guillén-Román C J, Guevara-González R G, Rocha-Guzmán N E, Mercado-Luna A, Pérez-Pérez M C I. 2018. Effect of nitrogen privation on the phenolics contents, antioxidant and antibacterial activities in Moringa oleifera leaves. Ind Crops Prod, 114: 45-51.
[46]	Harding K L, Aguayo V M, Masters W A, Webb P. 2018. Education and micronutrient deficiencies: An ecological study exploring interactions between women’s schooling and children’s micronutrient status. BMC Public Health, 18(1): 470.
[47]	Hossain A, Mottaleb K A, Farhad M, Barma N C D. 2019. Mitigating the twin problems of malnutrition and wheat blast by one wheat variety, ‘BARI Gom 33’ in Bangladesh. Acta Agrobot, 72(2): 1775.
[48]	Hu C, Zawistowski J, Ling W H, Kitts D D. 2003. Black rice (Oryza sativa L. indica) pigmented fraction suppresses both reactive oxygen species and nitric oxide in chemical and biological model systems. J Agric Food Chem, 51(18): 5271-5277.
[49]	Huang D, Yuan Y, Tang Z Z, Huang Y, Kang C Y, Deng X X, Xu Q. 2019. Retrotransposon promoter of Ruby1 controls both light- and cold-induced accumulation of anthocyanins in blood orange. Plant Cell Environ, 42(11): 3092-3104.
[50]	Insuan O, Chariyakornkul A, Rungrote Y, Wongpoomchai R. 2017. Antimutagenic and antioxidant activities of Thai rice brans. J Cancer Prev, 22(2): 89-97. PMID
[51]	Islam M Z, Shim M J, Jeong S Y, Lee Y T. 2022. Effects of soaking and sprouting on bioactive compounds of black and red pigmented rice cultivars. Int J Food Sci Technol, 57(1): 201-209.
[52]	Jaksomsak P, Yimyam N, Dell B, Prom-U-Thai C, Rerkasem B. 2015. Variation of seed zinc in a local upland rice germplasm from Thailand. Plant Genet Resour, 13(2): 168-175.
[53]	Jaksomsak P, Rerkasem B, Prom-U-Thai C. 2021. Variation in nutritional quality of pigmented rice varieties under different water regimes. Plant Prod Sci, 24(2): 244-255.
[54]	Jamjod S, Yimyam N, Lordkaew S, Prom-U-Thai C, Rerkasem B. 2017. Characterization of on-farm rice germplasm in an area of the crop’s center of diversity. CMUJ Nat Sci, 16(2): 85-98.
[55]	Jeng T L, Lai C C, Ho P T, Shih Y J, Sung J M. 2012. Agronomic, molecular and antioxidative characterization of red- and purple- pericarp rice (Oryza sativa L.) mutants in Taiwan. J Cereal Sci, 56(2): 425-431.
[56]	Ji C C, Li J L, Jiang C C, Zhang L, Shi L, Xu F S, Cai H M. 2021. Zinc and nitrogen synergistic act on root-to-shoot translocation and preferential distribution in rice. J Adv Res, 35: 187-198.
[57]	Jiang M M, Liu Y, Ren L, Lian H L, Chen H Y. 2016. Molecular cloning and characterization of anthocyanin biosynthesis genes in eggplant (Solanum melongena L.). Acta Physiol Plant, 38(7): 1-13.
[58]	Kashif M H, Tang D F, Li Z Q, Wei F, Liang Z C, Chen P. 2020a. Comparative cytological and gene expression analysis reveals potential metabolic pathways and target genes responsive to salt stress in kenaf (Hibiscus cannabinus L.). J Plant Growth Regul, 39(3): 1245-1260.
[59]	Kashif M H, Wei F, Tang D F, Tang M Q, Luo D J, Hai L, Li R, Chen P. 2020b. iTRAQ-based comparative proteomic response analysis reveals regulatory pathways and divergent protein targets associated with salt-stress tolerance in kenaf (Hibiscus cannabinus L.). Ind Crops Prod, 153: 112566.
[60]	Kawahigashi H, Hirose S, Iwai T, Ohashi Y, Sakamoto W, Maekawa M, Ohkawa Y. 2007. Chemically induced expression of rice OSB2 under the control of the OsPR1.1 promoter confers increased anthocyanin accumulation in transgenic rice. J Agric Food Chem, 55(4): 1241-1247.
[61]	Khampuang K, Rerkasem B, Lordkaew S, Prom-U-Thai C. 2021. Nitrogen fertilizer increases grain zinc along with yield in high yield rice varieties initially low in grain zinc concentration. Plant Soil, 467: 239-252.
[62]	Khan M U, Qasim M, Khan I. 2007. Effect of Zn fertilizer on rice grown in different soils of Dera Ismail Khan. Sarhad J Agric, 23(4): 1033-1040.
[63]	Khantarate S, Theanjumpol P, Krittigamas N, Suriyong S. 2022. Effect of heat treatment on starch granule structure and nutrient content of germinated purple rice. Food Sci Technol, 42: e63820.
[64]	Kim B G, Kim J H, Min S Y, Shin K H, Kim J H, Kim H Y, Ryu S N, Ahn J H. 2007. Anthocyanin content in rice is related to expression levels of anthocyanin biosynthetic genes. J Plant Biol, 50(2): 156-160.
[65]	Kováčik J, Bačkor M. 2007. Changes of phenolic metabolism and oxidative status in nitrogen-deficient Matricaria chamomilla plants. Plant Soil, 297(1-2): 255-265.
[66]	Krishnan V, Rani R, Awana M, Pitale D, Kulshreshta A, Sharma S, Bollinedi H, Singh A, Singh B, Singh A K, Praveen S. 2021. Role of nutraceutical starch and proanthocyanidins of pigmented rice in regulating hyperglycemia: Enzyme inhibition, enhanced glucose uptake and hepatic glucose homeostasis using in vitro model. Food Chem, 335: 127505.
[67]	Kushwaha U K S. 2016. Black rice anthocyanin content increases with increase in altitude of its plantation. Adv Plants Agric Res, 5(1): 469-472.
[68]	Kutman U B, Yildiz B, Cakmak I. 2011. Improved nitrogen status enhances zinc and iron concentrations both in the whole grain and the endosperm fraction of wheat. J Cereal Sci, 53(1): 118-125.
[69]	Leach K A, Hameleers A. 2001. The effects of a foliar spray containing phosphorus and zinc on the development, composition and yield of forage maize. Grass Forage Sci, 56(3): 311-315.
[70]	Li M, Yang X W, Tian X H, Wang S X, Chen Y L. 2014. Effect of nitrogen fertilizer and foliar zinc application at different growth stages on zinc translocation and utilization efficiency in winter wheat. Cereal Res Commun, 42(1): 81-90.
[71]	Li X Y, Zhou Y Z, Zhang J R. 2021. Status and associated human health risk of zinc accumulation in agricultural soils across China. Process Saf Environ Prot, 146: 867-876.
[72]	Ling Q L, Feng Y X, Lu C J, Lin Y J, Yu X Z. 2021. Genetic variation and gene expression of anthocyanin synthesis and transport related enzymes in Oryza sativa against thiocyanate. Plant Physiol Biochem, 160: 18-26.
[73]	Liu J, Yang M Y, Li H, Li D P, Shi X J, Zhang Y Q. 2017. Genetic processes of iron and zinc accumulation in edible portion of crops and their agro-biofortiﬁcation: A review. Am J Agric Forest, 5(3): 65-72.
[74]	Liu X W, Wang H Y, Zhou J M, Hu F Q, Zhu D J, Chen Z M, Liu Y Z. 2016. Effect of N fertilization pattern on rice yield, N use efficiency and fertilizer-N fate in the Yangtze River Basin, China. PLoS One, 11(11): e0166002.
[75]	Liu Z, Gao J, Gao F, Dong S T, Liu P, Zhao B, Zhang J W. 2018. Integrated agronomic practices management improve yield and nitrogen balance in double cropping of winter wheat-summer maize. Field Crops Res, 221: 196-206.
[76]	Lo Piccolo E, Landi M, Massai R, Remorini D, Guidi L. 2020. Girled-induced anthocyanin accumulation in red-leafed Prunus cerasifera: Effect on photosynthesis, photoprotection and sugar metabolism. Plant Sci, 294: 110456.
[77]	Luna-Vital D, Cortez R, Ongkowijoyo P, de Mejia E G. 2018. Protection of color and chemical degradation of anthocyanin from purple corn (Zea mays L.) by zinc ions and alginate through chemical interaction in a beverage model. Food Res Int, 105: 169-177. PMID
[78]	Mackon E, Jeazet Dongho Epse Mackon G C, Ma Y F, Haneef Kashif M, Ali N, Usman B, Liu P Q. 2021. Recent insights into anthocyanin pigmentation, synthesis, trafficking, and regulatory mechanisms in rice (Oryza sativa L.) caryopsis. Biomolecules, 11(3): 394.
[79]	Maganti S, Swaminathan R, Parida A. 2020. Variation in iron and zinc content in traditional rice genotypes. Agric Res, 9(3): 316-328.
[80]	Maret W. 2012. New perspectives of zinc coordination environments in proteins. J Inorg Biochem, 111: 110-116. PMID
[81]	Marles R J. 2017. Mineral nutrient composition of vegetables, fruits and grains: The context of reports of apparent historical declines. J Food Compos Anal, 56: 93-103.
[82]	Marschner H, Marschner P. 2012. Marschner’s Mineral Nutrition of Higher Plants. 3rd edn. San Diego, USA: Elsevier Academic Press: 1-651.
[83]	Mengel K, Kirkby E A, Kosegarten H, Appel T. 2001. Nitrogen: Principles of Plant Nutrition. Dordrecht, the Netherlands: Springer: 397-434.
[84]	Michalska A, Wojdyło A, Bogucka B. 2016. The influence of nitrogen and potassium fertilisation on the content of polyphenolic compounds and antioxidant capacity of coloured potato. J Food Compos Anal, 47: 69-75.
[85]	Min B, Chen M H, Green B W. 2009. Antioxidant activities of purple rice bran extract and its effect on the quality of low-NaCl, phosphate-free patties made from channel catfish (Ictalurus punctatus) belly flap meat. J Food Sci, 74(3): C268-C277.
[86]	Mousavi S R, Galavi M, Ahmadvand G. 2007. Effect of zinc and manganese foliar application on yield, quality and enrichment on potato (Solanum tuberosum L.). Asian J Plant Sci, 6(8): 1256-1260.
[87]	Nadeem S M, Zahir Z A, Naveed M, Nawaz S. 2013. Mitigation of salinity-induced negative impact on the growth and yield of wheat by plant growth-promoting rhizobacteria in naturally saline conditions. Ann Microbiol, 63(1): 225-232.
[88]	Nahar K, Ali M M, Khanom A, Alam M K, Azad M A K, Rahman M M. 2020. Levels of heavy metal concentrations and their effect on net nitrification rates and nitrifying Archaea/bacteria in paddy soils of Bangladesh. Appl Soil Ecol, 156: 103697.
[89]	Natasha N, Shahid M, Bibi I, Iqbal J, Khalid S, Murtaza B, Bakhat H F, Farooq A B U, Amjad M, Hammad H M, Niazi N K, Arshad M. 2022. Zinc in soil-plant-human system: A data- analysis review. Sci Total Environ, 808: 152024.
[90]	Nguyen P M, Niemeyer E D. 2008. Effects of nitrogen fertilization on the phenolic composition and antioxidant properties of basil (Ocimum basilicum L.). J Agric Food Chem, 56(18): 8685-8691.
[91]	Nilnumkhum A, Punvittayagul C, Chariyakornkul A, Wongpoomchai R. 2017. Effects of hydrophilic compounds in purple rice husk on AFB1-induced mutagenesis. Mol Cell Toxicol, 13(2): 171-178.
[92]	Niu J P, Zhang G J, Zhang W T, Goltsev V, Sun S, Wang J Z, Li P M, Ma F W. 2017. Anthocyanin concentration depends on the counterbalance between its synthesis and degradation in plum fruit at high temperature. Sci Rep, 7(1): 7684. PMID
[93]	Oikawa T, Maeda H, Oguchi T, Yamaguchi T, Tanabe N, Ebana K, Yano M, Ebitani T, Izawa T. 2015. The birth of a black rice gene and its local spread by introgression. Plant Cell, 27(9): 2401-2414.
[94]	Palmer C M, Guerinot M L. 2009. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol, 5(5): 333-340. PMID
[95]	Palumbo M J, Putz F E, Talcott S T. 2007. Nitrogen fertilizer and gender effects on the secondary metabolism of yaupon, a caffeine- containing North American holly. Oecologia, 151(1): 1-9.
[96]	Pedas P, Schjoerring J K, Husted S. 2009. Identification and characterization of zinc-starvation-induced ZIP transporters from barley roots. Plant Physiol Biochem, 47(5): 377-383.
[97]	Pengkumsri N, Chaiyasut C, Saenjum C, Sirilun S, Peerajan S, Suwannalert P, Sirisattha S, Sivamaruthi B S. 2015. Physicochemical and antioxidative properties of black, brown and red rice varieties of northern Thailand. Food Sci Technol (Campinas), 35(2): 331-338.
[98]	Prom-U-Thai C, Sanchai C, Rerkasem B, Jamjod S, Fukai S, Godwin I D, Huang L. 2007. Effect of grain morphology on degree of milling and iron loss in rice. Cereal Chem J, 84(4): 384-388.
[99]	Prom-U-Thai C, Rashid A, Ram H, Zou C Q, Guilherme L R G, Corguinha A P B, Guo S W, Kaur C, Naeem A, Yamuangmorn S, Ashraf M Y, Sohu V S, Zhang Y Q, Martins F A D, Jumrus S, Tutus Y, Yazici M A, Cakmak I. 2020. Simultaneous biofortification of rice with zinc, iodine, iron and selenium through foliar treatment of a micronutrient cocktail in five countries. Front Plant Sci, 11: 589835.
[100]	Rao S, Schwarz L J, Santhakumar A B, Chinkwo K A, Blanchard C L. 2018. Cereal phenolic contents as affected by variety and environment. Cereal Chem, 95(5): 589-602.
[101]	Reddy C K, Kimi L, Haripriya S, Kang N. 2017. Effects of polishing on proximate composition, physico-chemical characteristics, mineral composition and antioxidant properties of pigmented rice. Rice Sci, 24(5): 241-252.
[102]	Rehman A, Farooq M. 2016. Zinc seed coating improves the growth, grain yield and grain biofortification of bread wheat. Acta Physiol Plant, 38(10): 1-10.
[103]	Rerkasem B, Jumrus S, Yimyam N, Prom-U-Thai C. 2015. Variation of grain nutritional quality among Thai purple rice genotypes grown at two different altitudes. ScienceAsia, 41(6): 377-385.
[104]	Roohani N, Hurrell R, Kelishadi R, Schulin R. 2013. Zinc and its importance for human health: An integrative review. J Res Med Sci, 18(2): 144-157. PMID
[105]	Rowan D D, Cao M S, Wang K L, Cooney J M, Jensen D J, Austin P T, Hunt M B, Norling C, Hellens R P, Schaffer R J, Allan A C. 2009. Environmental regulation of leaf colour in red 35S: PAP1 Arabidopsis thaliana. New Phytol, 182(1): 102-115.
[106]	Rubio-Wilhelmi M, Sanchez-Rodriguez E, Leyva R, Blasco B, Romero L, Blumwald E, Ruiz J M. 2012. Response of carbon and nitrogen-rich metabolites to nitrogen deficiency in PSARK: IPT tobacco plants. Plant Physiol Biochem, 57: 231-237.
[107]	Saenchai C, Prom-U-Thai C, Jamjod S, Dell B, Rerkasem B. 2012. Genotypic variation in milling depression of iron and zinc concentration in rice grain. Plant Soil, 361: 271-278.
[108]	Sakulsingharoj C, Inta P, Sukkasem R, Pongjaroenkit S, Chowpongpang S, Sangtong V. 2014. Overexpression of OSB2 gene in transgenic rice up-regulated expression of structural genes in anthocyanin biosynthesis pathway. Thai J Genet, 7(3): 173-182.
[109]	Sani N A, Sawei J, Ratnam W, Rahman Z A. 2018. Physical, antioxidant and antibacterial properties of rice (Oryza sativa L.) and glutinous rice (Oryza sativa var. Glutinosa) from local cultivators and markets of Peninsular, Malaysia. Int Food Res J, 25(6): 2328-2336.
[110]	Shaked-Sachray L, Weiss D, Reuveni M, Nissim-Levi A, Oren- Shamir M. 2002. Increased anthocyanin accumulation in Aster flowers at elevated temperatures due to magnesium treatment. Physiol Plant, 114(4): 559-565. PMID
[111]	Sinilal B, Ovadia R, Nissim-Levi A, Perl A, Carmeli-Weissberg M, Oren-Shamir M. 2011. Increased accumulation and decreased catabolism of anthocyanins in red grape cell suspension culture following magnesium treatment. Planta, 234(1): 61-71. PMID
[112]	Somsana P, Wattana P, Suriharn B, Sanitchon J. 2013. Stability and genotype by environment interactions for grain anthocyanin content of Thai black glutinous upland rice (Oryza sativa). Sabrao J Breed Genet, 45: 523-532.
[113]	Soubeyrand E, Basteau C, Hilbert G, van Leeuwen C, Delrot S, Gomès E. 2014. Nitrogen supply affects anthocyanin biosynthetic and regulatory genes in grapevine cv. Cabernet-Sauvignon berries. Phytochemistry, 103: 38-49. PMID
[114]	Štampar F, Bizjak J, Veberič R, Jakopič J. 2015. Foliar application of phosphorus improves apple fruit color during ripening. Acta Univ Agric Silvic Mendelianae Brun, 63(4): 1195-1200.
[115]	Stanton C, Sanders D, Krämer U, Podar D. 2021. Zinc in plants: Integrating homeostasis and biofortification. Mol Plant, 15: 65-85. PMID
[116]	Steyn W J, Wand S J E, Holcroft D M, Jacobs G. 2002. Anthocyanins in vegetative tissues: A proposed unified function in photoprotection. New Phytol, 155(3): 349-361. PMID
[117]	Stintzing F C, Carle R. 2004. Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci Technol, 15(1): 19-38.
[118]	Swamy B P M, Rahman M A, Inabangan-Asilo M A, Amparado A, Manito C, Chadha-Mohanty P, Reinke R, Slamet-Loedin I H. 2016. Advances in breeding for high grain zinc in rice. Rice, 9(1): 49. PMID
[119]	Takahama U. 2004. Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: Physiological significance of the oxidation reactions. Phytochem Rev, 3: 207-219.
[120]	Tanaka Y, Sasaki N, Ohmiya A. 2008. Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids. Plant J, 54(4): 733-749.
[121]	Tang Y, Li X H, Chen P X, Zhang B, Hernandez M, Zhang H, Marcone M F, Liu R H, Tsao R. 2015. Characterisation of fatty acid, carotenoid, tocopherol/tocotrienol compositions and antioxidant activities in seeds of three Chenopodium quinoa Willd. genotypes. Food Chem, 174: 502-508. PMID
[122]	Tapiero H, Tew K D. 2003. Trace elements in human physiology and pathology: Zinc and metallothioneins. Biomed Pharmacother, 57(9): 399-411. PMID
[123]	Tisarum R, Theerawitaya C, Samphumphuang T, Cha-um S. 2018. Regulation of anthocyanin accumulation in rice (Oryza sativa L. subsp. indica) using MgSO₄ spraying and low temperature. Arch Agron Soil Sci, 64(12): 1663-1677.
[124]	Truong H A, Lee W J, Jeong C Y, Trịnh C S, Lee S, Kang C S, Cheong Y K, Hong S W, Lee H. 2018. Enhanced anthocyanin accumulation confers increased growth performance in plants under low nitrate and high salt stress conditions owing to active modulation of nitrate metabolism. J Plant Physiol, 231: 41-48.
[125]	Tuiwong P, Lordkaew S, Veeradittakit J, Jamjod S, Prom-U-Thai C. 2022. Seed priming and foliar application with nitrogen and zinc improve seedling growth, yield, and zinc accumulation in rice. Agriculture, 12(2): 144.
[126]	van Long H, Yabe M. 2011. The impact of environmental factors on the productivity and efficiency of rice production: A study in Vietnam’s Red River Delta. Eur J Soc Sci, 26(2): 218-230.
[127]	Vichapong J, Sookserm M, Srijesdaruk V, Swatsitang P, Srijaranai S. 2010. High performance liquid chromatographic analysis of phenolic compounds and their antioxidant activities in rice varieties. LWT Food Sci Technol, 43(9): 1325-1330.
[128]	Waewkum P, Singthong J. 2021. Functional properties and bioactive compounds of pigmented brown rice flour. Bioact Carbohydr Diet Fibre, 26: 100289.
[129]	Wang H L, Wang W, Zhang P, Pan Q H, Zhan J C, Huang W D. 2010. Gene transcript accumulation, tissue and subcellular localization of anthocyanidin synthase (ANS) in developing grape berries. Plant Sci, 179: 103-113.
[130]	Wang S X, Li M, Liu K, Tian X H, Li S, Chen Y L, Jia Z. 2017. Effects of Zn, macronutrients, and their interactions through foliar applications on winter wheat grain nutritional quality. PLoS One, 12(7): e0181276.
[131]	Waters B M, Sankaran R P. 2011. Moving micronutrients from the soil to the seeds: Genes and physiological processes from a biofortification perspective. Plant Sci, 180(4): 562-574. PMID
[132]	Welch R M, Graham R D. 1999. A new paradigm for world agriculture: Meeting human needs:Productive, sustainable, nutritious. Field Crops Res, 60: 1-10.
[133]	Wessels I, Rolles B, Rink L. 2020. The potential impact of zinc supplementation on COVID-19 pathogenesis. Front Immunol, 11: 1712. PMID
[134]	Wisetkomolmat J, Arjin C, Satsook A, Seel-Audom M, Ruksiriwanich W, Prom-U-Thai C, Sringarm K. 2022. Comparative analysis of nutritional components and phytochemical attributes of selected Thai rice bran. Front Nutr, 9: 833730.
[135]	Xia D, Zhou H, Wang Y P, Li P B, Fu P, Wu B, He Y Q. 2021. How rice organs are colored: The genetic basis of anthocyanin biosynthesis in rice. Crop J, 9(3): 598-608.
[136]	Xiongsiyee V, Rerkasem B, Veeradittakit J, Saenchai C, Lordkaew S, Prom-U-Thai C T. 2018. Variation in grain quality of upland rice from Luang Prabang Province, Lao PDR. Rice Sci, 25(2): 94-102.
[137]	Yadavi A, Aboueshaghi R S, Dehnavi M M, Balouchi H. 2014. Effect of micronutrients foliar application on grain qualitative characteristics and some physiological traits of bean (Phaseolus vulgaris L.) under drought stress. Indian J Fundam Applied Life Sci, 4(4): 124-131.
[138]	Yamuangmorn S, Dell B, Rerkasem B, Prom-U-Thai C. 2018. Applying nitrogen fertilizer increased anthocyanin in vegetative shoots but not in grain of purple rice genotypes. J Sci Food Agric, 98(12): 4527-4532.
[139]	Yamuangmorn S, Prom-U-Thai C. 2021. The potential of high- anthocyanin purple rice as a functional ingredient in human health. Antioxidants, 10(6): 833.
[140]	Yamuangmorn S, Rinsinjoy R, Lordkaew S, Dell B, Prom-U-Thai C. 2020. Responses of grain yield and nutrient content to combined zinc and nitrogen fertilizer in upland and wetland rice varieties grown in waterlogged and well-drained condition. J Soil Sci Plant Nutr, 20(4): 2112-2122.
[141]	Yawadio R, Tanimori S, Morita N. 2007. Identification of phenolic compounds isolated from pigmented rices and their aldose reductase inhibitory activities. Food Chem, 101(4): 1616-1625.
[142]	Yodmanee S, Karrila T T, Pakdeechanuan P. 2011. Physical, chemical and antioxidant properties of pigmented rice grown in Southern Thailand. Int Food Res J, 18(3): 901-906.
[143]	Zaidi S H R, Zakari S A, Zhao Q, Khan A R, Shah J M, Cheng F M. 2019. Anthocyanin accumulation in black kernel mutant rice and its contribution to ROS detoxification in response to high temperature at the filling stage. Antioxidants, 8(11): 510.
[144]	Zhang M W, Guo B J, Zhang R F, Chi J W, Wei Z C, Xu Z H, Zhang Y, Tang X J. 2006. Separation, purification and identification of antioxidant compositions in black rice. Agric Sci China, 5(6): 431-440.
[145]	Zhang M W, Zhang R F, Zhang F X, Liu R H. 2010. Phenolic profiles and antioxidant activity of black rice bran of different commercially available varieties. J Agric Food Chem, 58(13): 7580-7587.
[146]	Zhao M C, Huang C H, Mao Q Q, Zhou Z H, Xiang Y H, Zhang Q L, Lin Y J, Chen H. 2021. How anthocyanin biosynthesis affects nutritional value and anti-inflammatory effect of black rice. J Cereal Sci, 101: 103295.
[147]	Zhu Q L, Yu S Z, Zeng D C, Liu H M, Wang H C, Yang Z F, Xie X R, Shen R X, Tan J T, Li H Y, Zhao X C, Zhang Q Y, Chen Y L, Guo J X, Chen L T, Liu Y G. 2017. Development of “purple endosperm rice” by engineering anthocyanin biosynthesis in the endosperm with a high-efficiency transgene stacking system. Mol Plant, 10(7): 918-929.