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Pigments in Citrus Fruit: Mutants, Compounds, Genes, and Beyond

  • Chunxian ChenEmail author
Chapter
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Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Pigments in citrus fruit include chlorophylls, carotenoids, and flavonoids. While chlorophylls color green citrus fruit, carotenoids and flavonoids are synthesized predominantly in citrus fruit after the color breaker stage. Various carotenoids are responsible for a spectrum of characteristic red, orange, and yellow colors for mature citrus fruit. Lycopene is the carotenoid producing pink to red in some sweet orange and grapefruit mutants while other carotenes and xanthophylls contribute to commonly seen orange to yellow colors. Anthocyanins, a subgroup of colored flavonoids, yield additional blood red colors only in blood oranges. Citrus fruit mutants rich in red lycopene or anthocyanins that generate additional organoleptic attraction and marketing appeal have been extensively used in various pigment studies and comparisons. Most biosynthetic genes and some regulatory genes in the carotenoid and anthocyanin pathways have been cloned and characterized. Pigmentation and gene expression changes during citrus fruit postharvest degreening and storage were also gradually uncovered. Genetic knowledge of citrus fruit pigmentation facilitates continuing research on and variety improvement for beneficial pigment compounds. Dietetics of some citrus pigments has been studied from both nutritional and preventive medicinal perspectives, with emphasis on lycopene and anthocyanins due to the predominant content in popular red-fleshed cultivars, special marketing appeal, and potential health benefits. Nutraceutical and medicinal benefits of consumption of citrus fruit (juice) include substantially improved health biomarkers for lipid profiles, low risk of obesity and cardiovascular disease, and potential suppression of some cancers. Regular moderate consumption of fresh citrus fruit and/or orange juice should be encouraged as part of a daily healthy diet.

Keywords

Carotenoid Carotene Lycopene Xanthophyll β-cryptoxanthin Flavonoid Anthocyanin Cyanidin-3-glucoside Cyanidin-3-(6″-malonylglucoside) Biosynthesis Ethylene Degreening Dietetics Citrus sinensis C. paradisi 

References

  1. Alquezar B, Rodrigo MJ, Zacarias L (2008) Regulation of carotenoid biosynthesis during fruit maturation in the red-fleshed orange mutant Cara Cara. Phytochemistry 69:1997–2007PubMedCrossRefGoogle Scholar
  2. Alquezar B, Zacarias L, Rodrigo MJ (2009) Molecular and functional characterization of a novel chromoplast-specific lycopene beta-cyclase from Citrus and its relation to lycopene accumulation. J Exp Bot 60:1783–1797PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andrade-Souza V, Costa MGC, Chen CX, Gmitter FG, Costa MA (2011) Physical location of the carotenoid biosynthesis genes Psy and beta-Lcy in Capsicum annuum (Solanaceae) using heterologous probes from Citrus sinensis (Rutaceae). Genet Mol Res 10:404–409PubMedCrossRefGoogle Scholar
  4. Balestra C, Cimino F, Theunissen S, Snoeck T, Provyn S, Canali R, Bonina A, Virgili F (2016) A red orange extract modulates the vascular response to a recreational dive: a pilot study on the effect of anthocyanins on the physiological consequences of scuba diving. Nat Prod Res 30:2101–2106PubMedCrossRefGoogle Scholar
  5. Bendich A (1989) Carotenoids and the immune response. J Nutrition 119:112–115CrossRefGoogle Scholar
  6. Bernardi J, Licciardello C, Russo MP, Luisa Chiusano M, Carletti G, Recupero GR, Marocco A (2010) Use of a custom array to study differentially expressed genes during blood orange (Citrus sinensis L. Osbeck) ripening. J Plant Physiol 167:301–310PubMedCrossRefGoogle Scholar
  7. Bowen PE, Navsariwala V, Stacewicz-Sapuntzakis M (2015) Carotenoids in human nutrition. In: Chen C (ed) Pigments in fruits and vegetables: genomics and dietetics. Springer, New York, pp 31–67CrossRefGoogle Scholar
  8. Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255PubMedPubMedCentralCrossRefGoogle Scholar
  9. Carmona L, Zacarias L, Rodrigo MJ (2012) Stimulation of coloration and carotenoid biosynthesis during postharvest storage of ‘Navelina’ orange fruit at 12 degrees C. Postharvest Biol Technol 74:108–117CrossRefGoogle Scholar
  10. Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847CrossRefGoogle Scholar
  11. Chandler BV (1958) Anthocyanins of blood oranges. Nature 182:933–933PubMedCrossRefGoogle Scholar
  12. Chaudhary P, Jayaprakasha GK, Porat R, Patil BS (2012) Degreening and postharvest storage influences ‘Star Ruby’ grapefruit (Citrus paradisi Macf.) bioactive compounds. Food Chem 135:1667–1675PubMedCrossRefGoogle Scholar
  13. Chaudhary PR, Yu X, Jayaprakasha GK, Patil BS (2017) Influence of storage temperature and low-temperature conditioning on the levels of health-promoting compounds in Rio Red grapefruit. Food Sci Nutr 5:545–553PubMedCrossRefGoogle Scholar
  14. Chen C, Costa MGC, Yu Q, Moore GA, Gmitter FG (2010) Identification of novel members in sweet orange carotenoid biosynthesis gene families. Tree Genet Genom 6:905–914CrossRefGoogle Scholar
  15. Chen C (2015a) Overview of plant pigments. In: Chen C (ed) Pigments in fruits and vegetables: genomics and dietetics. Springer, New York, pp 1–7CrossRefGoogle Scholar
  16. Chen C (ed) (2015b) Pigments in fruits and vegetables: genomics and dietetics. Springer, New YorkGoogle Scholar
  17. Chen C, Lo Piero AR, Gmitter FG (2015) Pigments in citrus. In: Chen C (ed) Pigments in fruits and vegetables: genomics and dietetics. Springer, New York, pp 165–187CrossRefGoogle Scholar
  18. Costa MGC, Moreira CD, Melton JR, Otoni WC, Moore GA (2012) Characterization and developmental expression of genes encoding the early carotenoid biosynthetic enzymes in Citrus paradisi Macf. Mol Biol Rep 39:895–902PubMedCrossRefGoogle Scholar
  19. Cotroneo PS, Russo MP, Ciuni M, Recupero GR, Lo Piero AR (2006) Quantitative real-time reverse transcriptase-PCR profiling of anthocyanin biosynthetic genes during orange fruit ripening. J Am Soc Hortic Sci 131:537–543CrossRefGoogle Scholar
  20. Crifò T, Puglisi I, Petrone G, Recupero GR, Lo Piero AR (2011) Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476:1–9PubMedCrossRefGoogle Scholar
  21. Crifò T, Petrone G, Lo Cicero L, Lo Piero AR (2012) Short cold storage enhances the anthocyanin contents and level of transcripts related to their biosynthesis in blood oranges. J Agric Food Chem 60:476–481PubMedCrossRefGoogle Scholar
  22. Cunningham FX, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583PubMedCrossRefGoogle Scholar
  23. da Graça JV, Louzada ES, Sauls JW (2004) The origins of red pigmented grapefruits and the development of new varieties. In: Proceedings of the International Society of Citriculture, pp 369–374Google Scholar
  24. Dhuique-Mayer C, Fanciullino AL, Dubois C, Ollitrault P (2009) Effect of genotype and environment on citrus juice carotenoid content. J Agric Food Chem 57:9160–9168PubMedCrossRefGoogle Scholar
  25. Doostdar H, Shapiro JP, Niedz R, Burke MD, Mccollum TG, Mcdonald RE, Mayer RT (1995) A cytochrome-P450 mediated naringenin 3′-hydroxylase from sweet orange cell-cultures. Plant Cell Physiol 36:69–77Google Scholar
  26. Dourado GK, Stanilka JM, Percival SS, Cesar TB (2015) Chemopreventive actions of blond and red-fleshed sweet orange juice on the loucy leukemia cell line. Asian Pac J Cancer Prev 16:6491–6499PubMedCrossRefGoogle Scholar
  27. Fanciullino AL, Dhuique-Mayer C, Luro F, Casanova J, Morillon R, Ollitrault P (2006) Carotenoid diversity in cultivated citrus is highly influenced by genetic factors. J Agric Food Chem 54:4397–4406PubMedCrossRefPubMedCentralGoogle Scholar
  28. Garewal H, Meyskens F Jr, Friedman S, Alberts D, Ramsey L (1993) Oral cancer prevention: the case for carotenoids and anti-oxidant nutrients. Prev Med 22:701–711PubMedCrossRefGoogle Scholar
  29. Gmitter FG, Chen C, Machado MA, de Souza AA, Ollitrault P, Froehlicher Y, Shimizu T (2012) Citrus genomics. Tree Genet Genom 8:611–626CrossRefGoogle Scholar
  30. Gross J (1987) Pigments in fruits. Academic Press, London, OrlandoGoogle Scholar
  31. Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The Myb-homologous P-gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553PubMedCrossRefGoogle Scholar
  32. Hikita M, Motojima K, Kamata S, Yoshida T, Tanaka-Nakadate S, Nakadate K (2016) Protective efficacy of the ingestion of mandarin orange containing beta-cryptoxanthin on lipopolysaccharide-induced acute nephritis. Yakugaku Zasshi 136:1031–1040PubMedCrossRefGoogle Scholar
  33. Hillebrand S, Schwarz M, Winterhalter P (2004) Characterization of anthocyanins and pyranoanthocyanins from blood orange [Citrus sinensis (L.) Osbeck] juice. J Agric Food Chem 52:7331–7338PubMedCrossRefGoogle Scholar
  34. Jackson H, Braun CL, Ernst H (2008) The chemistry of novel xanthophyll carotenoids. Am J Cardiol 101:50D–57DPubMedCrossRefGoogle Scholar
  35. Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M (2004) Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol 134:824–837PubMedPubMedCentralCrossRefGoogle Scholar
  36. Kato M (2012) Mechanism of carotenoid accumulation in citrus fruit. J Japan Soc Hortic Sci 81:219–233CrossRefGoogle Scholar
  37. Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242PubMedPubMedCentralCrossRefGoogle Scholar
  38. Lado J, Cronje P, Alquezar B, Page A, Manzi M, Gomez-Cadenas A, Stead AD, Zacarias L, Rodrigo MJ (2015) Fruit shading enhances peel color, carotenes accumulation and chromoplast differentiation in red grapefruit. Physiol Plant 154:469–484PubMedCrossRefPubMedCentralGoogle Scholar
  39. Lee HS (2001) Characterization of carotenoids in juice of red navel orange (Cara Cara). J Agric Food Chem 49:2563–2568CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lee HS, Castle WS (2001) Seasonal changes of carotenoid pigments and color in Hamlin, Earlygold, and budd blood orange juices. J Agric Food Chem 49:877–882PubMedCrossRefGoogle Scholar
  41. Lee HS (2002) Characterization of major anthocyanins and the color of red-fleshed Budd Blood orange (Citrus sinensis). J Agric Food Chem 50:1243–1246PubMedCrossRefGoogle Scholar
  42. Lee HS, Coates GA (2002) Characterization of color fade during frozen storage of red grapefruit juice concentrates. J Agric Food Chem 50:3988–3991PubMedCrossRefGoogle Scholar
  43. Lester GE, Manthey JA, Buslig BS (2007) Organic vs conventionally grown Rio Red whole grapefruit and juice: comparison of production inputs, market quality, consumer acceptance, and human health-bioactive compounds. J Agric Food Chem 55:4474–4480PubMedCrossRefGoogle Scholar
  44. Liu Q, Xu J, Liu YZ, Zhao XL, Deng XX, Guo LL, Gu JQ (2007) A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). J Exp Bot 58:4161–4171PubMedCrossRefGoogle Scholar
  45. Lo Piero AR, Puglisi I, Rapisarda P, Petrone G (2005) Anthocyanins accumulation and related gene expression in red orange fruit induced by low temperature storage. J Agric Food Chem 53:9083–9088PubMedCrossRefGoogle Scholar
  46. Lo Piero AR, Puglisi I, Petrone G (2006a) Gene isolation, analysis of expression, and in vitro synthesis of glutathione S-transferase from orange fruit [Citrus sinensis L. (Osbeck)]. J Agric Food Chem 54:9227–9233PubMedCrossRefGoogle Scholar
  47. Lo Piero AR, Puglisi I, Petrone G (2006b) Gene characterization, analysis of expression and in vitro synthesis of dihydroflavonol 4-reductase from [Citrus sinensis (L.) Osbeck]. Phytochemistry 67:684–695PubMedCrossRefGoogle Scholar
  48. Lu S, Zhang Y, Zhu K, Yang W, Ye J, Chai L, Xu Q, Deng X (2018) the citrus transcription factor CsMADS6 modulates carotenoid metabolism by directly regulating carotenogenic genes. Plant Physiol 176:2657–2676PubMedPubMedCentralCrossRefGoogle Scholar
  49. Matsumoto H, Ikoma Y, Kato M, Kuniga T, Nakajima N, Yoshida T (2007) Quantification of carotenoids in citrus fruit by LC-MS and comparison of patterns of seasonal changes for carotenoids among citrus varieties. J Agric Food Chem 55:2356–2368PubMedCrossRefGoogle Scholar
  50. Matsumoto H, Ikoma Y, Kato M, Nakajima N, Hasegawa Y (2009) Effect of postharvest temperature and ethylene on carotenoid accumulation in the flavedo and juice sacs of satsuma mandarin (Citrus unshiu Marc.) Fruit. J Agric Food Chem 57:4724–4732PubMedCrossRefGoogle Scholar
  51. Melendez-Martinez AJ, Vicario IM, Heredia FJ (2007) Carotenoids, color, and ascorbic acid content of a novel frozen-marketed orange juice. J Agric Food Chem 55:1347–1355PubMedCrossRefGoogle Scholar
  52. Mendes AF, Chen C, Gmitter FG Jr, Moore GA, Costa MG (2011) Expression and phylogenetic analysis of two new lycopene beta-cyclases from Citrus paradisi. Physiol Plant 141:1–10PubMedCrossRefGoogle Scholar
  53. Middleton E Jr, Kandaswami C, Theoharides TC (2000) The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol Rev 52:673–751PubMedGoogle Scholar
  54. Mondello L, Cotroneo A, Errante G, Dugo G, Dugo P (2000) Determination of anthocyanins in blood orange juices by HPLC analysis. J Pharm Biomed Anal 23:191–195PubMedCrossRefGoogle Scholar
  55. Nogata Y, Sakamoto K, Shiratsuchi H, Ishii T, Yano M, Ohta H (2006) Flavonoid composition of fruit tissues of citrus species. Biosci Biotechnol Biochem 70:178–192PubMedCrossRefGoogle Scholar
  56. O’Neil CE, Nicklas TA, Rampersaud GC, Fulgoni VL III (2011) One hundred percent orange juice consumption is associated with better diet quality, improved nutrient adequacy, and no increased risk for overweight/obesity in children. Nutr Res 31:673–682PubMedCrossRefGoogle Scholar
  57. O’Neil CE, Nicklas TA, Rampersaud GC, Fulgoni VL III (2012) 100% Orange juice consumption is associated with better diet quality, improved nutrient adequacy, decreased risk for obesity, and improved biomarkers of health in adults: National Health and Nutrition Examination Survey, 2003–2006. Nutr J 11:107PubMedPubMedCentralCrossRefGoogle Scholar
  58. Paiva SA, Russell RM (1999) Beta-carotene and other carotenoids as antioxidants. J Am Coll Nutr 18:426–433PubMedCrossRefGoogle Scholar
  59. Pan Z, Liu Q, Yun Z, Guan R, Zeng W, Xu Q, Deng X (2009) Comparative proteomics of a lycopene-accumulating mutant reveals the important role of oxidative stress on carotenogenesis in sweet orange (Citrus sinensis [L.] osbeck). Proteomics 9:5455–5470PubMedCrossRefGoogle Scholar
  60. Parihar A, Grotewold E, Doseff AI (2015) Flavonoids dietetics: mechanisms and emerging roles of plant nutraceuticals. In: Chen C (ed) Pigments in fruits and vegetables: genomics and dietetics. Springer, New York, pp 93–126CrossRefGoogle Scholar
  61. Pupin AM, Dennis MJ, Toledo MCF (1999) HPLC analysis of carotenoids in orange juice. Food Chem 64:269–275CrossRefGoogle Scholar
  62. Rapisarda P, Pannuzzo P, Romano G, Russo G (2003) Juice components of a new pigmented citrus hybrid Citrus sinensis (L.) Osbeck × Citrus clementina Hort. ex Tan. J Agric Food Chem 51:1611–1616PubMedCrossRefGoogle Scholar
  63. Rapisarda P, Bellomo SE, Fabroni S, Russo G (2008) Juice quality of two new mandarin-like hybrids (Citrus clementina Hort. ex Tan × Citrus sinensis L. Osbeck) containing anthocyanins. J Agric Food Chem 56:2074–2078Google Scholar
  64. Rodrigo MJ, Zacarias L (2007) Effect of postharvest ethylene treatment on carotenoid accumulation and the expression of carotenoid biosynthetic genes in the flavedo of orange (Citrus sinensis L. Osbeck) fruit. Postharvest Biol Technol 43:14–22CrossRefGoogle Scholar
  65. Sanchez-Moreno C, Plaza L, De Ancos B, Cano MP (2003) Vitamin C, provitamin A carotenoids, and other carotenoids in high-pressurized orange juice during refrigerated storage. J Agric Food Chem 51:647–653PubMedCrossRefGoogle Scholar
  66. Sharoni Y, Linnewiel-Hermoni K, Khanin M, Salman H, Veprik A, Danilenko M, Levy J (2012) Carotenoids and apocarotenoids in cellular signaling related to cancer: a review. Mol Nutr Food Res 56:259–269PubMedCrossRefGoogle Scholar
  67. Silveira JQ, Dourado GK, Cesar TB (2015) Red-fleshed sweet orange juice improves the risk factors for metabolic syndrome. Int J Food Sci Nutr 66:830–836PubMedCrossRefGoogle Scholar
  68. Stewart I (1977) Provitamin A and carotenoid content of citrus juices. J Agric Food Chem 25:1132–1137PubMedCrossRefGoogle Scholar
  69. Stinco CM, Escudero-Gilete ML, Heredia FJ, Vicario IM, Melendez-Martinez AJ (2016) Multivariate analyses of a wide selection of orange varieties based on carotenoid contents, color and in vitro antioxidant capacity. Food Res Int 90:194–204PubMedCrossRefGoogle Scholar
  70. Tao N, Hu Z, Liu Q, Xu J, Cheng Y, Guo L, Guo W, Deng X (2007) Expression of phytoene synthase gene (Psy) is enhanced during fruit ripening of Cara Cara navel orange (Citrus sinensis Osbeck). Plant Cell Rep 26:837–843PubMedCrossRefGoogle Scholar
  71. Tao NG, Xu J, Cheng YJ, Deng XX (2005) Lycopene-epsilon-cyclase pre-mRNA is alternatively spliced in Cara Cara navel orange (Citrus sinensis Osbeck). Biotech Lett 27:779–782CrossRefGoogle Scholar
  72. Tao NG, Wang CF, Xu J, Cheng YJ (2012) Carotenoid accumulation in postharvest “Cara Cara” navel orange (Citrus sinensis Osbeck) fruits stored at different temperatures was transcriptionally regulated in a tissue-dependent manner. Plant Cell Rep 31:1667–1676PubMedCrossRefGoogle Scholar
  73. Vanamala J, Cobb G, Turner ND, Lupton JR, Yoo KS, Pike LM, Patil BS (2005) Bioactive compounds of grapefruit (Citrus paradisi Cv. Rio Red) respond differently to postharvest irradiation, storage, and freeze drying. J Agric Food Chem 53:3980–3985PubMedCrossRefGoogle Scholar
  74. Walter MH, Strack D (2011) Carotenoids and their cleavage products: Biosynthesis and functions. Nat Prod Rep 28:663–692PubMedCrossRefGoogle Scholar
  75. Wang Y, Li J, Yang J, Xia RX (2011) Expression of lycopene cyclase genes and their regulation on downstream carotenoids during fruit maturation of Guoqing No. 1 Satsuma mandarin and Cara Cara navel orange. Sci Hortic 127:267–274CrossRefGoogle Scholar
  76. Wei X, Chen CX, Yu QB, Gady A, Yu Y, Liang GL, Gmitter FG (2014a) Comparison of carotenoid accumulation and biosynthetic gene expression between Valencia and Rohde Red Valencia sweet oranges. Plant Sci 227:28–36PubMedCrossRefGoogle Scholar
  77. Wei X, Chen CX, Yu QB, Gady A, Yu Y, Liang GL, Gmitter FG (2014b) Novel expression patterns of carotenoid pathway-related genes in citrus leaves and maturing fruits. Tree Genet Genom 10:439–448CrossRefGoogle Scholar
  78. Wei X, Song M, Chen C, Tong H, Liang G, Gmitter FG Jr (2018) Juice volatile composition differences between Valencia orange and its mutant Rohde Red Valencia are associated with carotenoid profile differences. Food Chem 245:223–232PubMedCrossRefGoogle Scholar
  79. Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493PubMedPubMedCentralCrossRefGoogle Scholar
  80. Xu CJ, Fraser PD, Wang WJ, Bramley PM (2006) Differences in the carotenoid content of ordinary citrus and lycopene-accumulating mutants. J Agric Food Chem 54:5474–5481PubMedCrossRefGoogle Scholar
  81. Xu Q, Yu K, Zhu A, Ye J, Liu Q, Zhang J, Deng X (2009) Comparative transcripts profiling reveals new insight into molecular processes regulating lycopene accumulation in a sweet orange (Citrus sinensis) red-flesh mutant. BMC Genom 10:540CrossRefGoogle Scholar
  82. Yu K, Xu Q, Da X, Guo F, Ding Y, Deng X (2012) Transcriptome changes during fruit development and ripening of sweet orange (Citrus sinensis). BMC Genom 13:10CrossRefGoogle Scholar
  83. Zhou JY, Sun CD, Zhang LL, Dai XA, Xu CJ, Chen KS (2010) Preferential accumulation of orange-colored carotenoids in Ponkan (Citrus reticulata) fruit peel following postharvest application of ethylene or ethephon. Sci Hortic 126:229–235CrossRefGoogle Scholar
  84. Zhu F, Luo T, Liu C, Wang Y, Yang H, Yang W, Zheng L, Xiao X, Zhang M, Xu R, Xu J, Zeng Y, Xu J, Xu Q, Guo W, Larkin RM, Deng X, Cheng Y (2017) An R2R3-MYB transcription factor represses the transformation of alpha- and beta-branch carotenoids by negatively regulating expression of CrBCH2 and CrNCED5 in flavedo of Citrus reticulate. New Phytol 216:178–192PubMedCrossRefGoogle Scholar

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© This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2020

Authors and Affiliations

  1. 1.US Department of Agriculture, Agricultural Research ServiceSoutheastern Fruit and Tree Nut Research LaboratoryByronUSA

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