Abstract
Main conclusion
Sunlight boosts anthocyanin synthesis/accumulation in sunny pericarp of litchi fruit, directly leading to uneven pigmentation. Distribution discrepancy of mineral element aggravates uneven coloration by modulating synthesis/accumulation of anthocyanin and sugar.
Abstract
Uneven coloration, characterized by red pericarp on sunny side and green pericarp on shady side, impacts fruit quality of ‘Feizixiao’ (cv.) litchi. The mechanisms of this phenomenon were explored by investigating the distribution of chlorophyll, flavonoids, sugars, and mineral elements in both types of pericarp. Transcriptome analysis in pericarp was conducted as well. Sunny pericarp contained higher anthocyanins in an order of magnitude and higher fructose, glucose, co-pigments (flavanols, flavonols, ferulic acid), and mineral elements like Ca, Mg and Mn, along with lower N, P, K, S, Cu, Zn and B (P < 0.01), compared to shady pericarp. Sunlight regulated the expression of genes involved in synthesis/accumulation of flavonoids and sugars and genes functioning in nutrient uptake and transport, leading to asymmetric distribution of these substances. Anthocyanins conferred red color on sunny pericarp, sugars, Ca and Mg promoted synthesis/accumulation of anthocyanins, and co-pigments enhanced color display of anthocyanins. The insufficiencies of anthocyanins, sugars and co-pigments, and inhibition effect of excess K, S, N and P on synthesis/accumulation of anthocyanins and sugars, jointly contributed to green color of shady pericarp. These findings highlight the role of asymmetric distribution of substances, mineral elements in particular, on uneven pigmentation in litchi, and provide insights into coloration improvement via precise fertilization.
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Data availability
The data supporting the findings of this study are available from the corresponding author (Lixian Yao) upon request.
Abbreviations
- CHS:
-
Chalcone synthase
- UFGT:
-
UDP-glucose:flavonoid-3-O-glucosyltransferase
- DFR:
-
Dihydroflavonol-4-reductase
- CAXs:
-
Ca2+/H+ antiporters
- LDOX/ANS:
-
Leucoanthocyanidin dioxygenase
- GST:
-
Glutathione S-transferase
- CHS:
-
Chalcone synthase
References
Aarabi F, Kusajima M, Tohge T, Konishi T et al (2016) Sulfur deficiency-induced repressor proteins optimize glucosinolate biosynthesis in plants. Sci Adv 2(10):e1601087. https://doi.org/10.1126/sciadv.1601087
Abadie C, Tcherkez G (2019) Plant sulphur metabolism is stimulated by photorespiration. Commun Biol 2:379–379. https://doi.org/10.1038/s42003-019-0616-y
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1–15. https://doi.org/10.1104/pp.24.1.1
Azuma A, Yakushiji H, Koshita Y, Kobayashi S (2012) Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236(4):1067–1080. https://doi.org/10.1007/s00425-012-1650-x
Baublis AJ, Spomer A, Berber-Jimenez MD (1994) Anthocyanin pigments: comparison of extract stability. J Food Sci 59:1219–1221
Boulton R (2001) The copigmentation of anthocyanins and its role in the color of red wine: a critical review. Am J Enol Vitic 52(2):67–87
Castaneda-Ovando A, de Lourdes P-H, Elena Paez-Hernandez M et al (2009) Chemical studies of anthocyanins: a review. Food Chem 113(4):859–871. https://doi.org/10.1016/j.foodchem.2008.09.001
Chen H, Ou L, Li J et al (2019) Fruit scientific research in New China in the past 70 years: Litchi. J Fruit Sci 36(10):1399–1413. https://doi.org/10.13925/j.cnki.gsxb.Z14
Chen M, Zhu K, Xie J et al (2022) Genome-wide identification and expression analysis of AMT and NRT gene family in pecan (Carya illinoinensis) seedlings revealed a preference for NH4+-N. Int Mol Sci. https://doi.org/10.3390/ijms232113314
Dai Z, Meddar M, Renaud C et al (2014) Long-term in vitro culture of grape berries and its application to assess the effects of sugar supply on anthocyanin accumulation. J Exp Bot 65(16):4665–4677. https://doi.org/10.1093/jxb/ert489
Dimitrić M, Petranović NA, Baranac JM (2000) A spectrophotometric study of the copigmentation of malvin with caffeic and ferulic acids. J Agric Food Chem 48(11):5530–5536. https://doi.org/10.1021/jf000038v
Feng F, Li M, Ma F, Cheng L (2013) Phenylpropanoid metabolites and expression of key genes involved in anthocyanin biosynthesis in the shaded peel of apple fruit in response to sun exposure. Plant Physiol Biochem 69:54–61. https://doi.org/10.1016/j.plaphy.2013.04.020
Feng X, Wang Y, Zhang N et al (2020) Genome-wide systematic characterization of the HAK/KUP/KT gene family and its expression profile during plant growth and in response to low-K+ stress in Saccharum. BMC Plant Biol. https://doi.org/10.1186/s12870-019-2227-7
Fujita A, Goto-Yamamoto N, Aramaki I, Hashizume K (2006) Organ-specific transcription of putative flavonol synthase genes of grapevine and effects of plant hormones and shading on flavonol biosynthesis in grape berry skins. Biosc Biotechnol Biochem 70(3):632–638. https://doi.org/10.1271/bbb.70.632
Gomez-Miguez M, Gonzalez-Manzano S, Escribano-Bailon MT et al (2006) Influence of different phenolic copigments on the color of malvidin 3-glucoside. J Agric Food Chem 54(15):5422–5429. https://doi.org/10.1021/jf0604586
Gu Y, Yu F, Deng X et al (2017) Effect of bagging on yield, quality and benefit of litchi. South China Fruits 46(01):93–94. https://doi.org/10.13938/j.issn.1007-1431.20160172
Gutiérrez IH, Lorenzo ES-P, Espinosa AV (2005) Phenolic composition and magnitude of copigmentation in young and shortly aged red wines made from the cultivars, Cabernet Sauvignon, Cencibel, and Syrah. Food Chem 92(2):269–283. https://doi.org/10.1016/j.foodchem.2004.07.023
Henry-Kirk RA, Plunkett B, Hall M et al (2018) Solar UV light regulates flavonoid metabolism in apple (Malus x domestica). Plant Cell Environ 41(3):675–688. https://doi.org/10.1111/pce.13125
Huang H, Zhao XY, Xiao Q et al (2023) Identification of key genes induced by different potassium levels provides insight into the formation of fruit quality in grapes. Int J Mol Sci. https://doi.org/10.3390/ijms24021218
Jezek M, Zoerb C, Merkt N, Geilfus C-M (2018) Anthocyanin management in fruits by fertilization. J Agric Food Chem 66(4):753–764. https://doi.org/10.1021/acs.jafc.7b03813
Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86(1):27–44. https://doi.org/10.2307/3546567
Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004) Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136(4):4198–4204. https://doi.org/10.1104/pp.104.045625
Kim T-J, Yuk JB, Choi H-S et al (2010) Characterization of barley α-amylase chimeric enzymes expressed in Pichia pastoris. Korean J Microbiol 46(1):80–85
Klisurova D, Petrova I, Ognyanov M et al (2019) Co-pigmentation of black chokeberry (Aronia melanocarpa) anthocyanins with phenolic co-pigments and herbal extracts. Food Chem 279:162–170. https://doi.org/10.1016/j.foodchem.2018.11.125
Kokalj D, Zlatic E, Cigic B, Vidrih R (2019) Postharvest light-emitting diode irradiation of sweet cherries (Prunus avium L.) promotes accumulation of anthocyanins. Postharvest Biol Technol 148:192–199. https://doi.org/10.1016/j.postharvbio.2018.11.011
Lai B, Du L, Liu R et al (2016) Two LcbHLH transcription factors interacting with LcMYB1 in regulating late structural genes of anthocyanin biosynthesis in Nicotiana and Litchi chinensis during anthocyanin accumulation. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00166
Li P, Ma F, Cheng L (2013) Primary and secondary metabolism in the sun-exposed peel and the shaded peel of apple fruit. Physiol Plant 148(1):9–24. https://doi.org/10.1111/j.1399-3054.2012.01692.x
Liu H, Cao X, Liu X et al (2017) UV-B irradiation differentially regulates terpene synthases and terpene content of peach. Plant Cell Environ 40(10):2261–2275. https://doi.org/10.1111/pce.13029
Lu R (1999) Analysis method of soil agricultural chemistry. China Agricultural Science and Technology Press, Beijing
Martinez-Luscher J, Chen CCL, Brillante L, Kurtural SK (2017) Partial solar radiation exclusion with color shade nets reduces the degradation of organic acids and flavonoids of grape berry (Vitis vinifera L.). J Agric Food Chem 65(49):10693–10702. https://doi.org/10.1021/acs.jafc.7b04163
Molaeafard S, Jamei R, Marjani AP (2021) Co-pigmentation of anthocyanins extracted from sour cherry (Prunus cerasus L.) with some organic acids: color intensity, thermal stability, and thermodynamic parameters. Food Chem. https://doi.org/10.1016/j.foodchem.2020.128070
Montanaro G, Dichio B, Xiloyannis C, Celano G (2006) Light influences transpiration and calcium accumulation in fruit of kiwifruit plants (Actinidia deliciosa var. deliciosa). Plant Sci 170(3):520–527. https://doi.org/10.1016/j.plantsci.2005.10.004
Nikiforova V, Freitag J, Kempa S et al (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33(4):633–650. https://doi.org/10.1046/j.1365-313X.2003.01657.x
Oliveira H, Correia P, Pereira AR et al (2020) Exploring the applications of the photoprotective properties of anthocyanins in biological systems. Int J Mol Sci. https://doi.org/10.3390/ijms21207464
Peng H, Yang T, Whitaker BD et al (2016) Calcium/calmodulin alleviates substrate inhibition in a strawberry UDP-glucosyltransferase involved in fruit anthocyanin biosynthesis. BMC Plant Biol. https://doi.org/10.1186/s12870-016-0888-z
Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181(3):219–229. https://doi.org/10.1016/j.plantsci.2011.05.009
Pina F (2014) Chemical applications of anthocyanins and related compounds. A source of bioinspiration. J Agric Food Chem 62(29):6885–6897. https://doi.org/10.1021/jf404869m
Rhodes R, Miles N, Hughes JC (2018) Interactions between potassium, calcium and magnesium in sugarcane grown on two contrasting soils in South Africa. Field Crop Res 223:1–11. https://doi.org/10.1016/j.fcr.2018.01.001
Rietra RPJJ, Heinen M, Dimkpa CO, Bindraban PS (2017) Effects of nutrient antagonism and synergism on yield and fertilizer use efficiency. Commun Soil Sci Plant Anal 48(16):1895–1920. https://doi.org/10.1080/00103624.2017.1407429
Rumainum IM, Worarad K, Yamaki YT, Yamane K (2018) Effects of sucrose and plant hormone on the pigmentation of mesocarp of white- and red-fleshed peach fruits. AGRIVITA J Agric Sci. https://doi.org/10.17503/agrivita.v40i2.1094
Salman M, Ullah S, Razzaq K et al (2022) Combined foliar application of calcium, zinc, boron and time influence leaf nutrient status, vegetative growth, fruit yield, fruit biochemical and anti-oxidative attributes of “Chandler” strawberry. J Plant Nutr 45(12):1837–1848. https://doi.org/10.1080/01904167.2022.2035759
Sari P, Wijaya CH, Sajuthi D, Supratman U (2012) Colour properties, stability, and free radical scavenging activity of jambolan (Syzygium cumini) fruit anthocyanins in a beverage model system: natural and copigmented anthocyanins. Food Chem 132(4):1908–1914. https://doi.org/10.1016/j.foodchem.2011.12.025
Sarni-Manchado P, Fulcrand H, Souquet J et al (1996) Stability and color of unreported wine anthocyanin-derived pigments. J Food Sci 61(5):938–941. https://doi.org/10.1111/j.1365-2621.1996.tb10906.x
Sarni-Manchado P, Le Roux E, Le Guerneve C et al (2000) Phenolic composition of litchi fruit pericarp. J Agric Food Chem 48(12):5995–6002. https://doi.org/10.1021/jf000815r
Shaked-Sachray L, Weiss D, Reuveni M et al (2002) Increased anthocyanin accumulation in aster flowers at elevated temperatures due to magnesium treatment. Physiol Plant 114(4):559–565. https://doi.org/10.1034/j.1399-3054.2002.1140408.x
Shigaki T, Pittman JK, Hirschi KD (2003) Manganese specificity determinants in the Arabidopsis metal/H+ antiporter CAX2. J Biol Chem 278(8):6610–6617. https://doi.org/10.1074/jbc.M209952200
Sinilal B, Ovadia R, Nissim-Levi A et al (2011) Increased accumulation and decreased catabolism of anthocyanins in red grape cell suspension culture following magnesium treatment. Planta 234(1):61–71. https://doi.org/10.1007/s00425-011-1377-0
Socha AL, Guerinot ML (2014) Mn-euveringmanganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00106
Su X, Bai C, Wang X et al (2022a) Potassium sulfate spray promotes fruit color preference via regulation of pigment profile in litchi pericarp. Front Plant Sci. https://doi.org/10.3389/fpls.2022.925609
Su X, Zhu Y, Bai C et al (2022b) Dark pericarp disease in litchi is induced by manganese stress. Plant Soil 481(1):563–579. https://doi.org/10.1007/s11104-022-05658-0
Tavares S, Vesentini D, Fernandes JC et al (2013) Vitis vinifera secondary metabolism as affected by sulfate depletion: diagnosis through phenylpropanoid pathway genes and metabolites. Plant Physiol Biochem 66:118–126. https://doi.org/10.1016/j.plaphy.2013.01.022
Tian G, Qin H, Liu C et al (2023) Magnesium improved fruit quality by regulating photosynthetic nitrogen use efficiency, carbon-nitrogen metabolism, and anthocyanin biosynthesis in ‘Red Fuji’ apple. Front Plant Sci. https://doi.org/10.3389/fpls.2023.1136179
Wang HC, Huang XM, Hu GB et al (2005) A comparative study of chlorophyll loss and its related mechanism during fruit maturation in the pericarp of fast- and slow-degreening litchi pericarp. Sci Hortic 106(2):247–257. https://doi.org/10.1016/j.scienta.2005.03.007
Wang Y, Gao L, Shan Y et al (2012) Influence of shade on flavonoid biosynthesis in tea (Camellia sinensis (L.) O. Kuntze). Sci Horti 141:7–16. https://doi.org/10.1016/j.scienta.2012.04.013
Wang Z, Li S, Yuan M, Zhou K (2017a) De novo transcriptome assembly for pericarp in Litchi chinesis Sonn. cv. Feizixiao and identification of differentially expressed genes in response to Mg Foliar Nutrient. Sci Hortic 226:59–67. https://doi.org/10.1016/j.scienta.2017.08.023
Wang Z, Yuan M, Li S et al (2017b) Applications of magnesium affect pericarp colour in the Feizixiao lychee. J Horticult Sci Biotechnol 92(6):559–567. https://doi.org/10.1080/14620316.2017.1322922
Wang Y, Gao S, He X et al (2020) Response of total phenols, flavonoids, minerals, and amino acids of four edible fern species to four shading treatments. PeerJ. https://doi.org/10.7717/peerj.8354
Wang J, Cao K, Wang L et al (2022) Two MYB and three bHLH family genes participate in anthocyanin accumulation in the flesh of peach fruit treated with glucose, sucrose, sorbitol, and fructose in vitro. Plants (basel) 11(4):507. https://doi.org/10.3390/plants11040507
Williams M, Hrazdina G (1979) Anthocyanins as food colorants: effect of pH on the formation of anthocyanin-rutin complexes. J Food Sci 44(1):66–68. https://doi.org/10.1111/j.1365-2621.1979.tb10005.x
Wojcik P, Wojcik M (2006) Effect of boron fertilization on sweet cherry tree yield and fruit quality. J Plant Nutr 29(10):1755–1766. https://doi.org/10.1080/01904160600897471
Wrolstad RE, Erlandson JA (2010) Effect of metal ions on the color of strawberry puree. J Food Sci 38(3):460–463
Xu W, Peng H, Yang T et al (2014) Effect of calcium on strawberry fruit flavonoid pathway gene expression and anthocyanin accumulation. Plant Physiol Biochem 82:289–298. https://doi.org/10.1016/j.plaphy.2014.06.015
Xu N, Zhu J, Peng H et al (2015) Effects of different bagging treatments on fruit setting and quality of strawberry litchi. Agric Res Appl 06:6–8
Xu X, Qin H, Liu C et al (2022) Transcriptome and metabolome analysis reveals the effect of nitrogen-potassium on anthocyanin biosynthesis in “Fuji” apple. J Agric Food Chem. https://doi.org/10.1021/acs.jafc.2c06287
Yang BM, Yao L, Li GL et al (2015) Dynamic changes of nutrition in litchi foliar and effects of potassium-nitrogen fertilization ratio. J Soil Sci Plant Nutr 15:98–110
Yang J, Zhao X, Chen Y et al (2022) Identification, structural, and expression analyses of SPX genes in giant duckweed (Spirodela polyrhiza) reveals its role in response to low phosphorus and nitrogen stresses. Cells. https://doi.org/10.3390/cells11071167
Yoshimoto N, Inoue E, Saito K et al (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131(4):1511–1517. https://doi.org/10.1104/pp.014712
Yu J, Zhu M, Wang M et al (2020) Transcriptome analysis of calcium-induced accumulation of anthocyanins in grape skin. Sci Hortic. https://doi.org/10.1016/j.scienta.2019.108871
Zhang H, Li W, Wang H et al (2016) Transcriptome profiling of light-regulated anthocyanin biosynthesis in the pericarp of litch. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00963
Zhang X, Wei J, Tian J et al (2019) Enhanced anthocyanin accumulation of immature radish microgreens by hydrogen-rich water under short wavelength light. Sci Hortic 247:75–85. https://doi.org/10.1016/j.scienta.2018.11.060
Zhao J (2015) Flavonoid transport mechanisms: how to go, and with whom. Trends Plant Sci 20(9):576–585. https://doi.org/10.1016/j.tplants.2015.06.007
Zhao P, You Q, Lei M (2019) A CRISPR/Cas9 deletion into the phosphate transporter SlPHO1;1 reveals its role in phosphate nutrition of tomato seedlings. Physiol Plant 167(4):556–563. https://doi.org/10.1111/ppl.12897
Zhou K, Peters RJ (2009) Investigating the conservation pattern of a putative second terpene synthase divalent metal binding motif in plants. Phytochemistry 70(3):366–369. https://doi.org/10.1016/j.phytochem.2008.12.022
Zhou K, Su J, Xu Y (2007) Effects of P, K and Ca on the pigmentation of Sanyuehong litchi (Litchi chinensis Sonn. cv. Sanyuehong) fruits. Soil Fertil Sci China 06:54–57
Zhou H, Kui L, Wang H et al (2015) Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. Plant J 82(1):105–121. https://doi.org/10.1111/tpj.12792
Zou S, Zhuo M, Abbas F et al (2023) Transcription factor LcNAC002 coregulates chlorophyll degradation and anthocyanin biosynthesis in litchi. Plant Physiol. https://doi.org/10.1093/plphys/kiad118
Acknowledgements
We thank Ms. Pan Luyi at the Instrumental Analysis and Research Center of South China Agricultural University for her assistance in HPLC analysis. Mrs. Shengtong Luo at University College London is appreciated for her help in language polishing.
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This research was supported by China Agriculture Research System of MOF and MARA (CARS-32-06).
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LY and CB: conceptualization and design; XS, XZ, CB, HL, XC and LY: experimental work; XS, XZ, CB, XC and HL: sample analysis and data analysis; XS: writing of original draft; LY: funding acquisition, review and editing. All authors have read and agreed to the published version of the manuscript.
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Su, X., Zhang, X., Bai, C. et al. Asymmetric distribution of mineral nutrients aggravates uneven fruit pigmentation driven by sunlight exposure in litchi. Planta 258, 96 (2023). https://doi.org/10.1007/s00425-023-04250-9
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DOI: https://doi.org/10.1007/s00425-023-04250-9