Low soil pH enhances fruit acidity by inhibiting citric acid degradation in lemon (Citrus lemon L.)

Abstract

Fruit acidity significantly influences fruit flavor, but the specific impact of soil pH on fruit acidity remains unclear. This study investigated the effects of various soil pH levels on fruit acidity and citric acid (CA) metabolism in lemon (Citrus limon L.). High soil pH (pH 8) decreased total soluble solids concentrations in lemon fruits, while low soil pH (pH 4) increased titratable acid and CA concentrations. Although low soil pH reduced the synthesis of CA due to the decreased citrate synthase and phosphoenolpyruvate carboxylase activities, the elevated fruit acidity under low soil pH conditions is not directly related to CA synthesis. Instead, low soil pH was found to suppress the activity of cytosolic aconitase (Cyt-ACO), an iron-dependent enzyme, indicating a potential role for CA degradation inhibition in low soil pH-induced CA accumulation. Furthermore, low soil pH significantly reduced cytosolic iron (Cyt-Fe) concentration, which was positively correlated with Cyt-ACO activity. In conclusion, low soil pH contributes to increasing fruit acidity in lemon, partially by inhibiting CA degradation due to the reduced Cyt-Fe concentrations. Our work unravels the influence of soil pH on CA accumulation and provides important clues for modulating CA levels through microelement fertilization in citrus.

References

[1] An J, Sun M, van Velzen R, Ji C, Zheng Z, Limpens E, et al. . Comparative transcriptome analysis of Poncirus trifoliata identifies a core set of genes involved in arbuscular mycorrhizal symbiosis. J Exp Bot, 2018, 69: 5255-5264.

[2] Chen X, Yu W, Cai Y, Zhang S, Muneer MA, Zhu Q, et al. . How to identify and adopt cleaner strategies to improve the continuous acidification in orchard soils. J Clean Prod, 2022, 330: 129826.

[3] Etienne A, Génard M, Lobit P, Mbeguié-A-Mbéguié D, Bugaud C. What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. J Exp Bot, 2013, 64: 1451-1469.

[4] Ge S, Zhu Z, Jiang Y. Long-term impact of fertilization on soil pH and fertility in an apple production system. J Soil Sci Plant Nutr, 2018, 18: 282-293.

[5] Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, et al. . Significant acidification in major Chinese croplands. Science, 2010, 327: 1008-1010.

[6] Guo C, Pan Z, Peng S. Effect of biochar on the growth of Poncirus trifoliata (L.) Raf. seedlings in Gannan acidic red soil. Soil Sci Plant Nutr., 2016, 62: 194-200.

[7] Guo LX, Shi CY, Liu X, Ning DY, Jing LF, Yang H, et al. . Citrate accumulation-related gene expression and/or enzyme activity analysis combined with metabolomics provide a novel insight for an orange mutant. Sci Rep, 2016, 6: 29343.

[8] Hussain SB, Shi CY, Guo LX, Kamran HM, Sadka A, Liu YZ. Recent advances in the regulation of citric acid metabolism in citrus fruit. Crit Rev Plant Sci, 2017, 36: 241-256.

[9] Ji C, Song F, He C, An J, Huang S, Yu H, et al. . Integrated miRNA-mRNA analysis reveals candidate miRNA family regulating arbuscular mycorrhizal symbiosis of Poncirus trifoliata. Plant Cell Environ, 2023, 46: 1805-1821.

[10] Jiang Y, Zeng Q, Wei J, Jiang J, Li Y, Chen J, et al. . Growth, fruit yield, photosynthetic characteristics, and leaf microelement concentration of two blueberry cultivars under different long-term soil pH treatments. Agronomy, 2019, 9: 357.

[11] Li Y, Han MQ, Lin F, Ten Y, Lin J, Zhu DH, et al. . Soil chemical properties',Guanximiyou' pummelo leaf mineral nutrient status and fruit quality in the southern region of Fujian province. China J Soil Sci Plant Nutr, 2015, 15: 615-628.

[12] Li W, Li G, Yuan Z, Li M, Deng X, Tan M, et al. . Illustration of the variation in the content of flavanone rutinosides in various citrus germplasms from genetic and enzymatic perspectives. Hortic Res., 2022, 9: uhab017.

[13] Liang X, Chen Q, Rana MS, Dong Z, Liu X, Hu C, et al. . Effects of soil amendments on soil fertility and fruit yield through alterations in soil carbon fractions. J Soils Sediments, 2021, 21: 2628-2638.

[14] Lin Q, Qian J, Zhao C, Wang D, Liu C, Wang Z, et al. . Low temperature induced changes in citrate cmtabolism in Ponkan (Citrus reticulata Blanco cv. Ponkan) fruit during maturation. PLoS One., 2016, 11: e0156703.

[15] Marschner P Marschner's mineral nutrition of higher plants, 2011 3 Amsterdam Elsevier/Academic Press

[16] Muhammad N, Zvobgo G, Fu L, Lwalaba JLW, Zhang G. Physiological mechanisms for antagonistic interaction of manganese and aluminum in barley. J Plant Nutr, 2019, 42: 466-476.

[17] Sheng L, Shen D, Luo Y, Sun X, Wang J, Luo T, et al. . Exogenous γ-aminobutyric acid treatment affects citrate and amino acid accumulation to improve fruit quality and storage performance of postharvest citrus fruit. Food Chem, 2017, 216: 138-145.

[18] Shlizerman L, Marsh K, Blumwald E, Sadka A. Iron-shortage-induced increase in citric acid content and reduction of cytosolic aconitase activity in Citrus fruit vesicles and calli. Physiol Plant, 2007, 131: 72-79.

[19] Wu S, Sun X, Tan Q, Hu C. Molybdenum improves water uptake via extensive root morphology, aquaporin expressions and increased ionic concentrations in wheat under drought stress. Environ Exp Bot, 2019, 157: 241-249.

[20] Wu S, Zhang Y, Tan Q, Sun X, Wei W, Hu C. Biochar is superior to lime in improving acidic soil properties and fruit quality of Satsuma mandarin. Sci Total Environ, 2020, 714: 136722.

[21] Wu S, Zhang C, Li M, Tan Q, Sun X, Pan Z, et al. . Effects of potassium on fruit soluble sugar and citrate accumulations in Cara Cara navel orange (Citrus sinensis L. Osbeck). Sci Hortic., 2021, 283: 110057.

[22] Wu S, Li M, Zhang C, Tan Q, Yang X, Sun X, et al. . Effects of phosphorus on fruit soluble sugar and citric acid accumulations in citrus. Plant Physiol Biochem, 2021, 160: 73-81.

[23] Wu S, Li M, Zhang C, Tan Q, Yang X, Sun X, et al. . Effects of phosphorus on fruit soluble sugar and citric acid accumulations in citrus. Plant Physiol Biochem, 2021, 160: 73-81.

[24] Wu S, Liang S, Hu C, Tan Q, Zhang J, Dong Z. Ecological region division of soil based supplementary fertilization and decrement fertilization in China citrus orchards. J Huazhong Agricul Univ, 2022, 41: 9-19

[25] Wu K, Hu C, Wang J, Guo J, Sun X, Tan Q, et al. . Comparative effects of different potassium sources on soluble sugars and organic acids in tomato. Sci Hortic, 2023, 308: 111601.

[26] Yu Z, Chen HYH, Searle EB, Sardans J, Ciais P, Peñuelas J, et al. . Whole soil acidification and base cation reduction across subtropical China. Geoderma, 2020, 361,

[27] Zeng M, de Vries W, Bonten LTC, Zhu Q, Hao T, Liu X, et al. . Model-based analysis of the long-term effects of fertilization management on cropland soil acidification. Environ Sci Technol, 2017, 51: 3843-3851.

[28] Zhang Y, Hu C, Tan Q, Hu S, Zheng C, Zeng W, et al. . Effects of liming on nutrition status, quality of satsuma mandarin and acid soil nutrients availability of citrus orchard. J Huazhong Agric Univ, 2014, 33: 72-76

[29] Zhang Y, Hu C, Tan Q, Nie Z, Zheng C, Gui H, et al. . Soil application of boron and zinc influence fruit yield and quality of Satsuma Mandarin in acidic soils. Agron J, 2015, 107: 1-8.

[30] Zheng CS, Lan X, Tan QL, Zhang Y, Gui HP, Hu CX. Soil application of calcium and magnesium fertilizer influences the fruit pulp mastication characteristics of Nanfeng tangerine (Citrus reticulata Blanco cv. Kinokuni). Sci Hortic., 2015, 191: 121-6.

[31] Zhou Y, He W, Zheng W, Tan Q, Xie Z, Zheng C, et al. . Fruit sugar and organic acid were significantly related to fruit Mg of six citrus cultivars. Food Chem, 2018, 259: 278-285.

Funding

the Modern Citrus Industry Technology System of China,(CARS-26)