Phosphorus alleviates aluminum toxicity in Camellia oleifera seedlings by regulating the leaf metabolic profile: Insights from metabolomics

Abstract

Camellia oleifera Abel, recognized as one of the world’s four major woody edible oil sources, is extensively cultivated in the acidic red soil regions in southern China. This study focused on C. oleifera seedlings to investigate the mechanisms through which phosphorus (P) mitigates aluminum (Al) toxicity. The seedlings were subjected to various P-Al solutions at different concentration ratios, and a metabolomic analysis of their leaves was then conducted. The analysis identified a total of 509 metabolites, predominantly flavonoids and tannins. Among these, 466 flavonoids showed significant increases across all comparison groups, whereas 35 differentially abundant metabolites were consistently detected. Kyoto Encyclopedia of Genes and Genomes functional annotation and enrichment analysis highlighted the isoflavone biosynthesis pathway as the most significantly enriched pathway among the differentially abundant metabolites. Key metabolites identified as significantly differentially abundant included glycitin, naringenin, and 3,9-dihydroxypterocarpan. This research elucidates the metabolic alterations in C. oleifera seedlings under P and Al stress, suggesting that changes in flavonoid metabolites and the activation of the isoflavone biosynthesis pathway may be crucial adaptive strategies for C. oleifera to withstand such stresses. The findings not only offer a theoretical foundation for enhancing plant stress resistance but also provide valuable insights into the cultivation and management practices of C. oleifera.

Keywords

Camellia oleifera / Aluminum toxicity / Phosphorus / Flavonoids / Metabolomic

Funding

This research was supported by Fujian Key Laboratory of Plant Nutrition and Fertilizer, grant number 2023PNFKL21.

Conflict of interest

The authors declare they have no competing interests.

References

[1] Delhaize E, Ryan PR. Aluminum toxicity and tolerance in plants. Plant Physiol. 1995; 107(2):315. doi: 10.1104/pp.107.2.315

[2] Liu H, Zhu R, Shu K, Lv W, Wang S, Wang C. Aluminum stress signaling, response, and adaptive mechanisms in plants. Plant Signal Behav. 2022; 17(1):2057060. doi: 10.1080/15592324.2022.2057060

[3] Zhang X, Long Y, Huang J, Xia J. Molecular mechanisms for coping with Al toxicity in plants. Int J Mol Sci. 2019; 20(7):1551. doi: 10.3390/ijms20071551

[4] Kouki R, Ayachi R, Ferreira R, Sleimi N. Behavior of Cucumis sativus L. in presence of aluminum stress: Germination, plant growth, and antioxidant enzymes. Food Sci Nutr. 2021; 9(6):3280-3288. doi: 10.1002/fsn3.2294

[5] Ma L, Yang S. Growth and physiological response of Kandelia obovata and Bruguiera sexangula seedlings to aluminum stress. Environ Sci Pollut Res. 2022; 29(28):43251-43266. doi: 10.1007/s11356-021-17926-0

[6] Raza S, Zamanian K, Ullah S, Kuzyakov Y, Virto I, Zhou J. Inorganic carbon losses by soil acidification jeopardize global efforts on carbon sequestration and climate change mitigation. J Clean Prod. 2021; 315:128036. doi: 10.1016/j.jclepro.2021.128036

[7] von Uexküll HR, Mutert E. Global extent, development and economic impact of acid soils. Plant Soil. 1995; 171(1):1-15. doi: 10.1007/BF00009558

[8] Chauhan DK, Yadav V, Vaculík M, et al. Aluminum toxicity and aluminum stress-induced physiological tolerance responses in higher plants. Crit Rev Biotechnol. 2021; 41(5):715-730. doi: 10.1080/07388551.2021.1874282

[9] Hajiboland R, Panda CK, Lastochkina O, Gavassi MA, Habermann G, Pereira JF. Aluminum toxicity in plants: Present and future. J Plant Growth Regul. 2023; 42(7):3967-3999. doi: 10.1007/s00344-022-10866-0

[10] Kopittke PM, Moore KL, Lombi E, et al. Identification of the primary lesion of toxic aluminum in plant roots. Plant Physiol. 2015; 167(4):1402-1411. doi: 10.1104/pp.114.253229

[11] Kochian LV, Hoekenga OA, Piñeros MA. How do crop plants tolerate acid soils? mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol. 2004; 55:459-493. doi: 10.1146/annurev.arplant.55.031903.141655

[12] Cao Y, Lim E, Xu M, Weng J, Marelli B. Precision delivery of multiscale payloads to tissue-specific targets in plants. Adv Sci. 2020; 7(13):1903551. doi: 10.1002/advs.201903551

[13] Yu Y, Dong J, Li R, et al. Sodium hydrosulfide alleviates aluminum toxicity in Brassica napus through maintaining H2S, ROS homeostasis and enhancing aluminum exclusion. Sci Total Environ. 2023; 858:160073. doi: 10.1016/j.scitotenv.2022.160073

[14] Khan MN, Li Y, Mu Y, et al. Recent advances in nano-enabled plant salt tolerance: Methods of application, risk assessment, opportunities and future prospects. J Integr Agric. 2025; 24(5):1611-1630. doi: 10.1016/j.jia.2024.05.028

[15] Wang P, Dong Y, Zhu L, et al. The role of γ-aminobutyric acid in aluminum stress tolerance in a woody plant, Liriodendron chinense × tulipifera. Hortic Res. 2021; 8:80. doi: 10.1038/s41438-021-00517-y

[16] Liu C, Cheng H, Wang S, Yu D, Wei Y. Physiological and transcriptomic analysis reveals that melatonin alleviates aluminum toxicity in alfalfa (Medicago sativa L.). Int J Mol Sci. 2023; 24(24):17221. doi: 10.3390/ijms242417221

[17] Dissanayaka DMSB, Ghahremani M, Siebers M, Wasaki J, Plaxton WC. Recent insights into the metabolic adaptations of phosphorus-deprived plants. J Exp Bot. 2021; 72(2):199-223. doi: 10.1093/jxb/eraa482

[18] Qu X, Zhou J, Masabni J, Yuan J. Phosphorus relieves aluminum toxicity in oil tea seedlings by regulating the metabolic profiling in the roots. Plant Physiol Biochem. 2020; 152:12-22. doi: 10.1016/j.plaphy.2020.04.030

[19] Mwende Muindi E.Understanding soil phosphorus. Int J Plant Soil Sci. 2019; 31(2):1-18. doi: 10.9734/ijpss/2019/v31i230208

[20] Ofoe R, Thomas RH, Asiedu SK, Wang-Pruski G, Fofana B, Abbey L. Aluminum in plant: Benefits, toxicity and tolerance mechanisms. Front Plant Sci. 2023; 13:1085998. doi: 10.3389/fpls.2022.1085998

[21] Sun QB, Shen RF, Zhao XQ, Chen RF, Dong XY. Phosphorus enhances Al resistance in Al-resistant Lespedeza bicolor but not in Al-sensitive L. cuneata under relatively high Al stress. Ann Bot. 2008; 102(5):795-804. doi: 10.1093/aob/mcn166

[22] Liu B, Luo C, Li X, et al. Research on the threshold of aluminum toxicity and the alleviation effects of exogenous calcium, phosphorus, and nitrogen on the growth of Chinese fir seedlings under aluminum stress. Commun Soil Sci Plant Anal. 2014; 45(1):126-139. doi: 10.1080/00103624.2013.841917

[23] He G, Zhang J, Hu X, Wu J.Effect of aluminum toxicity and phosphorus deficiency on the growth and photosynthesis of oil tea (Camellia oleifera Abel.) seedlings in acidic red soils. Acta Physiol Plant. 2011; 33:1285-1292. doi: 10.1007/s11738-010-0659-7

[24] Wang Y, Cheng J, Wei S, et al. Metabolomic study of flavonoids in Camellia drupifera under aluminum stress by UPLC-MS/MS. Plants. 2023; 12(7):1432. doi: 10.3390/plants12071432

[25] Luo D, Li Q, Pang F, et al. Commonalities and specificities in wheat (Triticum aestivum L.) responses to aluminum toxicity and low phosphorus revealed by transcriptomics and targeted metabolomics. Int J Mol Sci. 2024; 25(17):9273. doi: 10.3390/ijms25179273

[26] Xia Y, Yu J, Miao W, Shuang Q. A UPLC-Q-TOF-MS-based metabolomics approach for the evaluation of fermented mare’s milk to koumiss. Food Chem. 2020; 320:126619. doi: 10.1016/j.foodchem.2020.126619

[27] Wang Y, Cheng J, Jiang W, Chen S. Metabolomics study of flavonoids in Coreopsis tinctoria of different origins by UPLC-MS/MS. PeerJ. 2022; 10:e14580. doi: 10.7717/peerj.14580

[28] Chu Z, Xiong R, Peng X, Cui G, Dong L, Li W. Delineating molecular regulatory of flavonoids indicated by transcriptomic and metabolomics analysis during flower development in Chrysanthemum morifolium “Boju.” Int J Mol Sci. 2024; 25(19):10261. doi: 10.3390/ijms251910261

[29] Jackson ML. Aluminum bonding in soils: A unifying principle in soil science. Soil Sci Soc Amer J. 1963; 27(1):1-10. doi: 10.2136/sssaj1963.03615995002700010008x

[30] Santos FCVD, Dores ALDM, Barbalho MGDS. Chemical attributes as indicators of soil quality when applied to the cerrado biome: A literature review. In: Águas e Florestas: Desafios Para Conservação e Utilização. 1st ed. Brasil: Editora Científica Digital; 2021. p. 131-148. doi: 10.37885/210404155

[31] Mierziak J, Kostyn K, Kulma A. Flavonoids as important molecules of plant interactions with the environment. Molecules. 2014; 19(10):16240-16265. doi: 10.3390/molecules191016240

[32] Samanta A, Das G, Das S. Roles of flavonoids in plants. Int J Pharm Sci Technol. 2011; 6:12-35.

[33] Baskar V, Venkatesh R, Ramalingam S. Flavonoids (antioxidants systems) in higher plants and their response to stresses. In: Gupta DK, Palma JM, Corpas FJ,editors. Antioxidants and Antioxidant Enzymes in Higher Plants. Berlin: Springer International Publishing; 2018. p. 253-268. doi: 10.1007/978-3-319-75088-0_12

[34] Luo D, Li Q, Pang F, et al. Exploration of the commonalities and specificities in wheat respond to aluminum toxicity and low phosphorus via transcriptomics and targeted metabolomics study. Int J Mol Sci. 2024; 25:9273. doi: 10.20944/preprints202408.0689.v1

[35] Ma D, Guo Y, Ali I, Lin J, Xu Y, Yang M. Accumulation characteristics of plant flavonoids and effects of cultivation measures on their biosynthesis: A review. Plant Physiol Biochem. 2024; 215:108960. doi: 10.1016/j.plaphy.2024.108960

[36] Shen N, Wang T, Gan Q, Liu S, Wang L, Jin B. Plant flavonoids: Classification, distribution, biosynthesis, and antioxidant activity. Food Chem. 2022; 383:132531. doi: 10.1016/j.foodchem.2022.132531

[37] Shomali A, Das S, Arif N, et al. Diverse physiological roles of flavonoids in plant environmental stress responses and tolerance. Plants (Basel). 2022; 11(22):3158. doi: 10.3390/plants11223158

[38] Harborne JB, Williams CA. Advances in flavonoid research since 1992. Phytochemistry. 2000; 55(6):481-504. doi: 10.1016/S0031-9422(00)00235-1

[39] Zhou Y, Olt P, Neuhäuser B, et al. Loss of LaMATE impairs isoflavonoid release from cluster roots of phosphorus-deficient white lupin. Physiol Plant. 2021; 173(3):1207-1220. doi: 10.1111/ppl.13515

[40] Chandra J, Keshavkant S. Mechanisms underlying the phytotoxicity and genotoxicity of aluminum and their alleviation strategies: A review. Chemosphere. 2021; 278:130384. doi: 10.1016/j.chemosphere.2021.130384

[41] Lin ZH, Chen LS, Chen RB, et al. Root release and metabolism of organic acids in tea plants in response to phosphorus supply. J Plant Physiol. 2011; 168(7):644-652. doi: 10.1016/j.jplph.2010.09.017

[42] Luo J, Liu Y, Zhang H, et al. Metabolic alterations provide insights into Stylosanthes roots responding to phosphorus deficiency. BMC Plant Biol. 2020; 20(1):85. doi: 10.1186/s12870-020-2283-z

[43] Saddique M, Kamran M, Shahbaz M. Differential responses of plants to biotic stress and the role of metabolites. In: Ahmad P, Ahanger MA, Singh VP, Tripathi DK, Alam P, Alyemeni MN,editors. Plant Metabolites and Regulation Under Environmental Stress. Ch. 4. United States: Academic Press; 2018. p. 69-87. doi: 10.1016/B978-0-12-812689-9.00004-2

[44] Lephatsi M, Nephali L, Meyer V, et al. Molecular mechanisms associated with microbial biostimulant-mediated growth enhancement, priming and drought stress tolerance in maize plants. Sci Rep. 2022; 12(1):10450. doi: 10.1038/s41598-022-14570-7

[45] Deng J, Qin W, Yang C, et al. Seed quality deterioration dynamics for isoflavones biosynthesis in soybean (Glycine max L. Merr.) seeds against field mildew stress. Acta Physiol Plant. 2019; 41(5):57. doi: 10.1007/s11738-019-2845-6

[46] Trush K, Pal’ove-Balang P. Biosynthesis and role of isoflavonoids in legumes under different environmental conditions. Plant Stress. 2023; 8:100153. doi: 10.1016/j.stress.2023.100153

[47] Woźniak A, Drzewiecka K, Kęsy J, et al. The influence of lead on generation of signalling molecules and accumulation of flavonoids in pea seedlings in response to pea aphid infestation. Molecules. 2017; 22(9):1404. doi: 10.3390/molecules22091404

[48] Kochian LV, Piñeros MA, Liu J, Magalhaes JV. Plant adaptation to acid soils: The molecular basis for crop aluminum resistance. Annu Rev Plant Biol. 2015; 66(1):571-598. doi: 10.1146/annurev-arplant-043014-114822