Abstract
Aims
Soil metabolites have a great influence on regulating the growth and development of plants and microbes in forest ecosystems. This study aims to reveal the characteristic metabolite profiles and their enriched metabolic pathways in the rhizosphere soil of Masson pine plantations at three different ages.
Method
The rhizosphere soil of Masson pine from 10, 31, and 52 years plantation was collected. The metabolites were analyzed using a soil pseudotargeted metabolomics approach and then the relationships between soil metabolites and chemical properties, enzyme activities were established.
Results
A total of 172 rhizosphere soil metabolites in 26 classes were identified. There was a decreasing trend in the total concentration of rhizosphere soil metabolites with increasing stand age. Seventy-two characteristic metabolites were screened, mainly saccharides, fatty acids, amino acids, phenolic acids, polyols and terpenoids. Among them, benzoic acid and galactonic acid contributed the most to the young forest, and stearic acid had the greatest influence on the near-mature forest plantation. Erythritol had great effects on the mature forest plantation. Seven metabolic pathways changed with increasing stand age. Correlation analysis showed that available potassium (AK) and soil alkaline protease (S-ALPT) were significantly positively correlated with phenolic acids, polyhydroxy carboxylic acids, etc.
Conclusion
The rhizosphere soil of Masson pine had different metabolite profiles at different developmental stages, and the soil nutrient pools were effectively improved. These results provide a reference for plantation management in Masson pine and a deeper understanding of forest metabolic characteristics.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-023-06378-9/MediaObjects/11104_2023_6378_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-023-06378-9/MediaObjects/11104_2023_6378_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-023-06378-9/MediaObjects/11104_2023_6378_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-023-06378-9/MediaObjects/11104_2023_6378_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-023-06378-9/MediaObjects/11104_2023_6378_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-023-06378-9/MediaObjects/11104_2023_6378_Fig6_HTML.png)
Similar content being viewed by others
Data availability
The datasets used during the current study are available from the corresponding author on reasonable request.
References
Alkorta I, Aizpurua A, Riga P, Albizu I, Amézaga I, Garbisu C (2003) Soil enzyme activities as biological indicators of soil health. Rev Environ Health 18:65–73. https://doi.org/10.1515/REVEH.2003.18.1.65
Bai Y, Chen QH, Zhou YP, Fang X, Liu XM (2020) Terpenoids in surface soils from different ecosystems on the Tibetan Plateau. Org Geochem 150:104125. https://doi.org/10.1016/j.orggeochem.2020.104125
Bai YX, Zhou YC, Gong JF (2021) Physiological mechanisms of the tolerance response to manganese stress exhibited by Pinusmassoniana, a candidate plant for the phytoremediation of Mn-contaminated soil. Environ Sci Pollut Res 28:45422–45433. https://doi.org/10.1007/s11356-021-13912-8
Berhin A, de Bellis D, Franke RB, Buono RA, Nowack MK, Nawrath C (2019) The root cap cuticle: a cell wall structure for seedling establishment and lateral root formation. Cell 176:1367–1378. https://doi.org/10.1016/j.cell.2019.01.005
Bi BY, Yuan Y, Zhang H, Wu ZH, Wang Y, Han FP (2022) Rhizosphere soil metabolites mediated microbial community changes of Pinus sylvestris var. Mongolica across stand ages in the mu Us Desert. Appl Soil Ecol 169:104222. https://doi.org/10.1016/j.apsoil.2021.104222
Brown RW, Chadwick DR, Zang H, Jones DL (2021) Use of metabolomics to quantify changes in soil microbial function in response to fertiliser nitrogen supply and extreme drought. Soil Boil Biochem 160:10835. https://doi.org/10.1016/j.soilbio.2021.108351
Cai K, Zhao Y, Kang Z, Ma R, Wright AL, Jiang X (2022) Pyrolysis-assisted transesterification for accurate quantification of phospholipid fatty acids: Application to microbial community analysis in 1000-years paddy soil chronosequence. Geoderma 406:115504. https://doi.org/10.1016/j.geoderma.2021.115504
Cai K, Zhao Y, Kang Z, Wang S, Wright AL, Jiang X (2023) Environmental pseudotargeted metabolomics: A high throughput and wide coverage method for metabolic profiling of 1000-year paddy soil chronosequences. Sci Total Environ 858:159978. https://doi.org/10.1016/j.scitotenv.2022.159978
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157. https://doi.org/10.3389/fpls.2019.00157
D’Amelia L, Dell’Aversana E, Woodrow P, Ciarmiello LF, Carillo P (2018) Metabolomics for crop improvement against salinity stress. In: Kumar V, Wani SH, Suprasanna P,Tran LS (eds) Salinity Responses and Tolerance in Plants, vol 2. Springer, Cham. pp 267–287. https://doi.org/10.1007/978-3-319-90318-711
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Das A, Rushton PJ, Rohila JS (2017) Metabolomic profiling of soybeans (Glycine max L.) reveals the importance of sugar and nitrogen metabolism under drought and heat stress. Plants 6:21. https://doi.org/10.3390/plants6020021
Fang X, Christenson LM, Wang F, Zeng J, Chen F (2016) Pine caterpillar outbreak and stand density impacts on nitrogen and phosphorus dynamics and their stoichiometry in Masson pine (Pinusmassoniana) plantations in subtropical China. Can J Forest Res 46:601–609. https://doi.org/10.1139/cjfr-2015-0357
Feduraev P, Skrypnik L, Riabova A, Pungin A, Tokupova E, Maslennikov P, Chupakhina G (2020) Phenylalanine and tyrosine as exogenous precursors of wheat (Triticum aestivum L.) secondary metabolism through PAL-associated pathways. Plants 9:476. https://doi.org/10.3390/plants9040476
Figas A, Siwik-Ziomek A, Kobierski M (2021) Heavy metals and sulphur in needles of Pinus sylvestris L. and soil in the forests of city agglomeration. Forests 12:1310. https://doi.org/10.3390/f12101310
Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358. https://doi.org/10.1093/jxb/erm121
Fujii K, Aoki M, Kitayama K (2012) Biodegradation of low molecular weight organic acids in rhizosphere soils from a tropical montane rain forest. Soil Boil Biochem 47:142–148. https://doi.org/10.1016/j.soilbio.2011.12.018
Ge XG, Zeng LX, Xiao WF, Huang ZL, Geng XS, Tan BW (2013) Effect of litter substrate quality and soil nutrients on forest litter decomposition: A review. Acta Ecol Sin 33:102–108. https://doi.org/10.1016/j.chnaes.2013.01.006
Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100. https://doi.org/10.1016/j.soilbio.2015.07.021
Hao L, Hsiang T, Goodwin PH (2006) Role of two cysteine proteinases in the susceptible response of Nicotiana benthamiana to Colletotrichum destructivum and the hypersensitive response to Pseudomonas syringaepv. tomato. Plant Sci 170:1001–1009. https://doi.org/10.1016/j.plantsci.2006.01.011
Hussein RA, El-Anssary AA (2019) Plants secondary metabolites: the key drivers of the pharmacological actions of medicinal plants. J Herb Med 1:3. https://doi.org/10.5772/intechopen.76139
Jain C, Khatana S, Vijayvergia R (2019) Bioactivity of secondary metabolites of various plants: a review. Int J Pharm Sci Res 10:494–504. https://doi.org/10.13040/IJPSR.0975-8232.10(2).494-04
Jenkins S, Swenson TL, Lau R, Rocha AM, Aaring A, Hazen TC, Northen TR (2017) Construction of viable soil defined media using quantitative metabolomics analysis of soil metabolites. Front Microbiol 8:2618. https://doi.org/10.3389/fmicb.2017.02618
Jorge TF, Mata AT, António C (2016) Mass spectrometry as a quantitative tool in plant metabolomics. Philos Trans Royal Soc A 374:20150370. https://doi.org/10.1098/rsta.0370
Li J, Zhou LJ, Lin WF (2019) Calla lily intercropping in rubber tree plantations changes the nutrient content, microbial abundance, and enzyme activity of both rhizosphere and non-rhizosphere soil and calla lily growth. Ind Crops Prod 132:344–351. https://doi.org/10.1016/j.indcrop.2019.02.045
Liu XL, Zhao N, Jia YY (2020) The role of phenolic acids in plant-soil-environment system. Hortic & Seeds 40:56–58
Lu M, Wei J, Han ZL (2011) Soil microbes and enzyme activities in four types of coniferous forests in West Bank of Dianchi lake, Kunming. J Northeast For Univ 39:56–59
Luo J (2015) Metabolite-based genome-wide association studies in plants. Curr Opin Plant Biol 24:31–38. https://doi.org/10.1016/j.pbi.2015.01.006
McNeal KS, Herbert BE (2009) Volatile organic metabolites as indicators of soil microbial activity and community composition shifts. Soil Sci Soc Am J 73:579–588. https://doi.org/10.2136/sssaj2007.0245
Meng XY (2006) Forest Mensuration, 3rd edn. China Forestry Publishing House, Beijing, pp 28–48. https://doi.org/10.13140/2.1.1880.0325
Mishra UN, Reddy MV, Prasad DT (2020) Plant serine protease inhibitor (SPI): A potent player with bactericidal, fungicidal, nematicidal and antiviral properties. Int J Chem Stud 8:2985–2993. https://doi.org/10.22271/chemi.2020.v8.i1at.8724
Munyai R, Raletsena MV, Modise DM (2022) LC-MS Based Metabolomics Analysis of Potato (Solanum tuberosum L.) Cultivars Irrigated with Quicklime Treated Acid Mine Drainage Water. Metabolites 12(3):221. https://doi.org/10.3390/metabo12030221
Palsson B (2000) The challenges of in silico biology. Nat Biotechnol 18:1147–1150. https://doi.org/10.1038/81125
Pan JW, Guo QQ, Li HE, Luo SQ, Zhang YQ, Yao S, Fan X, Sun XG, Qi YJ (2021) Dynamics of soil nutrients, microbial community structure, enzymatic activity, and their relationships along a chronosequence of Pinusmassoniana plantations. Forests 12:376. https://doi.org/10.3390/f12030376
Papadimitropoulos MEP, Vasilopoulou CG, Maga-Nteve C, Klapa MI (2018) Untargeted GC-MS Metabolomics. Metab Eng 1738:133–147. https://doi.org/10.1007/978-1-4939-7643-09
Schuster S, Fell DA, Dandekar T (2000) A general definition of metabolic pathways useful for systematic organization and analysis of complex metabolic networks. Nat Biotechnol 18:326–332. https://doi.org/10.1038/73786
Singh K, Chandra R, Purchase D (2022) Unraveling the secrets of rhizobacteria signaling in rhizosphere. Rhizosphere 21:100484. https://doi.org/10.1016/j.rhisph.2022.100484
Sobucki L, Ramos RF, Meireles LA, Antoniolli ZI, Jacques RJS (2021) Contribution of enzymes to soil quality and the evolution of research in Brazil. Rev Bras Ciência do Solo 45:e0210109. https://doi.org/10.36783/18069657rbcs20210109
Su YW, Wang J, Gao WY, Wang RB, Yang WQ, Zhang HY, Huang LQ, Guo LP (2023) Dynamic metabolites: A bridge between plants and microbes. Sci Total Environ 899:165612. https://doi.org/10.1016/j.scitotenv.2023.165612
Tang S, Ma Q, Zhou J, Pan W, Chadwick DR, Gregory AS, Jones DL (2023) Use of untargeted metabolomics to analyse changes in extractable soil organic matter in response to long-term fertilisation. Biol Fertil Soils 59:301–316. https://doi.org/10.1007/s00374-023-01706-8
Vogt DJ, Tilley JP, Edmonds RL (2015) Soil and Plant Analysis for Forest Ecosystem Characterization. In Ecosystem Science and Applications; Higher Education Press, Berlin, Germany, pp 17–168. https://doi.org/10.1515/9783110290479
Wang Y, Wang YC, Wang YM (2020) Apoplastic proteases: powerful weapons against pathogen infection in plants. Plant Commun 1:100085. https://doi.org/10.1016/j.xplc.2020.100085
Wang P, Zhou SJ, Li A, Xie LB (2022) Influence of aluminum at low pH on the rhizosphere processes of Masson pine (Pinusmassoniana Lamb). Plant Growth Regul 97:499–510. https://doi.org/10.1007/s10725-022-00816-x
Wu HL, Xiang WH, Ouyang SA, Xiao WF, Li SG, Chen L, Lei PF, Deng XW, Zeng YL, Zeng LX, Peng CH (2020) Tree growth rate and soil nutrient status determine the shift in nutrient-use strategy of Chinese fir plantations along a chronosequence. For Ecol Manage 460:117896. https://doi.org/10.1016/j.foreco.2020.117896
Xu H, Gao X, Yu C (2021) Physiological and transcriptomic analysis of Pinusmassoniana seedling response to osmotic stress. Biol Plant 65:145–156. https://doi.org/10.32615/bp.2021.016
Yang YH, Xu J, Li Y, He YC, Yang YQ, Liu DL, Wu CX (2023) Effects of Coumarin on Rhizosphere Microbiome and Metabolome of Lolium multiflorum. Plants 12:1096. https://doi.org/10.3390/plants12051096
Yu PY, Sun YP, Huang ZL, Zhu F, Sun YJ, Jiang LJ (2020) The effects of ectomycorrhizal fungi on heavy metals’transport in Pinusmassoniana and bacteria community in rhizosphere soil in mine tailing area. J Hazard Mater 381:121203. https://doi.org/10.1016/j.jhazmat.2019.121203
Zechmann B (2020) Subcellular roles of glutathione in mediating plant defense during biotic stress. Plants 9:1067. https://doi.org/10.3390/plants9091067
Zhang J, Zhang DJ, Jian Z, Zhou HY, Zhao YB, Wei DP (2019) Litter decomposition and the degradation of recalcitrant components in Pinusmassoniana plantations with various canopy densities. J For Res (harbin) 30:1395–1405. https://doi.org/10.1007/s11676-018-0715-5
Zhang KX, Gao DL, Guo H, Zeng J, Liu XZ (2022a) Forest structure characteristics on soil carbon and nitrogen storage of Pinusmassoniana plantations in southern subtropic region. Front For Global Change 5:1022221. https://doi.org/10.3389/ffgc.2022.1022221
Zhang M, Jin BJ, Bi QF, Li KJ, Sun CL, Lin XY, Zhu YG (2022b) Variations of earthworm gut bacterial community composition and metabolic functions in coastal upland soil along a 700-year reclamation chronosequence. Sci Total Environ 804:149994. https://doi.org/10.1016/j.scitotenv.2021.149994
Zhou XG, Yu GB, Wu FZ (2012) Responses of soil microbial communities in the rhizosphere of cucumber (Cucumissativus L.) to exogenously applied p-hydroxybenzoic acid. J Chem Ecol 38:975–983. https://doi.org/10.1007/s10886-012-0156-0
Zhou SJ, Zhang M, Chen SZ, Xu W, Zhu LT, Gong SR, He XQ, Wang P (2020) Acid resistance of Masson pine (Pinus massoniana Lamb.) families and their root morphology and physiological response to simulated acid deposition. Sci Rep 10:22066. https://doi.org/10.1038/s41598-020-79043-1
Funding
This work was supported by [the National Natural Science Foundation of China] (31960301), [the Postdoctoral Research Foundation of China] (2020M673583XB), [the Science and Technology Planning Project of Guizhou Province] (QKHPTRC[2018]5261 and QKHPTRC[2019]5102), [the Science and Technology Project of Guizhou Provincial Branch of the CNTC] (2023XM16) and [the Key Program for Science and Technology of CNTC] (110202202030), [the Young Elite Scientists Sponsorship Program of CNTC].
Author information
Authors and Affiliations
Contributions
Shuyue Qin: Methodology, Conceptualization, Data curation, Investigation, Formal analysis, Writing-Original draft preparation; Weichang Gao: Visualization, Validation; Yuan Jing: Investigation, Data curation; Wenxuan Quan: Investigation, Reviewing & Editing, Funding acquisition; Kai Cai: Writing, Conceptualization, Writing Reviewing, Supervision, Funding acquisition. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Responsible Editor: Mian Gu.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Appendix
ESM 1
(DOCX 4.08 MB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Qin, S., Gao, W., Jing, Y. et al. Soil pseudotargeted metabolomics reveals that planting years of masson pine (Pinus massoniana) affect soil metabolite profiles and metabolic pathways. Plant Soil 496, 505–520 (2024). https://doi.org/10.1007/s11104-023-06378-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06378-9