Plant–soil feedback alters plant–soil–microbial nutrient status and elemental-limitation status during secondary succession

Yong Cao , Zemin Ai , Xinghua Li , Mengjia Hou , Yuyan Yao , Yi Deng , Huan Liu , Jiaoyang Zhang , Guobin Liu , Sha Xue

Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (4) : 250335

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Soil Ecology Letters ›› 2025, Vol. 7 ›› Issue (4) : 250335 DOI: 10.1007/s42832-025-0335-x
RESEARCH ARTICLE

Plant–soil feedback alters plant–soil–microbial nutrient status and elemental-limitation status during secondary succession

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Abstract

The response of plant−soil−microbial nutrients and stoichiometry to plant−soil feedback (PSF) during secondary succession (SS) is an important driver of plant−community recovery. However, the plant−soil−microbe responses to PSFduring SS are unknown. The effects of PSF on plants at different successionalstages and successional soils regulated by these plants were tested in this study by potting experiments. Results indicated that soils conditioned by Setaria viridis (EarlySoil) and soils conditioned by Artemisia sacrorum (MidSoil) feedback significantly increased the potassium content of Artemisia sacrorum (MidSp) and Bothriochloa ischaemum (LateSp), respectively. MidSp and Setaria viridis (EarlySp) aboveground carbon, nitrogen, and phosphorus contents were promoted by soils conditioned by Bothriochloa ischaemum (LateSoil) and MidSoil, respectively, but provided negative feedbacks on below-ground carbon and phosphorus. The EarlySp and MidSp significantly increased other nutrients in the MidSoil and LateSoil except water-soluble nutrients, the LateSp and MidSp significantly increased the soil nutrients in the MidSoil and EarlySoil, and the MidSp significantly increased their enzyme activity most significantly. Despite the significant impact of PSF on plant stoichiometry, reducing the intensity of phosphorus limitation, plant growth was always phosphorus limited. PSF changed the nitrogen limit of microorganisms, but microorganisms were always limited by phosphorus. Soil physicochemical properties and microbial abundance regulated by MidSp (or EarlySp) were facilitated by LateSp (or MidSp), which ultimately accelerated the SS process. This confirmed the irreversibility of SS and provided new information on plant-soil-microbe dynamics during SS.

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Keywords

Loess Plateau / secondary succession / plant−soil feedback / ecological stoichiometry / nutrient usage strategies / element restriction status

Highlight

● LateSoil feedback will change EarlySp and MidSp nutrient utilization strategies.

● LateSp plant feedback will change the N restriction of microorganisms.

● The intensity of plant P limitation diminishes with succession.

● Enzyme activity more significantly affects plant nutrients than soil nutrients.

● N and P remain major influences on vegetation growth after PSF impacts.

● MidSp and LateSp are more affected by soil water-soluble and fast-acting nutrients.

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Yong Cao, Zemin Ai, Xinghua Li, Mengjia Hou, Yuyan Yao, Yi Deng, Huan Liu, Jiaoyang Zhang, Guobin Liu, Sha Xue. Plant–soil feedback alters plant–soil–microbial nutrient status and elemental-limitation status during secondary succession. Soil Ecology Letters, 2025, 7(4): 250335 DOI:10.1007/s42832-025-0335-x

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References

[1]

Ai, Z.M., Deng, Y., Li, X.H., Zhang, J.Y., Liu, H.F., Xu, H.W., Liu, G.B., Sha, X., 2023a. Effect of plant-soil feedback on soil microbial co-occurrence network depends on the stage of secondary succession. Rhizosphere27, 100733.

[2]

Ai, Z.M., Li, J.Y., Li, X.H., Zhang, J.Y., Liu, H.F., Xu, H.W., Liu, G.B., Xue, S., 2023b. Plant traits variably respond to plant–soil interactions during secondary succession on the Loess Plateau. Forests14, 726.

[3]

Aristidou, N., Eames, C., Sanchez-Molina, I., Bu, X.N., Kosco, J., Islam, M.S., Haque, S.A., 2017. Fast oxygen diffusion and iodide defects mediate oxygen-induced degradation of perovskite solar cells. Nature Communications8, 15218.

[4]

Badri, D.V., Vivanco, J.M., 2009. Regulation and function of root exudates. Plant, Cell & Environment32, 666–681.

[5]

Bai, X.J., Wang, B.R., An, S.S., Zeng, Q.C., Zhang, H.X., 2019. Response of forest species to C:N:P in the plant-litter-soil system and stoichiometric homeostasis of plant tissues during afforestation on the Loess Plateau, China. CATENA183, 104186.

[6]

Batterman, S.A., Hedin, L.O., Van Breugel, M., Ransijn, J., Craven, D.J., Hall, J.S., 2013. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature502, 224–227.

[7]

Bell, C., Carrillo, Y., Boot, C.M., Rocca, J.D., Pendall, E., Wallenstein, M.D., 2014. Rhizosphere stoichiometry: are C:N:P ratios of plants, soils, and enzymes conserved at the plant species-level. New Phytologist201, 505–517.

[8]

Berendsen, R.L., Pieterse, C.M.J., Bakker, P.A.H.M., 2012. The rhizosphere microbiome and plant health. Trends in Plant Science17, 478–486.

[9]

Bezemer, T.M., Fountain, M.T., Barea, J.M., Christensen, S., Dekker, S.C., Duyts, H., van Hal, R., Harvey, J.A., Hedlund, K., Maraun, M., Mikola, J., Mladenov, A.G., Robin, C., de Ruiter, P.C., Scheu, S., Setälä, H., Šmilauer, P., van der Putten, W.H., 2010. Divergent composition but similar function of soil food webs of individual plants: plant species and community effects. Ecology91, 3027–3036.

[10]

Bremner, J.M., Mulvaney, C.S., 1982. Nitrogen—total. In: Page, A.L., ed. Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties. American Society of Agronomy, Inc., Soil Science Society of America, Inc.595–624.

[11]

Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology and Biochemistry17, 837–842.

[12]

Burns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E., Wallenstein, M.D., Weintraub, M.N., Zoppini, A., 2013. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology and Biochemistry58, 216–234.

[13]

Castle, S.C., Lekberg, Y., Affleck, D., Cleveland, C.C., 2016. Soil abiotic and biotic controls on plant performance during primary succession in a glacial landscape. Journal of Ecology104, 1555–1565.

[14]

Cordell, D., Drangert, J.O., White, S., 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change19, 292–305.

[15]

De Deyn, G.B., Raaijmakers, C.E., Zoomer, H.R., Berg, M.P., de Ruiter, P.C., Verhoef, H.A., Bezemer, T.M., van der Putten, W.H., 2003. Soil invertebrate fauna enhances grassland succession and diversity. Nature422, 711–713.

[16]

Dominati, E., Patterson, M., Mackay, A., 2010. A framework for classifying and quantifying the natural capital and ecosystem services of soils. Ecological Economics69, 1858–1868.

[17]

Eckstein, R.L., Karlsson, P.S., Weih, M., 1999. Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytologist143, 177–189.

[18]

Fang, Z., Li, D.D., Jiao, F., Yao, J., Du, H.T., 2019. The latitudinal patterns of leaf and soil C:N:P stoichiometry in the Loess Plateau of China. Frontiers in Plant Science10, 85.

[19]

Fornara, D.A., Tilman, D., 2008. Plant functional composition influences rates of soil carbon and nitrogen accumulation. Journal of Ecology96, 314–322.

[20]

Frouz, J., 2024. Plant-soil feedback across spatiotemporal scales from immediate effects to legacy. Soil Biology and Biochemistry189, 109289.

[21]

Fu, B.J., Liu, Y., Lü, Y.H., He, C.S., Zeng, Y., Wu, B.F., 2011. Assessing the soil erosion control service of ecosystems change in the Loess Plateau of China. Ecological Complexity8, 284–293.

[22]

Garcia, C., Roldan, A., Hernandez, T., 2005. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma124, 193–202.

[23]

Gosz, J.R., Likens, G.E., Bormann, F.H., 1973. Nutrient release from decomposing leaf and branch litter in the Hubbard Brook Forest, New Hampshire. Ecological Monographs43, 173–191.

[24]

Güsewell, S., 2004. N: P ratios in terrestrial plants: variation and functional significance. New Phytologist164, 243–266.

[25]

Haynes, R.J., Williams, P.H., 1993. Nutrient cycling and soil fertility in the grazed pasture ecosystem. Advances in Agronomy49, 119–199.

[26]

Hinsinger, P., Gobran, G.R., Gregory, P.J., Wenzel, W.W., 2005. Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist168, 293–303.

[27]

Jia, X.X., Wei, X.R., Shao, M., Li, X.Z., 2012. Distribution of soil carbon and nitrogen along a revegetational succession on the Loess Plateau of China. CATENA95, 160–168.

[28]

Jing, J.Y., Bezemer, T.M., van der Putten, W.H., 2015. Complementarity and selection effects in early and mid-successional plant communities are differentially affected by plant–soil feedback. Journal of Ecology103, 641–647.

[29]

Kardol, P., Cornips, N.J., van Kempen, M.M.L., Bakx-Schotman, J.M.T., van der Putten, W.H., 2007. Microbe-mediated plant–soil feedback causes historical contingency effects in plant community assembly. Ecological Monographs77, 147–162.

[30]

Kardol, P., Martijn Bezemer, T., van der Putten, W.H., 2006. Temporal variation in plant–soil feedback controls succession. Ecology Letters9, 1080–1088.

[31]

Koerselman, W., Meuleman, A.F.M., 1996. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology,33, 1441–1450.

[32]

Koziol, L., Bever, J.D., 2017. The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession. Journal of Applied Ecology54, 1301–1309.

[33]

Kulmatiski, A., Beard, K.H., Stevens, J.R., Cobbold, S.M., 2008. Plant–soil feedbacks: a meta-analytical review. Ecology Letters11, 980–992.

[34]

Kuťáková, E., Herben, T., Münzbergová, Z., 2018. Heterospecific plant–soil feedback and its relationship to plant traits, species relatedness, and co-occurrence in natural communities. Oecologia187, 679–688.

[35]

Kuťáková, E., Mészárošová, L., Baldrian, P., Münzbergová, Z., 2020. Evaluating the role of biotic and chemical components of plant-soil feedback of primary successional plants. Biology and Fertility of Soils56, 345–358.

[36]

Leite, M.F.A., Liu, B.B., Gómez Cardozo, E., Silva, H.R.E., Luz, R.L., Muchavisoy, K.H.M., Moraes, F.H.R., Rousseau, G.X., Kowalchuk, G., Gehring, C., Kuramae, E.E., 2023. Microbiome resilience of Amazonian forests: agroforest divergence to bacteria and secondary forest succession convergence to fungi. Global Change Biology29, 1314–1327.

[37]

Li, F., Shen, K.X., Long, X.L., Wen, J.S., Xie, X.J., Zeng, X.Y., Liang, Y.Y., Wei, Y.S., Lin, Z.F., Huang, W.R., Zhong, R.D., 2016. Preparation and characterization of biochars from Eichor nia crassipes for cadmium removal in aqueous solutions. PLoS One11, e0148132.

[38]

Li, L.H., Chen, J.Q., Han, X.G., Zhang, W.H., Shao, C.L., 2020. Shrubby steppe ecosystem. In: Li, L.H., Chen, J.Q., Han, X.G., Zhang, W.H., Shao, C.L., eds. Grassland Ecosystems of China: A Synthesis and Resume. Singapore: Springer, 339–364.

[39]

Liu, J., Jia, X.Y., Yan, W.M., Zhong, Y.Q.W., Shangguan, Z.P., 2020. Changes in soil microbial community structure during long-term secondary succession. Land Degradation & Development31, 1151–1166.

[40]

Maharning, A.R., Mills, A.A.S., Adl, S.M., 2009. Soil community changes during secondary succession to naturalized grasslands. Applied Soil Ecology41, 137–147.

[41]

Marschner, H., Römheld, V., Cakmak, I., 1987. Root-induced changes of nutrient availability in the rhizosphere. Journal of Plant Nutrition10, 1175–1184.

[42]

McCarthy-Neumann, S., Kobe, R.K., 2010. Conspecific and heterospecific plant–soil feedbacks influence survivorship and growth of temperate tree seedlings. Journal of Ecology98, 408–418.

[43]

Ni, H.J., Su, W.H., Fan, S.H., Chu, H.Y., 2021. Effects of intensive management practices on rhizosphere soil properties, root growth, and nutrient uptake in Moso bamboo plantations in subtropical China. Forest Ecology and Management493, 119083.

[44]

Peacock, A.D., Macnaughton, S.J., Cantu, J.M., Dale, V.H., White, D.C., 2001. Soil microbial biomass and community composition along an anthropogenic disturbance gradient within a long-leaf pine habitat. Ecological Indicators1, 113–121.

[45]

Qu, Q., Xu, H.W., Liu, G.B., Xue, S., 2023. Soil legacy effects and plant–soil feedback contribution to secondary succession processes. Soil Ecology Letters5, 220131.

[46]

Raiesi, F., Salek-Gilani, S., 2018. The potential activity of soil extracellular enzymes as an indicator for ecological restoration of rangeland soils after agricultural abandonment. Applied Soil Ecology126, 140–147.

[47]

Sahu, N., Vasu, D., Sahu, A., Lal, N., Singh, S.K., 2017. Strength of microbes in nutrient cycling: a key to soil health. In: Meena, V.S., Mishra, P.K., Bisht, J.K., Pattanayak, A., eds. Agriculturally Important Microbes for Sustainable Agriculture: Volume I: Plant-Soil-Microbe Nexus. Singapore: Springer69–86.

[48]

Sardans, J., Peñuelas, J., 2012. The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiology160, 1741–1761.

[49]

Schade, J.D., Kyle, M., Hobbie, S.E., Fagan, W.F., Elser, J.J., 2003. Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecology Letters6, 96–101.

[50]

Sun, C.L., Chai, Z.Z., Liu, G.B., Xue, S., 2017. Changes in species diversity patterns and spatial heterogeneity during the secondary succession of grassland vegetation on the Loess Plateau, China. Frontiers in Plant Science8, 1465.

[51]

Tapia-Torres, Y., Elser, J.J., Souza, V., García-Oliva, F., 2015. Ecoenzymatic stoichiometry at the extremes: How microbes cope in an ultra-oligotrophic desert soil. Soil Biology and Biochemistry87, 34–42.

[52]

van der Putten, W.H., Bardgett, R.D., Bever, J.D., Bezemer, T.M., Casper, B.B., Fukami, T., Kardol, P., Klironomos, J.N., Kulmatiski, A., Schweitzer, J.A., Suding, K.N., Van De voorde, T.F.J., Wardle, D.A., 2013. Plant–soil feedbacks: the past, the present and future challenges. Journal of Ecology101, 265–276.

[53]

Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry19, 703–707.

[54]

Vitousek, P.M., Reiners, W.A., 1975. Ecosystem succession and nutrient retention: a hypothesis. Bioscience25, 376–381.

[55]

Walker, L.R., Wardle, D.A., Bardgett, R.D., Clarkson, B.D., 2010. The use of chronosequences in studies of ecological succession and soil development. Journal of Ecology98, 725–736.

[56]

Wallenius, K., Rita, H., Mikkonen, A., Lappi, K., Lindström, K., Hartikainen, H., Raateland, A., Niemi, R.M., 2011. Effects of land use on the level, variation and spatial structure of soil enzyme activities and bacterial communities. Soil Biology and Biochemistry43, 1464–1473.

[57]

Wang, B., Liu, G.B., Xue, S., Zhu, B.B., 2011. Changes in soil physico-chemical and microbiological properties during natural succession on abandoned farmland in the Loess Plateau. Environmental Earth Sciences62, 915–925.

[58]

Wang, C., Mao, Q.G., Mori, T., Huang, J., Mo, H., Mo, J.M., Lu, X.K., 2023. Resource allocation theory reveals sulfur shortage for microbes under phosphorus amendment in tropical forests with divergent land use history. Soil Biology and Biochemistry184, 109126.

[59]

Wang, C.J., Wang, Q.Q., Xu, H., Gao, H.J., Zhu, P., Xu, M.G., Zhang, W.J., 2018. Carbon, nitrogen, and phosphorus stoichiometry characteristics of bulk soil, organic matter, and soil microbial biomass under long-term fertilization in cropland. Acta Ecologica Sinica38, 3848–3858.

[60]

Wubs, E.R.J., Melchers, P.D., Bezemer, T.M., 2018. Potential for synergy in soil inoculation for nature restoration by mixing inocula from different successional stages. Plant and Soil433, 147–156.

[61]

Xiao, L., Liu, G.B., Li, P., Li, Q., Xue, S., 2020. Ecoenzymatic stoichiometry and microbial nutrient limitation during secondary succession of natural grassland on the Loess Plateau, China. Soil and Tillage Research200, 104605.

[62]

Xiao, L., Liu, G.B., Li, P., Xue, S., 2021. Ecological stoichiometry of plant-soil-enzyme interactions drives secondary plant succession in the abandoned grasslands of Loess Plateau, China. CATENA202, 105302.

[63]

Xu, H.W., Qu, Q., Li, G.W., Liu, G.B., Geissen, V., Ritsema, C.J., Xue, S., 2022a. Impact of nitrogen addition on plant-soil-enzyme C–N–P stoichiometry and microbial nutrient limitation. Soil Biology and Biochemistry170, 108714.

[64]

Xu, H.W., Qu, Q., Wang, Z.H., Xue, S., Xu, Z.F., 2022b. Plant-soil-enzyme C-N-P stoichiometry and microbial nutrient limitation responses to plant-soil feedbacks during community succession: a 3-year pot experiment in China. Frontiers in Plant Science13, 1009886.

[65]

Yan, E.R., Wang, X.H., Huang, J.J., 2006. Shifts in plant nutrient use strategies under secondary forest succession. Plant and Soil289, 187–197.

[66]

Zeng, Q.C., Li, X., Dong, Y.H., An, S.S., Darboux, F., 2016. Soil and plant components ecological stoichiometry in four steppe communities in the Loess Plateau of China. CATENA147, 481–488.

[67]

Zhang, C., Liu, G.B., Xue, S., Song, Z.L., 2011. Rhizosphere soil microbial activity under different vegetation types on the Loess Plateau, China. Geoderma161, 115–125.

[68]

Zhang, C., Liu, G.B., Xue, S., Wang, G.L., 2016. Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology and Biochemistry97, 40–49.

[69]

Zhang, J.T., 2005. Succession analysis of plant communities in abandoned croplands in the eastern Loess Plateau of China. Journal of Arid Environments63, 458–474.

[70]

Zhang, J.Y., Ai, Z.M., Xu, H.W., Liu, H.F., Wang, G.L., Deng, L., Liu, G.B., Xue, S., 2021. Plant-microbial feedback in secondary succession of semiarid grasslands. Science of the Total Environment760, 143389.

[71]

Zhang, W., Zhao, J., Pan, F.J., Li, D.J., Chen, H.S., Wang, K.L., 2015. Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in Southwest China. Plant and Soil391, 77–91.

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