The soil sterilization resulted deviation in biological plant-soil feedbacks

Abstract

Direct comparison of the difference in biomass between live and sterilized soils may result in deviations in biological plant-soil feedback (B-PSF) due to changes induced by sterilization in bulk soil microorganisms, soil structure, and nutrient availability. The sterilization-induced deviation (sterilization-effect, SS_c) to often-used method B-PSF_ou was corrected by adding a parallel experiment without conditioning by any plants (B-PSF_c). Plant-soil feedback experiments were conducted for two plants with contrasting in root traits and rhizosphere microbial community to test the reliability of the method (Kalidium foliatum and Reaumuria songaric). The specific root length (SRL), root tissue density (RTD) and of R. songarica was higher compared to that of K. foliatum, but the root diameter (RAD) of it was significantly lower than that of K. foliatum. The plasticity of root traits of K. foliatum was stronger than that of R. songarica. The B-PSF_ou of K. foliatum was four times negative than B-PSF_c, whereas there was no statistically significant difference of B-PSF_ou and B-PSF_c for R. songarica. The correlation between B-PSF_c and the relative abundance of pathogens and EcMF was found to be stronger compared to B-PSF_ou. We proposed method corrects the deviation in B-PSF. The variation of deviation between species may be related to root traits.

Graphical abstract

Keywords

plant soil feedback / biological plant soil feedback / soil sterilization effect / specific root length / root tissue density / plant pathogens

Highlight

	● The often-used calculation formula may result in deviations in biological plant-soil feedback (B-PSF) in sterilized soil.
	● We proposed method corrects the deviation in B-PSF.
	● The deviation varies between species.
	● The deviation may be related to root functional traits.
	● The plasticity of specific root length (SRL) and root tissue density (RTD) are two important traits that affect the size of deviation.

References

[1] Allington, G.R.H., Valone, T.J., 2014. Islands of fertility: a byproduct of grazing. Ecosystems17, 127–141.

[2] Bailey, C., Scholes, M., 1997. Rhizosheath occurrence in South African grasses. South African Journal of Botany63, 484–490.

[3] Bao, S.D., 2000. Soil and Agricultural Chemistry Analysis. 3rd ed. Beijing: China Agriculture Press.

[4] Bardgett, R.D., Manning, P., Morriën, E., De Vries, F.T., 2013. Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. Journal of Ecology101, 334–343.

[5] Bennett, J.A., Klironomos, J., 2019. Mechanisms of plant-soil feedback: interactions among biotic and abiotic drivers. New Phytologist222, 91–96.

[6] Bennett, J.A., Maherali, H., Reinhart, K.O., Lekberg, Y., Hart, M.M., Klironomos, J., 2017. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science355, 181–184.

[7] Bergmann, J., Verbruggen, E., Heinze, J., Xiang, D., Chen, B.D., Joshi, J., Rillig, M.C., 2016. The interplay between soil structure, roots, and microbiota as a determinant of plant-soil feedback. Ecology and Evolution6, 7633–7644.

[8] Bever, J.D., 1994. Feeback between plants and their soil communities in an old field community. Ecology75, 1965–1977.

[9] Bever, J.D., Mangan, S.A., Alexander, H.M., 2015. Maintenance of plant species diversity by pathogens. Annual Review of Ecology, Evolution, and Systematics46, 305–325.

[10] Brinkman, E.P., Van der Putten, W.H., Bakker, E.J., Verhoeven, K.J.F., 2010. Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. Journal of Ecology98, 1063–1073.

[11] Callaway, R.M., Thelen, G.C., Rodriguez, A., Holben, W.E., 2004. Soil biota and exotic plant invasion. Nature427, 731–733.

[12] 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.

[13] Chen, C., Chen, H.Y.H., Chen, X.L., Huang, Z. Q., 2019a. Meta-analysis shows positive effects of plant diversity on microbial biomass and respiration. Nature Communications10, 1332.

[14] Chen, L., Swenson, N.G., Ji, N.N., Mi, X.C., Ren, H.B., Guo, L.D., Ma, K.P., 2019b. Differential soil fungus accumulation and density dependence of trees in a subtropical forest. Science366, 124–128.

[15] Chen, T., Nan, Z.B., Kardol, P., Duan, T.Y., Song, H., Wang, J.F., Li, C.H., Hou, F.J., 2018. Effects of interspecific competition on plant-soil feedbacks generated by long-term grazing. Soil Biology and Biochemistry126, 133–143.

[16] Craine, J.M., Froehle, J., Tilman, G.D., Wedin, D.A., Chapin III, F.S., 2001. The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos93, 274–285.

[17] Crawford, K.M., Bauer, J.T., Comita, L.S., Eppinga, M.B., Johnson, D.J., Mangan, S.A., Queenborough, S.A., Strand, A.E., Suding, K.N., Umbanhowar, J., Bever, J.D., 2019. When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecology Letters22, 1274–1284.

[18] Day, N.J., Dunfield, K.E., Antunes, P.M., 2015. Temporal dynamics of plant-soil feedback and root-associated fungal communities over 100 years of invasion by a non-native plant. Journal of Ecology103, 1557–1569.

[19] Domínguez-Begines, J., Ávila, J.M., García, L.V., Gómez-Aparicio, L., 2021. Disentangling the role of oomycete soil pathogens as drivers of plant-soil feedbacks. Ecology102, e03430.

[20] Dostálek, T., Münzbergová, Z., Kladivová, A., Macel, M., 2016. Plant-soil feedback in native vs. invasive populations of a range expanding plant. Plant and Soil399, 209–220.

[21] Edgar, R.C., 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods10, 996–998.

[22] Egelkraut, D., Kardol, P., De Long, J.R., Olofsson, J., 2018. The role of plant-soil feedbacks in stabilizing a reindeer-induced vegetation shift in subarctic tundra. Functional Ecology32, 1959–1971.

[23] Eissenstat, D.M., 1991. On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytologist118, 63–68.

[24] Eissenstat, D.M., 1992. Costs and benefits of constructing roots of small diameter. Journal of Plant Nutrition15, 763–782.

[25] Eissenstat, D.M., Kucharski, J.M., Zadworny, M., Adams, T.S., Koide, R.T., 2015. Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytologist208, 114–124.

[26] Faucon, M.P., Houben, D., Reynoird, J.P., Mercadal-Dulaurent, A.M., Armand, R., Lambers, H., 2015. Advances and perspectives to improve the phosphorus availability in cropping systems for agroecological phosphorus management. Advances in Agronomy134, 51–79.

[27] Gao, L.L., Wei, C.Q., He, Y.F., Tang, X.F., Chen, W., Xu, H., Wu, Y.Q., Wilschut, R.A., Lu, X.M., 2023. Aboveground herbivory can promote exotic plant invasion through intra- and interspecific aboveground-belowground interactions. New Phytologist237, 2347–2359.

[28] García-Palacios, P., Bowker, M.A., Chapman, S.J., Maestre, F.T., Soliveres, S., Gallardo, A., Valladares, F., Guerrero, C., Escudero, A., 2011. Early-successional vegetation changes after roadside prairie restoration modify processes related with soil functioning by changing microbial functional diversity. Soil Biology and Biochemistry43, 1245–1253.

[29] Gardes, M., Bruns, T.D., 1993. ITS primers with enhanced specificity for basidiomycetes- application to the identification of mycorrhizae and rusts. Molecular Ecology2, 113–118.

[30] Gundale, M.J., Kardol, P., 2021. Multi-dimensionality as a path forward in plant-soil feedback research. Journal of Ecology109, 3446–3465.

[31] Haichar, F.E.Z., Santaella, C., Heulin, T., Achouak, W., 2014. Root exudates mediated interactions belowground. Soil Biology and Biochemistry77, 69–80.

[32] Hartnett, D.C., Wilson, G.W.T., Ott, J.P., Setshogo, M., 2013. Variation in root system traits among African semi-arid savanna grasses: implications for drought tolerance. Austral Ecology38, 383–392.

[33] Herms, D.A., Mattson, W.J., 1992. The dilemma of plants: to grow or defend. The Quarterly Review of Biology67, 283–335.

[34] Holdaway, R.J., Richardson, S.J., Dickie, I.A., Peltzer, D.A., Coomes, D.A., 2011. Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. Journal of Ecology99, 954–963.

[35] in ’t Zandt, D., van den Brink, A., de Kroon, H., Visser, E.J.W., 2019. Plant-soil feedback is shut down when nutrients come to town. Plant and Soil439, 541–551.

[36] Jiang, S.J., Liu, Y.J., Luo, J.J., Qin, M.S., Johnson, N.C., Öpik, M., Vasar, M., Chai, Y.X., Zhou, X.L., Mao, L., Du, G.Z., An, L.Z., Feng, H.Y., 2018. Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytologist220, 1222–1235.

[37] Kadowaki, K., Yamamoto, S., Sato, H., Tanabe, A.S., Hidaka, A., Toju, H., 2018. Mycorrhizal fungi mediate the direction and strength of plant-soil feedbacks differently between arbuscular mycorrhizal and ectomycorrhizal communities. Communications Biology1, 196.

[38] Kaisermann, A., de Vries, F.T., Griffiths, R.I., Bardgett, R.D., 2017. Legacy effects of drought on plant-soil feedbacks and plant-plant interactions. New Phytologist215, 1413–1424.

[39] Karasov, T.L., Chae, E., Herman, J.J., Bergelson, J., 2017. Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell29, 666–680.

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

[41] Ke, P.J., Wan, J., 2023. A general approach for quantifying microbial effects on plant competition. Plant and Soil485, 57–70.

[42] Klinerová, T., Dostál, P., 2020. Nutrient-demanding species face less negative competition and plant-soil feedback effects in a nutrient-rich environment. New Phytologist225, 1343–1354.

[43] Koffel, T., Boudsocq, S., Loeuille, N., Daufresne, T., 2018. Facilitation- vs. competition-driven succession: the key role of resource-ratio. Ecology Letters21, 1010–1021.

[44] Kong, D.L., Ma, C.G., Zhang, Q., Li, L., Chen, X.Y., Zeng, H., Guo, D.L., 2014. Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytologist203, 863–872.

[45] Kramer-Walter, K.R., Bellingham, P.J., Millar, T.R., Smissen, R.D., Richardson, S.J., Laughlin, D.C., 2016. Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. Journal of Ecology104, 1299–1310.

[46] Kuebbing, S.E., Classen, A.T., Call, J.J., Henning, J.A., Simberloff, D., 2015. Plant-soil interactions promote co-occurrence of three nonnative woody shrubs. Ecology96, 2289–2299.

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

[48] Laliberté, E., Lambers, H., Burgess, T.I., Wright, S.J., 2015. Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands. New Phytologist206, 507–521.

[49] Lambers, H., Albornoz, F., Kotula, L., Laliberté, E., Ranathunge, K., Teste, F.P., Zemunik, G., 2018. How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant and Soil424, 11–33.

[50] Li, J.J., Zheng, Y.M., Yan, J.X., Li, H.J., He, J.Z., 2013. Succession of plant and soil microbial communities with restoration of abandoned land in the Loess Plateau, China. Journal of Soils and Sediments13, 760–769.

[51] Li, S.F., Huang, X.B., Lang, X.D., Shen, J.Y., Xu, F.D., Su, J.R., 2020. Cumulative effects of multiple biodiversity attributes and abiotic factors on ecosystem multifunctionality in the Jinsha River valley of southwestern China. Forest Ecology and Management472, 118281.

[52] Liang, M.X., Liu, X.B., Gilbert, G.S., Zheng, Y., Luo, S., Huang, F.M., Yu, S.X., 2016. Adult trees cause density-dependent mortality in conspecific seedlings by regulating the frequency of pathogenic soil fungi. Ecology Letters19, 1448–1456.

[53] Liang, M.X., Shi, L.Q., Burslem, D.F.R.P., Johnson, D., Fang, M., Zhang, X.Y., Yu, S.X., 2021. Soil fungal networks moderate density-dependent survival and growth of seedlings. New Phytologist230, 2061–2071.

[54] Ma, H.K., Pineda, A., van der Wurff, A.W.G., Bezemer, T.M., 2018. Synergistic and antagonistic effects of mixing monospecific soils on plant-soil feedbacks. Plant and Soil429, 271–279.

[55] Meng, T.Z., Ren, G.D., Wang, G.F., Ma, Y., 2019. Impacts on soil microbial characteristics and their restorability with different soil disinfestation approaches in intensively cropped greenhouse soils. Applied Microbiology and Biotechnology103, 6369–6383.

[56] Milici, V.R., Dalui, D., Mickley, J.G., Bagchi, R., 2020. Responses of plant-pathogen interactions to precipitation: Implications for tropical tree richness in a changing world. Journal of Ecology108, 1800–1809.

[57] Mo, X.H., Wang, M.K., Zeng, H., Wang, J.J., 2023. Rhizosheath: distinct features and environmental functions. Geoderma435, 116500.

[58] Nguyen, N.H., Song, Z.W., Bates, S.T., Branco, S., Tedersoo, L., Menke, J., Schilling, J.S., Kennedy, P.G., 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology20, 241–248.

[59] Nilsson, R.H., Larsson, K.H., Taylor, A.F.S., Bengtsson-Palme, J., Jeppesen, T.S., Schigel, D., Kennedy, P., Picard, K., Glöckner, F.O., Tedersoo, L., Saar, I., Koljalg, U., Abarenkov, K., 2019. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research47, D259–D264.

[60] Ochoa-Hueso, R., Eldridge, D.J., Delgado-Baquerizo, M., Soliveres, S., Bowker, M.A., Gross, N., Le Bagousse-Pinguet, Y., Quero, J.L., García-Gómez, M., Valencia, E., Arredondo, T., Beinticinco, L., Bran, D., Cea, A., Coaguila, D., Dougill, A.J., Espinosa, C.I., Gaitán, J., Guuroh, R.T., Guzman, E., Gutiérrez, J.R., Hernández, R.M., Huber-Sannwald, E., Jeffries, T., Linstädter, A., Mau, R.L., Monerris, J., Prina, A., Pucheta, E., Stavi, I., Thomas, A.D., Zaady, E., Singh, B.K., Maestre, F.T., 2018. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. Journal of Ecology106, 242–253.

[61] Pan, F.J., Liang, Y.M., Wang, K.L., Zhang, W., 2018. Responses of fine root functional traits to soil nutrient limitations in a karst ecosystem of southwest China. Forests9, 743.

[62] Paz, H., 2003. Root/shoot allocation and root architecture in seedlings: variation among forest sites, microhabitats, and ecological groups. Biotropica35, 318–332.

[63] Pineda, A., Kaplan, I., Hannula, S.E., Ghanem, W., Bezemer, T.M., 2020. Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest. New Phytologist226, 595–608.

[64] Powlson, D.S., Jenkinson, D.S., 1976. The effects of biocidal treatments on metabolism in soil-II. gamma irradiation, autoclaving, air-drying and fumigation. Soil Biology and Biochemistry8, 179–188.

[65] Reich, P.B., 2014. The world-wide 'fast-slow' plant economics spectrum: a traits manifesto. Journal of Ecology102, 275–301.

[66] Reich, P.B., Tjoelker, M.G., Walters, M.B., Vanderklein, D.W., Buschena, C., 1998. Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Functional Ecology12, 327–338.

[67] Scharfy, D., Güsewell, S., Gessner, M.O., Venterink, H.O., 2010. Invasion of Solidago gigantea in contrasting experimental plant communities: effects on soil microbes, nutrients and plant-soil feedbacks. Journal of Ecology98, 1379–1388.

[68] Schroeder, J.W., Dobson, A., Mangan, S.A., Petticord, D.F., Herre, E.A., 2020. Mutualist and pathogen traits interact to affect plant community structure in a spatially explicit model. Nature Communications11, 2204.

[69] Semchenko, M., Barry, K.E., de Vries, F.T., Mommer, L., Moora, M., Maciá-Vicente, J.G., 2022. Deciphering the role of specialist and generalist plant-microbial interactions as drivers of plant-soil feedback. New Phytologist234, 1929–1944.

[70] Smakowska, E., Kong, J.X., Busch, W., Belkhadir, Y., 2016. Organ-specific regulation of growth-defense tradeoffs by plants. Current Opinion in Plant Biology29, 129–137.

[71] Song, W.C., Zhou, Y.J., 2021. Linking leaf δ¹⁵N and δ¹³C with soil fungal biodiversity, ectomycorrhizal and plant pathogenic abundance in forest ecosystems of China. CATENA200, 105176.

[72] Spitzer, C.M., Lindahl, B., Wardle, D.A., Sundqvist, M.K., Gundale, M.J., Fanin, N., Kardol, P., 2021. Root trait-microbial relationships across tundra plant species. New Phytologist229, 1508–1520.

[73] Su, Y., Tang, Y.F., Hu, Y., Liu, M.Y., Lu, X.Y., Duan, B.L., 2024. Exploring plant adaptation strategies to phosphorus limitation induced by nitrogen addition: foliar phosphorus allocation and root functional traits analysis in two dominant subalpine tree species. Journal of Plant Ecology17, rtae060.

[74] Teste, F.P., Kardol, P., Turner, B.L., Wardle, D.A., Zemunik, G., Renton, M., Laliberte, E., 2017. Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science355, 173–176.

[75] Thakur, M.P., van der Putten, W.H., Wilschut, R.A., Veen, G.F., Kardol, P., van Ruijven, J., Allan, E., Roscher, C., van Kleunen, M., Bezemer, T.M., 2021. Plant-soil feedbacks and temporal dynamics of plant diversity-productivity relationships. Trends in Ecology & Evolution36, 651–661.

[76] Trap, J., Bonkowski, M., Plassard, C., Villenave, C., Blanchart, E., 2016. Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil398, 1–24.

[77] Troelstra, S.R., Wagenaar, R., Smant, W., Peters, B.A.M., 2001. Interpretation of bioassays in the study of interactions between soil organisms and plants: involvement of nutrient factors. New Phytologist150, 697–706.

[78] 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.

[79] van der Putten, W.H., Bradford, M.A., Brinkman, E.P., van de Voorde, T.F.J., Veen, G.F., 2016. Where, when and how plant-soil feedback matters in a changing world. Functional Ecology30, 1109–1121.

[80] van der Putten, W.H., Kowalchuk, G.A., Brinkman, E.P., Doodeman, G.T.A., van der Kaaij, R.M., Kamp, A.F.D., Menting, F.B.J., Veenendaal, E.M., 2007. Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology88, 978–988.

[81] van Ruijven, J., Ampt, E., Francioli, D., Mommer, L., 2020. Do soil-borne fungal pathogens mediate plant diversity-productivity relationships? Evidence and future opportunities. Journal of Ecology108, 1810–1821.

[82] Veresoglou, S.D., Li, G.C., Chen, J.J., Johnson, D., 2022. Direction of plant-soil feedback determines plant responses to drought. Global Change Biology28, 3995–3997.

[83] Wei, W., Yang, M., Liu, Y.X., Huang, H.C., Ye, C., Zheng, J.F., Guo, C.W., Hao, M.W., He, X.H., Zhu, S.S., 2018. Fertilizer N application rate impacts plant-soil feedback in a sanqi production system. Science of the Total Environment633, 796–807.

[84] White, T.J., Bruns, T.D., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., eds. PCR protocols. San Diego: Academic Press.

[85] Yamamoto, T., Ultra Jr, V.U., Tanaka, S., Sakurai, K., Iwasaki, K., 2008. Effects of methyl bromide fumigation, chloropicrin fumigation and steam sterilization on soil nitrogen dynamics and microbial properties in a pot culture experiment. Soil Science and Plant Nutrition54, 886–894.

[86] Yang, Q., Carrillo, J., Jin, H.Y., Shang, L., Hovick, S.M., Nijjer, S., Gabler, C.A., Li, B., Siemann, E., 2013. Plant-soil biota interactions of an invasive species in its native and introduced ranges: implications for invasion success. Soil Biology and Biochemistry65, 78–85.

[87] 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.

[88] Zhang, P., Li, B., Wu, J.H., Hu, S.J., 2019. Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecology Letters22, 200–210.

[89] Zhang, T.A., Chen, H.Y.H., Ruan, H.H., 2018. Global negative effects of nitrogen deposition on soil microbes. The ISME Journal12, 1817–1825.

[90] Zhao, Z.M., Wang, L., Chen, H.Z., 2015. A novel steam explosion sterilization improving solid-state fermentation performance. Bioresource Technology192, 547–555.

[91] Zhou, M., Bai, W.M., Zhang, Y.S., Zhang, W.H., 2018. Multi-dimensional patterns of variation in root traits among coexisting herbaceous species in temperate steppes. Journal of Ecology106, 2320–2331.

RIGHTS & PERMISSIONS

Higher Education Press