Root exudates and their ecological consequences in forest ecosystems: Problems and perspective

YIN Hua-Jun1 ZHANG Zi-Liang1,2 LIU Qing1

(1.Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization of Chinese Academy of Sciences, and Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, China 610041)
(2.University of Chinese Academy of Sciences, Beijing, China 100049)

【Abstract】The research on the ecological processes in rhizosphere and the underlying mechanisms has become one of the active and sensitive hotspots in soil science. Root exudates have special roles in mediating the nutrient cycling and signal transduction within root–soil–microorganism interactions. They are the key driving factors regulating the functions of rhizosphere micro-ecosystem, and serve as a major premise for the concept and ecological processes in rhizosphere. However, due to the instinctive advantages of crops, such as short life cycles and convenient operation, the available studies on root exudates mainly focus on agricultural ecosystems and target at providing practical guidelines. In contrast, there have been few investigations on root exudates of trees, which highly limited the knowledge of the potential mechanisms of root exudates in mediating soil biogeochemical processes in forest ecosystems. Based on the main findings in our previous studies and the emerging frontiers in rhizosphere ecology, we specifically reviewed the ecological consequences and key challenges in the research on root exudates in forests. Finally, we put forward several topics and research outlooks for guiding future work to facilitate studies on root exudates and their ecological consequences in forest ecosystems.

【Keywords】 rhizosphere; root exudate; root-soil interactions; soil biogeochemical processes; rhizosphere functional traits; forest;

【DOI】

【Funds】 Frontier Science Key Research Programs of CAS (QYZDB-SSW-SMC023) National Natural Science Foundation of China (31670449 and 31872700) Sichuan Key Research and Development Program (2017SZ0038)

Download this article

    References

    Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233‒266.

    Bardgett RD, Mommer L, de Vries FT (2014). Going underground: Root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 692‒699.

    Cairney JWG (2012). Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biology & Biochemistry, 47, 198‒208.

    Cheng WX, Parton WJ, Gonzalez-Meler MA, Phillips R (2014). Synthesis and modeling perspectives of rhizosphere priming. New Phytologist, 201, 31‒44.

    Cleveland CC, Houlton BZ, Smith WK, Marklein AR, Reed SC, Parton W, Del Grosso SJ, Running SW (2013). Patterns of new versus recycled primary production in the terrestrial biosphere. Proceedings of the National Academy of Sciences of the United States of America, 110, 12733‒12737.

    Cleveland CC, Liptzin D (2007). C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass? Biogeochemistry, 85, 235‒252.

    Darrah PR (1991). Measuring the diffusion coefficient of rhizosphere exudates in soil. I. The diffusion of non-sorbing compounds. Journal of Soil Science, 42, 413‒420.

    Dessaux Y, Hinsinger P, Lemanceau P (2009). Rhizosphere: So many achievements and even more challenges. Plant and Soil, 321, 1‒3.

    Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013). Rhizosphere priming: A nutrient perspective. Frontiers in Microbiology, 4, 1‒4.

    Drake JE, Darby BA, Giasson MA, Kramer MA, Phillips RP, Finzi AC (2013). Stoichiometry constrains microbial response to root exudation—insights from a model and a field experiment in a temperate forest. Biogeosciences, 10, 821‒838.

    Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Tresder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011). Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecology Letters, 14, 349‒357.

    Erktan A, McCormack ML, Roumet C (2018). Frontiers in root ecology: Recent advances and future challenges. Plant and Soil, 424, 1‒9.

    Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP (2015). Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biology, 21, 2082‒2094.

    Fuhrer T, Zamboni N (2015). High-throughput discovery metabolomics. Current Opinion in Biotechnology, 31, 73‒78.

    Guo DL, Li H, Mitchell RJ, Han WX, Hendricks JJ, Fahey TJ, Hendrick RL (2008). Fine root heterogeneity by branch order: Exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytologist, 177, 443‒456.

    Guyonnet JP, Cantarel AAM, Simon L, Haichar FZ (2018). Root exudation rate as functional trait involved in plant nutrient-use strategy classification. Ecology and Evolution, 8, 8573‒8581.

    Haichar FE, Santaella C, Heulin T, Achouak W (2014). Root exudates mediated interactions belowground. Soil Biology & Biochemistry, 77, 69‒80.

    Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005). Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist, 168, 293‒303.

    Högberg P, Read DJ (2006). Towards a more plant physiological perspective on soil ecology. Trends in Ecology and Evolution, 21, 548‒554.

    Holz M, Zarebanadkouki M, Kuzyakov Y, Pausch J, Carminati A (2018). Root hairs increase rhizosphere extension and carbon input to soil. Annals of Botany, 121, 61‒69.

    Hu LF, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, van der Heijden MGA, Schlaeppi K, Erb M (2018). Root exudate metabolites drive plant–soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nature Communications, 9, 1‒13.

    Jilling A, Keiluweit M, Contosta AR, Frey S, Schimel J, Schnecker J, Smith RG, Tiemann L, Grandy AS (2018). Minerals in the rhizosphere: Overlooked mediators of soil nitrogen availability to plants and microbes. Biogeochemistry, 139, 103‒122.

    Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015). Mineral protection of soil carbon counteracted by root exudates. Nature Climate Change, 5, 588‒595.

    Kemmitt SJ, Lanyon CV, Waite IS, Wen Q, Addiscott TM, Bird NRA, O’Donnell AG, Brookes PC (2008). Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass a new perspective. Soil Biology & Biochemistry, 40, 61‒73.

    Klein T, Siegwolf RT, Körner C (2016). Belowground carbon trade among tall trees in a temperate forest. Science, 352, 342‒344.

    Kong CH, Li HB, Hu F (2006). Allelochemicals released by rice roots and residues in soil. Plant and Soil, 288, 47‒56.

    Kuzyakov Y (2002). Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, 165, 382‒396.

    Laliberté E (2017). Below-ground frontiers in trait-based plant ecology. New Phytologist, 213, 1597‒1603.

    Li X, Dong JL, Chu WY, Chen YJ, Duan ZQ (2018). The relationship between root exudation properties and root morphological traits of cucumber grown under different nitrogen supplies and atmospheric CO2 concentrations. Plant and Soil, 425, 415‒432.

    Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Eastmond PJ (2017). Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science, 356, 1175‒1178.

    Ma ZQ, Guo DL, Xu XL, Lu MZ, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018). Evolutionary history resolves global organization of root functional traits. Nature, 555, 94‒97.

    Martinière A, Gibrata R, Sentenaca H, Dumonta X, Gaillarda I, Parisa N (2018). Uncovering pH at both sides of the root plasma membrane interface using noninvasive imaging. Proceedings of the National Academy of Sciences of the United States of America, 115, 6488‒6493.

    McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015). Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytologist, 207, 505‒518.

    Meier IC, Pritchard SG, Brzostek ER, McCormack ML, Phillips RP (2015). The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. New Phytologist, 205, 1164‒1174.

    Moore JAM, Jiang J, Patterson CM, Mayes MA, Wang G, Classen AT (2015). Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes. Journal of Ecology, 103, 1442‒1453.

    Nakayama M, Tateno R (2018). Solar radiation strongly influences the quantity of forest tree root exudates. Trees, 32, 871‒879.

    Neumann G, George TS, Plassard C (2009). Strategies and methods for studying the rhizosphere—The plant science toolbox. Plant and Soil, 321, 431‒456.

    Oburge E, Jones DJ (2018). Sampling root exudates—Mission impossible? Rhizosphere, 6, 116‒133.

    Pérez-Hargunideguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson CJG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013). New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 61, 167‒234.

    Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008). A new approach for capturing soluble root exudates in forest soils. Functional Ecology, 22, 990‒999.

    Phillips RP, Finzi AC, Bernhardt ES (2011). Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecology Letters, 14, 187‒194.

    Preece C, Farré-Armengol G, Llusià J, Peñuelas J (2018). Thirsty tree roots exude more carbon. Tree Physiology, 38, 690‒695.

    Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002). Fine root architecture of nine North American trees. Ecological Monographs, 72, 293‒309.

    Proctor C, He YH (2017). Quantifying root extracts and exudates of sedge and shrub in relation to root morphology. Soil Biology & Biochemistry, 114, 168‒180.

    Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Cao K, Stokes A (2016). Root structure–function relationships in 74 species: Evidence of a root economics spectrum related to carbon economy. New Phytologist, 210, 815‒826.

    Sandnes A, Eldhuset TD, Wollebaek G (2005). Organic acids in root exudates and soil solution of Norway spruce and silver birch. Soil Biology & Biochemistry, 37, 259‒269.

    Shahzad T, Rashid MI, Maire V, Barot S, Perveen N, Alvarez G, Mougin C, Fontaine S (2018). Root penetration in deep soil layers stimulates mineralization of millennia old organic carbon. Soil Biology & Biochemistry, 124, 150‒160.

    Shipley B, Bello FD, Cornelissen JHC, Lalibert E, Laughlin DC, Reich PB (2016). Reinforcing loose foundation stones in trait-based plant ecology. Oecologia, 180, 923‒931.

    Singh BK, Millard P, Whiteley AS, Murrell JC (2004). Unravelling rhizosphere–microbial interactions: Opportunities and limitations. TRENDS in Microbiology, 12, 386‒393.

    Smith SE, Read D (2008). Mycorrhizal Symbiosis. 3rd edn. Academic Press, London.Strehmel N, Bottcher C, Schmidt S, Scheel D (2014). Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry, 108, 35‒46.

    Sun Y, Xu XL, Kuzyakov Y (2014). Mechanisms of rhizosphere priming effects and their ecological significance. Chinese Journal of Plant Ecology, 38, 62‒75.

    Sun Y, Xu XL, Kuzyakov Y (2014). Mechanisms of rhizosphere priming effects and their ecological significance. Chinese Journal of Plant Ecology, 38, 62‒75.

    Sun L, Lu YF, Yu FW, Kronzucker HJ, Shi WM (2016). Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytologist, 212, 646‒656.

    Tan WB, Wang GA, Huang CH, Gao RT, Xi BD, Zhu B (2017). Physico-chemical protection, rather than biochemical composition, governs the responses of soil organic carbon decomposition to nitrogen addition in a temperate agroecosystem. Science of the Total Environment, 598, 282‒288.

    Terrer C, Vicca S, Stocker BD, Hungate BA, Phillips RP, Reich PB, Prentice IC (2018). Ecosystem responses to elevated CO2 governed by plant–soil interactions and the cost of nitrogen acquisition. New Phytologist, 217, 507‒522.

    Treseder KK, Holden SR (2013). Fungal carbon sequestration. Science, 339, 1528‒1529.

    Tückmantel T, Leuschner C, Preusser S, Kandeler E, Angst G, Mueller CW, Meier IC (2017). Root exudation patterns in a beech forest: Dependence on soil depth, root morphology, and environment. Soil Biology & Biochemistry, 107, 188‒197.

    Uren NC (2000). Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinto R, Varanini Z, Nannipieri P eds. The Rhizosphere, Biochemistry and Organic Substances at the Soil-plant Interface. Marcel Dekker, New York. 19–40.

    van Dam NM, Bouwmeester HJ (2016). Metabolomics in the rhizosphere: Tapping into belowground chemical communication. Trends in Plant Science, 21, 256–265.

    Wallander H, Ekblad A, Bergh J (2011). Growth and carbon sequestration by ectomycorrhizal fungi in intensively fertilized Norway spruce forests. Forest Ecology and Management, 262, 999‒1007.

    Wallander H, Ekblad A, Godbold DL, Johnson D, Bahr A, Baldrian P, Bjork RG, Kieliszewska-Rokicka B, Kjoller R, Kraigher H, Plassard C, Rudawska M (2013). Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils—A review. Soil Biology & Biochemistry, 57, 1034‒1047.

    Warren CR (2016). Simultaneous efflux and uptake of metabolites by roots of wheat. Plant and Soil, 406, 359‒374.

    Wu LK, Lin XM, Lin WX (2014). Advances and perspective in research on plant–soil–microbe interactions mediated by root exudates. Chinese Journal of Plant Ecology, 38, 298‒310 (in Chinese).

    Wutzler T, Reichstein M (2013). Priming and substrate quality interactions in soil organic matter models. Biogeosciences, 10, 2089‒2103.

    Xia B, Zhou Y, Liu X, Xiao J, Liu Q, Gu YC, Ding LS (2012). Use of electrospray ionization ion-trap tandem mass spectrometry and principal component analysis to directly distinguish monosaccharides. Rapid Communications in Mass Spectrometry, 26, 1259‒1264.

    Yin LM, Dijkstra FA, Wang P, Zhu B, Cheng WX (2018). Rhizosphere priming effects on soil carbon and nitrogen dynamics among tree species with and without intraspecific competition. New Phytologist, 218, 1036‒1048.

    Yin HJ, Li YF, Xiao J, Cheng XY, Xu ZF, Liu Q (2013). Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Global Change Biology, 19, 2158‒2167.

    Yin HJ, Phillips RP, Liang RB, Xu ZF, Liu Q (2016). Resource stoichiometry mediates soil C loss and nutrient transformations in forest soils. Applied Soil Ecology, 108, 248‒257.

    Yin HJ, Wheeler E, Phillips RP (2014). Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biology & Biochemistry, 78, 213‒221.

    Yuan YS, Zhao WQ, Zhang ZL, Xiao J, Li DD, Liu Q, Yin HJ (2018). Impacts of oxalic acid and glucose additions on N transformation in microcosms via artificial roots. Soil Biology & Biochemistry, 121, 16‒23.

    Zhang DD, Liang XH, Wang J (2014). A review of plant root exudates. Agricultural Science Bulletin, 30, 314‒320 (in Chinese).

    Zhang FS, Shen JB (1999). Preliminary development of the theoretical concept on rhizosphere micro-ecosystem. Review of China Agriculture Science and Technology, (4), 15‒20 (in Chinese).

    Zhang ZL, Phillips RP, Zhao WQ, Yuan YS, Liu Q, Yin HJ (2018a). Mycelia-derived C contributes more to nitrogen cycling than root-derived C in ectomycorrhizal alpine forests. Functional Ecology, DOI: 10.1111/1365-2435.13236.

    Zhang ZL, Xiao J, Yuan YS, Zhao CZ, Liu Q, Yin HJ (2018b). Mycelium-and root-derived C inputs differ in their impacts on soil organic C pools and decomposition in forests. Soil Biology & Biochemistry, 123, 257‒265.

    Zhu B, Cheng WX (2012). Nodulated soybean enhances rhizosphere priming effects on soil organic matter decomposition more than non-nodulated soybean. Soil Biology & Biochemistry, 51, 56‒65.

    Zhu B, Gutknecht JLM, Herman DJ, Keck DC, Firestone MK, Cheng WX (2014). Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biology & Biochemistry, 76, 183‒192.

This Article

ISSN:1005-264X

CN:11-3397/Q

Vol 42, No. 11, Pages 1055-1070

November 2018

Downloads:2

Share
Article Outline

Abstract

  • 1 Ecological significance of forest root exudates in soil processes and functions
  • 2 Limited knowledge of the coupling of forest root exudates with soil ecological processes and the regulation mechanisms
  • 3 Perspectives
  • References