Legacy effect of elevated CO₂ and N fertilization on mineralization and retention of rice (Oryza sativa L.) rhizodeposit-C in paddy soil aggregates

Highlights

• Elevated CO₂ increased the amounts of rhizodeposits.

• The turnover of rhizodeposits derived from N soil was faster than no N soil.

• Rhizodeposits derived from elevated CO₂ decomposed slower than from ambient air.

• Microaggregates and silt-clay were the most and least affected fractions separately.

Abstract

Rhizodeposits in rice paddy soil are important in global C sequestration and cycling. This study explored the effects of elevated CO₂ and N fertilization during the rice growing season on the subsequent mineralization and retention of rhizodeposit-C in soil aggregates after harvest. Rice (Oryza sativa L.) was labeled with ¹³CO₂ under ambient (400 ppm) and elevated (800 ppm) CO₂ concentrations with and without N fertilization. After harvest, soil with labeled rhizodeposits was collected, separated into three aggregate size fractions, and flood-incubated for 100 d. The initial rhizodeposit-¹³C content of N-fertilized microaggregates was less than 65% of that of non-fertilized microaggregates. During the incubation of microaggregates separated from N-fertilized soils, 3%–9% and 9%–16% more proportion of rhizodeposit-¹³C was mineralized to ¹³CO₂, and incorporated into the microbial biomass, respectively,, while less was allocated to soil organic carbon than in the non-fertilized soils. Elevated CO₂ increased the rhizodeposit-¹³C content of all aggregate fractions by 10%–80%, while it reduced cumulative ¹³CO₂ emission and the bioavailable C pool size of rhizodeposit-C, especially in N-fertilized soil, except for the silt-clay fraction. It also resulted in up to 23% less rhizodeposit-C incorporated into the microbial biomass of the three soil aggregates, and up to 23% more incorporated into soil organic carbon. These results were relatively weak in the silt-clay fraction. Elevated CO₂ and N fertilizer applied in rice growing season had a legacy effect on subsequent mineralization and retention of rhizodeposits in paddy soils after harvest, the extent of which varied among the soil aggregates.

Graphical abstract

Keywords

Rice rhizodeposits / Isotope labeling / Aggregates / Elevated carbon dioxide / Nitrogen fertilizer

References

[1] Allard, V., Robin, C., Newton, P.C.D., Lieffering, M., Soussana, J.F., 2006. Short and long-term effects of elevated CO₂ on Lolium perenne rhizodeposition and its consequences on soil organic matter turnover and plant N yield. Soil Biology & Biochemistry 38, 1178–1187

[2] Atere, C.T., Ge, T., Zhu, Z., Tong, C., Jones, D.L., Shibistova, O., Guggenberger, G., Wu, J., 2017. Rice rhizodeposition and carbon stabilisation in paddy soil are regulated via drying-rewetting cycles and nitrogen fertilisation. Biology and Fertility of Soils 53, 407–417

[3] Aulakh, M.S., Wassmann, R., Bueno, C., Rennenberg, H., 2001. Impact of root exudates ofdifferent cultivars and plant development stages of rice (Oryza sativa L.) on methane production in a paddy soil. Plant and Soil 230, 77–86

[4] Bhattacharyya, P., Roy, K.S., Neogi, S., Manna, M.C., Adhya, T.K., Rao, K.S., Nayak, A.K., 2013. Influence of elevated carbon dioxide and temperature on below-ground carbon allocation and enzyme activities in tropical flooded soil planted with rice. Environmental Monitoring and Assessment 185, 8659–8671

[5] Bowsher, A.W., Evans, S., Tiemann, L.K., Friesen, M.L., 2018. Effects of soil nitrogen availability on rhizodeposition in plants: a review. Plant and Soil 423, 59–85

[6] Britto, D.T., Kronzucker, H.J., 2002. NH₄⁺ toxicity in higher plants: a critical review. Journal of Plant Physiology 159, 567–584

[7] Brookes, P.C., Chen, Y., Chen, L., Qiu, G., Luo, Y., Xu, J., 2017. Is the rate of mineralization of soil organic carbon under microbiological control? Soil Biology & Biochemistry 112, 127–139

[8] Brye, K.R., Olk, D.C., Schmid, B.T., 2012. Rice rotation and tillage effects on soil aggregation and aggregate carbon and nitrogen dynamics. Soil Science Society of America Journal 76, 994–1004

[9] Calvo, O.C., Franzaring, J., Schmid, I., Müller, M., Brohon, N., Fangmeier, A., 2017. Atmospheric CO₂ enrichment and drought stress modify root exudation of barley. Global Change Biology 23, 1292–1304

[10] Choudhury, S.G., Srivastava, S., Singh, R., Chaudhari, S.K., Sharma, D.K., Singh, S.K., Sarkar, D., 2014. Tillage and residue management effects on soil aggregation, organic carbon dynamics and yield attribute in rice–wheat cropping system under reclaimed sodic soil. Soil & Tillage Research 136, 76–83

[11] Cotrufo, M.F., Wallenstein, M.D., Boot, C.M., Denef, K., Paul, E., 2013. The microbial efficiency matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Global Change Biology 19, 988–995

[12] Cui, J., Zhu, Z., Xu, X., Liu, S., Jones, D.L., Kuzyakov, Y., Shibistova, O., Wu, J., Ge, T., 2020. Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. Soil Biology & Biochemistry 142, 107720

[13] Czarnes, S., Hallett, P.D., Bengough, A.G., Young, I.M., 2000. Root-and microbial-derived mucilages affect soil structure and water transport. European Journal of Soil Science 51, 435–443

[14] De Sosa, L.L., Glanville, H.C., Marshall, M.R., Schnepf, A., Cooper, D.M., Hill, P.W., Binley, A., Jones, D., 2018. Stoichiometric constraints on the microbial processing of carbon with soil depth along a riparian hillslope. Biology and Fertility of Soils 54, 949–963

[15] Denef, K., Zotarelli, L., Boddey, R.M., Six, J., 2007. Microaggregate associated C as a diagnostic fraction for management-induced changes in soil organic carbon in two Oxisols. Soil Biology & Biochemistry 39, 1165–1172

[16] Dormaar, J.F., 1992. Decomposition as a Process in Natural Grasslands. In: Couland, R.T., ed. Naturalgrasslands, Introduction and Western Hemisphere (ecosystems of the world). Amsterdam: Elsevier pp. 121–136.

[17] Elliott, E.T., 1986. Aggregate structure and carbon, nitrogen, and phosphorus in native and cultivated soils. Soil Science Society of America Journal 50, 627–633

[18] Fischer, H., Ingwersen, J., Kuzyakov, Y., 2010. Microbial uptake oflow-molecular-weight organic substances out-competes sorption in soil. European Journal of Soil Science 61, 504–513

[19] Fischer, H., Kuzyakov, Y., 2010. Sorption, microbial uptake and decomposition of acetate in soil: transformations revealed by position-specific ¹⁴C labelling. Soil Biology & Biochemistry 42, 186–192

[20] Ge, T., Li, B., Zhu, Z., Hu, Y., Yuan, H., Dorodnikov, M., Jones, D.L., Wu, J., Kuzyakov, Y., 2017. Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biology and Fertility of Soils 53, 37–48

[21] Ge, T., Liu, C., Yuan, H., Zhao, Z., Wu, X., Zhu, Z., Brookes, P., Wu, J., 2015. Tracking the photosynthesized carbon input into soil organic carbon pools in a rice soil fertilized with nitrogen. Plant and Soil 392, 17–25

[22] Ge, T., Luo, Y., He, X., 2019. Quantitative and mechanistic insights into the key process in the rhizodeposited carbon stabilization, transformation and utilization of carbon, nitrogen and phosphorus in paddy soil. Plant and Soil 445, 1–5

[23] Ge, T., Wu, X., Chen, H., Yuan, H.Z., Li, B., Zhou, P., Liu, C., Tong, C., Brookes, P., Wu, J., 2013. Microbial phototrophic fixation of atmospheric CO₂ in China subtropical available upland and paddy soils. Geochimica et Cosmochimica Acta 113, 70–78

[24] Gregory, P.J., 2006. Roots, rhizosphere and soil: the route to a better understanding of soil science? European Journal of Soil Science 57, 2–12

[25] Hooker, B., Morris, T., Peters, R., Cardon, Z., 2005. Long-term effects of tillage and corn stalk return on soil carbon dynamics. Soil Science Society of America Journal 69, 188–196

[26] Jastrow, J.D., Amonette, J.E., Bailey, V.L., 2007. Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Climatic Change 80, 5–23

[27] Johnson, J.M.F., Allmaras, R.R., Reicosky, D.C., 2006. Estimating source carbon from crop residues, roots and rhizodeposits using the National Grain-Yield Database. Agronomy Journal 98, 622–636

[28] Jones, D.L., Clode, P.L., Kilburn, M.R., Stockdale, E.A., Murphy, D.V., 2013. Competition between plant and bacterial cells at the microscale regulates the dynamics of nitrogen acquisition in wheat (Triticum aestivum). New Phytologist 200, 796–807

[29] Jones, D.L., Hodge, A., Kuzyakov, Y., 2004. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163, 459–480

[30] Jones, D.L., Nguyen, C., Finlay, R.D., 2009. Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil 321, 5–33

[31] Keiluweit, M., Bougoure, J.J., Nico, P.S., Pett-Ridge, J., Weber, P.K., Kleber, M., 2015. Mineral protection of soil carbon counteracted by root exudates. Nature Climate Change 5, 588–595

[32] Kong, A.Y., Six, J., Bryant, D.C., Denison, R.F., Van Kessel, C., 2005. The relationship between carbon input, aggregation, and soil organic carbon stabilization in sustainable cropping systems. Soil Science Society of America Journal 69, 1078–1085

[33] Kuzyakov, Y., 2002. Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science 165, 382–396

[34] Kuzyakov, Y., 2010. Priming effects: interactions between living and dead organic matter. Soil Biology & Biochemistry 42, 1363–1371

[35] Kuzyakov, Y., Jones, D.L., 2006. Glucose uptake by maize roots and its transformation in the rhizosphere. Soil Biology & Biochemistry 38, 851–860

[36] Kuzyakov, Y., Larionova, A.A., 2005. Root and rhizomicrobial respiration: a review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. Journal of Plant Nutrition and Soil Science 168, 503–520

[37] Leuschner, C., Gebel, S., Rose, L., 2013. Root trait responses of six temperate grassland species to intensive mowing and NPK fertilisation: a field study in a temperate grassland. Plant and Soil 373, 687–698

[38] Li, Q., Li, B.H., Kronzucker, H.J., Shi, W.M., 2010. Root growth inhibition by NH₄⁺ in Arabidopsis is mediated by the root tip and is linked to NH₄⁺ efflux and GMPase activity. Plant, Cell & Environment 33, 1529-1542

[39] Li, Y., Li, Y., Chang, S.X., Liang, X., Qin, H., Chen, J., Xu, Q., 2017. Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests. Soil Biology & Biochemistry 107, 19–31

[40] Linkohr, B.I., Williamson, L.C., Fitter, A.H., Leyser, H.M.O., 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant Journal 29, 751–760

[41] Liu, Y., Ge, T., Ye, J., Liu, S., Shibistova, O., Wang, P., Wang, J., Li, Y., Guggenberger, G., Kuzyakov, Y., Wu, J., 2019a. Initial utilization of rhizodeposits with rice growth in paddy soils: Rhizosphere and N fertilization effects. Geoderma 338, 30–39

[42] Liu, Y., Ge, T., Zhu, Z., Liu, S., Luo, Y., Li, Y., Wang, P., Gavrichkova, O., Xu, X., Wang, J., Wu, J., Guggenberger, G., Kuzyakov, Y., 2019b. Carbon input and allocation by rice into paddy soils: A review. Soil Biology & Biochemistry 133, 97–107

[43] Lopez-Sangil, L., Rovira, P., 2013. Sequential chemical extractions of the mineral-associated soil organic matter: An integrated approach for the fractionation of organo-mineral complexes. Soil Biology & Biochemistry 62, 57–67

[44] Lu, Y., Watanabe, A., Kimura, M., 2002. Contribution of plant- derived carbon to soil microbial biomass dynamics in a paddy rice microcosm. Biology and Fertility of Soils 36, 136–142

[45] Lu, Y., Watanabe, A., Kimura, M., 2003. Carbon dynamics of rhizodeposits, root- and shoot-residues in a rice soil. Soil Biology & Biochemistry 35, 1223–1230

[46] Luo, Y., Zhu, Z., Liu, S., Peng, P., Xu, J., Brookes, P., Ge, T., Wu, J., 2018. Nitrogen fertilization increases rice rhizodeposition and its stabilization in soil aggregates and the humus fraction. Plant and Soil 445, 1–11.

[47] Mooshammer, M., Wanek, W., Zechmeister-Boltenstern, S., Richter, A., 2014. Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Frontiers in Microbiology 5, 22

[48] Nguyen, C., 2009. Rhizodeposition of Organic C by Plant: Mechanisms and Controls. Dordrecht: Springer, pp. 97–123.

[49] Norby, R.J., Cotrufo, M.F., Ineson, P., O’Neill, E.G., Canadell, J.G., 2001. Elevated CO₂, litter chemistry, and decomposition: a synthesis. Oecologia 127, 153–165

[50] Oades, J.M., 1988. The retention of organic matter in soils. Biogeochemistry 5, 35–70

[51] Pan, G., Li, L., Wu, L., Zhang, X., 2004. Storage and sequestration potential of topsoil organic carbon in China’s paddy soils. Global Change Biology 10, 79–92

[52] Pan, G.X., Wu, L.S., Li, L.Q., Zhang, X.H., Gong, W., Wood, Y., 2008. Organic carbon stratification and size distribution of three typical paddy soils from Taihu Lake region China. Journal of Environmental Sciences (China) 20, 456–463

[53] Pausch, J., Tian, J., Riederer, M., Kuzyakov, Y., 2013. Estimation of rhizodeposition at field scale: upscaling of a ¹⁴C labelling study. Plant and Soil 364, 273–285

[54] Pendall, E., Mosier, A.R., Morgan, J.A., 2004. Rhizodeposition stimulated by elevated CO₂ in a semi-arid grassland. New Phytologist 162, 447–458

[55] Pett-Ridge, J., Firestone, M.K., 2017. Using stable isotopes to explore root-microbe-mineral interactions in soil. Rhizosphere 3, 244–253

[56] Phillips, R.P., Finzi, A.C., Bernhardt, E.S., 2011. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO₂ fumigation. Ecology Letters 14, 187–194

[57] Recous, S., Robin, D., Darwis, D., Mary, B., 1995. Soil inorganic N availability: effect on maize residue decomposition. Soil Biology & Biochemistry 27, 1529–1538

[58] Rillig, M.C., Mummey, D.L., 2006. Mycorrhizas and soil structure. New Phytologist 171, 41–53

[59] Schmidt, M.W., Torn, M.S., Abiven, S., Dittmar, T., Guggenberger, G., Janssens, I.A., Kleber, M., Kogel-Knabner, I., Lehmann, J., Manning, D.A., Nannipieri, P., Rasse, D.P., Weiner, S., Trumbore, S.E., 2011. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56

[60] Six, J., Conant, R.T., Paul, E.A., Paustian, K., 2002. Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant and Soil 241, 155–176

[61] Smith, A.P., Marín-Spiotta, E., De Graaff, M.A., Balser, T.C., 2014. Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biology & Biochemistry 77, 292–303

[62] Tarnawski, S., Aragno, M., 2006. The influence of elevated CO₂ on diversity, activity and biogeochemical function of rhizosphere and soil bacterial communities. In Nosberger, J., Long, S.P., Norby, R.J., Stitt, M., Hendrey, G.R., Blum, H., eds. Managed ecosystems and CO₂—Case Studies, Processes and Perspectives (Ecological studies series 187th ed.). Berlin: Springer, pp. 393–409

[63] Traore, O., Groleau-Renaud, V., Plantureux, S., Tubeileh, A., Boeuf-Tremblay, V., 2000. Effect of root mucilage and modelled root exudates on soil structure. European Journal of Soil Science 51, 575–581.

[64] von Lützow, M., Kögel-Knabner, I., Ekschmitt, K., Flessa, H., Guggenberger, G., Matzner, E., Marschner, B., 2007. SOM fractionation methods: relevance to functional pools and to stabilization mechanisms. Soil Biology & Biochemistry 39, 2183–2207

[65] Wei, X., Hu, Y., Peng, P., Zhu, Z., Atere, C.T., O’Donnell, A.G., Wu, J., Ge, T., 2017. Effect of P stoichiometry on the abundance of nitrogen-cycle genes in phosphorus-limited paddy soil. Biology and Fertility of Soils 53, 767–776

[66] Wei, X., Zhu, Z., Liu, Y., Luo, Y., Deng, Y., Xu, X., Liu, S., Richter, A., Guggenberger, G., Wu, J., Ge, T., 2020. C:N:P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil. Biology and Fertility of Soils

[67] Wei, X., Zhu, Z., Wei, L., Wu, J., Ge, T., 2019. Biogeochemical cycles of key elements in the paddy-rice rhizosphere: microbial mechanisms and coupling processes. Rhizosphere 10, 100145

[68] Wu, J., Joergensen, R.G., Pommerening, B., Chaussod, R., Brookes, P.C., 1990. Measurement of soil microbial biomass C by fumigation-extraction—an automated procedure. Soil Biology & Biochemistry 22, 1167–1169

[69] Wu, J.S., 2011. Carbon accumulation in paddy ecosystems in subtropical China: evidence from landscape studies. European Journal of Soil Science 62, 29–34

[70] Wu, Y., Wu, J., Ma, Y., Lian, Y., Sun, H., Xie, D., Li, Y., Brookes, P., Yao, H., 2019. Dynamic changes in soil chemical properties and microbial community structure in response to different nitrogen fertilizers in an acidified celery soil. Soil Ecology Letters 1, 105–113

[71] Xiao, M., Zang, H., Liu, S., Ye, R., Zhu, Z., Su, Y., Wu, J., Ge, T., 2019. Nitrogen fertilization alters the distribution and fates of photosynthesized carbon in rice–soil systems: A ¹³C–CO₂ pulse labeling study. Plant and Soil 445, 101–112

[72] Yang, Y.H., Luo, Y.Q., Lu, M., Schadel, C., Han, W.X., 2011. Terrestrial C:N stoichiometry in response to elevated CO₂ and N addition: a synthesis of two meta-analyses. Plant and Soil 343, 393–400

[73] Ye, R., Doane, T.A., Morris, J., Horwath, W.R., 2015. The effect of rice straw on the priming of soil organic matter and methane production in peat soils. Soil Biology & Biochemistry 81, 98–107

[74] Yuan, H., Zhu, Z., Liu, S., Ge, T., Jing, H., Li, B., Liu, Q., Lynn, T.M., Wu, J., Kuzyakov, Y., 2016. Microbial utilization of rice root exudates:¹³C labeling and PLFA composition. Biology and Fertility of Soils 52, 615–627

[75] Zang, H., Blagodatskaya, E., Wang, J., Xu, X., Kuzyakov, Y., 2017. Nitrogen fertilization increases rhizodeposit incorporation into microbial biomass and reduces soil organic matter losses. Biology and Fertility of Soils 53, 419–429

[76] Zang, H., Xiao, M., Wang, Y., Ling, N., Wu, J., Ge, T., Kuzyakov, Y., 2019. Allocation of assimilated carbon in paddies depending on rice age, chase period and N fertilization: Experiment with ¹³CO₂ labelling and literature synthesis. Plant and Soil 445, 113–123

[77] Zhao, Y., Shao, S., Schaeffer, S.M., Bao, X., Zhang, W., Zhu, B., He, H., Zhang, X., 2019. Methodological clarification for estimating the input of plant-derived carbon in soils under elevated CO₂ based on a ¹³C-enriched CO₂ labeling experiment. Plant and Soil 440, 569–580

[78] Zhao, Z., Ge, T., Gunina, A., Li, Y., Zhu, Z., Peng, P., Wu, J., Kuzyakov, Y., 2018. Carbon and nitrogen availability in paddy soil affects rice photosynthate allocation, microbial community composition, and priming: combining continuous ¹³C labeling with PLFA analysis. Plant and Soil 445, 137–152

[79] Zhen, S., Zhou, J., Deng, X., Zhu, G., Cao, H., Wang, Z., Yan, Y., 2016. Metabolite profiling of the response to high-nitrogen fertilizer during grain development of bread wheat (Triticum aestivum L.). Journal of Cereal Science 69, 85–94

[80] Zhu, Z., Ge, T., Hu, Y., Zhou, P., Wang, T., Shibistova, O., Guggenberger, G., Su, Y., Wu, J., 2017. Fate of rice shoot and root residues, rhizodeposits, and microbial assimilated carbon in paddy soil-part 2: turnover and microbial utilization. Plant and Soil 416, 243–257

[81] Zhu, Z., Ge, T., Liu, S., Hu, Y., Ye, R., Xiao, M., Tong, C., Kuzyakov, Y., Wu, J., 2018. Rice rhizodeposits affect organic matter priming in paddy soil: the role of N fertilization and plant growth for enzyme activities, CO₂ and CH₄ emissions. Soil Biology & Biochemistry 116, 369–377

[82] Zhu, Z., Zeng, G., Ge, T., Hu, Y., Tong, C., Shibistova, O., He, X., Wang, J., Guggenberger, G., Wu, J., 2016. Fate of rice shoot and root residues, rhizodeposits, and microbe-assimilated carbon in paddy soil – part 1: decomposition and priming effect. Biogeosciences 13, 4481–4489

[83] Ziska, L.H., Weerakoon, W., Namuco, O.S., Pamplona, R., 1996. The influence of nitrogen on the elevated CO₂ response in field-grown rice. Functional Plant Biology 23, 45–52

[84] Zou, P., Fu, J., Cao, Z., Ye, J., Yu, Q., 2015. Aggregate dynamics and associated soil organic matter in topsoils of two 2,000-year paddy soil chronosequences. Journal of Soils and Sediments 15, 510–522

Acknowledgments

This study was financially supported by the National Key Research and Development Program of China (2017YFD0301504), the National Natural Science Foundation of China (41671292; 41771334; 41877104; 42007097), the Japan-China Scientific Cooperation Program between NSFC and JSPS (41811540031), the Hunan Province Base for Scientific and Technological Innovation Cooperation (2018WK4012), the Innovation Group of Natural Science Foundation of Hunan Province (2019JJ10003), the Natural Science Foundation of Hunan Province for Excellent Young Scholars (2019JJ30028) and the Youth Innovation Team Project of ISA, CAS (2017QNCXTD_GTD). We also thank the Public Service Technology Center, the Institute of Subtropical Agriculture, and the Chinese Academy of Sciences for technical support.

Conflict of interest

The authors declare that they have no conflict of interest.

RIGHTS & PERMISSIONS

2020 Higher Education Press