Mechanisms of rhizosphere priming effects and their ecological significance

doi:10.3724/SP.J.1258.2014.00007

Abstract

Abstract:

Priming effects are defined as “strong short-term changes in the turnover of soil organic matter caused by moderate treatments of the soil”. Rhizosphere is the most important place, where the priming effects take place. Rhizosphere priming effects reflect the turnover rate of soil carbon and nitrogen, and affect the acquisition of competition for nutrients by plants and microorganisms, thus maintaining nutrient balance among the various components of an ecosystem. Although there has been a general understanding on the occurrence of rhizosphere priming effects, the mechanisms underlying their role in soil carbon and nitrogen transformations and their ecological significance are still not fully comprehended. This paper provides a synthesis of the latest advancement in studies of the rhizosphere priming effects. On the basis of reviews of research history and identification of the hotspots, we first put forward a mechanism underlying the occurrence of rhizosphere priming effects, and then examined the biotic and abiotic factors influencing the rhizosphere priming effects. The ecological significance and outlooks of research in the rhizosphere priming effects were discussed and clarified.

Key words: exoenzyme, rhizodeposition, rhizosphere priming effect, soil microorganisms

SUN Yue, XU Xing-Liang, Yakov KUZYAKOV. Mechanisms of rhizosphere priming effects and their ecological significance[J]. Chin J Plant Ecol, 2014, 38(1): 62-75.

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URL: https://www.plant-ecology.com/EN/10.3724/SP.J.1258.2014.00007

https://www.plant-ecology.com/EN/Y2014/V38/I1/62

Figures/Tables 2

Fig. 1 The hotspots of priming effects: detritusphere, rhizos- phere and drillosphere (after Beare et al. 1995 and Kladivko, 2001).

Fig. 2 Mechanism of rhizosphere priming effects. At low nutrient levels (left), plants allocate more photosynthates to belowground and supply soil microorganisms with carbon and energy. As a result, microbial biomass and activities increase and enhance production of extracellular enzymes by the rhizosphere microorganisms to decompose soil organic matter and release nutrients. Therefore, a positive priming effect takes place. In contrast, at high nutrient levels (right), microorganisms have less demand for nutrients and thus preferentially utilize root exudates, leading to reduced production of extracellular enzymes. Moreover, as plants invest less photosynthates in belowground, microbial biomass and activities will decrease. As a result, the decomposition of soil organic matter slows down and a negative priming effect occurs. The green, blue, and red arrow-lines represent the ecological processes mediated by plants, soil microorganisms, and exoenzymes, respectively. The thickness of an arrow-line indicates its relative magnitude of a flux or intensity of a process. Yellow colour of the available nitrogen pool indicates mineral nitrogen derived from mineralzation of soil organic matter. The area of the yellow colour represents the amount of mineral nitrogen derived from mineralzation of soil organic matter.

References 134

[1]	Alphei J, Bonkowski M, Scheu S (1996). Protozoa, Nematoda and Lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of micro-organisms and effects on plant growth. Oecologia, 106,111-126. DOI URL PMID
[2]	Amthor JS (1995). Terrestrial higher-plant response to increase- ing atmospheric [CO ₂] in relation to the global carbon cycle. Global Change Biology, 1,243-274.
[3]	Azam F, Simmons FW, Mulvaney RL (1993). Mineralization of N from plant residues and its interaction with native soil N. Soil Biology & Biochemistry, 25,1787-1792.
[4]	Beare MH, Coleman DC, Crossley Jr DA, Hendrix PF, Odum EP (1995). A hierarchical approach to evaluating the significance of soil biodiversity to biogeochemical cycling. In: Collins HP, Robertson GP, Klug MJ eds. The Significance and Regulation of Soil Biodiversity. Springer Press, The Netherlands. 5-22.
[5]	Bell TH, Henry HAL (2011). Fine scale variability in soil extracellular enzyme activity is insensitive to rain events and temperature in a mesic system. Pedobiologia, 54,141-146.
[6]	Bengtson P, Barker J, Grayston SJ (2012). Evidence of a strong coupling between root exudation, C and N availability, and stimulated SOM decomposition caused by rhizosphere priming effects. Ecology and Evolution, 2,1843-1852. DOI URL PMID
[7]	Billings SA, Lichter J, Ziegler SE, Hungate BA, Richter DB (2010). A call to investigate drivers of soil organic matter retention vs. mineralization in a high CO ₂ world. Soil Biology & Biochemistry, 42,665-668.
[8]	Bingeman CW, Varner JE, Martin WP (1953). The effect of the addition of organic materials on the decomposition of an organic soil. Soil Science Society of America Proceedings, 17,34-38.
[9]	Bird JA, Herman DJ, Firestone MK (2011). Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biology & Biochemistry, 43,718-725.
[10]	Bityutskii NP, Maiorov EI, Orlova NE (2012). The priming effects induced by earthworm mucus on mineralization and humification of plant residues. European Journal of Soil Biology, 50,1-6.
[11]	Blagodatskaya EV, Kuzyakov Y (2013). Active microorg- anisms in soil: critical review of estimation criteria and approaches. Soil Biology & Biochemistry, 67,192-211.
[12]	Blagodatskaya EV, Anderson TH (1998). Interactive effects of pH and substrate quality on the fungal-to-bacterial ratio and QCO ₂of microbial communities in forest soils. Soil Biology & Biochemistry, 30,1269-1274.
[13]	Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2007). Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Applied Soil Ecology, 37,95-105.
[14]	Blagodatskaya ЕV, Kuzyakov Y (2008). Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biology and Fertility of Soils, 45,115-131.
[15]	Bodelier PLE, Wijlhuizen AG, Blom CWPM, Laanbroek HJ (1997). Effects of photoperiod on growth of and denitrification by Pseudomonas chlororaphis in the root zone of Glyceria maxima, studied in a gnotobiotic microcosm. Plant and Soil, 190,91-103.
[16]	Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013). Soil enzymes in a changing environment: current knowledge and future directions. Soil Biology & Biochemistry, 58,216-234.
[17]	Chapin FS III, Matson PA, Vitousek PM (2011). Principles of Terrestrial Ecosystem Ecology.2nd edn. Springer Press, New York.
[18]	Chen CM, Xie ZB, Zhu JG (2006). Advances in research on priming effect of soil organic carbon. Soils, 38,359-365. (in Chinese with English abstract)
	[ 陈春梅, 谢祖彬, 朱建国. 2006. 土壤有机碳激发效应研究进展. 土壤, 38,359-365.]
[19]	Cheng L, Booker FL, Tu C, Burkey KO, Zhou LS, Shew HD, Rufty TW, Hu SJ (2012). Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO ₂. Science, 337,1084-1087.
[20]	Cheng WX (2009). Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biology & Biochemistry, 41,1795-1801.
[21]	Cheng WX, Johnson DW, Fu SL (2003). Rhizosphere effects on decomposition: controls of plant species, phenology, and fertilization. Soil Science Society of America Journal, 67,1418-1427.
[22]	Cheng WX, Kuzyakov Y (2005). Root effects on soil organic matter decomposition. In: Zobel RW, Wright SF eds. Roots and Soil Management: Interactions Between Roots and the Soil. Agronomy Monograph No. 48, American Society of Agronomy, Crop Science Society of America, Soil Science Society of America, Madison, USA. 119-143.
[23]	Cheng WX, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD (2013). Synthesis and modeling perspectives of rhizosphere priming. New Phytologist, doi: 10.1111/nph.12440.
[24]	Cleveland CC, Liptzin D (2007). C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass? Biogeochemistry, 85,235-252.
[25]	Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins FM, Hyvönen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Megan Steinweg J, Wallenstein MD, Martin Wetterstedt JÅ, Bradford MA (2011). Temperature and soil organic matter decomposition rates―synthesis of current knowledge and a way forward. Global Change Biology, 17,3392-3404.
[26]	Craine JM, Fierer N, McLauchlan KK, Elmore AJ (2013). Reduction of the temperature sensitivity of soil organic matter decomposition with sustained temperature increase. Biogeochemistry, 113,359-368.
[27]	Craine JM, Morrow C, Fierer N (2007). Microbial nitrogen limitation increases decomposition. Ecology, 88,2105-2113. URL PMID
[28]	Dakora FD, Phillips DA (2002). Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil, 245,35-47.
[29]	de Graaff MA, van Groenigen KJ, Six J, Hungate B, van Kessel C (2006). Interactions between plant growth and soil nutrient cycling under elevated CO ₂: a meta-analysis. Global Change Biology, 12,2077-2091.
[30]	de Nobili M, Contin M, Mondini C, Brookes C (2001). Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biology & Biochemistry, 33,1163-1170.
[31]	Degens B, Sparling G (1996). Changes in aggregation do not correspond with changes in labile organic C fractions in soil amended with C ¹⁴-glucose. Soil Biology & Biochemistry, 28,453-462.
[32]	Dijkstra FA, Carrillo Y, Pendall E, Pendall E, Morgan JA (2013). Rhizosphere priming: a nutrient perspective. Frontiers in Microbiology, 39,600-606.
[33]	Dijkstra FA, Cheng WX (2007a). Interactions between soil and tree roots accelerate long-term soil carbon decomposition. Ecology Letters, 10,1046-1053. URL PMID
[34]	Dijkstra FA, Cheng WX (2007b). Moisture modulates rhizosphere effects on C decomposition in two different soil types. Soil Biology & Biochemistry, 39,2264-2274.
[35]	Dijkstra FA, Pendall E, Mosier AR, King JY, Milchunas DG, Morgan JA (2008). Long-term enhancement of N availability and plant growth under elevated CO ₂ in a semi-arid grassland. Functional Ecology, 22,975-982.
[36]	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.
[37]	Edwards KL, Scott TK (1974). Rapid growth responses of corn root segments: effect of pH on elongation. Planta, 119,27-37. URL PMID
[38]	Fierer N, Schimel JP (2003). A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Science Society of America Journal, 67,798-805.
[39]	Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004a). Carbon input to soil may decrease soil carbon content. Ecology Letters, 7,314-320.
[40]	Fontaine S, Bardoux G, Benest D, Verdier B, Mariotti A, Abbadie L (2004b). Mechanisms of the priming effect in a savannah soil amended with cellulose. Soil Science Society of American Journal, 68,125-131.
[41]	Fontaine S, Barot S (2005). Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecology Letters, 8,1075-1087.
[42]	Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011). Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biology & Biochemistry, 43,86-96.
[43]	Fontaine S, Mariotti A, Abbadie L (2003). The priming effect of organic matter: a question of microbial competition? Soil Biology & Biochemistry, 35,837-843.
[44]	Fu SL, Cheng WX (2002). Rhizosphere priming effects on the decomposition of soil organic matter in C ₄ and C ₃ grassland soils. Plant and Soil, 238,289-294.
[45]	Fu SL, Cheng WX, Susfalk R (2002). Rhizosphere respiration varies with plant species and phenology: a greenhouse pot experiment. Plant and Soil, 239,133-140.
[46]	Garcia-Pausas J, Paterson E (2011). Microbial community abundance and structure are determinants of soil organic matter mineralisation in the presence of labile carbon. Soil Biology & Biochemistry, 43,1705-1713.
[47]	Gärdenäs AI, Ågren GI, Bird JA, Clarholm M, Hallin S, Ineson P, Kätterer T, Knicker H, Nilsson SI, Näsholm T, Ogle S, Paustian K, Persson T, Stendah J (2011). Knowledge gaps in soil carbon and nitrogen interactions―from molecular to global scale. Soil Biology & Biochemistry, 43,702-717.
[48]	Geisseler D, Horwath WR, Scow KM (2011). Soil moisture and plant residue addition interact in their effect on extracellular enzyme activity. Pedobiologia, 54,71-78.
[49]	George TS, Fransson AM, Hammond JP, White PJ (2011). Phosphorus nutrition: rhizosphere processes, plant response and adaptations. In: Bünemann E, Oberson A, Frossard E eds. Phosphorus in Action. Springer Press, Berlin. 245-271.
[50]	Gerber S, Joos F, Prentice IC (2004). Sensitivity of a dynamic global vegetation model to climate and atmospheric CO ₂. Global Change Biology, 10,1223-1239.
[51]	Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB (2002). Nonlinear grassland responses to past and future atmospheric CO ₂. Nature, 417,279-282. URL PMID
[52]	Gorissen A, Tietema A, Joosten NN, Estiarte M, Peñuelas J, Sowerby A, Emmett BA, Beier C (2004). Climate change affects carbon allocation to the soil in shrublands. Ecosystems, 7,650-661. .
[53]	Guenet B, Juarez S, Bardoux, G, Abbadie L, Chenu C (2012). Evidence that stable C is as vulnerable to priming effect as is more labile C in soil. Soil Biology & Biochemistry, 52,43-48.
[54]	Guggenberger G, Elliott ET, Frey SD, Six J, Paustian K (1999). Microbial contributions to the aggregation of a cultivated grassland soil amended with starch. Soil Biology & Biochemistry, 31,407-419.
[55]	Hamer U, Marschner B (2005). Priming effects in soils after combined and repeated substrate additions. Geoderma, 128,38-51.
[56]	Herman JL, Osmundson EO, Ayala C, Schneider S, Timms M (2006). The nature and impact of teachers’ formative assessment practices. CSE Technical report 703. Angeles: National Center for Research on Evaluation, Standards, and Student Testing.
[57]	Hodge A, Fitter AH (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceeding of National Academy of Sciences of Sciences of the United States of America, 107,13754-13759.
[58]	Hodge A, Graystone SJ, Ord BG (1996). A novel method for characterisation and quantification of plant root exudates. Plant and Soil, 184,97-104.
[59]	Holland EA, Neff JC, Townsend AR, McKeown B (2000). Uncertainties in the temperature sensitivity of decomposition in tropical and subtropical ecosystems: implications for models. Global Biogeochemical Cycles, 14,1137-1151.
[60]	Hopkins F, Gonzalez-Meler MA, Flower CE, Lynch DJ, Czimczik C, Tang JW, Subke JA (2013). Ecosystem- level controls on root-rhizosphere respiration. New Phytologist, 199,339-351.
[61]	Huang WZ, Zhao XL, Zhu JG, Xie ZB, Zhu CW (2007). Priming effect of soil carbon pools. Chinese Journal of Soil Science, 38,149-154. (in Chinese with English abstract)
	[ 黄文昭, 赵秀兰, 朱建国, 谢祖彬, 朱春梧 (2007). 土壤碳库激发效应. 土壤通报, 38,149-154.]
[62]	Hütsch BW, Augustin J, Merbach W (2002). Plant rhizodeposition―an important source for carbon turnover in soils. Journal of Plant Nutrition and Soil Science, 165,397-407.
[63]	Jenkinson DS, Fox RH, Rayner JH (1985). Interactions between fertilizer nitrogen and soil nitrogen the so-called “priming” effect. Journal of Soil Science, 36,425-444.
[64]	Jones DL, Hodge A, Kuzyakov Y (2004). Plant and mycorrhizal regulation of rhizodeposition. New Phytologist, 163,459-480.
[65]	Joos F, Prentice IC, Sitch S, Meyer R, Hooss G, Plattner GK, Gerber S, Hasselmann K (2001). Global warming feedbacks on terrestrial carbon uptake under the Intergovernmental Panel on Climate Change (IPCC) emission scenarios. Global Biogeochemical Cycles, 15,891-907.
[66]	Kemmitt SJ, Lanyon CV, Waite IS, Wen Q, Addiscot TM, Bird NRA, Donnell AGO, 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.
[67]	Kladivko EJ (2001). Tillage systems and soil ecology. Soil and Tillage Research, 61(1),61-76.
[68]	Kuzyakov Y (2002). Review: factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, 165,382-396.
[69]	Kuzyakov Y (2010). Priming effects: interactions between living and dead organic matter. Soil Biology & Biochemistry, 42,1363-1371. DOI URL
[70]	Kuzyakov Y, Cheng W (2001). Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biology & Biochemistry, 33,1915-1925.
[71]	Kuzyakov Y, Cheng W (2004). Photosynthesis controls of CO ₂ efflux from maize rhizosphere. Plant and Soil, 263,85-99.
[72]	Kuzyakov Y, Ehrensberger H, Stahr K (2001). Carbon partitioning and below-ground translocation by Lolium perenne. Soil Biology & Biochemistry, 33,61-74.
[73]	Kuzyakov Y, Friedel JK, Stahr K (2000). Review of mechanisms and quantification of priming effects. Soil Biology & Biochemistry, 32,1485-1498.
[74]	Kuzyakov Y, Hill PW, Jones DL (2007). Root exudate components change litter decomposition in a simulated rhizosphere depending on temperature. Plant and Soil, 290,293-305.
[75]	Kuzyakov Y, Siniakina SV, Ruehlmann J, Domanski G, Stahr K (2002). Effect of nitrogen fertilisation on below-ground carbon allocation in lettuce. Journal of the Science of Food and Agriculture, 82,1432-1441.
[76]	Kuzyakov Y, Xu XL (2013). Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist, 198,656-669.
[77]	Lal R (2004). Soil carbon sequestration impacts on global climate change and food security. Science, 304,1623-1627. DOI URL PMID
[78]	Lavelle P, Lattaud D, Trogo D, Barois I (1995). Mutualism and biodiversity in soils. Plant and Soil, 170,23-33.
[79]	LeBauer DS, Treseder KK (2008). Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology, 89,371-379. DOI URL PMID
[80]	Li ZY, Li SQ, Li SX (2008). Priming effect of ammonium nitrogen fertilizer on soil nitrogen in typical soils of Loess Plateau. Plant Nutrition and Fertilizer Science, 14,866-873. (in Chinese with English abstract)
	[ 李紫燕, 李世清, 李生秀 (2008). 铵态氮肥对黄土高原典型土壤氮素激发效应的影响. 植物营养与肥料学报, 14,866-873.]
[81]	Liljeroth E, Kuikman P, van Veen JA (1994). Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant and Soil, 161,233-240.
[82]	Liu LL, Greaver TL (2010). A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecology Letters, 13,819-828. URL PMID
[83]	Liu P, Huang JH, Sun OJ, Han XG (2010). Litter decomposition and nutrient release as affected by soil nitrogen availability and litter quality in a semiarid grassland ecosystem. Oecologia, 162,771-780. DOI URL PMID
[84]	Lodge DJ, McDowell WH, McSwiney CP (1994). The importance of nutrient pulses in tropical forests. Trends in Ecology & Evolution, 9,384-387. DOI URL PMID
[85]	Löhnis F (1926). Nitrogen availability of green manures. Soil Science, 22,253-290.
[86]	Lützow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006). Stabiliza- tion of organic matter in temperate soils: mechanisms and their relevance under different soil conditions―a review. European Journal of Soil Science, 57,426-445.
[87]	Ma CE, Kong DL, Chen ZX, Guo JF (2012). Root growth into litter layer and its impact on litter decomposition: a review. Chinese Journal of Plant Ecology, 36,1197-1204. (in Chinese with English abstract)
	[ 马承恩, 孔德良, 陈正侠, 郭俊飞 (2012). 根系在凋落物层中的生长及其对凋落物分解的影响. 植物生态学报, 36,1197-1204.]
[88]	Macdonald CA, Anderson IC, Bardgett RD, Singh BK (2011). Role of nitrogen in carbon mitigation in forest ecosystems. Current Opinion in Environmental Sustainability, 3,303-310. DOI URL
[89]	Marxsen J, Witzei KP (1991). Significance of extracellular enzymes for organic matter degradation and nutrient regeneration in small streams. In: Ryszard JC ed. Microbial Enzymes in Aquatic Environments. Springer Press, New York. 270-285.
[90]	Merbach W, Mirus E, Knof G, Remus R, Ruppel S, Russow R, Gransee A, Schulze J (1999). Release of carbon and nitrogen compounds by plant roots and their possible ecological importance. Journal of Plant Nutrition and Soil Science, 162,373-383. DOI URL
[91]	Moore-Kucera J, Dick RP (2008). Application of ¹³C-labeled litter and root materials for in situ decomposition studies using phospholipid fatty acids. Soil Biology & Biochemistry, 40,2485-2493.
[92]	Morita RY (1990). The starvation-survival state of microorganisms in nature and its relationship to the bioavailable energy. Experientia, 46,813-817.
[93]	Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003). Microbial diversity and soil functions. European Journal of Soil Science, 54,655-670.
[94]	Nottingham AT, Griffiths H, Chamberlain PM, Stott AW, Tanner EVJ (2009). Soil priming by sugar and leaf-litter substrates: a link to microbial groups. Applied Soil Ecology, 42,183-190.
[95]	Nottingham AT, Turner BL, Chamberlain PM, Stott AW, Tanner EVJ (2012). Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry, 111,219-237.
[96]	Nyborg M, Solberg ED, Malhi SS, Isauralde RC (1995). Fertiliser N, crop residue, and tillage alter soil C and N content in a decade. In: Lal R, Kimble J, Levine E, Stewart BA eds. Soil Management and Greenhouse Effect. CRC Press, Boca Raton. 93-101.
[97]	Ohm H, Hamer U, Marschner B (2007). Priming effects in soil size fractions of a podzol Bs horizon after addition of fructose and alanine. Journal of Plant Nutrition and Soil Science, 170,551-559. DOI URL
[98]	Otten W, Hall D, Harris K, Ritz K, Young IM, Gilligan CA (2001). Soil physics, fungal epidemiology and the spread of Rhizoctonia solani. New Phytologist, 151,459-468.
[99]	Pascault N, Ranjard L, Kaisermann A, Bachar D, Christen R, Terrat S, Mathieu O, Lévêque J, Mougel C, Henault C, Lemanceau P, Péan M, Boiry S, Fontaine S, Maron PA (2013). Stimulation of different functional groups of bacteria by various plant residues as a driver of soil priming effect. Ecosystems, 16,810-822. DOI URL
[100]	Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007). Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist, 173,600-610.
[101]	Paterson E, Hall JM, Rattray EAS, Griffiths BS, Ritz K, Killham K (1997). Effect of elevated CO ₂ on rhizosphere carbon flow and soil microbial processes. Global Change Biology, 3,363-377.
[102]	Paterson E, Sim A (1999). Rhizodeposition and C-partitioning of Lolium perenne in axenic culture affected by nitrogen supply and defoliation. Plant and Soil, 216,155-164.
[103]	Pausch J, Zhu B, Kuzyakov Y, Cheng WX (2013). Plant inter-species effects on rhizosphere priming of soil organic matter decomposition. Soil Biology & Biochemistry, 57,91-99.
[104]	Phillips RP, Bernhardt ES, Schlesinger WH (2009). Elevated CO ₂ increases root exudation from loblolly pine ( Pinus taeda) seedlings as an N-mediated response. Tree Physiology, 29,1513-1523. DOI URL PMID
[105]	Phillips RP, Finzi AC, Bernhardt ES (2011). Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO ₂ fumigation. Ecology Letters, 14,187-194. URL PMID
[106]	Phillips RP, Meier IC, Bernhardt ES, Grandy AS, Wickings K, Finzi AC (2012). Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO ₂. Ecology Letters, 15,1042-1049. DOI URL
[107]	Qiao N, Schaefer D, Blagodatskaya E, Zou XM, Xu XL, Kuzyakov Y (2013). Labile carbon retention compensates for CO ₂ released by priming in forest soils. Global Change Biology, doi: 10.1111/gcb.12458. DOI URL PMID
[108]	Rasmussen C, Southard RJ, Horwath WR (2007). Soil mineralogy affects conifer forest soil carbon source utilization and microbial priming. Soil Science Society of America Journal, 71,1141-1150.
[109]	Read DJ, Perez-Moreno J (2003). Mycorrhizas and nutrient cycling in ecosystems―a journey towards relevance? New Phytologist, 157,475-492.
[110]	Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006). Nitrogen limitation constrains sustainability of ecosystem response to CO ₂. Nature, 440,922-925. URL PMID
[111]	Rukshana F, Butterly CR, Baldock JA, Xu JM, Tang C (2012). Model organic compounds differ in priming effects on alkalinity release in soils through carbon and nitrogen mineralisation. Soil Biology & Biochemistry, 51,35-43.
[112]	Rukshana F, Butterly CR, Xu JM, Baldock JA, Tang C (2013). Soil organic carbon contributes to alkalinity priming induced by added organic substrates. Soil Biology & Biochemistry, 65,217-226.
[113]	Sayer EJ, Heard MS, Grant HK, Marthews TR, Tanner EVJ (2011). Soil carbon release enhanced by increased tropical forest litterfall. Nature Climate Change, 1,304-307.
[114]	Schimel DS (1995). Terrestrial ecosystems and the carbon cycle. Global Change Biology, 1,77-91.
[115]	Shahzad T, Chenu C, Repinçay C, Mougin C, Ollier JL, Fontaine S (2012). Plant clipping decelerates the mineralization of recalcitrant soil organic matter under multiple grassland species. Soil Biology & Biochemistry, 51,73-80.
[116]	Shang WH, Shu W, Li YT, Hoosbeek MR, Scarascia-Mugnozza GE (2008). Influence of FACE experiment on soft organic matter pools and priming effect. Ecology and Environment, 17,1518-1522. (in Chinese with English abstract)
	[ 尚卫辉, 舒薇, 李永涛, Hoosbeek MR, Scarascia-Mugnozza GE (2008). FACE试验对土壤有机质库组分及其激发效应的影响. 生态环境, 17,1518-1522.]
[117]	Six J, Jastrow JD (2002). Organic matter turnover. In: Lal R ed. Encyclopedia of Soil Science. Marcel Dekker, New York. 936-942.
[118]	Soon YK (1998). Crop residue and fertilizer management effects on some biological and chemical properties of a Dark Grey Solod. Canadian Journal of Soil Science, 78,707-713.
[119]	Stenström J, Svensson K, Johansson M (2001). Reversible transition between active and dormant microbial states in soil. FEMS Microbiology Ecology, 36,93-104. DOI URL PMID
[120]	Sullivan BW, Hart SC (2013). Evaluation of mechanisms controlling the priming of soil carbon along a substrate age gradient. Soil Biology & Biochemistry, 58,293-301.
[121]	Talbot JM, Allison SD, Treseder KK. (2008). Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Functional Ecology, 22,955-963.
[122]	Thiessen S, Gleixner G, Wutzler T, Reichstein M (2013). Both priming and temperature sensitivity of soil organic matter decomposition depended on microbial biomass―an incubation study. Soil Biology & Biochemistry, 57,739-748.
[123]	Toberman H, Chen CR, Xu ZH (2011). Rhizosphere effects on soil nutrient dynamics and microbial activity in an Australian tropical lowland rainforest. Soil Research, 49,652-660.
[124]	Treseder KK (2008). Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecology Letters, 11,1111-1120. DOI URL PMID
[125]	Trumbore SE, Chadwick OA, Amundson R (1996). Rapid ex- change between soil carbon and atmospheric carbon diox- ide driven by temperature change. Science, 272,393-396.
[126]	von Lützow M, Kögel-Knabner I (2009). Temperature sensitivity of soil organic matter decomposition―What do we know? Biology and Fertility of Soils, 46,1-15.
[127]	Wang RM, Dong KH, He NP, Zhu JZ, Dai J, Shi KK (2013). Effect of enclosure on soil C mineralization and priming effect in Stipa grandis grassland of Inner Mongolia. Acta Ecologica Sinica, 33,3622-3629. (in Chinese with English abstract)
	[ 王若梦, 董宽虎, 何念鹏, 朱剑兴, 代景忠, 施侃侃 (2013). 围封对内蒙古大针茅草地土壤碳矿化及其激发效应的影响. 生态学报, 33,3622-3629.]
[128]	Warembourg FR, Estelrich HD (2001). Plant phenology and soil fertility effects on below-ground carbon allocation for an annual ( Bromus madritensis) and a perennial ( Bromus erectus) grass species. Soil Biology & Biochemistry, 33,1291-1303.
[129]	Zhang FS, Shen JB, Li L, Liu XJ (2004). An overview of rhizosphere processes related with plant nutrition in major cropping systems in China. Plant and Soil, 260,89-99.
[130]	Zhang WD, Wang SL (2012). Effects of NH ₄ ⁺and NO ₃ ^-on litter and soil organic carbon decomposition in a Chinese fir plantation forest in South China. Soil Biology & Biochemistry, 47,116-122.
[131]	Zhang WD, Wang XF, Wang SL (2013). Addition of external organic carbon and native soil organic carbon decom- position: a meta-analysis. PLoS One, 8,e54779. DOI URL PMID
[132]	Zhu B, Cheng WX (2011). Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition. Global Change Biology, 17,2172-2183.
[133]	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.
[134]	Zhu ZX (1963). Study the mechanism of fertilization and several practical issues by exploring manure’s priming effects. Zhejiang Agriculture Science, (3),104-109. (in Chinese with English abstract)
	[ 朱祖祥 (1963). 从绿肥的起爆效应探讨它的肥料机制及其在使用上的若干问题. 浙江农业科学, (3),104-109.]