Chinese Journal of Plant Ecology >
Review
Effects of drought on plant root exudates and associated rhizosphere priming effect: review and prospect
- LONG Ji-Lan ,
- JIANG Zheng ,
- LIU Ding-Qin ,
- MIAO Yu-Xuan ,
- ZHOU Ling-Yan ,
- FENG Ying ,
- PEI Jia-Ning ,
- LIU Rui-Qiang ,
- ZHOU Xu-Hui ,
- FU Yu-Ling
Expand
- 1Zhejiang Tiantong Forest Ecosystem National Observation and Research Station, School of Ecological and Environmental Sciences, East China Normal University, Shanghai 200241, China
2Eco-environmental Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai 201403, China
3School of Forestry, Northeast Forestry University, Harbin 150040, China
Received date: 2023-08-18
Accepted date: 2024-01-16
Online published: 2024-01-22
Supported by
National Natural Science Foundation of China(32271675);National Natural Science Foundation of China(31930072);National Natural Science Foundation of China(42261144688);Natural Science Foundation of Shanghai(21ZR1419200)
Abstract
Root exudates play an important role in soil carbon balance, acting as an important medium for material and energy exchange and information transfer between plant roots and soil, and also the crucial forms for plant response to environmental changes. Frequent extreme drought events accompanied with global climate change have imposed a profound impact on both above- and below-ground plant growth processes. However, significant limitation exists in understanding the responses of root exudates and their mediated rhizosphere priming effect to drought due to the complexity of root-soil interface interactions and the limitation in devices and methods for collecting root exudates. This paper reviews the effects of drought on the quantity and quality of plant root exudates, with emphasis on the rhizosphere priming effect mediated by root exudates under drought stress. The future research focuses on root exudates was also discussed. This study will provide suggestion for soil carbon sink assessment under the future climate change.
Cite this article
LONG Ji-Lan , JIANG Zheng , LIU Ding-Qin , MIAO Yu-Xuan , ZHOU Ling-Yan , FENG Ying , PEI Jia-Ning , LIU Rui-Qiang , ZHOU Xu-Hui , FU Yu-Ling . Effects of drought on plant root exudates and associated rhizosphere priming effect: review and prospect[J]. Chinese Journal of Plant Ecology, 2024 , 48(7) : 817 -827 . DOI: 10.17521/cjpe.2023.0238
References
| [1] | Allard-Massicotte R, Tessier L, Lécuyer F, Lakshmanan V, Lucier J-F, Garneau D, Caudwell L, Vlamakis H, Bais HP, Beauregard PB (2016). Bacillus subtilis early colonization of Arabidopsis thaliana roots involves multiple chemotaxis receptors. mBio, 7, e01664-16. DOI: 10.1128/mBio.01664-16. |
| [2] | Blagodatskaya E, Kuzyakov Y (2013). Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biology & Biochemistry, 67, 192-211. |
| [3] | Brimecombe MJ, de Leij FAAM, Lynch JM (1999). Effect of introduced Pseudomonas fluorescens strains on soil nematode and protozoan populations in the rhizosphere of wheat and pea. Microbial Ecology, 38, 387-397. |
| [4] | Brunn M, Hafner BD, Zwetsloot MJ, Weikl F, Pritsch K, Hikino K, Ruehr NK, Sayer EJ, Bauerle TL (2022). Carbon allocation to root exudates is maintained in mature temperate tree species under drought. New Phytologist, 235, 965-977. |
| [5] | Callesen I, Liski J, Raulund-Rasmussen K, Olsson MT, Tau-Strand L, Vesterdal L, Westman CJ (2003). Soil carbon stores in Nordic well-drained forest soils-relationships with climate and texture class. Global Change Biology, 9, 358-370. |
| [6] | Calvo OC, Franzaring J, Schmid I, Fangmeier A (2019). Root exudation of carbohydrates and cations from barley in response to drought and elevated CO2. Plant and Soil, 438, 127-142. |
| [7] | Calvo OC, 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. |
| [8] | Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019). Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science, 10, 157. DOI: 10.3389/fpls.2019.00157. |
| [9] | Canarini A, Merchant A, Dijkstra FA (2016). Drought effects on Helianthus annuus and Glycine max metabolites: from phloem to root exudates. Rhizosphere, 2, 85-97. |
| [10] | Cesari A, Paulucci N, López-Gómez M, Hidalgo-Castellanos J, Plá CL, Dardanelli MS (2019). Restrictive water condition modifies the root exudates composition during peanut-PGPR interaction and conditions early events, reversing the negative effects on plant growth. Plant Physiology & Biochemistry, 142, 519-527. |
| [11] | Chai YN, Schachtman DP (2022). Root exudates impact plant performance under abiotic stress. Trends in Plant Science, 27, 80-91. |
| [12] | Chari NR, Taylor BN (2022). Soil organic matter formation and loss are mediated by root exudates in a temperate forest. Nature Geoscience, 15, 1011-1016. |
| [13] | Chen YL, Yao ZM, Sun Y, Wang EZ, Tian CJ, Sun Y, Liu J, Sun CY, Tian L (2022). Current studies of the effects of drought stress on root exudates and rhizosphere microbiomes of crop plant species. International Journal of Molecular Sciences, 23, 2374. DOI: 10.3390/ijms23042374. |
| [14] | Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD (2014). Synthesis and modeling perspectives of rhizosphere priming. New Phytologist, 201, 31-44. |
| [15] | de Vries FT, Brown C, Stevens CJ (2016). Grassland species root response to drought: consequences for soil carbon and nitrogen availability. Plant and Soil, 409, 297-312. |
| [16] | de Vries FT, Williams A, Stringer F, Willcocks R, McEwing R, Langridge H, Straathof AL (2019). Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling. New Phytologist, 224, 132-145. |
| [17] | 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, et al. (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. |
| [18] | 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. |
| [19] | Gagné-Bourque F, Bertrand A, Claessens A, Aliferis KA, Jabaji S (2016). Alleviation of drought stress and metabolic changes in timothy (Phleum pratense L.) colonized with Bacillus subtilis B26. Frontiers in Plant Science, 7, 584. DOI: 10.3389/fpls.2016.00584. |
| [20] | Gargallo-Garriga A, Preece C, Sardans J, Oravec M, Urban O, Pe?uelas J (2018). Root exudate metabolomes change under drought and show limited capacity for recovery. Scientific Reports, 8, 12696. DOI: 10.1038/s41598-018-30150-0. |
| [21] | Ghatak A, Schindler F, Bachmann G, Engelmeier D, Bajaj P, Brenner M, Fragner L, Varshney RK, Subbarao GV, Chaturvedi P, Weckwerth W (2022). Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity. Biology & Fertility of Soils, 58, 291-306. |
| [22] | Guenet B, Camino-Serrano M, Ciais P, Tifafi M, Maignan F, Soong JL, Janssens IA (2018). Impact of priming on global soil carbon stocks. Global Change Biology, 24, 1873-1883. |
| [23] | Hagedorn F, Joseph J, Peter M, Luster J, Pritsch K, Geppert U, Kerner R, Molinier V, Egli S, Schaub M, Liu J, Li M, Sever K, Weiler M, Siegwolf RTW, et al. (2016). Recovery of trees from drought depends on belowground sink control. Nature Plants, 2, 16111. DOI: 10.1038/nplants.2016.111. |
| [24] | Hartmann H, Moura CF, Anderegg WRL, Ruehr NK, Salmon Y, Allen CD, Arndt SK, Breshears DD, Davi H, Galbraith D, Ruthrof KX, Wunder J, Adams HD, Bloemen J, Cailleret M, et al. (2018). Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytologist, 218, 15-28. |
| [25] | Henry A, Doucette W, Norton J, Bugbee B (2007). Changes in crested wheatgrass root exudation caused by flood, drought, and nutrient stress. Journal of Environmental Quality, 36, 904-912. |
| [26] | Henry C, John GP, Pan R, Bartlett MK, Fletcher LR, Scoffoni C, Sack L (2019). A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nature Communications, 10, 3398. DOI: 10.1038/s41467-019-11006-1. |
| [27] | Huo CF, Luo YQ, Cheng WX (2017). Rhizosphere priming effect: a meta-analysis. Soil Biology & Biochemistry, 111, 78-84. |
| [28] | Jia X, Wang WK, Chen ZH, He YH, Liu JX (2014). Concentrations of secondary metabolites in tissues and root exudates of wheat seedlings changed under elevated atmospheric CO2 and cadmium-contaminated soils. Environmental & Experimental Botany, 107, 134-143. |
| [29] | Jiang Z, Fu Y, Zhou L, He Y, Zhou G, Dietrich P, Long J, Wang X, Jia S, Ji Y, Jia Z, Song B, Liu R, Zhou X (2023). Plant growth strategy determines the magnitude and direction of drought-induced changes in root exudates in subtropical forests. Global Change Biology, 29, 3476-3488. |
| [30] | Jiang Z, Thakur MP, Liu R, Zhou G, Zhou L, Fu Y, Zhang P, He Y, Shao J, Gao J, Li N, Wang X, Jia S, Chen Y, Zhang C, Zhou X (2022). Soil P availability and mycorrhizal type determine root exudation in sub-tropical forests. Soil Biology & Biochemistry, 171, 108722. DOI: 10.1016/j.soilbio.2022.108722. |
| [31] | Johnson DM, Domec JC, Carter Berry Z, Schwantes AM, McCulloh KA, Woodruff DR, Wayne Polley H, Wortemann R, Swenson JJ, Scott Mackay D, McDowell NG, Jackson RB (2018). Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought. Plant, Cell & Environment, 41, 576-588. |
| [32] | Karlowsky S, Augusti A, Ingrisch J, Akanda MKU, Bahn M, Gleixner G (2018). Drought-induced accumulation of root exudates supports post-drought recovery of microbes in mountain grassland. Frontiers in Plant Science, 9, 1593. DOI: 10.3389/fpls.2018.01593. |
| [33] | Karst J, Gaster J, Wiley E, Landh?usser SM (2017). Stress differentially causes roots of tree seedlings to exude carbon. Tree Physiology, 37, 154-164. |
| [34] | 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. |
| [35] | Kuzyakov Y (2010). Priming effects: interactions between living and dead organic matter. Soil Biology & Biochemistry, 42, 1363-1371. |
| [36] | Kuzyakov Y, Friedel JK, Stahr K (2000). Review of mechanisms and quantification of priming effects. Soil Biology & Biochemistry, 32, 1485-1498. |
| [37] | Li M, Zhao XZ, Wang HY, Lu ZK, Ding GJ (2022). Effects of drought stress and ectomycorrhizal fungi on the root morphology and exudates of Pinus massoniana seedlings. Scientia Silvae Sinicae, 58(7), 63-72. |
| [李敏, 赵熙州, 王好运, 卢中科, 丁贵杰 (2022). 干旱胁迫及外生菌根菌对马尾松幼苗根系形态及分泌物的影响. 林业科学, 58(7), 63-72.] | |
| [38] | Li YM, Yang F, Han PL, Zhou WL, Wang JH, Yan XF, Lin JX (2022). Research progress on the mechanism of root exudates in response to abiotic stresses. Chinese Journal of Applied & Environmental Biology, 28, 1384-1392. |
| [李月明, 杨帆, 韩沛霖, 周万里, 王竞红, 阎秀峰, 蔺吉祥 (2022). 植物根系分泌物响应非生物胁迫机理研究进展. 应用与环境生物学报, 28, 1384-1392.] | |
| [39] | 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 (2019). Carbon input and allocation by rice into paddy soils: a review. Soil Biology & Biochemistry, 133, 97-107. |
| [40] | Lu J, Dijkstra FA, Wang P, Cheng W (2018a). Rhizosphere priming of grassland species under different water and nitrogen conditions: a mechanistic hypothesis of C-N interactions. Plant and Soil, 429, 303-319. |
| [41] | Lu T, Ke M, Lavoie M, Jin Y, Fan X, Zhang Z, Fu Z, Sun L, Gillings M, Pe?uelas J, Qian H, Zhu Y (2018b). Rhizosphere microorganisms can influence the timing of plant flowering. Microbiome, 6, 231. DOI: 10.1186/s40168-018-0615-0. |
| [42] | Luo DD, Wang CK, Jin Y (2021). Response mechanisms of hydraulic systems of woody plants to drought stress. Chinese Journal of Plant Ecology, 45, 925-941. |
| [罗丹丹, 王传宽, 金鹰 (2021). 木本植物水力系统对干旱胁迫的响应机制. 植物生态学报, 45, 925-941.] | |
| [43] | Ma ZL (2020). Responses of root exudative carbon and nitrogen inputs to warming in an alpine scrub ecosystem on the eastern Qinghai-Tibet Plateau. Ecology & Environmental Sciences, 29, 643-649. |
| [马志良 (2020). 青藏高原东缘高寒灌丛根系分泌物碳氮输入对增温的响应. 生态环境学报, 29, 643-649.] | |
| [44] | Mao MX, Zhu F (2021). Progress and perspective in research on plant resistance mediated by root exudates. Chinese Journal of Eco-Agriculture, 29, 1649-1657. |
| [毛梦雪, 朱峰 (2021). 根系分泌物介导植物抗逆性研究进展与展望. 中国生态农业学报(中英文), 29, 1649-1657.] | |
| [45] | McLaughlin S, Zhalnina K, Kosina S, Northen TR, Sasse J (2023). The core metabolome and root exudation dynamics of three phylogenetically distinct plant species. Nature Communications, 14, 1649. DOI: 10.1038/s41467-023-37164-x. |
| [46] | Mommer L, Hinsinger P, Prigent-Combaret C, Visser EJW (2016). Advances in the rhizosphere: stretching the interface of life. Plant and Soil, 407, 1-8. |
| [47] | Monohon SJ, Manter DK, Vivanco JM (2021). Conditioned soils reveal plant-selected microbial communities that impact plant drought response. Scientific Reports, 11, 21153. DOI: 10.1038/s41598-021-00593-z. |
| [48] | Murphy CJ, Baggs EM, Morley N, Wall DP, Paterson E (2017). Nitrogen availability alters rhizosphere processes mediating soil organic matter mineralisation. Plant and Soil, 417, 499-510. |
| [49] | Naylor D, Coleman-Derr D (2018). Drought stress and root-associated bacterial communities. Frontiers in Plant Science, 8, 2223. DOI: 10.3389/fpls.2017.02223. |
| [50] | Oburger E, Jones DL (2018). Sampling root exudates-mission impossible? Rhizosphere, 6, 116-133. |
| [51] | Ouédraogo DY, Mortier F, Gourlet-Fleury S, Freycon V, Picard N (2013). Slow-growing species cope best with drought: evidence from long-term measurements in a tropical semi-deciduous moist forest of Central Africa. Journal of Ecology, 101, 1459-1470. |
| [52] | Pan FJ, Liang YM, Zhang W, Zhao J, Wang KL (2016). Enhanced nitrogen availability in karst ecosystems by oxalic acid release in the rhizosphere. Frontiers in Plant Science, 7, 687. DOI: 10.3389/fpls.2016.00687. |
| [53] | Pausch J, Kuzyakov Y (2018). Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale. Global Change Biology, 24, 1-12. |
| [54] | 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. |
| [55] | Piao SL, Zhang XP, Chen AP, Liu Q, Lian X, Wang XH, Peng SS, Wu XC (2019). The impacts of climate extremes on the terrestrial carbon cycle: a review. Science China Earth Sciences, 49, 1321-1334. |
| [朴世龙, 张新平, 陈安平, 刘强, 连旭, 王旭辉, 彭书时, 吴秀臣 (2019). 极端气候事件对陆地生态系统碳循环的影响. 中国科学: 地球科学, 49, 1321-1334.] | |
| [56] | Preece C, Farré-Armengol G, Llusià J, Pe?uelas J (2018). Thirsty tree roots exude more carbon. Tree Physiology, 38, 690-695. |
| [57] | Preece C, Farré-Armengol G, Verbruggen E, Pe?uelas J (2021). Interactive effects of soil water content and nutrients on root exudation in two Mediterranean tree species. Soil Biology & Biochemistry, 163, 108453. DOI: 10.1016/j.soilbio.2021.108453. |
| [58] | Preece C, Pe?uelas J (2016). Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant & Soil, 409, 1-17. |
| [59] | Pretzsch H, Grams T, H?berle KH, Pritsch K, Bauerle T, R?tzer T (2020). Growth and mortality of Norway spruce and European beech in monospecific and mixed-species stands under natural episodic and experimentally extended drought. Results of the KROOF throughfall exclusion experiment. Trees, 34, 957-970. |
| [60] | Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012). Carbon allocation in grassland communities under drought stress followed by 14C pulse labeling. Soil Biology & Biochemistry, 55, 132-139. |
| [61] | Schmidt JE, Bowles TM, Gaudin ACM (2016). Using ancient traits to convert soil health into crop yield: impact of selection on maize root and rhizosphere function. Frontiers in Plant Science, 7, 373. DOI: 10.3389/fpls.2016.00373. |
| [62] | Staszel K, Lasota J, B?ońska E (2022). Effect of drought on root exudates from Quercus petraea and enzymatic activity of soil. Scientific Reports, 12, 7635. DOI: 10.1038/s41598-022-11754-z. |
| [63] | Su B, Huang J, Fischer T, Wang Y, Kundzewicz ZW, Zhai J, Sun H, Wang A, Zeng X, Wang G, Tao H, Gemmer M, Li X, Jiang T (2018). Drought losses in China might double between the 1.5 °C and 2.0 °C warming. Proceedings of the National Academy of Sciences of the United States of America, 115, 10600-10605. |
| [64] | Sulman BN, Phillips RP, Oishi AC, Shevliakova E, Pacala SW (2014). Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nature Climate Change, 4, 1099-1102. |
| [65] | Sun LJ, Ataka M, Han MG, Han YF, Gan DY, Xu TL, Guo YP, Zhu B (2021). Root exudation as a major competitive fine-root functional trait of 18 coexisting species in a subtropical forest. New Phytologist, 229, 259-271. |
| [66] | Tan B, Li YH, Liu TG, Tan X, He YX, You XJ, Leong KH, Liu C, Li LG (2021). Response of plant rhizosphere microenvironment to water management in soil- and substrate-based controlled environment agriculture (CEA) systems: a review. Frontiers in Plant Science, 12, 691651. DOI: 10.3389/fpls.2021.691651. |
| [67] | Ulrich DEM, Clendinen CS, Alongi F, Mueller RC, Chu R, Toyoda J, Gallegos-Graves LV, Goemann HM, Peyton B, Sevanto S, Dunbar J (2022). Root exudate composition reflects drought severity gradient in blue grama (Bouteloua gracilis). Scientific Reports, 12, 12581. DOI: 10.1038/s41598-022-16408-8. |
| [68] | Vranova V, Rejsek K, Skene KR, Janous D, Formanek P (2013). Methods of collection of plant root exudates in relation to plant metabolism and purpose: a review. Journal of Plant Nutrition & Soil Science, 176, 175-199. |
| [69] | Wang R, Bicharanloo B, Shirvan MB, Cavagnaro TR, Jiang Y, Keitel C, Dijkstra FA (2021a). A novel 13C pulse-labelling method to quantify the contribution of rhizodeposits to soil respiration in a grassland exposed to drought and nitrogen addition. New Phytologist, 230, 857-866. |
| [70] | Wang R, Cavagnaro T, Jiang Y, Keitel C, Dijkstra F (2021b). Carbon allocation to the rhizosphere is affected by drought and nitrogen addition. Journal of Ecology, 109, 3699-3709. |
| [71] | Wen Z, Li H, Shen Q, Tang X, Xiong C, Li H, Pang J, Ryan MH, Lambers H, Shen J (2019). Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytologist, 223, 882-895. |
| [72] | Williams A, de Vries FT (2020). Plant root exudation under drought: implications for ecosystem functioning. New Phytologist, 225, 1899-1905. |
| [73] | Wu C, Xiong DC, Zhong XF (2021). Effects of warming on plant fine root exudates: a review. Journal of Subtropical Resources & Environment, 16, 80-85. |
| [吴晨, 熊德成, 钟羡芳 (2021). 增温对植物根系分泌物特征的影响研究进展. 亚热带资源与环境学报, 16, 80-85.] | |
| [74] | 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. |
| [吴林坤, 林向民, 林文雄 (2014). 根系分泌物介导下植物-土壤-微生物互作关系研究进展与展望. 植物生态学报, 38, 298-310.] | |
| [75] | Xu MH, Peng F, You QG, Guo J, Tian XF, Xue X, Liu M (2015). Year-round warming and autumnal clipping lead to downward transport of root biomass, carbon and total nitrogen in soil of an alpine meadow. Environmental & Experimental Botany, 109, 54-62. |
| [76] | Yan ZQ, Kang EZ, Zhang KR, Li Y, Hao YB, Wu HD, Li M, Zhang XD, Wang JZ, Yan L, Kang XM (2021). Plant and soil enzyme activities regulate CO2 efflux in alpine peatlands after 5 years of simulated extreme drought. Frontiers in Plant Science, 12, 756956. DOI: 10.3389/fpls.2021.756956. |
| [77] | Yin H, Wheeler E, Phillips RP (2014). Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biology & Biochemistry, 78, 213-221. |
| [78] | Yin HJ, Zhang ZL, Liu Q (2018). Root exudates and their ecological consequences in forest ecosystems: problems and perspective. Chinese Journal of Plant Ecology, 42, 1055-1070. |
| [尹华军, 张子良, 刘庆 (2018). 森林根系分泌物生态学研究: 问题与展望. 植物生态学报, 42, 1055-1070.] | |
| [79] | Zeng ZQ, Wu WX, Li YM, Huang C, Zhang XQ, Pe?uelas J, Zhang Y, Gentine P, Li ZL, Wang XY, Huang H, Ren XS, Ge QS (2023). Increasing meteorological drought under climate change reduces terrestrial ecosystem productivity and carbon storage. One Earth, 6, 1326-1339. |
| [80] | Zhang FS, Shen JB (1999). Preliminary development of the theoretical concept on rhizosphere micro-ecosystem. Review of China Agricultural Science & Technology, 1, 15-20. |
| [张福锁, 申建波 (1999). 根际微生态系统理论框架的初步构建. 中国农业科技导报, 1, 15-20.] | |
| [81] | Zhang XZ, Li TX, Wang YD (2007). Relationship between growth environment and root exudates of plants: a review. Chinese Journal of Soil Science, 38, 785-789. |
| [张锡洲, 李廷轩, 王永东 (2007). 植物生长环境与根系分泌物的关系. 土壤通报, 38, 785-789.] | |
| [82] | Zhao M, Zhao J, Yuan J, Hale L, Wen T, Huang Q, Vivanco JM, Zhou J, Kowalchuk GA, Shen Q (2021). Root exudates drive soil-microbe-nutrient feedbacks in response to plant growth. Plant, Cell & Environment, 44, 613-628. |
| [83] | Zhou GY, Li L, Wu AC (2020). Effect of drought on forest ecosystem under warming climate. Journal of Nanjing University of Information Science & Technology (Natural Science Edition), 12, 81-88. |
| [周国逸, 李琳, 吴安驰 (2020). 气候变暖下干旱对森林生态系统的影响. 南京信息工程大学学报(自然科学版), 12, 81-88.] | |
| [84] | Zhou GY, Zhou LY, Shao JJ, Zhou XH (2020). Effects of extreme drought on terrestrial ecosystems: review and prospects. Chinese Journal of Plant Ecology, 44, 515-525. |
| [周贵尧, 周灵燕, 邵钧炯, 周旭辉 (2020). 极端干旱对陆地生态系统的影响: 进展与展望. 植物生态学报, 44, 515-525.] | |
| [85] | Zhu B, Gutknecht JLM, Herman DJ, Keck DC, Firestone MK, Cheng W (2014). Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biology & Biochemistry, 76, 183-192. |
Options