Abstract
Purpose
Plants growing in the soils of karst forests associate with arbuscular mycorrhizae (AM) or ectomycorrhizae (ECM) to acquire nutrients. We researched how these different mycorrhizal associations affect rhizosphere soil nutrient economy in these calcareous soils.
Methods
Bulk and rhizosphere soils were sampled beneath 25 AM and 9 ECM plants growing in primary forests at the Puding Karst Critical Zone Observatory. Nutrient contents and potential enzyme activities were analyzed to test the effect of different types of mycorrhizal association on rhizosphere soil nitrogen (N) and phosphorus (P) economies.
Results
The contents of nitrate-N and available-P were markedly lower in the rhizospheres of ECM plants compared to AM plants. Ectomycorrhizal plants promoted relatively greater investment in N-acquisition enzymes, in contrast, AM plants caused relatively greater investment in P-acquisition enzymes. The decreased pH in the rhizospheres of AM plants likely promoted the greater P availability.
Conclusion
Our results revealed how plants that form contrasting mycorrhizal associations have fundamentally different effects on rhizospheric nutrient economies in the low fertility karst soils of southwest China. Differentiation in N- and P-acquisition capacity of these plants have implications for species coexistence and the high levels of plant biodiversity observed in these forests.
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Data availability
Requests for data or other materials should be directed to Xinyu Zhang (zhangxy@igsnrr.ac.cn).
Code availability
Not applicable.
Change history
03 July 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11104-021-05032-6
References
Averill C (2016) Slowed decomposition in ectomycorrhizal ecosystems is independent of plant chemistry. Soil Biol Biochem 102:52–54. https://doi.org/10.1016/j.soilbio.2016.08.003
Bao SD (2008) Soil and agricultural chemistry analysis, 3rd edn. China Agricultural Press, Beijing
Bödeker ITM, Lindahl BD, Olson Å, Clemmensen KE, Treseder K (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978. https://doi.org/10.1111/1365-2435.12677
Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017. https://doi.org/10.1111/j.1365-313X.2010.04385.x
Bunn RA, Simpson DT, Bullington LS, Lekberg Y, Janos DP (2019) Revisiting the 'direct mineral cycling' hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why? ISME J 13:1891–1898. https://doi.org/10.1038/s41396-019-0403-2
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 Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Cheeke TE, Phillips RP, Brzostek ER, Rosling A, Bever JD, Fransson P (2017) Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function. New Phytol 214:432–442. https://doi.org/10.1111/nph.14343
Chen X, Ding ZJ, Tang M, Zhu B (2018) Greater variations of rhizosphere effects within mycorrhizal group than between mycorrhizal group in a temperate forest. Soil Biol Biochem 126:237–246. https://doi.org/10.1016/j.soilbio.2018.08.026
Du YX, Pan GX, Li LQ, Hu ZL, Wang XZ (2010) Leaf N/P ratio and nutrient reuse between dominant species and stands: predicting phosphorus deficiencies in karst ecosystems, southwestern China. Environ Earth Sci 64:299–309. https://doi.org/10.1007/s12665-010-0847-1
Fransson P, Andersson A, Norström S, Bylund D, Bent E (2016) Ectomycorrhizal exudates and pre-exposure to elevated CO2 affects soil bacterial growth and community structure. Fungal Ecol 20:211–224. https://doi.org/10.1016/j.funeco.2016.01.003
Guo ZM, Zhang XY, Green SM, Dungait JAJ, Wen XF, Quine TA (2019) Soil enzyme activity and stoichiometry along a gradient of vegetation restoration at the karst critical zone Observatory in Southwest China. Land Degrad Dev 30:1916–1927. https://doi.org/10.1002/ldr.3389
Hinsinger P, Brauman A, Devau N, Gérard F, Jourdan C, Laclau JP, Le Cadre E, Jaillard B, Plassard C (2011) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61. https://doi.org/10.1007/s11104-011-0903-y
Hu YJ, Xia YH, Sun Q, Liu KP, Chen XB, Ge TD, Zhu BL, Zhu ZK, Zhang ZH, Su YR (2018) Effects of long-term fertilization on phoD-harboring bacterial community in karst soils. Sci Total Environ 628-629:53–63. https://doi.org/10.1016/j.scitotenv.2018.01.314
Jacobs LM, Sulman BN, Brzostek ER, Feighery JJ, Phillips RP (2018) Interactions among decaying leaf litter, root litter and soil organic matter vary with mycorrhizal type. J Ecol 106:502–513. https://doi.org/10.1111/1365-2745.12921
Keller AB, Phillips RP (2019) Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. New Phytol 222:556–564. https://doi.org/10.1111/nph.15524
Keller AB, Brzostek ER, Craig ME, Fisher JB, Phillips RP (2021) Root-derived inputs are major contributors to soil carbon in temperate forests, but vary by mycorrhizal type. Ecol Lett 24:626–635. https://doi.org/10.1111/ele.13651
Kilpeläinen J, Barbero-López A, Adamczyk B, Aphalo PJ, Lehto T (2019) Morphological and ecophysiological root and leaf traits in ectomycorrhizal, arbuscular-mycorrhizal and non-mycorrhizal Alnus incana seedlings. Plant Soil 436:283–297. https://doi.org/10.1007/s11104-018-03922-w
Kong DL, Ma CE, Zhang Q, Li L, Chen XY, Zeng H, Guo DL (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203:863–872. https://doi.org/10.1111/nph.12842
Kou L, Guo DL, Yang H, Gao WL, Li SG (2015) Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtropical China. Plant Soil 391:207–218. https://doi.org/10.1007/s11104-015-2420-x
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199. https://doi.org/10.1016/j.soilbio.2015.01.025
Li HB, Liu BT, McCormack ML, Ma ZQ, Guo DL (2017) Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient. New Phytol 216:1140–1150. https://doi.org/10.1111/nph.14710
Li DD, Zhang XY, Green SM, Dungait JAJ, Wen XF, Tang YQ, Guo ZM, Yang Y, Sun XM, Quine TA (2018) Nitrogen functional gene activity in soil profiles under progressive vegetative recovery after abandonment of agriculture at the Puding karst critical zone observatory, SW China. Soil Biol Biochem 125:93–102. https://doi.org/10.1016/j.soilbio.2018.07.004
Lin GG, Guo DL, Li L, Ma CE, Zeng DH (2018) Contrasting effects of ectomycorrhizal and arbuscular mycorrhizal tropical tree species on soil nitrogen cycling: the potential mechanisms and corresponding adaptive strategies. OIKOS 127:518–530. https://doi.org/10.1111/oik.04751
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. https://doi.org/10.1038/nature25783
Midgley MG, Phillips RP (2016) Resource stoichiometry and the biogeochemical consequences of nitrogen deposition in a mixed deciduous forest. Ecology 97:3369–3378
Midgley MG, Brzostek E, Phillips RP, Austin A (2015) Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees. J Ecol 103:1454–1463. https://doi.org/10.1111/1365-2745.12467
Ni J, Luo DH, Xia J, Zhang ZH, Hu G (2015) Vegetation in karst terrain of southwestern China allocates more biomass to roots. Solid Earth 6:799–810. https://doi.org/10.5194/se-6-799-2015
Phillips RP, Fahey TJ (2006) Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Ecology 87:1302–1313
Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221
Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP (2016) Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytol 209:1184–1195. https://doi.org/10.1111/nph.13720
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315. https://doi.org/10.1016/s0038-0717(02)00074-3
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798. https://doi.org/10.1038/nature08632
Soil Survey Staff (2010) Keys to soil taxonomy, eleventh. edn. USDA Natural Resources Conservation Service, Washington DC
Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GDA, Reich PB, Nabuurs GJ, de-Miguel S, Zhou M, Picard N, Herault B, Zhao X, Zhang C, Routh D, Peay KG, consortium G (2019) Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569:404–408. https://doi.org/10.1038/s41586-019-1128-0
Tedersoo L, Bahram M (2019) Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes. Biol Rev 94:1857–1880. https://doi.org/10.1111/brv.12538
Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367:eaba1223. https://doi.org/10.1126/science.aba1223
Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304. https://doi.org/10.1111/j.1574-6941.2007.00337.x
van der Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:1–15
Waring BG, Adams R, Branco S, Powers JS (2016) Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytol 209:845–854. https://doi.org/10.1111/nph.13654
Yin HJ, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221. https://doi.org/10.1016/j.soilbio.2014.07.022
Zhang L, Shi N, Fan J, Wang F, George TS, Feng G (2018) Arbuscular mycorrhizal fungi stimulate organic phosphate mobilization associated with changing bacterial community structure under field conditions. Environ Microbiol 20:2639–2651. https://doi.org/10.1111/1462-2920.14289
Zhang ZL, Yuan YS, Liu Q, Yin HJ (2019) Plant nitrogen acquisition from inorganic and organic sources via root and mycelia pathways in ectomycorrhizal alpine forests. Soil Biol Biochem 136:107517. https://doi.org/10.1016/j.soilbio.2019.06.013
Zhu J, Li M, Whelan M (2018a) Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ 612:522–537. https://doi.org/10.1016/j.scitotenv.2017.08.095
Zhu K, McCormack ML, Lankau RA, Egan JF, Wurzburger N (2018b) Association of ectomycorrhizal trees with high carbon-to-nitrogen ratio soils across temperate forests is driven by smaller nitrogen not larger carbon stocks. J Ecol 106:524–535. https://doi.org/10.1111/1365-2745.12918
Acknowledgements
This study was jointly financed by the State Key, General and Science Centre Projects of National Natural Science Foundation of China (Nos. 41830860, 41877091, 31988102), National Key Research and Development Program ‘Intergovernmental Cooperation in International Science and Technology Innovation’ Key Special Project (2019YFE0126500), and the National Environmental Research Council and Newton of the UK (Grant No. NE/N007603/1). This study was conducted at the Puding Karst Ecosystem Station of Chinese Academy of Sciences.
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X. Z. and X. W. planned and designed the research. X. Z., Y. Y., D. L. and Z. G. conducted fieldwork. Y. Y. performed experiments and analyzed data. Y. Y., X. Z., I. P. H., J. A. J. D. and T. A. Q. wrote the manuscript. All authors contributed substantially to the drafts and gave final approval for publication.
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The original online version of this article was revised: In Figure 5, the AM and ECM photos were put in the opposite place. No other aspects of the results presented in the publication were affected. The caption of the figure stays unchanged. Also, in Table S1 of the supplementary materials, Xylosma racemosum which was in the last row of the Table S1, was assigned to wrong Mycorrhizal type. It should be AM.
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Yang, Y., Zhang, X., Hartley, I.P. et al. Contrasting rhizosphere soil nutrient economy of plants associated with arbuscular mycorrhizal and ectomycorrhizal fungi in karst forests. Plant Soil 470, 81–93 (2022). https://doi.org/10.1007/s11104-021-04950-9
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DOI: https://doi.org/10.1007/s11104-021-04950-9