Abstract
Key message
The quantity of root exudate carbon produced by Quercus crispula Blume was strongly influenced by the amount of solar radiation 1 day before collection.
Abstract
We aimed to investigate seasonality in the quantity of root exudate produced, and the factors affecting exudate quantity, in mature Quercus crispula Blume trees throughout the growing season. We also aimed to understand the timespan of exudation, from production of photosynthate to release as exudate. We measured the amount of root exudate C produced by Q. crispula, as well as environmental factors including solar radiation and soil and air temperature throughout the growing season. The model best explaining the amount of exudate C, based on the lowest Akaike’s information criterion, was selected to determine the environmental factors that affect exudation. The quantity of exudates did not show clear seasonality, and instead varied widely among sampling dates. A regression model with daily solar radiation for 1 day before sample collection as the sole factor affecting the quantity of exudates was selected as the best model. Solar radiation, which fluctuated greatly among days, more strongly affected the quantity of exudates produced than factors that fluctuated seasonally, such as average temperature. Furthermore, most root exudates from Q. crispula are released within 1 day of being generated by photosynthesis, rather than over several days.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98. https://doi.org/10.1016/j.tplants.2013.11.006
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192. https://doi.org/10.1016/S0038-0717(03)00179-2
Bekkara F, Jay M, Viricel MR, Rome S (1998) Distribution of phenolic compounds within seed and seedlings of two Vicia faba cvs differing in their seed tannin content, and study of their seed and root phenolic exudations. Plant Soil 203:27–36. https://doi.org/10.1023/A:1004365913726
Bertin C, Yang XH, Weston L (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83. https://doi.org/10.1023/A:1026290508166
Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673. https://doi.org/10.1016/j.tplants.2017.05.004
Ekblad A, Nordgren A (2002) Is growth of soil microorganisms in boreal forests limited by carbon or nitrogen availability? Plant Soil 242:115–122. https://doi.org/10.1023/A:1019698108838
Epron D, Ngao J, Mannoura M, Bakker MR, Zeller B, Bazot S, Bosc A, Plain C, Lata JC, Priault P, Barthes L, Loustau D (2011) Seasonal variations of belowground carbon transfer assessed by in situ 13CO2 pulse labelling of trees. Biogeosci Discuss 8:885–919. https://doi.org/10.5194/bg-8-1153-2011
Epron D, Bahn M, Derrien D, Lattanzi FA, Pumpanen J, Gessler A, Högberg P, Maillard P, Dannoura M, Gérant D, Buchmann N (2012) Pulse-labelling trees to study carbon allocation dynamics: a review of methods, current knowledge and future prospects. Tree Physiol 32:776–798. https://doi.org/10.1093/treephys/tps057
Fahey TJ, Siccama TG, Driscoll CT, Likens GE, Campbell J, Johnson CE, Aber JD, Cole JJ, Fisk MC, Groffman PM, Hamburg SP, Holmes RT, Schwarz PA, Yanai RD (2005) The biogeochemistry of carbon at Hubbard Brook. Biogeochemistry 75:109–176. https://doi.org/10.1007/s10533-004-6321-y
FAO (2015) World reference base for soil resources 2014. http://www.fao.org/3/a-i3794e.pdf. Accessed Oct 2017
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. Glob Chang Biol 21:2082–2094. https://doi.org/10.1111/gcb.12816
Fischer H, Ingwersen J, Kuzyakov Y (2010) Microbial uptake of low-molecular-weight organic substances out-competes sorption in soil. Eur J Soil Sci 61:504–513. https://doi.org/10.1111/j.1365-2389.2010.01244.x
Haichar FEZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. https://doi.org/10.1016/j.soilbio.2014.06.017
Hosokawa N, Isobe K, Urakawa R, Tateno R, Fukuzawa K, Watanabe T, Shibata H (2017) Soil freeze-thaw with root litter alters N transformations during the dormant season in soils under two temperate forests in northern Japan. Soil Biol Biochem 114:270–278. https://doi.org/10.1016/j.soilbio.2017.07.025
Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B, Rasche F, Strauss J, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2011) Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92:1036–1051. https://doi.org/10.1890/10-1011.1
Karst J, Gaster J. Wiley E, Landhäusser SM (2017) Stress differentially causes roots of tree seedlings to exude carbon. Tree physiol 37:154–164. https://doi.org/10.1093/treephys/tpw090
Kuzyakov Y, Cheng W (2001) Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biol Biochem 33:1915–1925. https://doi.org/10.1016/S0038-0717(01)00117-1
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10. https://doi.org/10.1007/BF00011685
McDougall BM, Rovira AD (1965) Carbon-14 labelled photosynthate in wheat root exudates. Nature 207:1104–1105. https://doi.org/10.1038/2071104a0
Moore JC, McKann K, Setälä H, de Ruiter PC (2003) Top–down is bottom–up: does predation in the rhizosphere regulate aboveground dynamics? Ecology 84:846–857. https://doi.org/10.1890/0012-9658(2003)084[0846:TIBDPI]2.0.CO;2
Moore-Kucera J, Dick RP (2008) PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb Ecol 55:500–511. https://doi.org/10.1007/s00248-007-9295-1
Moran-Zuloaga D, Dippold M, Glaser B, Kuzyakov Y (2015) Organic nitrogen uptake by plants: reevaluation by position-specific labeling of amino acids. Biogeochemistry 125:359–374. https://doi.org/10.1007/s10533-015-0130-3
Neumann G, Römheld V (2000) The release of root exudates as affected by the plant’s physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc, New York, pp 41–93
Phillips RP, Erlitz Y, Bier R, Bernhardt ES (2008) New approach for capturing soluble root exudates in forest soils. Funct Ecol 22:990–999. https://doi.org/10.1111/j.1365-2435.2008.01495.x
Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol 29:1513–1523. https://doi.org/10.1093/treephys/tpp083
Phillips RP, Finzi A, Bernhardt E (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194. https://doi.org/10.1111/j.1461-0248.2010.01570.x
Pramanik MHR, Nagal M, Asao M, Matsui Y (2000) Effect of temperature amd photoperiod on phytotoxic root exudates of cucumber (Cucumis sativus) in hydroponic culture. J Chem Ecol 26:1953–1967. https://doi.org/10.1023/A:1005509110317
Preece C. Farré-Armengol G, Llusià J, Peñuelas J (2018) Thirsty tree roots exude more carbon. Tree Physiol. https://doi.org/10.1093/treephys/tpx163
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rovira AD (1969) Plant root exudates. Bot Rev 35:35–57. https://doi.org/10.1007/BF02859887
Sanaullah M, Chabbi A, Rumpel C, Kuzyakov Y (2012) Carbon allocation in grassland communities under drought stress followed by 14C pulse labeling. Soil Biol Biochem 55:132–139. https://doi.org/10.1016/j.soilbio.2012.06.004
Scheidemann P, Wetzel A (1997) Identification and characterization of flavonoids in the root exudate of Robinia pseudoacacia. Trees 11:316–321. https://doi.org/10.1007/PL00009677
Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563. https://doi.org/10.1016/S0038-0717(03)00015-4
Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microb 67:4742–4751. https://doi.org/10.1128/AEM.67.10.4742-4751.2001
Smith WH (1972) Influence of artificial defoliation on exudates of sugar maple. Soil Biol Biochem 4:111–113. https://doi.org/10.1016/0038-0717(72)90050-8
Smith WH (1976) Character and significance of forest tree root exudates. Ecology 57:324–331. https://doi.org/10.2307/1934820
Sun L, Kominami Y, Yoshimura K, Kitayama K (2017) Root-exudate flux variations among four co-existing canopy species in a temperate forest, Japan. Ecol Res 32:331–339. https://doi.org/10.1007/s11284-017-1440-9
Takeuchi M (1981) Studies on the freezing and thawing of the volcanic ash soils in eastern Hokkaido (II): soil freezing and thawing in a grassland (Sasa nipponica) and a brush cutting area. Bull Kyoto Univ Forests 53:205–215 (Japanese with English summary)
Thornton B, Paterson E, Midwood AJ, Sim A, Pratt SM (2004) Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labelling. Physiol Plant 120:434–441 doi. https://doi.org/10.1111/j.0031-9317.2004.00250.x
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 Biol Biochem 107:188–197. https://doi.org/10.1016/j.soilbio.2017.01.006
Uren NC (2000) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc, New York, pp 19–40
Vuković R, Bauer N, Curković-Perica M (2013) Genetic elicitation by inducible expression of β-cryptogein stimulates secretion of phenolics from Coleus blumei hairy roots. Plant Sci 199–200:18–28. https://doi.org/10.1016/j.plantsci.2012.10.009
Watt M, Evans JR (1999) Linking development and determinacy with organic acid efflux from proteoid roots of Lupinus albus L. grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120:705–716. https://doi.org/10.1104/pp.120.3.705
Yuan HZ, Zhu ZK, Liu SL, Ge TD, Jing HZ, Li BZ, Liu Q, Lynn TM, Wu JS, Kuzyakov Y (2016) Microbial utilization of rice root exudates: 13C labeling and PLFA composition. Biol Fertil Soils 52:615–627. https://doi.org/10.1007/s00374-016-1101-0
Acknowledgements
We would like to thank Chikae Iwaoka and Makoto Yasumatsu for supporting chemical analysis, Karibu Fukuzawa and the member of Forest Information Laboratory for their helpful suggestions. We also thank the staffs of Hokkaido forest research station, Field Science Education and Research Center, Kyoto University for helping with the experiments and for providing meteorological data. This study was supported by JSPS-KAKENHI (Nos. 26292085,16H04937and 17H03833).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nakayama, M., Tateno, R. Solar radiation strongly influences the quantity of forest tree root exudates. Trees 32, 871–879 (2018). https://doi.org/10.1007/s00468-018-1685-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-018-1685-0