Abstract
Aim
A growing number of studies show a discrepancy between the isotopic composition of xylem water and plant water sources. We tested the effect of arbuscular mycorrhizal fungi (AMF) on the isotopic composition of Acacia caven xylem water. As the most common plant-fungal association, AMF might explain this isotopic mismatch.
Methods
Seedlings were grown with and without AMF and irrigated with the same water. After 120 days, stem and soil samples were collected and following cryogenic distillation, H and O isotopic composition of xylem and soil water, as well as irrigation water, was measured.
Results
Xylem water of non-mycorrhizal seedlings was significantly depleted in 2H compared to soil water (differences up to −15.6‰). When AMF were present, the depletion was significantly higher and appeared for both H and O (differences up to −24.6‰ for δ2H and − 2.9‰ for δ18O between soil and xylem water).
Conclusions
Results suggest that isotopic fractionation occurred during water uptake in this xerophytic species. To explain this, we propose an aquaporin-driven mechanism mediating water transport via transmembrane passage. Furthermore, we show for the first time, that AMF enhance the observed discrimination against heavy isotopes, probably by enforcing water passage through aquaporins. Given their ubiquity, AMF could question the fractionation-free assumption during root water uptake.
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References
Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297
Araguás-Araguás L, Rozanski K, Gonfiantini R, Louvat D (1995) Isotope effects accompanying vacuum extraction of soil water for stable isotope analyses. J Hydrol 168:159–171
Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42
Barbeta A, Jones S, Clavé L et al (2019) Unexplained hydrogen isotope offsets complicate the identification and quantification of tree water sources in a riparian forest. Hydrol Earth Syst Sc Discuss:1–31. https://doi.org/10.5194/hess-2018-631
Bárzana G, Aroca R, Paz JA, Chaumont F, Martinez-Ballesta MC, Carvajal M, & Ruiz-Lozano JM (2012). Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Annals of Botany 109(5):1009-1017.
Berry ZC, Evaristo J, Moore G, Poca M, Steppe K, Verrot L, Asbjornsen H, Borma L, Bretfeld M, Hervé-Fernández P, Seyfried M, Schwendenmann L, Sinacore K, De Wispelaere L, McDonnell JJ (2018) The two water worlds hypothesis: addressing multiple working hypotheses and proposing a way forward. Ecohydrology 11(3):e1843
Blake GR, Hartge KH (1986) Bulk density 1. Methods of Soil Analysis: Part 1 - Physical and Mineralogical Methods, pp 363–375
Brooks JR, Barnard HR, Coulombe R, McDonnell JJ (2010) Ecohydrologic separation of water between trees and streams in a Mediterranean climate. Nat Geosci 3:100–104
Bryla DR, Duniway JM (1997) Water uptake by safflower and wheat roots infected with arbuscular mycorrhizal fungi. New Phytol 136:591–601
Bryla DR, Duniway JM (1998) The influence of the mycorrhiza Glomus etunicatum on drought acclimation in safflower and wheat. Physiol Plant 104:87–96
Cabido M, Zeballos SR, Zak M, Carranza ML, Giorgis MA, Cantero JJ, Acosta AT (2018) Native woody vegetation in Central Argentina: classification of Chaco and Espinal forests. Appl Veg Sci 21:298–311
Castillo CG, Borie F, Godoy R, Rubio R, Sieverding E (2006) Diversity of mycorrhizal plant species and arbuscular mycorrhizal fungi in evergreen forest, deciduous forest and grassland ecosystems of southern Chile. J Appl Bot Food Qual 80:40–47
Cernusak LA, Farquhar GD, Pate JS (2005) Environmental and physiological controls over oxygen and carbon isotope composition of Tasmanian blue gum, Eucalyptus globulus. Tree Physiol 25:129–146
Chu-Chou M, Grace LJ (1982) Mycorrhizal fungi of Eucalyptus in the north island of New Zealand. Soil Biol Biochem 14:133–137
Clark ID, Fritz P (1997) Environmental isotopes in hydrogeology. CRC press
Corrales A, Mangan SA, Turner BL, Dalling JW (2016) An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol Lett 19:383–392
Daft MJ, Clelland DM, Gardner IC (1985) Symbiosis with endomycorrhizas and nitrogen-fixing organisms. P Roy Soc Edinb B 85:283–298
Dawson TE, Ehleringer JR (1991) Streamside trees that do not use stream water. Nature 350:335–337
Dawson TE, Ehleringer JR (1993) Isotopic enrichment of water in the" woody" tissues of plants: implications for plant water source, water uptake, and other studies which use stable isotopic composition of cellulose. Geochi Cosmochim Ac 57:3487–3487, 3492
Eamus D, Cleverly J, Boulain N, Grant N, Faux R, Villalobos-Vega R (2013) Carbon and water fluxes in an arid-zone Acacia savanna woodland: an analyses of seasonal patterns and responses to rainfall events. Agric For Meteorol 182:225–238
Ehleringer JR, Dawson TE (1992) Water uptake by plants: perspectives from stable isotope composition. Plant Cell Environ 15:1073–1082
Eller CB, Lima AL, Oliveira RS (2013) Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). New Phytol 199:151–162
Ellsworth PZ, Sternberg LS (2015) Seasonal water use by deciduous and evergreen woody species in a scrub community is based on water availability and root distribution. Ecohydrology 8:538–551
Ellsworth PZ, Williams DG (2007) Hydrogen isotope fractionation during water uptake by woody xerophytes. Plant Soil 291:93–107
Evaristo J, Jasechko S, McDonnell JJ (2015) Global separation of plant transpiration from groundwater and streamflow. Nature 525:91–94
Evaristo J, McDonnell JJ, Scholl MA, Bruijnzeel LA, Chun KP (2016) Insights into plant water uptake from xylem-water isotope measurements in two tropical catchments with contrasting moisture conditions. Hydrol Process 30:3210–3227
Fitter AH (1988) Water relations of red clover Trifolium pratense L. as affected by VA mycorrhizal infection and phosphorus supply before and during drought. J Exp Bot 39:595–603
Gat JR (1996) Oxygen and hydrogen isotopes in the hydrologic cycle. Annu Rev Earth Pl Sc 24:225–262
Geris J, Tetzlaff D, McDonnell J, Anderson J, Paton G, Soulsby C (2015) Ecohydrological separation in wet, low energy northern environments? A preliminary assessment using different soil water extraction techniques. Hydrol Process 29:5139–5152
Goldsmith GR, Muñoz-Villers LE, Holwerda F, McDonnell JJ, Asbjornsen H, Dawson TE (2012) Stable isotopes reveal linkages among ecohydrological processes in a seasonally dry tropical montane cloud forest. Ecohydrology 5:779–790
Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162
Gröning M (2011) Improved water δ2H and δ18O calibration and calculation of measurement uncertainty using a simple software tool. Rapid Comm Mass Sp 25:2711–2720
Hacke UG, Laur J (2016) Aquaporins: channels for the molecule of life. In: eLS. 10(9780470015902), a9780470001289
Hervé-Fernández P, Oyarzún C, Brumbt C, Huygens D, Bodé S, Verhoest NEC, Boeckx P (2016) Assessing the ‘two water worlds’ hypothesis and water sources for native and exotic evergreen species in south-Central Chile. Hydrol Process 30:4227–4241
Hobbie EA, Macko SA, Shugart HH (1999) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360
Högberg P, Högberg MN, Quist ME, Ekblad ALF, Näsholm T (1999) Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris. New Phytol 142:569–576
Ibijbijen J, Urquiaga S, Ismaili M, Alves BJR, Boddey RM (1996) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition and nitrogen fixation of three varieties of common beans (Phaseolus vulgaris). New Phytol 134:353–360
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488
Kozono D, Yasui M, King LS, Agre P (2002) Aquaporin water channels: atomic structure molecular dynamics meet clinical medicine. J Clin Invest 109:1395–1399
Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90
Kuppel S, Tetzlaff D, Maneta M, Soulsby C (2018) EcH2O-iso 1.0: water isotopes and age tracking in a process-based, distributed ecohydrological model. Geosci Model Dev 11:3045–3069
Leibundgut C, Maloszewski P, Külls C (2009) Tracers in hydrology. Wiley-Blackwell
Lin G, da SL Sternberg, L (1993) hydrogen isotopic fractionation by plant roots during water uptake in coastal wetland plants. In Stable isotopes and plant carbon-water relations (pp. 497–510). Elsevier
Longo S, Nouhra E, Goto BT, Berbara RL, Urcelay C (2014) Effects of fire on arbuscular mycorrhizal fungi in the mountain Chaco Forest. Forest Ecol Manag 315:86–94
Mamonov AB, Coalson RD, Zeidel ML, Mathai JC (2007) Water and deuterium oxide permeability through aquaporin 1: MD predictions and experimental verification. J Gen Physiol 130:111–116
Martín-Gómez P, Barbeta A, Voltas J, Peñuelas J, Dennis K, Palacio S, Dawson TE, Ferrio JP (2015) Isotope-ratio infrared spectroscopy: a reliable tool for the investigation of plant-water sources? New Phytol 207:914–927
Martín-Gómez P, Serrano L, Ferrio JP (2016) Short-term dynamics of evaporative enrichment of xylem water in woody stems: implications for ecohydrology. Tree Physiol 37:511–522
McDonnell JJ (2014) The two water worlds hypothesis: ecohydrological separation of water between streams and trees? WIRES Water 1:323–329
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytol 115:495–501
Michener R, Lajtha K (eds) (2008) Stable isotopes in ecology and environmental science. John Wiley & Sons
Oerter E, Finstad K, Schaefer J, Goldsmith GR, Dawson T, Amundson R (2014) Oxygen isotope fractionation effects in soil water via interaction with cations (mg, ca, K, Na) adsorbed to phyllosilicate clay minerals. J Hydrol 515:1–9
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture, Washington
Orlowski N, Breuer L, McDonnell JJ (2016) Critical issues with cryogenic extraction of soil water for stable isotope analysis. Ecohydrology 9:1–5
Oshun J, Dietrich WE, Dawson TE, Fung I (2016) Dynamic, structured heterogeneity of water isotopes inside hillslopes. Water Resour Res 52:164–189
Otieno DO, Schmidt MWT, Adiku S, Tenhunen J (2005) Physiological and morphological responses to water stress in two Acacia species from contrasting habitats. Tree Physiol 25:361–371
Pansu M, Gautheyrou J (2006) Pipette method after Robinson-köhn or andreasen. In: Handbook of soil analysis: mineralogical, organic and inorganic methods. Springer Science & Business Media, pp 35–42
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Pennington HG, Bidartondo MI, Barsoum N (2011) A few exotic mycorrhizal fungi dominate eucalypts planted in England. Fungal Ecol 4:299–302
Perez M, Urcelay C (2009) Differential growth response to arbuscular mycorrhizal fungi and plant density in two wild plants belonging to contrasting functional types. Mycorrhiza 19:517–523
R Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria
Raab N, Meza FJ, Franck N, Bambach N (2015) Empirical stomatal conductance models reveal that the isohydric behavior of an Acacia caven Mediterranean Savannah scales from leaf to ecosystem. Agric For Meteorol 213:203–216
Rodríguez-Gamir J, Xue J, Clearwater MJ, Meason DF, Clinton PW, Domec JC (2019) Aquaporin regulation in roots controls plant hydraulic conductance, stomatal conductance, and leaf water potential in Pinus radiata under water stress. Plant Cell Environ 42:717–729
Rozanski K, Araguás-Araguás L, Gonfiantini R (1993) Isotopic patterns in modern global precipitation. In: Climate change in continental isotopic records, vol 78, pp 1–36
Ruiz-Lozano JM, Aroca R (2010) Modulation of aquaporin genes by the arbuscular mycorrhizal symbiosis in relation to osmotic stress tolerance. In: Seckbach J, Grube M. eds. Symbioses and stress: joint ventures in biology, cellular origin, life in extreme habitats and astrobiology. Dordrecht: springer science+business. Media:359–374
Rundel PW, Ehleringer JR, Nagy KA (Eds.) (2012) Stable isotopes in ecological research (Vol. 68). Springer Science & Business Media
Ryan J, Estefan G, Rashid A (2001) Soil and plant analysis laboratory manual. International center for agricultural research in the dry areas (ICARDA), Aleppo, Syria
Schlesinger WH, Bernhardt ES (2013) Biogeochemistry: an analysis of global change. Academic press
Smith SSE (1980) Mycorrhizas of autotrophic higher plants. Biol Rev 55:475–510
Smith SSE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York, ISBN, 440026354, 605
Soudzilovskaia NA, Douma JC, Akhmetzhanova AA, van Bodegom PM, Cornwell WK, Moens EJ, Treseder KK, Tibbett M, Wang YP, Cornelissen JHC (2015) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr 24:371–382
Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194
Urcelay C, Tecco PA, Chiarini F (2005) Micorrizas arbusculares del tipo 'Arum' y 'Paris' y endófitos radicales septados oscuros en Miconia ioneura y Tibouchina paratropica (Melastomataceae). B Soc Argent Bot 40:151–155
Vargas AI, Schaffer B, Yuhong L, Sternberg LDSL (2017) Testing plant use of mobile vs immobile soil water sources using stable isotope experiments. New Phytol 215(2):582–594
Vega-Frutis R, López JC, Flandes C, Guevara R (2015) Have male trees of the tropical rain forest evolved to minimize the interactions with mycorrhizal symbionts? Perspect Plant Ecol 17:444–453
Venier P, Cabido M, Funes G (2017) Germination characteristics of five coexisting neotropical species of Acacia in seasonally dry Chaco forests in Argentina. Plant Spec Biol 32:134–146
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363
West AG, Patrickson SJ, Ehleringer JR (2006) Water extraction times for plant and soil materials used in stable isotope analysis. Rapid Comm Mass Sp 20:1317–1321
Wu QS, Srivastava AK, Zou YN (2013) AMF-induced tolerance to drought stress in citrus: a review. Sci Hortic 164:77–87
Zhao L, Wang L, Cernusak LA, Liu X, Xiao H, Zhou M, Zhang S (2016) Significant difference in hydrogen isotope composition between xylem and tissue water in Populus euphratica. Plant Cell Environ 39:1848–1857
Zimmermann U, Ehhalt D, Münnich KO (1967) Soil-water movement and evapotranspiration: changes in the isotopic composition of the water. In: Isotopes in hydrology. In Conference on isotopes in hydrology, pp 567–585
Acknowledgements
The authors are thankful to the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), the Universidad Nacional de Córdoba (UNC) and the Isotope Bioscience Laboratory (ISOFYS) of the Faculty of Bioscience Engineering, Ghent University, which provided facilities used for this study. We thank Ana Ferreras who generously provided the Acacia caven seeds for the experiment. We appreciate the assistance of Silvana Longo, Nicolás Marro and Noelia Cofré during the experiment and mycorrhizal colonization identification. M.P. and O.C. specially thank Pedro Hervé-Fernandez for his inspiring introduction to the intriguing isotope world and for providing insightful comments on previous versions of the manuscript. We appreciate the comments of two anonymous reviewers and the responsible editor that improved significantly the quality of the manuscript. O.C. acknowledges the Commissie Wetenschappelijk Onderzoek (CWO), Faculty of Bioscience Engineering, UGent for a travel scholarship for performing the experiment in Argentina. The Secretaría de Ciencia y Tecnología (SECyT) - Universidad Nacional de Córdoba provided financial support to this study.
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Poca, M., Coomans, O., Urcelay, C. et al. Isotope fractionation during root water uptake by Acacia caven is enhanced by arbuscular mycorrhizas. Plant Soil 441, 485–497 (2019). https://doi.org/10.1007/s11104-019-04139-1
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DOI: https://doi.org/10.1007/s11104-019-04139-1