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Spatiotemporal patterns of enzyme activities in the rhizosphere: effects of plant growth and root morphology

Abstract

Lentil and lupine, having contrasting root morphologies, were chosen to investigate the effects of plant growth and root morphology on the spatial distribution of β-glucosidase, cellobiohydrolase, leucine aminopeptidase, and acid phosphomonoesterase activities. Lentil kept as vegetative growth and the rhizosphere extent was constant, while the enzyme activities at the root surface kept increasing. Lupine entered reproductive growth in the seventh week after planting, the rhizosphere extent was broader in the eighth week than in the first and fourth weeks. However, enzyme activity at the root surface of lupine decreased by 10–50% in comparison to the preceding vegetative stage (first and fourth weeks). Lupine lateral roots accounted for 1.5–3.5 times more rhizosphere volume per root length than taproots, with 6–14-fold higher enzyme activity per root surface area. Therefore, we conclude that plant growth and root morphology influenced enzyme activity and shape the rhizosphere as follows: the enzyme activity in the rhizosphere increased with plant growth until reproductive stage; lateral roots have much larger rhizosphere volume per unit root length and higher enzyme activity per root surface area than the taproots.

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References

  • Acuña JJ, Durán P, Lagos LM, Ogram A, de la Luz MM, Jorquera MA (2016) Bacterial alkaline phosphomonoesterase in the rhizospheres of plants grown in Chilean extreme environments. Biol Fertil Soils 52:763–773

    Article  CAS  Google Scholar 

  • Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340

    Article  CAS  Google Scholar 

  • Aon MA, Cabello M, Sarena D, Colaneri A, Franco M, Burgos J, Cortassa S (2001) Spatio-temporal patterns of soil microbial and enzymatic activities in an agricultural soil. Appl Soil Ecol 18:239–254

    Article  Google Scholar 

  • Asmar F, Eiland F, Nielsen NE (1994) Effect of extracellular-enzyme activities on solubilization rate of soil organic nitrogen. Biol Fertil Soils 17:32–38

    Article  CAS  Google Scholar 

  • Aulakh M, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148

    Article  CAS  Google Scholar 

  • Badalucco L, Kuikman PJ (2001). Mineralization and immobilization in the rhizosphere. In: Pinton, R, Varanini, Z, Nannipieri, P (Eds.) The rhizosphere. biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 141–196

  • Baraniya D, Puglisi E, Ceccherini MT, Pietramellara G, Giagnoni L, Arenella M, Nannipieri P, Renella G (2016) Protease encoding microbial communities and protease activity of the rhizosphere and bulk soils of two maize lines with different N uptake efficiency. Soil Biol Biochem 96:176–179

    Article  CAS  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  PubMed  CAS  Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. The ISME J 8:790–803

    Article  PubMed  CAS  Google Scholar 

  • Croser JS, Pazos-Navarro M, Bennett RG, Tschirren S, Edwards K, Erskine W, Creasy R, Ribalta FM (2016) Time to flowering of temperate pulses in vivo and generation turnover in vivo-in vitro of narrow-leaf lupin accelerated by low red to far-red ratio and high intensity in the far-red region. Plant Cell Tissue Organ Cult 127:591–599

    Article  CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47

    Article  CAS  Google Scholar 

  • Dazzo FB, Gantner S (2012) The rhizosphere. In: Schmidt TM, Schaechter M (eds) Topics in ecological and environmental microbiology. Academic Press, San Diego, pp 466–480

    Google Scholar 

  • De-la-Peña C, Badri DV, Lei Z, Watson BS, Brandão MM, Silva-Filho MC, Sumner LW, Vivanco JM (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285:30654–30665

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292

    Article  CAS  Google Scholar 

  • Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837

    Article  Google Scholar 

  • Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant Soil 235:211–219

    Article  CAS  Google Scholar 

  • Gambetta GA, Fei J, Rost TL, Knipfer T, Matthews MA, Shackel KA, Walker MA, McElrone AJ (2013) Water uptake along the length of grapevine fine roots: developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiol 163:1254–1265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giagnoni L, Pastorelli R, Mocali S, Arenella M, Nannipieri P, Renella G (2016) Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency. Appl Soil Ecol 98:30–38

    Article  Google Scholar 

  • Gransee A, Wittenmayer L (2000) Qualitative and quantitative analysis of water-soluble root exudates in relation to plant species and development. J Plant Nutr Soil Sci 163:381–385

    Article  CAS  Google Scholar 

  • Grayston S, Vaughan D, Jones D (1997) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56

    Article  Google Scholar 

  • Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683

    Article  PubMed  Google Scholar 

  • Güsewell S, Schroth MH (2017) How functional is a trait? Phosphorus mobilization through root exudates differs little between carex species with and without specialized dauciform roots. New Phytol 215:1438–1450

    Article  PubMed  CAS  Google Scholar 

  • Hallett PD, Bengough AG (2013) Managing the soil physical environment for plants. In: Gregory PJ, Nortcliff S (eds) Soil conditions and plant growth. Wiley-Blackwell, Chichester, pp 238–268

    Chapter  Google Scholar 

  • Henry HA (2012) Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem 47:53–59

    Article  CAS  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152

    Article  CAS  Google Scholar 

  • Hoang DT, Razavi BS, Kuzyakov Y, Blagodatskaya E (2016) Earthworm burrows: kinetics and spatial distribution of enzymes of C-, N-and P-cycles. Soil Biol Biochem 99:94–103

    Article  CAS  Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33

    Article  CAS  Google Scholar 

  • Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129

    Article  CAS  Google Scholar 

  • Kelley AM, Fay PA, Polley HW, Gill RA, Jackson RB (2011) Atmospheric CO2 and soil extracellular enzyme activity: a meta-analysis and CO2 gradient experiment. Ecosphere 2:1–20

    Article  Google Scholar 

  • Koch O, Tscherko D, Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Glob Biogeochem Cycles 21:GB4017

    Article  CAS  Google Scholar 

  • Kramer S, Marhan S, Ruess L, Armbruster W, Butenschoen O, Haslwimmer H, Kuzyakov Y, Pausch J, Scheunemann N, Schoene J (2012) Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. Pedobiologia 55:111–119

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669

    Article  PubMed  CAS  Google Scholar 

  • Lagos LM, Acuña JJ, Maruyama F, Ogram A, de la Luz MM, Jorquera MA (2016) Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol Fertil Soils 52:1007–1019

    Article  CAS  Google Scholar 

  • Lam L, Lee S-W, Suen CY (1992) Thinning methodologies—a comprehensive survey. IEEE Trans Pattern Anal Mach Intell 14:869–885

    Article  Google Scholar 

  • Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Bucio J, Cruz-Ramırez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  CAS  Google Scholar 

  • Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen Q (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biol Fertil Soils 53:375–388

    Article  CAS  Google Scholar 

  • Ma X, Razavi BS, Holz M, Blagodatskaya E, Kuzyakov Y (2017) Warming increases hotspot areas of enzyme activity and shortens the duration of hot moments in the root-detritusphere. Soil Biol Biochem 107:226–233

    Article  CAS  Google Scholar 

  • Ma X, Zarebanadkouki M, Kuzyakov Y, Blagodatskaya E, Pausch J, Razavi BS (2018) Spatial patterns of enzyme activities in the rhizosphere: effects of root hairs and root radius. Soil Biol Biochem 118:69–78

    Article  CAS  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    Article  PubMed  Google Scholar 

  • Miralles I, Domingo F, Cantón Y, Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2012) Hydrolase enzyme activities in a successional gradient of biological soil crusts in arid and semi-arid zones. Soil Biol Biochem 53:124–132

    Article  CAS  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2007) Microbial diversity and microbial activity in the rhizosphere. Cien Suelo 25:89–97

    Google Scholar 

  • Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Obreson A, Frossard E (eds) Phosphorus in action. Springer, Berlin, pp 215–243

    Chapter  Google Scholar 

  • Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762

    Article  Google Scholar 

  • Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19

    Article  CAS  Google Scholar 

  • 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, New York, pp 41–93

    Google Scholar 

  • Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396

    Article  CAS  Google Scholar 

  • Odell RE, Dumlao MR, Samar D, Silk WK (2008) Stage-dependent border cell and carbon flow from roots to rhizosphere. Am J Bot 95:441–446

    Article  PubMed  Google Scholar 

  • Pausch J, Tian J, Riederer M, Kuzyakov Y (2013) Estimation of rhizodeposition at field scale: upscaling of a 14C labeling study. Plant Soil 364:273–285

    Article  CAS  Google Scholar 

  • Pausch J, Loeppmann S, Kühnel A, Forbush K, Kuzyakov Y, Cheng W (2016) Rhizosphere priming of barley with and without root hairs. Soil Biol Biochem 100:74–82

    Article  CAS  Google Scholar 

  • Philippot L, Raaijmakers JM, Lemanceau P, Van Der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799

    Article  PubMed  CAS  Google Scholar 

  • Proctor C, He Y (2017) Quantifying root extracts and exudates of sedge and shrub in relation to root morphology. Soil Biol Biochem 114:168–180

    Article  CAS  Google Scholar 

  • Razavi BS, Zarebanadkouki M, Blagodatskaya E, Kuzyakov Y (2016) Rhizosphere shape of lentil and maize: spatial distribution of enzyme activities. Soil Biol Biochem 96:229–237

    Article  CAS  Google Scholar 

  • Read D, Bengough AG, Gregory PJ, Crawford JW, Robinson D, Scrimgeour C, Young IM, Zhang K, Zhang X (2003) Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil. New Phytol 157:315–326

    Article  CAS  Google Scholar 

  • Remenant B, Grundmann GL, Jocteur-Monrozier L (2009) From the micro-scale to the habitat: assessment of soil bacterial community structure as shown by soil structure directed sampling. Soil Biol Biochem 41:29–36

    Article  CAS  Google Scholar 

  • Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Roberts E, Summerfield R, Muehlbauer F, Short R (1986) Flowering in lentil (Lens culinaris Medic.): the duration of the photoperiodic inductive phase as a function of accumulated daylength above the critical photoperiod. Ann Bot 58:235–248

    Article  Google Scholar 

  • Sanaullah M, Razavi BS, Blagodatskaya E, Kuzyakov Y (2016) Spatial distribution and catalytic mechanisms of β-glucosidase activity at the root-soil interface. Biol Fertil Soils 52:505–514

    Article  CAS  Google Scholar 

  • Šarapatka B, Dudová L, Kršková M (2004) Effect of pH and phosphate supply on acid phosphatase activity in cereal roots. Biologia 59:127–131

    Google Scholar 

  • Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:1–11

    Article  CAS  Google Scholar 

  • Schimel J, Becerra CA, Blankinship J (2017) Estimating decay dynamics for enzyme activities in soils from different ecosystems. Soil Biol Biochem 114:5–11

    Article  CAS  Google Scholar 

  • Schmidt H, Eickhorst T (2014) Detection and quantification of native microbial populations on soil-grown rice roots by catalyzed reporter deposition-fluorescence in situ hybridization. FEMS Microbiol Ecol 87:390–402

    Article  PubMed  CAS  Google Scholar 

  • Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393

    Article  PubMed  CAS  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  PubMed  Google Scholar 

  • Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788

    CAS  Google Scholar 

  • Tarafdar J, Jungk A (1987) Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus. Biol Fertil Soils 3:199–204

    Article  CAS  Google Scholar 

  • Tovar J (1996) Bioavailability of carbohydrates in legumes: digestible and indigestible fractions. Arch Latinoam Nutr 44:36S–40S

    PubMed  CAS  Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106

    Article  CAS  Google Scholar 

  • Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29

    Article  CAS  Google Scholar 

  • Zarebanadkouki M, Carminati A (2014) Reduced root water uptake after drying and rewetting. J Plant Nutr Soil Sci 177:227–236

    Article  CAS  Google Scholar 

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Acknowledgements

We gratefully acknowledge the China Scholarship Council (CSC) (201506300073 and 201406300014), for supporting Xiaomin Ma and Yuan Liu, respectively. The contribution of Evgenia Blagodatskaya was supported by the Russian Scientific Foundation (project no. 14-14-00625). The publication was prepared with the support of the “RUDN University program 5-100”. This study was supported by the German Research Foundation (DFG) within the Research Unit (FOR 918) “Carbon Flow in Belowground Food Webs assessed by Isotope Tracers” (KU 1184/13-2) and “Biopores as hotspots of nutrient acquisition from subsoil” (PAK 888; KU 1184/29-1). We thank three anonymous reviewers and the editor for their very helpful suggestions.

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Correspondence to Xiaomin Ma, Yuan Liu or Evgenia Blagodatskaya.

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Ma, X., Liu, Y., Zarebanadkouki, M. et al. Spatiotemporal patterns of enzyme activities in the rhizosphere: effects of plant growth and root morphology. Biol Fertil Soils 54, 819–828 (2018). https://doi.org/10.1007/s00374-018-1305-6

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  • DOI: https://doi.org/10.1007/s00374-018-1305-6

Keywords

  • Rhizosphere extent
  • Enzyme spatial distribution
  • Zymography
  • Plant growth stage
  • Root morphology
  • Visualization approaches