Abstract
Aim
The rate of nitrate (NO3 −) uptake and changes in rhizosphere properties were studied growing seedlings of two maize inbred lines differing in nitrogen use efficiency (NUE) in rhizoboxes.
Results
Changes in NO3 − uptake rates occurred in response to anion addition (induction) in seedlings grown both in hydroponic culture and in soil in rhizoboxes. The characterization of root exudate composition showed a line-specific metabolite profile, which was also affected by NO3 − availability. The induction affected respiration, nitrification, ammonification and enzyme activities of the rhizosphere. Furthermore, the composition of rhizosphere bacterial communities of the two maize lines differed suggesting the selective capacity of plants.
Conclusions
Overall, results showed a strong and fast modification of rhizospheric soil properties in response to physiological changes in plants caused by fluctuating NO3 − availability.
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References
Alef K, Kleiner D (1986) Arginine ammonification, a simple method to estimate microbial activity potentials in soils. Soil Biol Biochem 18:233–235. https://doi.org/10.1016/0038-0717(86)90033-7
Badalucco L, Nannipieri P (2007) Nutrient transformations in the rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, pp 111–133
Balconi C, Brosio D, Motto M (1997) Analysis of nitrogen partitioning in maize. Maize Genet Coop News Lett 71:10–11
Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 32:921–950. https://doi.org/10.1081/CSS-100104098
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. https://doi.org/10.1016/j.soilbio.2016.02.001
Barber SA (1995) Soil nutrient bioavailability: a mechanistic approach, 2nd edn. John Wiley, New York
Barraclough D (1997) The direct or MIT route for nitrogen immobilization: a 15N mirror image study with leucine and glycine. Soil Biol Biochem 29:101–108
Bassard J-E, Ullmann P, Bernier F, Werck-Reichhart D (2010) Phenolamides: bridging polyamines to the phenolic metabolism. Phytochemistry 71:1808–1824. https://doi.org/10.1016/j.phytochem.2010.08.003
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. https://doi.org/10.1111/j.1574-6941.2009.00654.x
Blackmer AM, Bremner JM (1977) Gas chromatographic analysis of soil atmosphere. Soil Sci Soc Am J 41:908–912
Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein- dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bremner JM, Mulvaney CS (1982) Nitrogen-Total. In: Al P, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Academic Press, New York, pp 595–624. https://doi.org/10.2134/agronmonogr9.2.2ed.c31
Brimecombe MJ, FAAM DL, Lynch JM (2007) Rhizodeposition and microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, pp 73–109
Cambier V, Hance T, de Hoffmann E (1999) Non-injured maizecontains several 1,4-benzoxazin-3one related compounds but only as glucoconjugates. Phytochem Anal 10:119–126. https://doi.org/10.1002/(SICI)1099-1565(199905/06)10:3
Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263. https://doi.org/10.1007/s002480000087
DeAngelis KM, Ji P, Firestone MK, Lindow SE (2005) Two novel bacterial biosensors for detection of nitrate availability in the rhizosphere. Appl Environ Microbiol 71:8537–8547. https://doi.org/10.1128/AEM.71.12.8537-8547.2005
Dixon DP, Sellars JD, Kenwright AM, Steel PG (2012) The maize benzoxazinone DIMBOA reacts with glutathione and other thiols to form spirocyclic adducts. Phytochemistry 77:171–178. https://doi.org/10.1016/j.phytochem.2012.01.019
Forbush B (1983) Assay of Na, K-ATPase in plasma-membrane preparations: increasing the permeability of membrane-vesicles using sodium dodecyl-sulfate buffered with bovine serum- albumin. Anal Biochem 128:159–163. https://doi.org/10.1016/0003-2697(83)90356-1
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. https://doi.org/10.1016/j.apsoil.2015.09.004
Gogstad GO, Krutnes MB (1982) Measurement of protein in cell-suspensions using the coomassie brilliant blue dye-binding assay. Anal Biochem 126:355–359. https://doi.org/10.1016/0003-2697(82)90527-9
Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491. https://doi.org/10.1128/AEM.66.12.5488-5491.2000
Harms H, Wells MC, van der Meer JR (2006) Whole-cell living biosensors–are they ready for environmental application? Appl Microbiol Biotechnol 70:273–280. https://doi.org/10.1007/s00253-006-0319-4
Hawes MC, Bengough G, Cassab G, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21:352–367. https://doi.org/10.1007/s00344-002-0035-y
Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Skrumsager Møller I, White P (2012) Functions of macronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, London, pp 135–189
Jensen LE, Nybroe O (1999) Nitrogen availability to Pseudomonas fluorescens DF57 is limited during decomposition of barley straw in bulk soil and in the barley rhizosphere. Appl Environ Microbiol 65:4320–4328
Jonczyk R, Schmidt H, Osterrieder A, Fiesselmann A, Schullehner K, Haslbeck M, Sicker D, Hofmann D, Yalpani N, Simmons C, Frey M, Gierl A (2008) Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiol 146:1053–1063. https://doi.org/10.1104/pp.107.111237
Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Röser A, Koops H-P, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051
Kragelund L, Christoffersen B, Nybroe O, de Bruijn FJ (1995) Isolation of lux reporter gene fusions in Pseudomonas fluorescens DF57 inducible by nitrogen or phosphorus starvation. FEMS Microbiol Ecol 17:95–106. https://doi.org/10.1111/j.1574-6941.1995.tb00134.x
Kragelund L, Hosbond C, Nybroe O (1997) Distribution of metabolic activity and phosphate starvation response of lux-tagged Pseudomonas fluorescens reporter bacteria in the barley rhizosphere. Appl Environ Microbiol 63:4920–4928
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669
Ladd JN, Butler JH (1972) Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol Biochem 4:19–30. https://doi.org/10.1016/0038-0717(72)90038-7
Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci U S A 82:6955–6959. https://doi.org/10.1073/pnas.82.20.6955
Leveau JH, Lindow SE (2002) Bioreporters in microbial ecology. Curr Opin Microbiol 5:259–265. https://doi.org/10.1016/S1369-5274(02)00321-1
Li YL, Zhang YL, Hu J, Shen QR (2007) Contribution of nitrification happened in rhizospheric soil growing with different rice cultivars to N nutrition. Biol Fertil Soils 43:417–425. https://doi.org/10.1007/s00374-006-0119-0
Locci G, Santi S, Monte R, Pinton R, Varanini Z (2001) Involvement of plasma membrane H+-ATPase in nitrate uptake by maize genotypes. In: Horst WJ, Schenk MK, Bürkert A, Classsen N, Flessa H, Frommer WB, Goldbach H, Olfs H-W, Römheld V, Sattelmacher B, Schmidhalter U, Schubert S, von Virén N, Wittenmayer L (eds) Plant nutrition-food security and sustainability of agro-ecosystems through basic and applied research. Kluwer Academic Publishers, Netherlands, pp 184–185. https://doi.org/10.1007/0-306-47624-X_88
Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286. https://doi.org/10.1016/S0065-2911(04)49005-5
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10. https://doi.org/10.1007/BF00011685
Marstop H, Witter E (1999) Extractable dsDNA and product formation as measures of microbial growth in soil upon substrate addition. Soil Biol Biochem 31:1443–1453. https://doi.org/10.1016/S0038-0717(99)00065-6
Marti G, Erb M, Boccard J, Glauser G, Doyen GR, Villard N, Robeet CAM, Turlings TCJ, Rudaz S, Wolfender J-L (2013) Metabolomics reveals herbivore-induced metabolites of resistance and susceptibility in maize leaves and roots. Plant Cell Environ 36:621–639. https://doi.org/10.1111/pce.12002
Meihls LN, Handrick V, Glauser G, Barbier H, Kaur H, Haribal MM, Lipka AE, Gershenzon J, Buckler ES, Erb M, Köllner TG, Jander G (2013) Natural variation in maize aphid resistance is associated with DIMBOA-Glc methyltransferase activity. Plant Cell 25:2341–2355. https://doi.org/10.1105/tpc.113.112409
Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S (2014) Rhizospheric organic compounds in the soil–microorganism–plant system: their role in iron availability. Eur J Soil Sci 65:629–642. https://doi.org/10.1111/ejss.12158
Nannipieri P, Ceccanti B, Cervelli S, Sequi P (1974) Use of 0.1 M pyrophosphate to extract urease for podzol. Soil Biol Biochem 6:359–362. https://doi.org/10.1016/0038-0717(74)90044-3
Nannipieri P, Ascher J, Ceccherini MT, Guerri G, Renella G, Pietramellara G (2008) Recent advances in functional genomics and proteomics of plant associated microbes. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Heidelberg, pp 215–241. https://doi.org/10.1007/978-3-540-75575-3
Negrel J, Javelle F (1997) Purification, characterization and partial amino acid sequencing of hydroxycinnamoyl-CoA:tyramine N-(hydroxycinnamoyl) transferase from tobacco cell-suspension cultures. Eur J Biochem 247:1127–1135. https://doi.org/10.1111/j.1432-1033.1997.01127.x
Neumann G, Romheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, pp 23–72. https://doi.org/10.1201/9781420005585.ch2
Pathan S, Ceccherini MT, Pietramellara G, Puschenreiter M, Giagnoni L, Arenella M, Varanini Z, Nannpieri P, Renella G (2015a) Enzyme activity and microbial community structure in the rhizosphere of two maize lines differing in N use efficiency. Plant Soil 387:413–424. https://doi.org/10.1007/s11104-014-2306-3
Pathan SI, Ceccherini MT, Hansen MA, Giagnoni L, Ascher J, Arenella M, Sørensen SJ, Pietramellara G, Nannipieri P, Renella G (2015b) Maize lines with different nitrogen use efficiency select bacterial communities with different β-glucosidase-encoding genes and glucosidase activity in the rhizosphere. Biol Fertil Soils 51:995–1004. https://doi.org/10.1007/s00374-015-1045-9
Peiffer JA, Spor A, Koren O, Jin Z, Green Tringed S, Dangle JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553. https://doi.org/10.1073/pnas.1302837110
Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition processes. A review. Biol Fertil Soils 51:403–415. https://doi.org/10.1007/s00374-015-0996-1
Pii Y, Alessandrini M, Dall’Osto L, Guardini K, Prinsi B, Espen L, Zamboni A, Varanini Z (2016a) Time-resolved investigation of molecular components involved in the induction of NO3 − high affinity transport system in maize roots. Front Plant Sci 7:1657. https://doi.org/10.3389/fpls.2016.01657
Pii Y, Borrusso L, Brusetti L, Cesco S, Mimmo T (2016b) How do plants-having different exudation patterns-shape a similar microbial community? Res Rev J Bot Sci 5:61–64
Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T (2016c) The interaction between iron nutrition, plant species and soil type shapes the rhizosphere microbiome. Plant Physiol Biochem 99:39–48. https://doi.org/10.1016/j.plaphy.2015.12.002
Pinton R, Cesco S, Iacolettig G, Astolfi S, Varanini Z (1999) Modulation of NO3 −-uptake by water-extractable humic substances: involvement of root plasma membrane H+ ATPase. Plant Soil 215:155–161. https://doi.org/10.1023/A:1004752531903
Renella G, Landi L, Valori F, Nannipieri P (2007) Microbial hydrolase activity after release of low molecular weight organic compounds by a model root surface in a clayey and a sandy soil. Appl Soil Ecol 36:124–129. https://doi.org/10.1016/j.apsoil.2007.01.001
Rice CW, Tiedje JM (1989) Regulation of nitrate assimilation by ammonium in soils and in isolated soil microorganisms. Soil Biol Biochem 21:597–602. https://doi.org/10.1016/0038-0717(89)90135-1
Sauvé S, Dumestre A, McBride M, Gillett JW, Berthelin J, Hendershot W (1999) Nitrification potential in field-collected soils contaminated with Pb or Cu. Appl Soil Ecol 12:29–39. https://doi.org/10.1016/S0929-1393(98)00166-8
Scagliola M, Pii Y, Mimmo T, Cesco S, Ricciuti P, Crecchio C (2016) Characterization of plant growth promoting traits of bacterial isolates from the rhizosphere of barley (Hordeum vulgare L.) and tomato (Solanum lycopersicon L.) grown under Fe sufficiency and deficiency. Plant Physiol Biochem 107:187–196. https://doi.org/10.1016/j.plaphy.2016.06.002
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310. https://doi.org/10.1371/journal.pone.0027310
Subbarao GV, Sahrawat KL, Nakahara K, Ishikawa T, Kishii M, Rao IM, Hash CT, George TS, Srinivasa Rao P, Nardi P, Bonnett D, Berry W, Suenaga K, Lata JC (2012) Chapter six- biological nitrification inhibition - a novel strategy to regulate nitrification in agricultural systems. Adv Agron 114:249–302. https://doi.org/10.1016/B978-0-12-394275-3.00001-8
Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. Academic Press, New York, pp 903–947
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40:1971–1974. https://doi.org/10.1016/j.soilbio.2008.02.017
Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32:465–475. https://doi.org/10.1111/j.1365-3040.2009.01938.x
Töwe S, Wallisch S, Bannert A, Fischer D, Hai B, Haesler F, Kleineidam K, Schloter M (2011) Improved protocol for the simultaneous extraction and column-based separation of DNA and RNA from different soils. J Microbiol Methods 84:406–412. https://doi.org/10.1016/j.mimet.2010.12.028
Uren NC (2007) 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. CRC Press, Boca Raton, pp 1–21. https://doi.org/10.1201/9781420005585.ch1
van der Meer JR, Tropel D, Jaspers M (2004) Illuminating the detection chain of bacterial bioreporters. Environ Microbiol 6:1005–1020. https://doi.org/10.1111/j.1462-2920.2004.00655.x
Villagrasa M, Guillamón M, Navarro A, Eljarrat E, Barceló D (2008) Development of a pressurized liquid extraction-solid-phase extraction followed by liquid chromatography-electrospray ionization tandem mass spectrometry method for the quantitative determination of benzoxazolinones and their degradation products in agricultural soil. J Chromatogr A 1179:190–197. https://doi.org/10.1016/j.chroma.2007.11.087
Watson CJ, Kilpatrick DJ, Cooper JE (1994) The effect of increasing application rate of granular calcium ammonium nitrate on net nitrification in a laboratory study of grassland soils. Fert Res 40:155–161. https://doi.org/10.1007/BF00750101
Werlen C, Jaspers MCM, van der Meer JR (2004) Measurement of biologically available naphthalene in gas and aqueous phases by use of a Pseudomonas putida biosensor. Appl Environ Microbiol 70:43–51. https://doi.org/10.1128/AEM.70.1.43-51.2004
Yeomans CV, Porteous F, Paterson E, Meharg AA, Killham K (1999) Assessment of lux-marked Pseudomonas fluorescens for reporting on organic carbon compounds. FEMS Microbiol Lett 176:79–83. https://doi.org/10.1111/j.1574-6968.1999.tb13645.x
Zamboni A, Astolfi S, Zuchi S, Pii Y, Guardini K, Tononi P, Varanini Z (2014) Nitrate induction triggers different transcriptional changes in a high and a low nitrogen use efficiency maize inbred line. J Integr Plant Biol 56:1080–1094. https://doi.org/10.1111/jipb.12214
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ESM 2
Chromatographic profiles of root exudates collected by roots of seedling not treated with NO3- (control) of Lo5 and T250 lines. (PDF 39 kb)
ESM 3
ID, m/z (-) value (in negative ionization mode) m/z (+) value (in positive ionization mode), retention time (rt), putative identification of signal. (XLSX 14 kb)
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Row ID, Row m/z (in negative ionization mode), retention time, putative identification, p1 and pq(corr)1 and p-value of t-test of multivariate and t-test analysis performed of each comparisons or samples. (XLSX 631 kb)
ESM 5
ID, m/z (-) value (in negative ionization mode), m/z (+) value (in positive ionization mode), retention time (rt), putative identification, ms/ms value and ms3 value for each fragment. I %= percentage of intensity of the signal compared to the higher signal (=100%). (PDF 162 kb)
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Varanini, Z., Cesco, S., Tomasi, N. et al. Nitrate induction and physiological responses of two maize lines differing in nitrogen use efficiency: effects on N availability, microbial diversity and enzyme activity in the rhizosphere. Plant Soil 422, 331–347 (2018). https://doi.org/10.1007/s11104-017-3452-1
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DOI: https://doi.org/10.1007/s11104-017-3452-1