Phosphorus; Root system architecture; Rhizobacteria; PGPR; Phosphorus use efficiency; in vitro
Abstract :
[en] Mineral phosphorus (P) fertilisers must be used wisely in order to preserve rock phosphate, a limited and non-renewable resource. The use of bio-inoculants to improve soil nutrient availability and trigger an efficient plant response to nutrient deficiency is one potential strategy in the attempt to decrease P inputs in agriculture.
An in vitro co-cultivation system was used to study the response of Brachypodium distachyon to contrasted P supplies (soluble and poorly soluble forms of P) and inoculation with P solubilizing bacteria. Brachypodium's responses to P conditions and inoculation with bacteria were studied in terms of developmental plasticity and P use efficiency.
Brachypodium showed plasticity in its biomass allocation pattern in response to variable P conditions, specifically by prioritizing root development over shoot productivity under poorly soluble P conditions. Despite the ability of the bacteria to solubilize P, shoot productivity was depressed in plants inoculated with bacteria, although the root system development was maintained. The negative impact of bacteria on biomass production in Brachypodium might be attributed to inadequate C supply to bacteria, an increased competition for P between both organisms under P-limiting conditions, or an accumulation of toxic bacterial metabolites in our cultivation system. Both P and inoculation treatments impacted root system morphology. The modulation of Brachypodium’s developmental response to P supplies by P solubilizing bacteria did not lead to improved P use efficiency.
Our results support the hypothesis that plastic responses of Brachypodium cultivated under P-limited conditions are modulated by P solubilizing bacteria. The considered experimental context impacts plant–bacteria interactions. Choosing experimental conditions as close as possible to real ones is important in the selection of P solubilizing bacteria. Both persistent homology and allometric analyses proved to be useful tools that should be considered when studying the impact of bio-inoculants on plant development in response to varying nutritional context.
Delory, Benjamin; Leuphana University, Lüneburg, Germany > Institute of Ecology
Spaepen, Stijn; University of Leuven, Belgium > Leuven Institute for Beer Research
du Jardin, Patrick ; Université de Liège - ULiège > Département GxABT > Plant Sciences
Delaplace, Pierre ; Université de Liège - ULiège > Département GxABT > Plant Sciences
Language :
English
Title :
Developmental plasticity of Brachypodium distachyon in response to P deficiency: modulation by inoculation with phosphate-solubilizing bacteria
Alternative titles :
[fr] Plasticité developpementale de Brachypodium distachyon en réponse à la déficience en phosphore: modulation par inoculation de bactéries solubilisatrices du phosphate
We thank Assucopie, the Belgian society for the management of the collective rights of educational, academic,
scientific and university authors, for its grant to support the publication.
Arvalis, Institut du Végétal. Carence en phosphore (P). Retrieved from http://www.fiches.arvalis-infos.fr/fiche_accident/fiches_accidents.php?type_cul=3&id_acc=98
Bakhshandeh, E., Rahimian, H., Pirdashti, H., & Nematzadeh, G.A. (2015). Evaluation of phosphate-solubilizing bacteria on the growth and grain yield of rice (Oryza sativa L.) cropped in northern Iran. Journal of Applied Microbiology, 119, (5), 1371–1382. http://dx.doi.org/10.1111/jam.12938
Bashan, Y., Kamnev, A. A., & de-Bashan, L. E. (2013). Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: A proposal for an alternative procedure. Biology and Fertility of Soils, 49(4), 465–479. https://doi.org/10.1007/s00374-012-0737-7
Bradáčová, K., Sittinger, M., Tietz, K., Neuhäuser, B., Kandeler, E., Berger, N., Ludewig, U., & Neumann, G. (2019). Maize inoculation with microbial consortia: Contrasting effects on rhizosphere activities, nutrient acquisition and early growth in different soils. Microorganisms, 7(9), 329. https://doi.org/10.3390/microorganisms7090329
Brouwer, R. (1963). Some aspects of the equilibrium between overground and underground plant parts. Jaarb. Van Het Inst. Voor Biol. En Scheikd. Onderz. Van Landbouwgewassen, 1963, 31–39.
Collavino, M. M., Sansberro, P. A., Mroginski, L. A., & Aguilar, O. M. (2010). Comparison of in vitro solubilization activity of diverse phosphate-solubilizing bacteria native to acid soil and their ability to promote Phaseolus vulgaris growth. Biology and Fertility of Soils, 46(7), 727–738. https://doi.org/10.1007/s00374-010-0480-x
Cooper, J., Lombardi, R., Boardman, D., & Carliell-Marquet, C. (2011). The future distribution and production of global phosphate rock reserves. Resources, Conservation and Recycling, 57, 78–86. https://doi.org/10.1016/j.resconrec.2011.09.009
Cordell, D., Drangert, J.-O., & White, S. (2009). The story of phosphorus: Global food security and food for thought. Global Environmental Change, 19(2), 292–305. https://doi.org/10.1016/j.gloenvcha.2008.10.009
Cordell, D., & White, S. (2011). Peak phosphorus: Clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability, 3(10), 2027–2049. https://doi.org/10.3390/su3102027
Delaplace, P., Delory, B. M., Baudson, C., Mendaluk-Saunier de Cazenave, M., Spaepen, S., Varin, S., Brostaux, Y., & du Jardin, P. (2015). Influence of rhizobacterial volatiles on the root system architecture and the production and allocation of biomass in the model grass Brachypodium distachyon (L.) P. Beauv. BMC Plant Biology, 15(195). https://doi.org/10.1186/s12870-015-0585-3
Delory, B. M., Baudson, C., Brostaux, Y., Lobet, G., du Jardin, P., Pagès, L., & Delaplace, P. (2016). archiDART: An R package for the automated computation of plant root architectural traits. Plant and Soil, 398, 351–365. https://doi.org/10.1007/s11104-015-2673-4
Delory B. M., Li M., Topp C. N., & Lobet, G. (2018). archiDART v3.0: A new data analysis pipeline allowing the topological analysis of plant root systems. F1000Research, 7, 22. http://dx.doi.org/10.12688/f1000research.13541.1
Delory B. M., Weidlich E. W. A., Meder L., Lütje A., van Duijnen R., Weidlich R., & Temperton V. M. (2017). Accuracy and bias of methods used for root length measurements in functional root research. Methods in Ecology and Evolution, 8, (11), 1594–1606. http://dx.doi.org/10.1111/2041-210x.12771
du Jardin P. (2015). Plant biostimulants: Definition, concept, main categories and regulation. Scientia Horticulturae, 196, 3–14. http://dx.doi.org/10.1016/j.scienta.2015.09.021
European Commission. (2014). Communication from the Commission: On the review of the list of critical raw materials for the EU and the implementation of the Raw Materials Initiative COM(2014) 297 final. European Commission.
European Parliament and Council of the EU, (2019). Regulation (EU) 2019/1009 of the European Parliament and of the Council of 5 June 2019 laying down rules on the making available on the market of EU fertilising products and amending Regulations (EC) No 1069/2009 and (EC) No 1107/2009 and repealing Regulation (EC) No 2003/2003. Official Journal of the European Union 25.06.2019 L170/1-114.
Fernández L., Agaras B., Zalba P., Wall L. G., & Valverde C. (2012). Pseudomonas spp. isolates with high phosphate-mobilizing potential and root colonization properties from agricultural bulk soils under no-till management. Biology and Fertility of Soils, 48, (7), 763–773. http://dx.doi.org/10.1007/s00374-012-0665-6
Giles, C. D., Brown, L. K., Adu, M. O., Mezeli, M. M., Sandral, G. A., Simpson, R. J., Wendler, R., Shand, C. A., Menezes-Blackburn, D., Darch, T., Stutter, M. I., Lumsdon, D. G., Zhang, H., Blackwell, M. S. A., Wearing, C., Cooper, P., Haygarth, P. M., & George, T. S. (2017). Response-based selection of barley cultivars and legume species for complementarity: Root morphology and exudation in relation to nutrient source. Plant Science, 255, 12–28. https://doi.org/10.1016/j.plantsci.2016.11.002
Giles, C. D., Hsu, P.-C., Richardson, A. E., Hurst, M. R. H., & Hill, J. E. (2014). Plant assimilation of phosphorus from an insoluble organic form is improved by addition of an organic anion producing Pseudomonas sp. Soil Biology & Biochemistry, 68, 263–269. https://doi.org/10.1016/j.soilbio.2013.09.026
Goh, C.-H., Veliz Vallejos, D. F., Nicotra, A. B., & Mathesius, U. (2013). The impact of beneficial plant-associated microbes on plant phenotypic plasticity. Journal of Chemical Ecology, 39(7), 826–839. https://doi.org/10.1007/s10886-013-0326-8
Haling, R. E., Yang, Z., Shadwell, N., Culvenor, R. A., Stefanski, A., Ryan, M. H., Sandral, G. A., Kidd, D. R., Lambers, H., & Simpson, R. J. (2016). Growth and root dry matter allocation by pasture legumes and a grass with contrasting external critical phosphorus requirements. Plant and Soil, 407, 67–79. https://doi.org/10.1007/s11104-016-2808-2
Haygarth, P. M., Jarvie, H. P., Powers, S. M., Sharpley, A. N., Elser, J. J., Shen, J., Peterson, H. M., Chan, N.-I., Howden, N. J. K., Burt, T., Worrall, F., Zhang, F., & Liu, X. (2014). Sustainable phosphorus management and the need for a long-term perspective: The legacy hypothesis. Environmental Science and Technology, 48, 8417–8419. https://doi.org/10.1021/es502852s
Hinsinger, P., Plassard, C., Tang, C., & Jaillard, B. (2003). Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant and Soil, 248, 43–59. https://doi.org/10.1023/A:1022371130939
Hothorn T., Bretz F., & Westfall P. (2008). Simultaneous Inference in General Parametric Models. Biometrical Journal, 50, (3), 346–363. http://dx.doi.org/10.1002/bimj.200810425
Idris E. E., Iglesias D. J., Talon M., & Borriss R. (2007). Tryptophan-Dependent Production of Indole-3-Acetic Acid (IAA) Affects Level of Plant Growth Promotion by Bacillus amyloliquefaciens FZB42. Molecular Plant-Microbe Interactions, 20, (6), 619–626. http://dx.doi.org/10.1094/mpmi-20-6-0619
Idriss E. E., Makarewicz O., Farouk A., Rosner K., Greiner R., Bochow H., Richter T., & Borriss R. (2002). Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology, 148, (7), 2097–2109. http://dx.doi.org/10.1099/00221287-148-7-2097.
Koevoets, I. T., Venema, J. H., Elzenga, J. T. M., & Testerink, C. (2016). Roots withstanding their environment: Exploiting root system architecture responses to abiotic stress to improve crop tolerance. Frontiers in Plant Science, 07. https://doi.org/10.3389/fpls.2016.01335
Li, M., Duncan, K., Topp, C. N., & Chitwood, D. H. (2017). Persistent homology and the branching topologies of plants. American Journal of Botany, 104(3), 349–353. https://doi.org/10.3732/ajb.1700046
Li, M., Frank, M. H., Coneva, V., Mio, W., Chitwood, D. H., & Topp, C. N. (2018). The persistent homology mathematical framework provides enhanced genotype-to-phenotype associations for plant morphology. Plant Physiology, 177, 1382–1395. https://doi.org/10.1104/pp.18.00104
Li, Y., Liu, X., Hao, T., & Chen, S., (2017). Colonization and maize growth promotion induced by phosphate solubilizing bacterial isolates. International Journal of Molecular Sciences, 18, (7), 1253. http://dx.doi.org/10.3390/ijms18071253
Liu, Z., Li, Y. C., Zhang, S., Fu, Y., Fan, X., Patel, J. S., & Zhang, M. (2015). Characterization of phosphate-solubilizing bacteria isolated from calcareous soils. Applied Soil Ecology, 96, 217–224. https://doi.org/10.1016/j.apsoil.2015.08.003
Lobet, G., Paez-Garcia, A., Schneider, H., Junker, A., Atkinson, J. A., & Tracy, S. (2019). Demystifying roots: A need for clarification and extended concepts in root phenotyping. Plant Science, 282, 11–13. https://doi.org/10.1016/j.plantsci.2018.09.015
Lobet, G., Pagès, L., & Draye, X. (2011). A novel image-analysis toolbox enabling quantitative analysis of root system architecture. Plant Physiology, 157(1), 29–39. https://doi.org/10.1104/pp.111.179895
Lynch, J. P. (2011). Root phenes for enhanced soil exploration and phosphorus acquisition: Tools for future crops. Plant Physiology, 156(3), 1041–1049. https://doi.org/10.1104/pp.111.175414
Lynch, J., Marschner, P., & Rengel, Z. (2012). Effect of internal and external factors on root growth and development. Marschner’s Miner. Nutr. High. Plants. Elsevier Ltd.
Menezes-Blackburn, D., Giles, C., Darch, T., George, T. S., Blackwell, M., Stutter, M., Shand, C., Lumsdon, D., Cooper, P., Wendler, R., Brown, L., Almeida, D. S., Wearing, C., Zhang, H., & Haygarth, P. M. (2018). Opportunities for mobilizing recalcitrant phosphorus from agricultural soils: A review. Plant and Soil, 427, 5–16. https://doi.org/10.1007/s11104-017-3362-2
Müller, I., Schmid, B., & Weiner, J. (2000). The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspectives in Plant Ecology, Evolution and Systematics, 3(2), 115–127. https://doi.org/10.1078/1433-8319-00007
Murphy, J., & Riley, J. P. (1962). A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31–36.
Myresiotis C. K., Vryzas Z., & Papadopoulou-Mourkidou E. (2015). Effect of specific plant-growth-promoting rhizobacteria (PGPR) on growth and uptake of neonicotinoid insecticide thiamethoxam in corn (Zea mays L.) seedlings. Pest Management Science, 71(9), 1258–1266. http://dx.doi.org/10.1002/ps.3919
Nautiyal C. S. (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters, 170(1), 265–270. http://dx.doi.org/10.1111/j.1574-6968.1999.tb13383.x
Neto, A. P., Favarin, J. L., Hammond, J. P., Tezotto, T., & Couto, H. T. Z. (2016). Analysis of phosphorus use efficiency traits in Coffea genotypes reveals Coffea arabica and Coffea canephora have contrasting phosphorus uptake and utilization efficiencies. Frontiers in Plant Science, 7, https://doi.org/10.3389/fpls.2016.00408
Nico, M., Ribaudo, C. M., Gori, J. I., Cantore, M. L., & Curá, J. A. (2012). Uptake of phosphate and promotion of vegetative growth in glucose-exuding rice plants (Oryza sativa) inoculated with plant growth-promoting bacteria. Applied Soil Ecology, 61, 190–195. https://doi.org/10.1016/j.apsoil.2011.10.016
Nicotra, A. B., Atkin, O. K., Bonser, S. P., Davidson, A. M., Finnegan, E. J., Mathesius, U., Poot, P., Purugganan, M. D., Richards, C. L., Valladares, F., & van Kleunen, M. (2010). Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15(12), 684–692. https://doi.org/10.1016/j.tplants.2010.09.008
Nosrati, R., Owlia, P., Saderi, H., Rasooli, I., & Malboobi, M. A. (2014). Phosphate solubilization characteristics of efficient nitrogen fixing soil Azotobacter strains. Iranian Journal of Microbiology, 6(4), 285–295.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., & Wagner, H. H. (2019). vegan: Community Ecology Package. R package version 2.5-4. https://CRAN.R-project.org/package=vegan
Oteino N., Lally R. D., Kiwanuka S., Lloyd A., Ryan D., Germaine K. J., & Dowling D. N. (2015). Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Frontiers in Microbiology, 6, http://dx.doi.org/10.3389/fmicb.2015.00745
Owen D., Williams A.P., Griffith G.W., & Withers P.J.A. (2015). Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Applied Soil Ecology, 86, 41–54. http://dx.doi.org/10.1016/j.apsoil.2014.09.012
Pereira S. I. A., & Castro P. M. L. (2014). Phosphate-solubilizing rhizobacteria enhance Zea mays growth in agricultural P-deficient soils. Ecological Engineering, 73, 526–535. http://dx.doi.org/10.1016/j.ecoleng.2014.09.060.
Pierret, A., Gonkhamdee, S., Jourdan, C., & Maeght, J.-L. (2013). IJ_Rhizo: An open-source software to measure scanned images of root samples. Plant and Soil, 373, 531–539. https://doi.org/10.1007/s11104-013-1795-9
Poiré R., Chochois V., Sirault X. R. R., Vogel J. P., Watt M., & Furbank R. T. (2014). Digital imaging approaches for phenotyping whole plant nitrogen and phosphorus response inBrachypodium distachyon. Journal of Integrative Plant Biology, 56, (8), 781–796. http://dx.doi.org/10.1111/jipb.12198
Poorter H., & Nagel O. (2000). The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Functional Plant Biology, 27, (6), 595. http://dx.doi.org/10.1071/pp99173
Poorter, H., Niklas, K. J., Reich, P. B., Oleksyn, J., Poot, P., & Mommer, L. (2012). Biomass allocation to leaves, stems and roots: Meta-analyses of interspecific variation and environmental control. New Phytologist, 193, 30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x
Poorter, H., & Sack, L. (2012). Pitfalls and possibilities in the analysis of biomass allocation patterns in plants. Frontiers in Plant Science, 3. https://doi.org/10.3389/fpls.2012.00259
Richardson, A. E., Lynch, J. P., Ryan, P. R., Delhaize, E., Smith, F. A., Smith, S. E., Harvey, P. R., Ryan, M. H., Veneklaas, E. J., Lambers, H., Oberson, A., Culvenor, R. A., & Simpson, R. J. (2011). Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil, 349, 121–156. https://doi.org/10.1007/s11104-011-0950-4
Rowe, H., Withers, P. J. A., Baas, P., Chan, N. I., Doody, D., Holiman, J., Jacobs, B., Li, H., MacDonald, G. K., McDowell, R., Sharpley, A. N., Shen, J., Taheri, W., Wallenstein, M., & Weintraub, M. N. (2016). Integrating legacy soil phosphorus into sustainable nutrient management strategies for future food, bioenergy and water security. Nutrient Cycling in Agroecosystems, 104(3), 393–412. https://doi.org/10.1007/s10705-015-9726-1
Gerardo R., Gutierrez Boem F. H., & Fernández M. C. (2013). Severe Phosphorus Stress Affects Sunflower and Maize but Not Soybean Root to Shoot Allometry. Agronomy Journal, 105, (5), 1283–1288. http://dx.doi.org/10.2134/agronj2013.0123
Havlin, J. L., Tisdale, S. L., Nelson, W. L., & Beaton, J. D. (2013). Soil fertility and Fertilizers. An introduction to nutrient management, 8th edition, Pearson.
Rybakova, D., Schmuck, M., Wetzlinger, U., Varo-Suarez, A., Murgu, O., Müller, H., & Berg, G. (2016). Kill or cure? The interaction between endophytic Paenibacillus and Serratia strains and the host plant is shaped by plant growth conditions. Plant and Soil, 405, 65–79. https://doi.org/10.1007/s11104-015-2572-8
Sandhu, N., Raman, K. A., Torres, R. O., Audebert, A., Dardou, A., Kumar, A., & Henry, A. (2016). Rice root architectural plasticity traits and genetic regions for adaptability to variable cultivation and stress conditions. Plant Physiology, 171(4), 2562–2576. https://doi.org/10.1104/pp.16.00705
Sattari, S. Z., Bouwman, A. F., Giller, K. E., & van Ittersum, M. K. (2012). Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proceedings of the National Academy of Sciences, 109(16), 6348–6353. https://doi.org/10.1073/pnas.1113675109
Schmid, B. (1992). Phenotypic variation in plants. Evolutionary Trends in Plants, 6(1), 45–60.
Schneider C. A., Rasband W. S., & Eliceiri K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675. http://dx.doi.org/10.1038/nmeth.2089
Shaharoona, B., Naveed, M., Arshad, M., & Zahir, Z. A. (2008). Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Applied Microbiology and Biotechnology, 79(1), 147–155. https://doi.org/10.1007/s00253-008-1419-0
Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., Zhang, W., & Zhang, F. (2011). Phosphorus dynamics: from soil to plant. Plant Physiology, 156(3), 997–1005. https://doi.org/10.1104/pp.111.175232
Shipley, B., & Meziane, D. (2002). The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Functional Ecology, 16(3), 326–331. https://doi.org/10.1046/j.1365-2435.2002.00626.x
Sims, L., Pastor, J., Lee, T., & Dewey, B. (2012). Nitrogen, phosphorus and light effects on growth and allocation of biomass and nutrients in wild rice. Oecologia, 170(1), 65–76. https://doi.org/10.1007/s00442-012-2296-x
Talboys, P. J., Owen, D. W., Healey, J. R., Withers, P. J. A., & Jones, D. L. (2014). Auxin secretion by Bacillus amyloliquefaciens FZB42 both stimulates root exudation and limits phosphorus uptake in Triticum aestivium. BMC Plant Biology, 14, 51. https://doi.org/10.1186/1471-2229-14-51
Taller, B. J., & Wong, T. (1989). Medium cytokinins in Azotobacter vinelandii culture medium. Applied and Environment Microbiology, 55(1), 266–268. https://doi.org/10.1128/AEM.55.1.266-267.1989
Timmusk, S., Kim, S.-B., Nevo, E., Abd El Daim, I., Ek, B. O., Bergquist, J., & Behers, L. (2015). Sfp-type PPTase inactivation promotes bacterial biofilm formation and ability to enhance wheat drought tolerance. Frontiers in Microbiology, 6, https://doi.org/10.3389/fmicb.2015.00387
Topp, C. N. (2016). Hope in change: The role of root plasticity in crop yield stability. Plant Physiology, 172(1), 5–6. https://doi.org/10.1104/pp.16.01257
van Dijk, K. C., Lesschen, J. P., & Oenema, O. (2016). Phosphorus flows and balances of the European Union Member States. Science of the Total Environment, 542, 1078–1093. https://doi.org/10.1016/j.scitotenv.2015.08.048
Wang, Y., & Lambers, H. (2020). Root-released organic anions in response to low phosphorus availability: Recent progress, challenges and future perspectives. Plant and Soil, 447, 135–156. https://doi.org/10.1007/s11104-019-03972-8
Warton D. I., Duursma R. A., Falster D. S., & Taskinen S. (2012). smatr 3 - an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3(2), 257–259. http://dx.doi.org/10.1111/j.2041-210x.2011.00153.x
Warton, D. I., Wright, I. J., Falster, D. S., & Westoby, M. (2006). Bivariate line-fitting methods for allometry. Biological Reviews of the Cambridge Philosophical Society, 81(2), 259–291. https://doi.org/10.1017/S1464793106007007
Weiner J. (2004). Allocation, plasticity and allometry in plants. Perspectives in Plant Ecology, Evolution and Systematics, 6(4), 207–215. http://dx.doi.org/10.1078/1433-8319-00083
Wickam, H. (2016). ggplot2: Elegant graphics for data analysis, 2nd Edition, Springer.
Wu Y.-N., Feng Y.-L., Paré P. W., Chen Y.-L., Xu R., Wu S., Wang S.-M., Zhao Q., Li H.-R., Wang Y.-Q., & Zhang J.-L. (2016). Beneficial soil microbe promotes seed germination, plant growth and photosynthesis in herbal crop Codonopsis pilosula. Crop and Pasture Science, 67, (1), 91–98. http://dx.doi.org/10.1071/cp15110.
Xie, J.-B., Xu, G.-Q., Jenerette, G. D., Bai, Y.-F., Wang, Z.-Y., & Li, Y. (2015). Apparent plasticity in functional traits determining competitive ability and spatial distribution: A case from desert. Scientific Reports, 5(1), https://doi.org/10.1038/srep12174
Yu, X., Liu, X. U., Zhu, T. H., Liu, G. H., & Mao, C. (2011). Isolation and characterization of phosphate-solubilizing bacteria from walnut and their effect on growth and phosphorus mobilization. Biology and Fertility of Soils, 47(4), 437–446. https://doi.org/10.1007/s00374-011-0548-2
Zabihi H. R., Savaghebi G. R., Khavazi K., Ganjali A., & Miransari M. (2011). Pseudomonas bacteria and phosphorous fertilization, affecting wheat (Triticum aestivum L.) yield and P uptake under greenhouse and field conditions. Acta Physiologiae Plantarum, 33(1), 145–152. http://dx.doi.org/10.1007/s11738-010-0531-9
Zhang, J.-L., Aziz, M., Qiao, Y., Han, Q.-Q., Li, J., Wang, Y.-Q., Shen, X., Wang, S.-M., & Paré, P. W. (2014). Soil microbe Bacillus subtilis (GB03) induces biomass accumulation and salt tolerance with lower sodium accumulation in wheat. Crop and Pasture Science, 65(5), 423–427. https://doi.org/10.1071/CP13456
Zhou, D., Huang, X.-F., Chaparro, J. M., Badri, D. V., Manter, D. K., Vivanco, J. M., & Guo, J. (2016). Root and bacterial secretions regulate the interaction between plants and PGPR leading to distinct plant growth promotion effects. Plant and Soil, 401(1–2), 259–272. https://doi.org/10.1007/s11104-015-2743-7
