Phosphorus is one of the most important nutrients required for plant growth and development. While substantial amounts of total phosphorus are present in many soil types, plants are unable to utilize some organic phosphorus sources. The main goal of this study was to characterize the spectrum of secreted plant proteins, organic acids and other metabolites that can potentially contribute to utilization of various phosphorus compounds. Our data indicate that the composition of extracellular proteins secreted by plant roots varies depending on the specific source of P in the growth medium. Furthermore, some root-secreted metabolites, such as citrate, appear to be specific to a subset of ecotypes, while tartrate, succinate and oxalate are secreted by a number of A. thaliana ecotypes. We observed secretion of phenolic compounds, such as tannins, and deoxycytidine derivatives. Taken together, while no single secreted polypeptide, organic acid or secondary metabolite can be pinpointed as specific to plant growth in particular phosphorus conditions, our data indicate that A. thaliana ecotypes differ in their physiological responses to the source of phosphorus in the growth medium. Overall, these results suggest that physiological changes in plant responses to nutrient limitation are modulated by interactions between soil phosphorus source and the specific genotype of Arabidopsis plants.
Hanif, M.K., Hameed, S., Imran, A., Naqqash, T., Shahid, M. and Van Elsas, J.D. (2015) Isolation and Characterization of a β-Propeller Gene Containing Phosphobacterium Bacillus subtilis Strain KPS-11 for Growth Promotion of Potato (Solanum tuberosum L.). Frontiers in Microbiology, 6, 583. https://doi.org/10.3389/fmicb.2015.00583
Yuan, H. and Liu, D. (2008) Signaling Components Involved in Plant Responses to Phosphate Starvation. Journal of Integrative Plant Biology, 50, 849-859. https://doi.org/10.1111/j.1744-7909.2008.00709.x
Miller, S.S., Liu, J., Allan, D.L., Menzhuber, C., Federova, M. and Vance, C.P. (2001) Molecular Control of Acid Phosphatase Secretion into the Rhizosphere of Proteoid Roots. Plant Physiology, 127, 594-606. https://doi.org/10.1104/pp.010097
Bozzo, G.G., Raghothama, K.G. and Plaxton, W.C. (2002) Purification and Characterization of Two Secreted Purple Acid Phosphatase Isozymes from Phosphate-Starved Tomato (Lycopersicon esculentum) Cell Cultures. European Journal of Biochemistry, 269, 6278-6286. https://doi.org/10.1046/j.1432-1033.2002.03347.x
Liang, C., Tian, J., Lam, H.M., Lim, B.L., Yan, X. and Liao, H. (2010) Biochemical and Molecular Characterization of PvPAP3, a Novel Purple Acid Phosphatase Isolated from Common Bean Enhancing Extracellular ATP Utilization. Plant Physiology, 152, 854-865. https://doi.org/10.1104/pp.109.147918
Lung, S.-C., Leung, A., Kuang, R., Wang, Y., Leung, P. and Lim, B.-L. (2008) Phytase Activity in Tobacco (Nicotiana tabacum) Root Exudates Is Exhibited by a Purple Acid Phosphatase. Phytochemistry, 69, 365-373. https://doi.org/10.1016/j.phytochem.2007.06.036
Tran, L.S., Nishiyama, R., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2010) Potential Utilization of NAC Transcription Factors to Enhance Abiotic Stress Tolerance in Plants by Biotechnological Approach. GM Crops, 1, 32-39. https://doi.org/10.4161/gmcr.1.1.10569
Richardson, A.E., Barea, J.-M., McNeill, A.M. and Prigent-Combaret, C. (2009) Acquisition of Phosphorus and Nitrogen in the Rhizosphere and Plant Growth Promotion by Microorganisms. Plant Soil, 321, 305-339. https://doi.org/10.1007/s11104-009-9895-2
Rugova, A., Puschenreiter, M., Santner, J., Fischer, L., Neubauer, S. and Koellensperger, G. (2014) Speciation Analysis of Orthophosphate and Myo-Inositol Hexakisphosphate in Soil- and Plant-Related Samples by Highperformance Ion Chromatography Combined with Inductively Coupled Plasma Mass Spectrometry. Journal of Separation Science, 37, 1711-1719. https://doi.org/10.1002/jssc.201400026
Xiao, K., Katagi, H., Harrison, M. and Wang, Z.Y. (2006) Improved Phosphorus Acquisition and Biomass Production in Arabidopsis by Transgenic Expression of a Purple Acid Phosphatase Gene from M. truncatula. Plant Science, 170, 191-202. https://doi.org/10.1016/j.plantsci.2005.08.001
Ma, X.F., Wright, E., Ge, Y., Bell, J., Xi, Y., Bouton, J.H. and Wang, Z.Y. (2009) Improving Phosphorus Acquisition of White Clover (Trifolium repens L.) by Transgenic Expression of Plant-Derived Phytase and Acid Phosphatase Genes. Plant Science, 176, 479-488. https://doi.org/10.1016/j.plantsci.2009.01.001
Wang, X., Wang, Y., Tian, J., Lim, B.L., Yan, X. and Liao, H. (2009) Overexpressing AtPAP15 Enhances Phosphorus Efficiency in Soybean. Plant Physiology, 151, 233-240. https://doi.org/10.1104/pp.109.138891
Valeeva, L., Nyamsuren, Ch., Sharipova, M. and Shakirov, E. (2018) Plant Stimulates Arabidopsis thaliana Growth on Phytate. Frontiers in Plant Science, 9, 1-14. https://doi.org/10.3389/fpls.2018.00186
George, T.S., Simpson, R.J., Hadobas, P.A. and Richardson, A.E. (2005) Expression of a Fungal Phytase Gene in Nicotiana tabacum Improves Phosphorus Nutrition in Plants Grown in Amended Soil. Plant Biotechnology Journal, 3, 129-140. https://doi.org/10.1111/j.1467-7652.2004.00116.x
Mudge, S.R., Smith, F.W. and Richardson, A.E. (2003) Root Specific and Phosphate Regulated Expression of Phytase under the Control of a Phosphate Transporter Promoter Enables Arabidopsis to Grow on Phytate as a Sole P Source. Plant Science, 165, 871-878. https://doi.org/10.1016/S0168-9452(03)00286-3
Murashige, T. and Skoog, F. (1962) A Revised Medium for Rapid Growth and Bio-Assays with Tobacco Tissue Cultures. Physiologia Plantarum, 15, 473-497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Tocquin, P., Corbesier, L., Havelange, A., Pieltain, A., Kurtem, E., Bernier, G. and Perilleux, C. (2003) A Novel High Efficiency, Low Maintenance, Hydroponic System for Synchronous Growth and Flowering of Arabidopsis thaliana. BMC Plant Biology, 3, 1-10. https://doi.org/10.1186/1471-2229-3-2
Dundek, P., Holik, L., Rohlik, T., Hromadko, L., Vranova, V., Rejchek, K. and Formanek, P. (2011) Methods of Plant Root Exudates Analysis: A Review. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 3, 241-246. https://doi.org/10.11118/actaun201159030241
Song, L., Jenner, M., Masschelein, J., Jones, C., Bull, M.J., Harris, S.R., Hartkoorn, R.C., Vocat, A., Romero-Canelon, I., Coupland, P., Webster, G., Dunn, M., Weiser, R., Paisey, C., Cole, S.T., Parkhill, J., Mahenthiralingam, E. and Challis, G.L. (2017) Discovery and Biosynthesis of Gladiolin: A Burkholderia gladioli Antibiotic with Promising Activity against Mycobacterium tuberculosis. Journal of the American Chemical Society, 139, 7974-7981. https://doi.org/10.1021/jacs.7b03382
Lee, H.S. (1993) HPLC Method for Separation and Determination of Nonvolatile Organic Acids in Orange Juice. Journal of Agricultural and Food Chemistry, 41, 1991-1993. https://doi.org/10.1021/jf00035a033
Basu, U., Francis, J.L., Whittal, R.M., Stephens, J.L., Wang, Y., Zaiane, O.R., Goebel, R., Muench, D.G., Good, A.G. and Taylor, G.J. (2006) Extracellular Proteomes of Arabidopsis thaliana and Brassica napus Roots: Analysis and Comparison by MudPIT and LCMS/MS. Plant Soil, 286, 357-376. https://doi.org/10.1007/s11104-006-9048-9
Yao, X., Li, J., Liu, J. and Liu, K. (2015) An Arabidopsis Mitochondria-Localized RRL Protein Mediates Abscisic Acid Signal Transduction through Mitochondrial Retrograde Regulation Involving ABI4. Journal of Experimental Botany, 66, 6431-6445. https://doi.org/10.1093/jxb/erv356
Veyres, N., Danon, A., Aono, M., Galliot, S., Karibasappa, Y.B., Diet, A., Grandmottet, F., Tamaoki, M., Lesur, D., Pilard, S., Boitel-Conti, M., Sangwan-Norreel, B.S. and Sangwan, R.S. (2008) The Arabidopsis Sweetie Mutant Is Affected in Carbohydrate Metabolism and Defective in the Control of Growth, Development and Senescence. The Plant Journal, 55, 665-686. https://doi.org/10.1111/j.1365-313X.2008.03541.x
https://www.arabidopsis.org
Golani, Y., Kayea, Y., Gilhara, O., Ercetinb, M., Gillaspyb, G. and Levinea, A. (2013) Inositol Polyphosphate Phosphatidylinositol 5-Phosphatase9 (At5PTase9) Controls Plant Salt Tolerance by Regulating Endocytosis. Molecular Plant, 6, 1781-1794. https://doi.org/10.1093/mp/sst072
Deeks, M.J., Calcutt, J.R., Ingle, E.K.S., Hawkins, T.J., Chapman, S., Richardson, A.C., Mentlak, D.A., Dixon, M.R., Cartwright, F., Smertenko, A.P., Oparka, K. and Hussey, P.J. (2012) A Superfamily of Actin-Binding Proteins at the Actin-Membrane Nexus of Higher Plants. Current Biology, 22, 1595-1600. https://doi.org/10.1016/j.cub.2012.06.041
Laudert, D., Pfannschmidt, U., Lottspeich, F., Hollnder-Czytko, H. and Weiler, E.W. (1996) Cloning, Molecular and Functional Characterization of Arabidopsis thaliana Allene Oxide Synthase (CYP 74), the First Enzyme of the Octadecanoid Pathway to Jasmonates. Plant Molecular Biology, 31, 323-335. https://doi.org/10.1007/BF00021793
Ma, S., Gong, Q. and Bohnert, H.J. (2006) Dissecting Salt Stress Pathways. Journal of Experimental Botany, 57, 1097-1107. https://doi.org/10.1093/jxb/erj098
Suttangkakul, A., Li, F., Chung, T. and Vierstra, R.D. (2011) The ATG1/ATG13 Protein Kinase Complex Is Both a Regulator and a Target of Autophagic Recycling in Arabidopsis. The Plant Cell Preview, 10, 3761-3779. https://doi.org/10.1105/tpc.111.090993
Wang, Y.-L., Almvik, M., Clarke, N., Eich-Greatorex, S., Ogaard, A.F., Krogstad, T., Lambers, H. and Clarke, J.L. (2015) Contrasting Responses of Root Morphology and Rootexuded Organic Acids to Low Phosphorus Availability in Three Important Food Crops with Divergent Root Traits. AoB Plants, 7, plv097. https://doi.org/10.1093/aobpla/plv097
Zhang, F.S., Ma, J. and Cao, Y.P. (1997) Phosphorus Deficiency Enhances Root Exudation of Low-Molecular Weight Organic Acids and Utilization of Sparingly Soluble Inorganic Phosphates by Radish (Raghanus satiuvs L.) and Rape (Brassica napus L.) Plants. Plant and Soil, 196, 261-264. https://doi.org/10.1007/978-94-009-0047-9_88
Balzergue, C., Dartevelle, T., Godon, C., Laugier, E., Meisrimler, C., Teulon, J.-M., Creff, A., Bissler, M., Brouchoud, C., Hagege, A., Muller, J., Chiarenza, S., Javot, H., Becuwe-Linka, N., David, P., Peret, B., Delannoy, E., Thibaud, M.-C., Armengaud, J., Abel, S., Pellequer, J.-L., Nussaume, L. and Desnos, T. (2017) Low Phosphate Activates STOP1-ALMT1 to Rapidly Inhibit Root Cell Elongation. Nature Communications, 8, Article No. 15300. https://doi.org/10.1038/ncomms15300
Sakurai, T., Yamada, Y., Sawada, Y., Matsuda, F., Akiyama, K., Shinozaki, K., Hirai, M.Y. and Saito, K. (2013) PRIMe Update: Innovative Content for Plant Metabolomics and Integration of Gene Expression and Metabolite Accumulation. Plant and Cell Physiology, 54, 1-8. https://doi.org/10.1093/pcp/pcs184
Yin, X., Bellaloui, N., McClure, A.M., Tyler, D.D. and Mengistu, A. (2016) Phosphorus Fertilization Differentially Influences Fatty Acids, Protein, and Oil in Soybean. American Journal of Plant Science, 7, 1975-1992. https://doi.org/10.4236/ajps.2016.714180
Kachroo, A., Venugopal, S.C., Lapchyk, L., Falcone, D., Hildebrand, D. and Kachroo, P. (2004) Oleic Acid Levels Regulated by Glycerolipid Metabolism Modulate Defense Gene Expression in Arabidopsis. PNAS, 101, 5152-5157. https://doi.org/10.1073/pnas.0401315101
Liu, S., Dunwell, T.L., Pfeifer, G.P., Dunwell, J.M., Ullah, I. and Wang, Y. (2013) Detection of Oxidation Products of 5-Methyl-2’-Deoxycytidine in Arabidopsis DNA. PLoS ONE, 8, e84620. https://doi.org/10.1371/journal.pone.0084620
Hassanpour, S., Maherisis, N., Eshratkhah, B. and Baghbani Mehmandar, F. (2011) Plants and Secondary Metabolites (Tannins): A Review. International Journal of Forest, Soil and Erosion, 1, 47-53.
Davies, R.I., Coulson, C.B. and Leisw, D.A. (1964) Polyphenols Is Plant, Humus, and Soil IV. Factors Leading to Increase in Biosynthesis of Polyphenol in Leaves and Their Relationship to Mull and More Formation. Journal of Soil Science, 15, 310. https://doi.org/10.1111/j.1365-2389.1964.tb02228.x