P and N deficiency change the relative abundance and function of rhizosphere microorganisms during cluster root development of white lupin (Lupinus albus L.)

References

• Adams MA, Pate JS 1992: Availability of organic and inorganic forms of phosphorus to lupins (Lupinus spp.). Plant Soil, 145, 107–113. doi:10.1007/BF00009546
   Web of Science ®Google Scholar
• Dessaux Y, Grandclément C, Faure D 2016: Engineering the rhizosphere. Trends Plant Sci., 21, 266–278. doi:10.1016/j.tplants.2016.01.002
   PubMed Web of Science ®Google Scholar
• Dessureault-Rompré J, Nowack B, Schulin R, Luster J 2006: Modified micro suction cup/rhizobox approach for the in-situ detection of organic acids in rhizosphere soil solution. Plant Soil, 286, 99–107. doi:10.1007/s11104-006-9029-z
   Web of Science ®Google Scholar
• Dinkelaker B, Marschner H 1992: In vivo demonstration of acid phosphatase activity in the rhizosphere of soil-grown plants. Plant Soil, 144, 199–205. doi:10.1007/BF00012876
   Web of Science ®Google Scholar
• Dissanayaka DMSB, Maruyama H, Masuda G, Wasaki J 2015: Interspecific facilitation of P acquisition in the intercropping of maize with white lupin in two contrasting soils as influenced by different rates and forms of P supply. Plant Soil, 390, 223–236. doi:10.1007/s11104-015-2392-x
   Web of Science ®Google Scholar
• Dissanayaka DMSB, Wickramasinghe WMKR, Marambe B, Wasaki J 2017: Phosphorus-mobilization strategy based on carboxylate exudation in lupins (Lupinus, Fabaceae): a mechanism facilitating the growth and phosphorus acquisition of neighboring plants under phosphorus-limited conditions. Exp. Agr., 53, 308–319. doi:10.1017/S0014479716000351
   Web of Science ®Google Scholar
• Esfahani MN, Kusano M, Nguyen KH, Watanabe Y, Ha CV, Saito K, Sulieman S, Herrera-Estrella L, Tran LSP 2016: Adaptation of the symbiotic Mesorhizobium–chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism. Proc. Natl. Acad. Sci. USA, 113, E4610–E4619. doi:10.1073/pnas.1609440113
   PubMed Web of Science ®Google Scholar
• Gardner WK, Barber DA, Parbery DG 1983: The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil, 70, 107–124. doi:10.1007/BF02374754
   Web of Science ®Google Scholar
• Hagström J, James WM, Skene KR 2001: A comparison of structure, development and function in cluster roots of Lupinus albus L. under phosphate and iron stress. Plant Soil, 232, 81–90. doi:10.1023/A:1010334003073
   Web of Science ®Google Scholar
• Hawkins H-J, Wolf G, Stock WD 2005: Cluster roots of Leucadendron laureolum (Proteaceae) and Lupinus albus (Fabaceae) take up glycine intact: an adaptive strategy to low mineral nitrogen in soils? Ann. Bot., 96, 1275–1282. doi:10.1093/aob/mci279
   PubMed Web of Science ®Google Scholar
• Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH 1997: Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol., 63, 3233–3241.
   PubMed Web of Science ®Google Scholar
• Hue NV 2009: Iron and phosphorus fertilizations and the development of proteoid roots in macadamia (Macadamia integrifolia). Plant Soil, 318, 93–100. doi:10.1007/s11104-008-9820-0
   Web of Science ®Google Scholar
• Khamna S, Yokota A, Lumyong S 2009: Actinomycetes isolated from medicinal plant rhizosphere soils: diversity and screening of antifungal compounds, indole-3-acetic acid and siderophore production. World J. Mirobiol. Biotechnol., 25, 649–655. doi:10.1007/s11274-008-9933-x
   Web of Science ®Google Scholar
• Lambers H, Clements JC, Nelson MN 2013: How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am. J. Bot., 100, 263–288. doi:10.3732/ajb.1200474
   PubMed Web of Science ®Google Scholar
• Lamont B 1972a: ‘Proteoid’ roots in the legume Viminaria juncea. Search, 3, 90–91.
   Google Scholar
• Lamont B 1972b: The morphology and anatomy of proteoid roots in the genus Hakea. Aust. J. Bot., 20, 155–174. doi:10.1071/BT9720155
   Web of Science ®Google Scholar
• Lamont BB, Pérez-Fernández M, Rodríguez-Sánchez J 2014: Soil bacteria hold the key to root cluster formation. New Phytol., 206, 1156–1162. doi:10.1111/nph.13228
   PubMed Web of Science ®Google Scholar
• Le Bayon CC, Weisskopf L, Martinoia E, Jansa J, Frossard E, Keller F, Föllmi KB, Gobat JM 2006: Soil phosphorus uptake by continuously cropped Lupinus albus: a new microcosm design. Plant Soil, 283, 309–321. doi:10.1007/s11104-006-0021-4
   Web of Science ®Google Scholar
• Le Roux MR, Khan SZ, Valentine AJ 2009: Nitrogen and carbon costs of soybean and lupin root systems during phosphate starvation. Symbiosis, 48, 102–109. doi:10.1007/BF03179989
   Web of Science ®Google Scholar
• Li MG, Tadano T 1996: Comparison of characteristics of acid phosphatases secreted from roots of lupin and tomato. Soil Sci. Plant Nutr., 42, 753–763. doi:10.1080/00380768.1996.10416623
   Web of Science ®Google Scholar
• Marschner P, Neumann G, Kania A, Weisskopf L, Lieberei R 2002: Spatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinus albus L.). Plant Soil, 246, 167–174. doi:10.1023/A:1020663909890
   Web of Science ®Google Scholar
• Miller SS, Liu J, Allan DL, Menzhuber CJ, Fedorova M, Vance CP 2001: Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. Plant Physiol., 127, 594–606. doi:10.1104/pp.010097
   PubMed Web of Science ®Google Scholar
• Naether A, Foesel BU, Naegele V et al. 2012: Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl. Environ. Microbiol., 78, 7398–7406. doi:10.1128/AEM.01325-12
   PubMed Web of Science ®Google Scholar
• Neumann G, Martinoia E 2002: Cluster roots – an underground adaptation for survival in extreme environments. Trends Plant Sci., 7, 162–167. doi:10.1016/S1360-1385(02)02241-0
   PubMed Web of Science ®Google Scholar
• Ozawa K, Osaki M, Matsui H, Honma M, Tadano T 1995: Purification and properties of acid phosphatase secreted from lupin roots under phosphorus-deficiency conditions. Soil Sci. Plant Nutr., 41, 461–469. doi:10.1080/00380768.1995.10419608
   Web of Science ®Google Scholar
• Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S 2008: Plants can use protein as a nitrogen source without assistance from other organisms. PNAS, 105, 4524–4529. doi:10.1073/pnas.0712078105
   PubMed Web of Science ®Google Scholar
• Paungfoo-Lonhienne C, Schenk PM, Lonhienne TGA, Brackin R, Meier S, Rentsch D, Schmidt S 2009: Nitrogen affects cluster root formation and expression of putative peptide transporters. J. Exp. Bot., 60, 2665–2676. doi:10.1093/jxb/erp111
   PubMed Web of Science ®Google Scholar
• Rath M, Salas J, Parhy B et al. 2010: Identification of genes induced in proteoid roots of white lupin under nitrogen and phosphorus deprivation, with functional characterization of a formamidase. Plant Soil, 334, 137–150. doi:10.1007/s11104-010-0373-7
   Web of Science ®Google Scholar
• Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M 2008: Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci. Plant Nutr., 54, 62–71. doi:10.1111/j.1747-0765.2007.00210.x
   Web of Science ®Google Scholar
• Sas L, Rengel Z, Tang C 2002: The effect of nitrogen nutrition on cluster root formation and proton extrusion by Lupinus albus. Ann. Bot., 89, 435–442. doi:10.1093/aob/mcf066
   PubMed Web of Science ®Google Scholar
• Schmidt S, Mason M, Sangtiean T, Stewart GR 2003: Do cluster roots of Hakea actities (Proteaceae) acquire complex organic nitrogen? Plant Soil, 248, 157–165. doi:10.1023/A:1022352415728
   Web of Science ®Google Scholar
• Schulze J, Temple G, Temple SJ, Beschow H, Vance CP 2006: Nitrogen fixation by white lupin under phosphorus deficiency. Ann. Bot., 98, 731–740. doi:10.1093/aob/mcl154
   PubMed Web of Science ®Google Scholar
• Sessitsch A, Howieson JG, Perret X, Antoun H, Martínez-Romero E 2002: Advances in Rhizobium research. Crit. Rev. Plant Sci., 21, 323–378. doi:10.1080/0735-260291044278
   Web of Science ®Google Scholar
• Shane MW, Lambers H 2005: Cluster roots: a curiosity in context. Plant Soil, 274, 101–125. doi:10.007/s11104-004-2725-7
   Web of Science ®Google Scholar
• Sulieman S, Tran LSP 2015: Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci., 239, 36–43. doi:10.1016/j.plantsci.2015.06.018
   PubMed Web of Science ®Google Scholar
• Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H 1993: Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil, 155–156, 95–98. doi:10.1007/BF00024992
   Web of Science ®Google Scholar
• Trinick MJ 1977: Vesicular-arbuscular infection and soil phosphorus utilization in Lupinus spp. New Phytol., 78, 297–304. doi:10.1111/j.1469-8137.1977.tb04833.x
   Web of Science ®Google Scholar
• Truog E 1930: The determination of the readily available phosphorus in soils. J. Am. Soc. Agron., 22, 874–882. doi:10.2134/agronj1930.00021962002200100008x
   Google Scholar
• Unno Y, Okubo K, Wasaki J, Shinano T, Osaki M 2005: Plant growth promotion abilities and micro-scale bacterial dynamics in the rhizosphere of lupin analyzed by phytate utilization ability. Environ. Microbiol., 7, 396–404. doi:10.1111/j.1462-2920.2004.00701.x
   PubMed Web of Science ®Google Scholar
• Verbon EH, Liberman LM 2016: Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci., 21, 218–229. doi:10.1016/j.tplants.2016.01.013
   PubMed Web of Science ®Google Scholar
• Wang Q, Garrity GM, Tiedje JM, Cole JR 2007: Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol., 73, 5261–5267. doi:10.1128/AEM.00062-07
   PubMed Web of Science ®Google Scholar
• Wasaki J, Omura M, Ando M, Dateki H, Shinano T, Osaki M, Ito H, Matsui H, Tadano T 2000: Molecular cloning and root specific expression of secretory acid phosphatase from phosphate deficient lupin (Lupinus albus L.). Soil Sci. Plant Nutr., 46, 427–437. doi:10.1080/00380768.2000.10408796
   Web of Science ®Google Scholar
• Wasaki J, Rothe A, Kania A, Neumann G, Römheld V, Shinano T, Osaki M, Kandeler E 2005: Root exudation, P acquisition and microbial diversity in the rhizosphere of Lupinus albus as affected by P supply and atmospheric CO2 concentration. J. Environ. Qual., 34, 2157–2166. doi:10.2134/jeq2004.0423
   PubMed Web of Science ®Google Scholar
• Wasaki J, Yamamura T, Shinano T, Osaki M 2003: Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant Soil, 248, 129–136. doi:10.1023/A:1022332320384
   Web of Science ®Google Scholar
• Watanabe T, Osaki M, Tadano T 1998: Effects of nitrogen source and aluminum on growth of tropical tree seedlings adapted to low pH soils. Soil Sci. Plant Nutr., 44, 655–666. doi:10.1080/00380768.1998.10414489
   Web of Science ®Google Scholar
• Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E 2006: White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ., 29, 919–927. doi:10.1111/j.1365-3040.2005.01473.x
   PubMed Web of Science ®Google Scholar
• Weisskopf L, Heller S, Eberl L 2011: Burkholderia species are major inhabitants of white lupin cluster roots. Appl. Environ. Microbiol., 77, 7715–7720. doi:10.1128/AEM.05845-11
   PubMed Web of Science ®Google Scholar