Skip to main content
SpringerLink
Log in

White Lupin: A Model System for Understanding Plant Adaptation to Low Phosphorus Availability

  • Chapter
  • First Online:
Legume Nitrogen Fixation in Soils with Low Phosphorus Availability

Abstract

Phosphorus (P), in its ionized form (Pi), is one of the most limiting nutrients for plant growth and development. White lupin is a dinitrogen (N2)-fixing legume that can increase Pi availability in soils. Under Pi deficiency, white lupin develops cluster roots, also known as proteoid roots. Cluster roots are densely packed lateral roots, resembling bottlebrushes. The resulting increase in root surface, together with coordinated biochemical responses, releases bound Pi and makes it available for plant uptake. The most noticeable biochemical responses that increase Pi availability include excretion of organic anions and phosphatases. As a consequence, white lupin can grow without addition of Pi fertilizer, and its ability to fix N2 is less inhibited by Pi deficiency, compared to other legumes. However, formation of cluster roots requires additional carbon (C) and nitrogen (N). Thus, white lupin needs to carefully balance C use with the formation of cluster roots and nodules. High-throughput approaches, particularly RNA-seq, have revealed many of the genes involved in cluster root formation and function and are beginning to reveal networks that regulate Pi acquisition and use. A better understanding of white lupin’s responses to low nutrients may help to overcome inhibition of N2 fixation by low Pi availability in other legumes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ainouche A-K, Bayer RJ (1999) Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Am J Bot 86(4):590–607

    Article  CAS  PubMed  Google Scholar 

  • Ainouche A, Bayer R, Misset M-T (2004) Molecular phylogeny, diversification and character evolution in Lupinus (Fabaceae) with special attention to Mediterranean and African lupines. Plant Syst Evol 246(3–4):211–222

    CAS  Google Scholar 

  • Alexova R, Millar AH (2013) Proteomics of phosphate use and deprivation in plants. Proteomics 13(3–4):609–623

    Article  CAS  PubMed  Google Scholar 

  • Barakate A, Stephens J (2016) An overview of CRISPR-based tools and their improvements: new opportunities in understanding plant–pathogen interactions for better crop protection. Front Plant Sci 7:765

    Article  PubMed  PubMed Central  Google Scholar 

  • Batjes N (1997) A world dataset of derived soil properties by FAO–UNESCO soil unit for global modelling. Soil Use Manag 13(1):9–16

    Article  Google Scholar 

  • Baveye PC (2015) Looming scarcity of phosphate rock and intensification of soil phosphorus research. Rev Bras Ciênc Solo 39(3):637–642

    Article  CAS  Google Scholar 

  • Baxter I (2015) Should we treat the ionome as a combination of individual elements, or should we be deriving novel combined traits? J Exp Bot 66(8):2127–2131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baxter I, Vitek O, Lahner B, Muthukumar B, Borghi M, Morrissey J, Guerinot M, Salt D (2008) The leaf ionome as a multivariable system to detect a plant’s physiological status. Proc Natl Acad Sci U S A 105(33):12081–12086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bobadilla R, Berr A (2016) Histone methylation-a cornerstone for plant responses to environmental stresses? In: Shanker A, Shanker C (eds) Abiotic and biotic stress in plants - recent advances and future perspectives. Intech. doi:10.5772/61733

    Google Scholar 

  • Borquez A, Serrano E, Dantagnan P, Carrasco J, Hernandez A (2011) Feeding high inclusion of whole grain white lupin (Lupinus albus) to rainbow trout (Oncorhynchus mykiss): effects on growth, nutrient digestibility, liver and intestine histology and muscle fatty acid composition. Aquac Res 42(8):1067–1078

    Article  CAS  Google Scholar 

  • Braum S, Helmke P (1995) White lupin utilizes soil phosphorus that is unavailable to soybean. Plant Soil 176(1):95–100

    Article  CAS  Google Scholar 

  • Brebaum S, Boland G (1995) Sweet white lupin: a potential crop for Ontario. Can J Plant Sci 75(4):841–849

    Article  Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154(2):275–304

    Article  Google Scholar 

  • Campbell C, Sage R (2002) Interactions between atmospheric CO2 concentration and phosphorus nutrition on the formation of proteoid roots in white lupin (Lupinus albus L.) Plant Cell Environ 25(8):1051–1059

    Article  Google Scholar 

  • Campbell CD, Sage RF (2006) Interactions between the effects of atmospheric CO2 content and P nutrition on photosynthesis in white lupin (Lupinus albus L.) Plant Cell Environ 29(5):844–853

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, May GD, Jackson SA (2009) Three sequenced legume genomes and many crop species: rich opportunities for translational genomics. Plant Physiol 151(3):970–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Bucciarelli B, Liu J, Zinn K, Miller S, Patton-Vogt J, Allan D, Shen J, Vance CP (2011) White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiol 156(3):1131–1148. doi:pp.111.173724 [pii]10.1104/pp.111.173724

  • Cheng L, Tang X, Vance CP, White PJ, Zhang F, Shen J (2014) Interactions between light intensity and phosphorus nutrition affect the phosphate-mining capacity of white lupin (Lupinus albus L.) J Exp Bot 65(12):2995–3003. doi:10.1093/jxb/eru135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin JH, Gamuyao R, Dalid C, Bustamam M, Prasetiyono J, Moeljopawiro S, Wissuwa M, Heuer S (2011) Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol. 156(3):1202–1216. doi:pp.111.175471 [pii]10.1104/pp.111.175471

  • Choi C-S, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Gen Genomics 277(5):589–600

    Article  CAS  Google Scholar 

  • Choi H-K, Mun J-H, Kim D-J, Zhu H, Baek J-M, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci U S A 101(43):15289–15294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christeller JT, Laing W, Sutton WD (1977) Carbon dioxide fixation by lupin root nodules I. Characterization, association with phosphoenolpyruvate carboxylase, and correlation with nitrogen fixation during nodule development. Plant Physiol 60(1):47–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clements J, Buirchell B, Yang H, Smith P, Sweetingham M, Smith C (2005) Chapter 9: lupin. In: Singh R, Jauhar P (eds) Genetic resources, chromosome engineering, and crop improvement, series-II Grain Legumes. CRC Press, Boca Raton

    Google Scholar 

  • Cordell D, Drangert J, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19(2):292–305

    Article  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218(6):900–905

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57(3):581–588

    Article  CAS  PubMed  Google Scholar 

  • Correll DL (1998) The role of phosphorus in the eutrophication of receiving waters: a review. J Environ Qual 27(2):261–266

    Article  CAS  Google Scholar 

  • Cowling W, Huyghe C, Swiecicki W, Gladstones J, Atkins C, Hamblin J (1998) Lupin breeding. In: Lupins as crop plants: biology, production and utilization. CAB International, Wallingford, pp 93–120

    Google Scholar 

  • Cramer MD (2010) Phosphate as a limiting resource: introduction. Plant Soil 334(1–2):1–10

    Article  CAS  Google Scholar 

  • Cramer M, Shane M, Lambers H (2005) Physiological changes in white lupin associated with variation in root-zone CO2 concentration and cluster-root P mobilization. Plant Cell Environ 28(10):1203–1217

    Article  CAS  Google Scholar 

  • Croxford AE, Rogers T, Caligari PD, Wilkinson MJ (2008) High-resolution melt analysis to identify and map sequence-tagged site anchor points onto linkage maps: a white lupin (Lupinus albus) map as an exemplar. New Phytol 180(3):594–607

    Article  CAS  PubMed  Google Scholar 

  • Cu ST, Hutson J, Schuller KA (2005) Mixed culture of wheat (Triticum aestivum L.) with white lupin (Lupinus albus L.) improves the growth and phosphorus nutrition of the wheat. Plant Soil 272(1–2):143–151

    Article  CAS  Google Scholar 

  • Dessureault-Rompré J, Nowack B, Schulin R, Luster J (2007) Spatial and temporal variation in organic acid anion exudation and nutrient anion uptake in the rhizosphere of Lupinus albus L. Plant Soil 301(1–2):123–134

    Article  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(3):285–292

    Article  CAS  Google Scholar 

  • Dinkelaker B, Hengeler C, Marschner HJBA (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200

    Article  Google Scholar 

  • Durrett T, Gassmann W, Rogers E (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144(1):197–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edixhoven J, Gupta J, Savenije H (2014) Recent revisions of phosphate rock reserves and resources: a critique. Earth Syst Dynam 5(2):491

    Article  Google Scholar 

  • Egle K, Römer W, Keller H (2003) Exudation of low molecular weight organic acids by Lupinus albus L., Lupinus angustifolius L. and Lupinus luteus L. as affected by phosphorus supply. Agronomie 23(5–6):511–518

    Article  CAS  Google Scholar 

  • El-Sherif NA, Mohamed AA, Saad M, Barakat H, Aly S (2016) Genetic variation in Egyptian white lupin (Lupinus albus L.) genotypes based on combined data of ISSR and fluorescence-based AFLP markers. Egypt J Genet Cytol 43(1):1–23

    Google Scholar 

  • Felderer B, Vontobel P, Schulin R (2015) Cluster root allocation of white lupin (Lupinus albus L.) in soil with heterogeneous phosphorus and water distribution. Soil Sci Plant Nutr 61(6):940–950

    Article  CAS  Google Scholar 

  • Florez-Sarasa I, Lambers H, Wang X, Finnegan PM, Ribas-Carbo M (2014) The alternative respiratory pathway mediates carboxylate synthesis in white lupin cluster roots under phosphorus deprivation. Plant Cell Environ 37(4):922–928. doi:10.1111/pce.12208

    Article  CAS  PubMed  Google Scholar 

  • Funayama-Noguchi S, Noguchi K, Terashima I (2015) Comparison of the response to phosphorus deficiency in two lupin species, Lupinus albus and L. angustifolius, with contrasting root morphology. Plant Cell Environ 38(3):399–410

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT, Tester M (2011) Phenomics–technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16(12):635–644

    Article  CAS  PubMed  Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48(8):1081–1091

    Article  CAS  PubMed  Google Scholar 

  • Gardner W, Boundy K (1983) The acquisition of phosphorus by Lupinus albus L. IV. The effect of interplanting wheat and white lupin on the growth and mineral composition of the two species. Plant Soil 70:391–402

    Article  CAS  Google Scholar 

  • Gardner W, Parbery D, Barber D (1982) The acquisition of phosphorus by Lupinus albus LI some characteristics of the soil/root interface. Plant Soil:19–32

    Google Scholar 

  • Gaxiola RA, Edwards M, Elser JJ (2011) A transgenic approach to enhance phosphorus use efficiency in crops as part of a comprehensive strategy for sustainable agriculture. Chemosphere 84 (6):840–845. doi:S0045-6535(11)00102-0 [pii]10.1016/j.chemosphere.2011.01.062

  • Gerke J, Römer W, Jungk A (1994) The excretion of citric and malic acid by proteoid roots of Lupinus albus L.; effects on soil solution concentrations of phosphate, iron, and aluminum in the proteoid rhizosphere in samples of an oxisol and a luvisol. Z Pflanzenernähr Bodenkd 157(4):289–294

    Article  CAS  Google Scholar 

  • Gilbert G, Knight J, Vance C, Allan DJP (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ 22(7):801–810

    Article  CAS  Google Scholar 

  • Gilbert GA, Knight JD, Vance CP, Allan DL (2000) Proteoid root development of phosphorus deficient lupin is mimicked by auxin and phosphonate. Ann Bot 85(6):921–928

    Article  CAS  Google Scholar 

  • Gladstones J (1994) A historical review of lupins in Australia. In: Dracup M, Palta J (eds) Proceedings of the 1st Australian Lupin Technical Symposium. Perth, Western Australia, pp 1–34

    Google Scholar 

  • Gladstones JS, Atkins C, Hamblin J (1998) Lupins as crop plants: biology, production and utilization. CAB international, Cambridge, UK

    Google Scholar 

  • Gomez DA, Carpena RO (2014) Effect of 1-naphthaleneacetic acid on organic acid exudation by the roots of white lupin plants grown under phosphorus-deficient conditions. J Plant Physiol 171(15):1354–1361. doi:10.1016/j.jplph.2014.05.008

    Article  CAS  PubMed  Google Scholar 

  • Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. Plant Cell 22(3):623–639

    Article  CAS  PubMed  Google Scholar 

  • Gregory PJ, Bengough AG, Grinev D, Schmidt S, Thomas WBT, Wojciechowski T, Young IM (2009) Root phenomics of crops: opportunities and challenges. Funct Plant Biol 36(11):922–929

    Article  Google Scholar 

  • Gustafsson A, Gadd I (1965) Mutations and crop improvement. II. The genus Lupinus (Leguminosae). Hereditas 53(1–2):15–39

    Google Scholar 

  • Hagström J, James W, Skene KJP (2001) A comparison of structure, development and function in cluster roots of Lupinus albus L. under phosphate and iron stress. Plant Soil 232(1):81–90

    Article  Google Scholar 

  • Hane JK, Ming Y, Kamphuis LG, Nelson MN, Garg G, Atkins CA, Bayer PE, Bravo A, Bringans S, Cannon S (2016) A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: insights into plant–microbe interactions and legume evolution. Plant Biotechnol J 1–13

    Google Scholar 

  • Hermans C, Hammond J, White P, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11(12):610–617

    Article  CAS  PubMed  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237(2):173–195

    Article  CAS  Google Scholar 

  • Hocking P, Jeffery S (2004) Cluster-root production and organic anion exudation in a group of old-world lupins and a new-world lupin. Plant Soil 258(1):135–150

    Article  CAS  Google Scholar 

  • Hogh-Jensen H, Schjoerring J, Soussana JF (2002) The influence of phosphorus deficiency on growth and nitrogen fixation of white clover plants. Ann Bot 90(6):745–753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X-Y, Salt DE (2016) Plant ionomics: from elemental profiling to environmental adaptation. Mol Plant 9(6):787–797

    Article  CAS  PubMed  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci 103(27):10334–10339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson J, Allan D, Vance C (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol 104(2):657–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson JF, Allan DL, Vance CP, Weiblen G (1996) Root carbon dioxide fixation by phosphorus-deficient Lupinus albus (contribution to organic acid exudation by proteoid roots). Plant Physiol 112(1):19–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jost R, Pharmawati M, Lapis-Gaza HR, Rossig C, Berkowitz O, Lambers H, Finnegan PM (2015) Differentiating phosphate-dependent and phosphate-independent systemic phosphate-starvation response networks in Arabidopsis thaliana through the application of phosphite. J Exp Bot 66(9):2501–2514. doi:10.1093/jxb/erv025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung JKHM, McCouch SRM (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keerthisinghe G, Hocking P, Ryan P, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.) Plant Cell Environ 21(5):467–478

    Article  CAS  Google Scholar 

  • Kim J-M, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114

    PubMed  PubMed Central  Google Scholar 

  • Kuo HF, Chiou TJ (2011) The role of MicroRNAs in phosphorus deficiency signaling. Plant Physiol 156(3):1016–1024. doi:pp.111.175265 [pii]10.1104/pp.111.175265

  • Lambers H, Atkin OK, Scheurwater I (1996) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 2nd edn. Marcel Dekker, New York

    Google Scholar 

  • Lambers H, Cramer MD, Shane MW, Wouterlood M, Poot P, Veneklaas EJ (2003) Structure and functioning of cluster roots and plant responses to phosphate deficiency, introduction. Plant Soil 248(1–2):ix–xix

    Article  CAS  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(4):693–713. doi:10.1093/aob/mcl114

    Article  PubMed  PubMed Central  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23(2):95–103. doi:S0169–5347(07)00357–6 [pii]10.1016/j.tree.2007.10.008

  • Lambers H, Bishop JG, Hopper SD, Laliberte E, Zuniga-Feest A (2012) Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems. Ann Bot 110(2):329–348. doi:10.1093/aob/mcs130

    Article  CAS  PubMed  PubMed Central  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(2):263–288. doi:10.3732/ajb.1200474

    Article  CAS  PubMed  Google Scholar 

  • Le Roux M, Khan S, Valentine A (2009) Nitrogen and carbon costs of soybean and lupin root systems during phosphate starvation. Symbiosis 48(1–3):102–109

    Article  Google Scholar 

  • Li J, Dai X, Liu T, Zhao PX (2012) LegumeIP: an integrative database for comparative genomics and transcriptomics of model legumes. Nucleic Acids Res 40(D1):D1221–D1229

    Article  CAS  PubMed  Google Scholar 

  • Liang G, Ai Q, Yu D (2015) Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Scientific reports 5

    Google Scholar 

  • Lin S, Chiou T (2008) Long-distance movement and differential targeting of microRNA399s. Plant Signal Behav 3(9):730–732

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin R, Renshaw D, Luckett D, Clements J, Yan G, Adhikari K, Buirchell B, Sweetingham M, Yang H (2009) Development of a sequence-specific PCR marker linked to the gene “pauper” conferring low-alkaloids in white lupin (Lupinus albus L.) for marker assisted selection. Mol Breed 23(1):153–161

    Article  CAS  Google Scholar 

  • Lin XY, Ye YQ, Fan SK, Jin CW, Zheng SJ (2016) Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant Physiol 170(2):907–920

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Vance CP (2010) Crucial roles of sucrose and microRNA399 in systemic signaling of P deficiency: a tale of two team players? Plant Signal Behav 5(12):1556–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Uhde-Stone C, Li A, Vance C, DJPaS A (2001) A phosphate transporter with enhanced expression in proteoid roots of white lupin (Lupinus albus L.) Plant Soil 237(2):257–266

    Article  CAS  Google Scholar 

  • Liu J, Samac D, Bucciarelli B, Allan D, Vance C (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41(2):257–268

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Hu R, Palla KJ, Tuskan GA, Yang X (2016) Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research. Curr Opin Plant Biol 30:70–77

    Article  CAS  PubMed  Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156(3):1041–1049. doi:pp.111.175414 [pii] 1104/pp.111.175414

    Google Scholar 

  • Lynch JP, Beebe SE (1995) Adaptation of beans (Phaseolus vulgaris L.) to low phosphorus availability. HortScience 30(6):1165

    CAS  Google Scholar 

  • Lynch JP, Brown KM (2001) Topsoil foraging–an architectural adaptation of plants to low phosphorus availability. Plant Soil 237(2):225–237

    Article  CAS  Google Scholar 

  • Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269(1–2):45–56

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press Inc, San Diego

    Google Scholar 

  • Massonneau A, Langlade N, Léon S, Smutny J, Vogt E, Neumann G, Martinoia E (2001) Metabolic changes associated with cluster root development in white lupin (Lupinus albus L.): relationship between organic acid excretion, sucrose metabolism and energy status. Planta 213(4):534–542

    Article  CAS  PubMed  Google Scholar 

  • Maxwell C, Vance C, Heichel G, Stade S (1984) CO2 fixation in alfalfa and birdsfoot trefoil root nodules and partitioning of 14C to the plant. Crop Sci 24(2):257–264

    Article  CAS  Google Scholar 

  • Meng ZB, Chen LQ, Suo D, Li GX, Tang CX, Zheng SJ (2012) Nitric oxide is the shared signalling molecule in phosphorus-and iron-deficiency-induced formation of cluster roots in white lupin (Lupinus albus). Ann Bot 109(6):1055–1064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng ZB, You XD, Suo D, Chen YL, Tang C, Yang JL, Zheng SJ (2013) Root-derived auxin contributes to the phosphorus-deficiency-induced cluster-root formation in white lupin (Lupinus albus). Physiol Plant 148(4):481–489

    Article  CAS  PubMed  Google Scholar 

  • Muller J, Godde V, Niehaus K, Zorb C (2015) Metabolic adaptations of white lupin roots and shoots under phosphorus deficiency. Front Plant Sci 6:1014. 10.3389/fpls.2015.01014

  • Naganowska B, Wolko B, Śliwińska E, Kaczmarek Z, Schifino-Wittmann M (2005) 2C DNA variation and relationships among new world species of the genus Lupinus (Fabaceae). Plant Syst Evol 256(1–4):147–157

    Article  CAS  Google Scholar 

  • Nagarajan VK, Smith AP (2012) Ethylene’s role in phosphate starvation signaling: more than just a root growth regulator. Plant Cell Physiol 53(2):277–286

    Article  CAS  PubMed  Google Scholar 

  • Neumann G, Martinoia EJTPS (2002) Cluster roots–an underground adaptation for survival in extreme environments. Trends Plant Sci 7(4):162–167

    Article  CAS  PubMed  Google Scholar 

  • Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211(1):121–130

    Article  CAS  Google Scholar 

  • Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208(3):373–382

    Article  CAS  Google Scholar 

  • Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Römheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.) Ann Bot 85(6):909–919

    Article  CAS  Google Scholar 

  • O’Rourke JA, Yang SS, Miller SS, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu ZJ, Allan D, Gronwald JW, Vance CP (2013) An RNA-seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161(2):705–724. doi:10.1104/pp.112.209254

    Article  PubMed  CAS  Google Scholar 

  • O’Rourke JA, Bolon Y-T, Bucciarelli B, Vance CP (2014) Legume genomics: understanding biology through DNA and RNA sequencing. Ann Bot 113(7):1107–1120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53(5):731–738. doi:10.1111/j.1365-313X.2007.03363.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pant BD, Pant P, Erban A, Huhman D, Kopka J, Scheible WR (2015) Identification of primary and secondary metabolites with phosphorus status-dependent abundance in Arabidopsis, and of the transcription factor PHR1 as a major regulator of metabolic changes during phosphorus limitation. Plant Cell Environ 38(1):172–187. doi:10.1111/pce.12378

    Article  CAS  PubMed  Google Scholar 

  • Paul S, Datta SK, Datta K (2015) miRNA regulation of nutrient homeostasis in plants. Front Plant Sci 6:232

    Article  PubMed  PubMed Central  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MD, Lambers H (2006a) Triticum aestivum Shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere. New Phytol 169(3):515–524. doi:10.1111/j.1469-8137.2005.01614.x

    Article  CAS  PubMed  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MD, Lambers H (2006b) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant Soil 288(1–2):127–139

    Article  CAS  Google Scholar 

  • Penaloza E, Gutierrez A, Martinez J, Munoz G, Bravo LA, Corcuera LJ (2002) Differential gene expression in proteoid root clusters of white lupin (Lupinus albus). Physiol Plant 116(1):28–36

    Article  CAS  PubMed  Google Scholar 

  • Phan HT, Ellwood SR, Adhikari K, Nelson MN, Oliver RP (2007) The first genetic and comparative map of white lupin (Lupinus albus L.): identification of QTLs for anthracnose resistance and flowering time, and a locus for alkaloid content. DNA Res 14(2):59–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214. doi:10.1146/annurev.arplant.47.1.185

    Article  CAS  PubMed  Google Scholar 

  • Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25(2):159–198

    Article  CAS  Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156(3):1006–1015. doi:pp.111.175281 [pii]10.1104/pp.111.175281

  • Puchta H (2016) Using CRISPR/Cas in three dimensions: towards synthetic plant genomes, transcriptomes and epigenomes. Plant J 87:5–15

    Article  CAS  PubMed  Google Scholar 

  • Raghothama K (1999) Phosphate acqisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693. doi:10.1146/annurev.arplant.50.1.665

    Article  CAS  PubMed  Google Scholar 

  • Raghothama K, Karthikeyan A (2005) Phosphate acquisition. In: Root physiology: from gene to function. Springer Netherlands, Dordrecht, pp 37–49

    Google Scholar 

  • Rai V, Sanagala R, Sinilal B, Yadav S, Sarkar AK, Dantu PK, Jain A (2015) Iron availability affects phosphate deficiency-mediated responses, and evidences of cross talk with auxin and zinc in arabidopsis. Plant Cell Physiol 56:1107–1123

    Article  CAS  PubMed  Google Scholar 

  • Rath M, Salas J, Parhy B, Norton R, Menakuru H, Sommerhalter M, Hatlstad G, Kwon J, Allan D, Vance C, Uhde-Stone C (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(1):137–150

    Article  CAS  Google Scholar 

  • Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29(1):115–125

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Medina C, Atkins CA, Mann AJ, Jordan ME, Smith PM (2011) Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.). BMC Plant Biol 11:36. doi:1471–2229–11-36 [pii]10.1186/1471-2229-11-36

  • Rogers E, Wu X, Stacey G, Nguyen H (2009) Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol 166(13):1453–1459

    Article  CAS  PubMed  Google Scholar 

  • Rosemarin A, Schröder J, Dagerskog L, Cordell D, Smit A Future supply of phosphorus in agriculture and the need to maximise efficiency of use and reuse. In: International Fertiliser Society at a Conference in Cambridge, on 10th December 2010, 2011. International Fertiliser Society

    Google Scholar 

  • Rosendahl L, Vance CP, Pedersen WB (1990) Products of dark CO2 fixation in pea root nodules support bacteroid metabolism. Plant Physiol 93(1):12–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Runge-Metzger A (1995) Closing the cycle: obstacles to efficient P management for improved global food security, vol 54. Scope-Scientific Committee on Problems of the Environment International Council of Scientific Unions, Indianapolis, pp 27–42

    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(4):435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37(5):645–653

    Article  CAS  PubMed  Google Scholar 

  • Sbabou L, Brhada F, Alami IT, Maltouf AF (2010a) Genetic diversity of Moroccan Lupinus germplasm investigated using ISSR and AFLP markers. Int J Agric Biol 12:26–32

    CAS  Google Scholar 

  • Sbabou L, Bucciarelli B, Miller S, Liu J, Berhada F, Filali-Maltouf A, Allan D, Vance C (2010b) Molecular analysis of SCARECROW genes expressed in white lupin cluster roots. J Exp Bot 61(5):1351–1363. doi:erp400 [pii]10.1093/jxb/erp400

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116(2):447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiml S, Puchta H (2016) Revolutionizing plant biology: multiple ways of genome engineering by CRISPR/Cas. Plant Methods 12(1):1

    Article  CAS  Google Scholar 

  • Scholz RW, Wellmer F-W (2015) Comment on: “Recent revisions of phosphate rock reserves and resources: a critique” by Edixhoven et al. (2014) – Phosphate reserves and resources: what conceptions and data do stakeholders need for sustainable action? Earth Syst Dynam Discuss 6:49

    Article  Google Scholar 

  • Schulze J, Tesfaye M, Litjens R, Bucciarelli B, Trepp G, Miller S, Samac D, Allan D, Vance C (2002) Malate plays a central role in plant nutrition. In: Progress in plant nutrition: plenary lectures of the XIV international plant nutrition colloquium. Springer Netherlands, Dordrecht, pp 133–139

    Google Scholar 

  • Schulze J, Temple G, Temple S, Beschow H, Vance C (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98(4):731–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Secco D, Wang C, Arpat BA, Wang Z, Poirier Y, Tyerman SD, Wu P, Shou H, Whelan J (2012) The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol 193(4):842–851

    Article  CAS  PubMed  Google Scholar 

  • Secco D, Shou H, Whelan J, Berkowitz O (2014) RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin. BMC Genomics 15:230. doi:10.1186/1471-2164-15-230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sengbusch R (1942) Süsslupinen und Öllupinen. Die Emntstehungsgeschichte einiger neuen Kulturpflanzen. Landw Jb 91:723–880

    Google Scholar 

  • Shane M, De Vos M, De Roock S, Lambers H (2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26(2):265–273

    Article  CAS  Google Scholar 

  • Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant Soil 248(1–2):199–206

    Article  CAS  Google Scholar 

  • Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Sci 168(3):837–845

    Article  CAS  Google Scholar 

  • Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156(3):997–1005. doi:pp.111.175232 [pii]10.1104/pp.111.175232

  • Shi L, Shi T, Broadley MR, White PJ, Long Y, Meng J, Xu F, Hammond JP (2013) High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities. Ann Bot 112(2):381–389

    Article  CAS  PubMed  Google Scholar 

  • Shu L, Shen J, Rengel Z, Tang C, Zhang F (2007) Cluster root formation by Lupinus albus is modified by stratified application of phosphorus in a split-root system. J Plant Nutr 30(2):271–288

    Article  CAS  Google Scholar 

  • Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86(6):1060–1064

    Article  Google Scholar 

  • Skene KR (2000) Pattern formation in cluster roots: some developmental and evolutionary considerations. Ann Bot 85(6):901–908

    Article  Google Scholar 

  • Tadele Y (2015) White lupin (Lupinus albus) grain, a potential source of protein for ruminants: a review. Res J Agric Env Manage 4(4):180–188

    Google Scholar 

  • Tang H, Li X, Zu C, Zhang F, Shen J (2013) Spatial distribution and expression of intracellular and extracellular acid phosphatases of cluster roots at different developmental stages in white lupin. J Plant Physiol 170(14):1243–1250

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Zheng X, Qi Y, Zhang D, Cheng Y, Tang A, Voytas DF, Zhang Y (2016) A single transcript CRISPR-Cas9 system for efficient genome editing in plants. Mol plant 9:1088–1091

    Google Scholar 

  • Tesfaye M, Liu J, Allan DL, Vance CP (2007) Genomic and genetic control of phosphate stress in legumes. Plant Physiol 144(2):594–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theodorou ME, Cornel FA, Duff SM, Plaxton WC (1992) Phosphate starvation-inducible synthesis of the alpha-subunit of the pyrophosphate-dependent phosphofructokinase in black mustard suspension cells. J Biol Chem 267(30):21901–21905

    CAS  PubMed  Google Scholar 

  • Thuynsma R, Valentine A, Kleinert A (2014) Short-term supply of elevated phosphate alters the belowground carbon allocation costs and functions of lupin cluster roots and nodules. J Plant Physiol 171(8):648–654

    Article  CAS  PubMed  Google Scholar 

  • Tian L, Peel G, Lei Z, Aziz N, Dai X, He J, Watson B, Zhao P, Sumner L, Dixon R (2009) Transcript and proteomic analysis of developing white lupin (Lupinus albus L.) roots. BMC Plant Biol 9:1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ticconi C, Lucero R, Sakhonwasee S, Adamson A, Creff A, Nussaume L, Desnos T, Abel S (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci U S A 106(33):14174–14179. doi:0901778106[pii]10.1073/pnas.0901778106

  • Tiessen H (2008) Phosphorus in the global environment. In: The ecophysiology of plant-phosphorus interactions. Springer, Dordrecht, pp 1–7

    Chapter  Google Scholar 

  • 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(7):1971–1974

    Article  CAS  Google Scholar 

  • Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32(5):465–475

    Article  CAS  PubMed  Google Scholar 

  • Uauy R, Gattas V, Yanez E (1995) Sweet lupins in human nutrition. In: Plants in human nutrition. Karger Publishers, Basel, Switzerland, pp 75–88

    Google Scholar 

  • Uhde-Stone C, Zinn KE, Ramirez-Yanez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131(3):1064–1079. doi:10.1104/pp.102.016881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uhde-Stone C, Liu J, Zinn KE, Allan DL, Vance CP (2005) Transgenic proteoid roots of white lupin: a vehicle for characterizing and silencing root genes involved in adaptation to P stress. Plant J 44(5):840–853. doi:10.1111/j.1365-313X.2005.02573.x

    Article  CAS  PubMed  Google Scholar 

  • Ulrich AE, Frossard E (2014) On the history of a reoccurring concept: phosphorus scarcity. Sci Total Environ 490:694–707

    Article  CAS  PubMed  Google Scholar 

  • Van der Werf A, Welschen R, Lambers H (1992) Respiratory losses increase with decreasing inherent growth rate of a species and with decreasing nitrate supply: a search for explanations for these observations. In: Lambers H, Van der Plas L, Kafkaki U, Munns R (eds) Molecular, biochemical and physiological aspects of plant respiration, SPB Academic Publishing, The Hague, pp 421–432

    Google Scholar 

  • Vance CP (2010) Quantitative trait loci, epigenetics, sugars, and microRNAs: quaternaries in phosphate acquisition and use. Plant Physiol 154(2):582–588. doi:154/2/582 [pii]10.1104/pp.110.161067

  • Vance CP, Chiou TJ (2011) Phosphorus focus editorial. Plant Physiol 156(3):987–988. doi:156/3/987 [pii]10.1104/pp.111.900415

  • Vance CP, Stade S, Maxwell CA (1983) Alfalfa root nodule carbon dioxide fixation : I. Association with nitrogen fixation and incorporation into amino acids. Plant Physiol 72(2):469–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Vázquez S, Agha R, Granado A, Sarro M, Esteban E, Peñalosa J, Carpena R (2006) Use of white lupin plant for phytostabilization of Cd and as polluted acid soil. Water Air Soil Pollut 177(1–4):349–365

    Article  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Tang X, Cheng L, Zhang A, Zhang W, Zhang F, Liu J, Cao Y, Allan D, Vance C (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187(4):1112–1123

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Straub D, Yang H, Kania A, Shen J, Ludewig U, Neumann G (2014) The regulatory network of cluster-root function and development in phosphate-deficient white lupin (Lupinus albus) identified by transcriptome sequencing. Physiol Plant 151(3):323–338

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Veneklaas EJ, Pearse SJ, Lambers H (2015a) Interactions among cluster-root investment, leaf phosphorus concentration, and relative growth rate in two Lupinus species. Am J Bot 102(9):1529–1537

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Rahman AB, Wang G, Ludewig U, Shen J, Neumann G (2015b) Hormonal interactions during cluster-root development in phosphate-deficient white lupin (Lupinus albus L.) J Plant Physiol 177:74–82. doi:10.1016/j.jplph.2014.10.022

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Shen J, Ludewig U, Neumann G (2015c) A re-assessment of sucrose signaling involved in cluster-root formation and function in phosphate-deficient white lupin (Lupinus albus). Physiol Plant 154(3):407–419

    Article  CAS  PubMed  Google Scholar 

  • Ward J, Lahner B, Yakubova E, Salt D, Raghothama K (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147(3):1181–1191

    Article  CAS  PubMed  PubMed Central  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(1–2):129–136

    Article  CAS  Google Scholar 

  • Wasaki J, Rothe A, Kania A, Neumann G, Romheld V, Shinano T, Osaki M, Kandeler E (2005) Root exudation, phosphorus acquisition, and microbial diversity in the rhizosphere of white lupine as affected by phosphorus supply and atmospheric carbon dioxide concentration. J Environ Qual 34(6):2157–2166. doi:10.2134/jeq2004.0423

    Article  CAS  PubMed  Google Scholar 

  • Watt M, Evans JR (1999) Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120(3):705–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watt M, Evans JR (2003) Phosphorus acquisition from soil by white lupin (Lupinus albus L.) and soybean (Glycine max L.), species with contrasting root development. Plant Soil 248(1–2):271–283

    Article  CAS  Google Scholar 

  • Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006a) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29(5):919–927

    Article  CAS  PubMed  Google Scholar 

  • Weisskopf L, Tomasi N, Santelia D, Martinoia E, Langlade NB, Tabacchi R, Abou-Mansour E (2006b) Isoflavonoid exudation from white lupin roots is influenced by phosphate supply, root type and cluster-root stage. New Phytol 171(3):657–668

    CAS  PubMed  Google Scholar 

  • Wiche O, Székely B, Moschner C, Heilmeier H (2015) Intercropping with white lupin (Lupinus albus L.); a promising tool for phytoremediation and phytomining research. In: EGU General Assembly Conference Abstracts, p 4588

    Google Scholar 

  • Wiche O, Székely B, Kummer N-A, Moschner C, Heilmeier H (2016) Effects of intercropping of oat (Avena sativa L.) with white lupin (Lupinus albus L.) on the mobility of target elements for phytoremediation and phytomining in soil solution. Int J Phytoremediation 18(9):900–907

    Article  CAS  PubMed  Google Scholar 

  • Yamagishi M, Masuta C, Suzuki M, Netsu O (2015) Peanut stunt virus-induced gene silencing in white lupin (Lupinus albus). Plant Biotechnol 32:181–191

    Google Scholar 

  • Yang H, Lin R, Renshaw D, Li C, Adhikari K, Thomas G, Buirchell B, Sweetingham M, Yan G (2010) Development of sequence-specific PCR markers associated with a polygenic controlled trait for marker-assisted selection using a modified selective genotyping strategy: a case study on anthracnose disease resistance in white lupin (Lupinus albus L.) Mol Breed 25(2):239–249

    Article  CAS  Google Scholar 

  • Yang H, Tao Y, Zheng Z, Zhang Q, Zhou G, Sweetingham MW, Howieson JG, Li C (2013) Draft genome sequence, and a sequence-defined genetic linkage map of the legume crop species Lupinus angustifolius L. PLoS One 8(5):e64799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W-H, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol 136(3):3771–3783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Dixon RA (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15(2):72–80

    Article  CAS  PubMed  Google Scholar 

  • Zhou K, Yamagishi M, Osaki M, Masuda K (2008) Sugar signalling mediates cluster root formation and phosphorus starvation-induced gene expression in white lupin. J Exp Bot 59(10):2749–2756. doi:ern130 [pii]10.1093/jxb/ern130

  • Zhou Z, Wang Z, Lv Q, Shi J, Zhong Y, Wu P, Mao C (2015) SPX proteins regulate Pi homeostasis and signaling in different subcellular level. Plant Signal Behav 10(9):e1061163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu H, Choi H-K, Cook DR, Shoemaker RC (2005a) Bridging model and crop legumes through comparative genomics. Plant Physiol 137(4):1189–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Yan F, Zorb C, Schubert S (2005b) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46(6):892–901. doi:10.1093/pcp/pci094

    Article  CAS  PubMed  Google Scholar 

  • Zhu YY, Zeng HQ, Dong CX, Yin XM, Shen QR, Yang ZM (2010) microRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.) Plant Sci 178(1):23–29

    Article  CAS  Google Scholar 

Download references

Acknowledgment

I gratefully acknowledge the review of this manuscript by Saad Sulieman. I also wish to thank my colleague Chris Baysdorfer for critically reading this manuscript and for many inspiring conversations.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, California State University, East Bay, Hayward, CA, 94542, USA

    Claudia Uhde-Stone

Authors
  1. Claudia Uhde-Stone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudia Uhde-Stone .

Editor information

Editors and Affiliations

  1. Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North, Sudan

    Saad Sulieman

  2. Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science (CSRS), Tsurumi, Yokohama, Japan

    Lam-Son Phan Tran

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Uhde-Stone, C. (2017). White Lupin: A Model System for Understanding Plant Adaptation to Low Phosphorus Availability. In: Sulieman, S., Tran, LS. (eds) Legume Nitrogen Fixation in Soils with Low Phosphorus Availability. Springer, Cham. https://doi.org/10.1007/978-3-319-55729-8_13

Download citation

Publish with us

Policies and ethics

Search

Navigation