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Rhizoeconomics: Carbon costs of phosphorus acquisition

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Abstract

Plants display a wide array of physiological adaptations to low soil phosphorus availability. Here we discuss metabolic and ecological costs associated with these strategies, focusing on the carbon costs of root traits related to phosphorus acquisition in crop plants. We propose that such costs are an important component of adaptation to low phosphorus soils. In common bean, genotypes with superior low phosphorus adaptation express traits that reduce the respiratory burden of root growth, including greater allocation to metabolically inexpensive root classes, such as adventitious roots, and greater formation of cortical aerenchyma, which reduces specific root respiration. Root hair formation increases phosphorus acquisition at minimal carbon cost, but may have other unknown ecological costs. Mycorrhizas and root exudates enhance phosphorus acquisition in some taxa, but at significant carbon cost. Root architectural patterns that enhance topsoil foraging enhance phosphorus acquisition but appear to incur tradeoffs for water acquisition and spatial competition. A better understanding of the metabolic and ecological costs associated with phosphorus acquisition strategies is needed for an intelligent deployment of such traits in crop improvement programs.

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References

  • J S Amthor (2000) ArticleTitleThe McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later Ann. Bot. 86 1–20 Occurrence Handle10.1006/anbo.2000.1175 Occurrence Handle1:CAS:528:DC%2BD3cXktlSntL8%3D

    Article  CAS  Google Scholar 

  • G Anderson (1980) Assessing organic phosphorus in soils F E Khasawneh E C Sample E J Kamprath (Eds) The Role of Phosphorus in Agriculture ASA, CSSA, SSSA Madison, USA 411–431

    Google Scholar 

  • T Bates J Lynch (2000a) ArticleTitlePlant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae) Amer. J. Bot. 87 958–963 Occurrence Handle1:CAS:528:DC%2BD3cXlvVemsb0%3D

    CAS  Google Scholar 

  • T R Bates J P Lynch (2000b) ArticleTitleThe efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition Amer. J. Bot. 87 964–970 Occurrence Handle1:CAS:528:DC%2BD3cXlvVemsbs%3D

    CAS  Google Scholar 

  • T R Bates J P Lynch (2001) ArticleTitleRoot hairs confer a competitive advantage under low phosphorus availability Plant Soil 236 243–250 Occurrence Handle10.1023/A:1012791706800 Occurrence Handle1:CAS:528:DC%2BD3MXptlKhu7w%3D

    Article  CAS  Google Scholar 

  • T R Bates J P Lynch (1996) ArticleTitleStimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability Plant Cell Environ. 19 529–538 Occurrence Handle1:CAS:528:DyaK28XktlGgt78%3D

    CAS  Google Scholar 

  • A J Bloom F S I Chapin H A Mooney (1985) ArticleTitleResource limitation in plants – An economic analogy Ann. Rev. Ecol. Syst. 16 33–392

    Google Scholar 

  • A M Bonser J Lynch S Snapp (1996) ArticleTitleEffect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris New Phytol. 132 281–288 Occurrence Handle1:STN:280:DC%2BD3MnlvFOjtg%3D%3D Occurrence Handle11541132

    CAS  PubMed  Google Scholar 

  • B Casper H J Schenk R Jackson (2003) ArticleTitleDefining a plant’s belowground zone of influence Ecology 84 2313–2321

    Google Scholar 

  • F S Chapin A J Bloom C B Field R H Waring (1987) ArticleTitlePlant responses to multiple environmental factors Biosci. 37 49–57

    Google Scholar 

  • W K Chu S C Chang (1966) ArticleTitleSurface activity of inorganic soil phosphorus Soil Sci. 101 459–464 Occurrence Handle1:CAS:528:DyaF28Xks1Sgurk%3D

    CAS  Google Scholar 

  • CIAT 1999 Bean Project: Annual Report. CIAT (Centro Internacional de Agricultura Tropical), Cali, Columbia

  • I Ciereszko A Gniazdowska M Mikulska A M Rychter (1996) ArticleTitleAssimilate translocation in bean plants (Phaseolus vulgaris L.) during phosphate deficiency J. Plant Physiol. 149 343–348 Occurrence Handle1:CAS:528:DyaK28XmtFGqur4%3D

    CAS  Google Scholar 

  • T J DeWitt A Sih D S Wilson (1998) ArticleTitleCosts and limits of phenotypic plasticity Trends Ecol. Evol. 13 77–81 Occurrence Handle10.1016/S0169-5347(97)01274-3

    Article  Google Scholar 

  • H G Diem E Duhoux H Zaid M Arahou (2000) ArticleTitleCluster roots in Casuarinaceae: role and relationship to soil nutrient factors Ann. Bot. 85 929–936 Occurrence Handle10.1006/anbo.2000.1127 Occurrence Handle1:CAS:528:DC%2BD3cXjs12hu7w%3D

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • B Dinkelaker V Romheld H Marschner (1989) ArticleTitleCitric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.) Plant Cell Environ. 12 285–292 Occurrence Handle1:CAS:528:DyaL1MXmtFertrY%3D

    CAS  Google Scholar 

  • D D Douds C R Johnson K E Koch (1988) ArticleTitleCarbon cost of the fungal symbiont relative to net leaf-P accumulation in a split-root VA mycorrhizal symbiosis Plant Physiol. 86 491–496 Occurrence Handle1:CAS:528:DyaL1cXhs1Crsbk%3D

    CAS  Google Scholar 

  • M C Drew C He P W Morgan (2000) ArticleTitleProgrammed cell death and aerenchyma formation in roots Trends Plant Sci. 5 123–127 Occurrence Handle10.1016/S1360-1385(00)01570-3 Occurrence Handle1:STN:280:DC%2BD3MvnslKntw%3D%3D Occurrence Handle10707078

    Article  CAS  PubMed  Google Scholar 

  • M C Drew C J He P W Morgan (1989) ArticleTitleDecreased ethylene biosynthesis, and induction of Aerenchyma, by nitrogen-starvation or phosphate-starvation in adventitious roots of Zea-mays L Plant Physiol. 91 266–271 Occurrence Handle1:CAS:528:DyaL1MXmtFert7o%3D

    CAS  Google Scholar 

  • D Eissenstat (1992) ArticleTitleCosts and benefits of constructing roots of small diameter J. Plant Nutr. 15 763–782

    Google Scholar 

  • D M Eissenstat J H Graham J P Syvertsen D L Drouillard (1993) ArticleTitleCarbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status Ann. Bot. 71 1–10 Occurrence Handle10.1006/anbo.1993.1001 Occurrence Handle1:CAS:528:DyaK3sXhs1ygsrs%3D

    Article  CAS  Google Scholar 

  • G C Elliott J Lynch A Läuchli (1984) ArticleTitleInflux and efflux of P in roots of intact maize plants. Double-labeling with 32P and 33P Plant Physiol. 76 336–341 Occurrence Handle1:CAS:528:DyaL2cXmt12gtr4%3D

    CAS  Google Scholar 

  • W O Enwezor A W Moore (1966) ArticleTitlePhosphorus status of some Nigerian soils Soil Sci. 102 322–328 Occurrence Handle1:CAS:528:DyaF2sXhvVegsA%3D%3D

    CAS  Google Scholar 

  • A Eshel K Nielsen J Lynch (1995) Response of bean root systems to low level of P Plant Roots – From Cells to Systems 14th Long Ashton International Symposium. IACR-Long Ashton Res. St. Bristol, England Bristol, England 63

    Google Scholar 

  • M S Fan J M Zhu C Richards K M Brown J P Lynch (2003) ArticleTitlePhysiological roles for aerenchyma in phosphorus-stressed roots Funct. Plant Biol. 30 493–506 Occurrence Handle10.1071/FP03046

    Article  Google Scholar 

  • M C T Fisher D M Eissenstat J P Lynch (2002) ArticleTitleLack of evidence for programmed root senescence in common bean (Phaseolus vulgaris L.) grown at different levels of phosphorus supply New Phytol. 153 63–71 Occurrence Handle10.1046/j.0028-646X.2001.00285.x

    Article  Google Scholar 

  • D Foehse N Claassen A Jungk (1991) ArticleTitlePhosphorus efficiency of plants II Significance of root radius, root hairs and cation-anion balance for phosphorus influx in seven plant species Plant Soil 132 261–272 Occurrence Handle1:CAS:528:DyaK3MXktVOmtbc%3D

    CAS  Google Scholar 

  • D Foehse A Jungk (1983) ArticleTitleInfluence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants Plant Soil 74 359–368 Occurrence Handle10.1007/BF02181353 Occurrence Handle1:CAS:528:DyaL2cXhtF2qt7g%3D

    Article  CAS  Google Scholar 

  • T S Gahoonia N E Nielsen O B Lyshede (1999) ArticleTitlePhosphorus (P) acquisition of cereal cultivars in the field at three levels of P fertilization Plant Soil 211 269–281 Occurrence Handle10.1023/A:1004742032367 Occurrence Handle1:CAS:528:DyaK1MXntlKisb8%3D

    Article  CAS  Google Scholar 

  • W Gardner D Barber D Parberry (1983) ArticleTitleThe 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 Occurrence Handle1:CAS:528:DyaL3sXhsF2ls7k%3D

    CAS  Google Scholar 

  • Z Y Ge G Rubio J P Lynch (2000) ArticleTitleThe importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: Results from a geometric simulation model Plant Soil 218 159–171 Occurrence Handle10.1023/A:1014987710937 Occurrence Handle1:CAS:528:DC%2BD3cXhvVGrtLc%3D Occurrence Handle11543364

    Article  CAS  PubMed  Google Scholar 

  • M Gersani J S Brown E O’Brien G G Maina Z Abramsky (2001) ArticleTitleTragedy of the commons as a result of root competition J. Ecol. 89 661–669 Occurrence Handle10.1046/j.0022-0477.2001.00609.x

    Article  Google Scholar 

  • S Gleeson D Tilman (1992) ArticleTitlePlant allocation and the multiple limitation hypothesis Amer. Nat. 139 1322–1343

    Google Scholar 

  • J P Grime J M L Mackey (2002) ArticleTitleThe role of plasticity in resource capture by plants Evol. Ecol. 16 299–307 Occurrence Handle10.1023/A:1019640813676

    Article  Google Scholar 

  • V Gutschick (1993) ArticleTitleNutrient-limited growth rates: Roles of nutrient-use efficiency and of adaptations to increase uptake rate J. Exp. Bot. 44 41–51

    Google Scholar 

  • C W Hansen J Lynch C O Ottosen (1998) ArticleTitleResponse to phosphorus availability during vegetative and reproductive growth of chrysanthemum: I. Whole-plant carbon dioxide exchange J. Amer. Soc. Hort. Sci. 123 215–222

    Google Scholar 

  • D Harris E Paul (1987) Carbon requirements of vesicular-arbuscular mycorrhizae G R Safir (Eds) Ecophysiology of VA Mycorrhizae CRC Press Boca Raton, FL 93–105

    Google Scholar 

  • P Hinsinger (2001) ArticleTitleBioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: A review Plant Soil 237 173–195 Occurrence Handle10.1023/A:1013351617532 Occurrence Handle1:CAS:528:DC%2BD38XovVWlsQ%3D%3D

    Article  CAS  Google Scholar 

  • P Hinsinger C Plassard C X Tang B Jaillard (2003) ArticleTitleOrigins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review Plant Soil 248 43–59 Occurrence Handle10.1023/A:1022371130939 Occurrence Handle1:CAS:528:DC%2BD3sXhtFCqsr8%3D

    Article  CAS  Google Scholar 

  • M D Ho B M McCannon J P Lynch (2004) ArticleTitleOptimization modeling of root architecture for water and phosphorus acquisition J. Theor. Biol. 226 331–340 Occurrence Handle10.1016/j.jtbi.2003.09.011 Occurrence Handle1:CAS:528:DC%2BD3sXpt1SjtL4%3D Occurrence Handle14643647

    Article  CAS  PubMed  Google Scholar 

  • Horton J L, Hart S C 1998 Hydraulic lift: A potentially important ecosystem process. Trends Ecol. Evol. 13

  • B Huang D M Eissenstat (2000) Root plasticity in exploiting water and nutrient heterogeneity R E Wilkinson (Eds) Plant-environment Interactions Marcel Dekker, Inc. Ney Work, NY

    Google Scholar 

  • M B Jackson W Armstrong (1999) ArticleTitleFormation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence Plant Biol. 1 274–287 Occurrence Handle1:CAS:528:DyaK1MXjsVKjsbk%3D

    CAS  Google Scholar 

  • R B Jackson M M Caldwell (1996) ArticleTitleIntegrating resource heterogeneity and plant plasticity: modelling nitrate and phosphate uptake in a patchy soil environment J. Ecol. 84 891–903

    Google Scholar 

  • I Jakobsen L Rosendahl (1990) ArticleTitleCarbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants New Phytol. 115 77–83

    Google Scholar 

  • J F Johnson D L Allan C P Vance G Weiblen (1996a) ArticleTitleRoot carbon dioxide fixation by phosphorus-deficient Lupinus albus: Contribution to organic acid exudation by proteoid roots Plant Physiol. 112 1930 Occurrence Handle10.1104/pp.112.1.31

    Article  Google Scholar 

  • J F Johnson C P Vance D L Allan (1996b) ArticleTitlePhosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase Plant Physiol. 112 31–41 Occurrence Handle10.1104/pp.112.1.31 Occurrence Handle1:CAS:528:DyaK28XlvFKhsL8%3D

    Article  CAS  Google Scholar 

  • D L Jones (1998) ArticleTitleOrganic acids in the rhizosphere – A critical review Plant Soil 205 25–44 Occurrence Handle10.1023/A:1004356007312 Occurrence Handle1:CAS:528:DyaK1MXhtlGjs78%3D

    Article  CAS  Google Scholar 

  • J K A Keter P A Ahn (1986) ArticleTitleProfile characteristics, and form and surface activity of inorganic phosphorus in a deep red Kenya coffee soil (Nitosol) J. Soil Sci. 37 89–97 Occurrence Handle1:CAS:528:DyaL28XhvVGnsr0%3D

    CAS  Google Scholar 

  • G J D Kirk E E Santos G R Findenegg (1999) ArticleTitlePhosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil Plant Soil 211 11–18 Occurrence Handle10.1023/A:1004539212083 Occurrence Handle1:CAS:528:DyaK1MXnt1Krtrk%3D

    Article  CAS  Google Scholar 

  • K E Koch C R Johnson (1984) ArticleTitlePhotosynthate partitioning in split root citrus seedlings with mycorrhizal and non-mycorrhizal root systems Plant Physiol. 75 26–30 Occurrence Handle1:CAS:528:DyaL2cXktlKhsr0%3D

    CAS  Google Scholar 

  • R Koide (1991) ArticleTitleNutrient supply, nutrient demand and plant response to mycorrhizal infection New Phytol. 117 365–386 Occurrence Handle1:CAS:528:DyaK3MXkt1yisbw%3D

    CAS  Google Scholar 

  • R Koide G Elliott (1989) ArticleTitleCost, Benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis Funct. Ecol. 3 252–255

    Google Scholar 

  • R T Koide M D Goff I A Dickie (2000) ArticleTitleComponent growth efficiencies of mycorrhizal and nonmycorrhizal plants New Phytol. 148 163–168

    Google Scholar 

  • H Konings G Verschuren (1980) ArticleTitleFormation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply Physiol. Plant. 49 265–279 Occurrence Handle1:CAS:528:DyaL3cXltFeisLo%3D

    CAS  Google Scholar 

  • H Lambers O Atkin F F Millenaar (2002) Respiratory patterns in roots in relation to their functioning Y Waisel A Eshel U Kafkaki (Eds) Plant Roots, the Hidden Half EditionNumber3 Marcel Dekker, Inc New York, NY 521–552

    Google Scholar 

  • H Liao G Rubio X L Yan A Q Cao K M Brown J P Lynch (2001) ArticleTitleEffect of phosphorus availability on basal root shallowness in common bean Plant Soil 232 69–79 Occurrence Handle10.1023/A:1010381919003 Occurrence Handle1:CAS:528:DC%2BD3MXlsVCks7s%3D Occurrence Handle11729851

    Article  CAS  PubMed  Google Scholar 

  • J Lopez-Bucio M F Nieto-Jacobo V Ramirez-Rodriguez L Herrera-Estrella (2000) ArticleTitleOrganic acid metabolism in plants: From adaptive physiology to transgenic varieties for cultivation in extreme soils Plant Sci. 160 1–13 Occurrence Handle1:CAS:528:DC%2BD3MXnsVeisA%3D%3D Occurrence Handle11164572

    CAS  PubMed  Google Scholar 

  • Y Lu R Wassmann H U Neue C Huang (1999) ArticleTitleImpact of phosphorus supply on root exudation, aerenchyma formation and methane emission of rice plants Biochemistry 47 203–218

    Google Scholar 

  • J Lynch (1998) The role of nutrient efficient crops in modern agriculture Z Rengel (Eds) Nutrient Use in Crop Production Food Products Press New York

    Google Scholar 

  • J Lynch (1995) ArticleTitleRoot architecture and plant productivity Plant Physiol. 109 7–13 Occurrence Handle1:CAS:528:DyaK2MXotFWmsr0%3D Occurrence Handle12228579

    CAS  PubMed  Google Scholar 

  • J Lynch J Deikman (1998) Phosphorus in Plant Biology: Regulatory Roles in Molecular, Cellular, Organismic, and Ecosystem Processes American Society of Plant Physiologists Rockville, MD

    Google Scholar 

  • J Lynch A Lauchli E Epstein (1991) ArticleTitleVegetative growth of the common bean in response to phosphorus nutrition Crop Sci. 31 380–387 Occurrence Handle1:CAS:528:DyaK3MXisVKgurc%3D

    CAS  Google Scholar 

  • J Lynch N S Rodriguez (1994) ArticleTitlePhotosynthetic nitrogen-use efficiency in relation to leaf longevity in common bean Crop Sci. 34 1284–1290

    Google Scholar 

  • J P Lynch S E Beebe (1995) ArticleTitleAdaptation of beans to low soil phosphorus availability HortSci. 30 1165–1171 Occurrence Handle1:CAS:528:DyaK2MXptV2rsro%3D

    CAS  Google Scholar 

  • J P Lynch K M Brown (2001) ArticleTitleTopsoil foraging – An architectural adaptation of plants to low phosphorus availability Plant Soil 237 225–237 Occurrence Handle10.1023/A:1013324727040 Occurrence Handle1:CAS:528:DC%2BD38XovVWltA%3D%3D

    Article  CAS  Google Scholar 

  • Z Ma D G Bielenberg K M Brown J P Lynch (2001a) ArticleTitleRegulation of root hair density by phosphorus availability in Arabidopsis thaliana Plant Cell Environ. 24 459–467 Occurrence Handle10.1046/j.1365-3040.2001.00695.x Occurrence Handle1:CAS:528:DC%2BD3MXjtFyjtb0%3D

    Article  CAS  Google Scholar 

  • Z Ma T C Walk A Marcus J P Lynch (2001b) ArticleTitleMorphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: A modeling approach Plant Soil 236 221–235 Occurrence Handle10.1023/A:1012728819326 Occurrence Handle1:CAS:528:DC%2BD3MXptlKhu74%3D

    Article  CAS  Google Scholar 

  • E Malusa E Laurenti I Juszczuk R P Ferrari A M Rychter (2002) ArticleTitleFree radical production in roots of Phaseolus vulgaris subjected to phosphate deficiency stress Plant Physiol. Biochem. 40 963–967 Occurrence Handle1:CAS:528:DC%2BD38XovFCisbc%3D

    CAS  Google Scholar 

  • H Marschner V Römheld (1996) Root-induced changes in the availability of micronutrients in the Rhizosphere Y Waisel A Eshel U Kafkaki (Eds) Plant Roots, the Hidden Half EditionNumber2 Marcel Dekker, Inc New York, NY 521–552

    Google Scholar 

  • C R Miller I Ochoa K L Nielsen D Beck J P Lynch (2003) ArticleTitleGenetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils Funct. Plant Biol. 30 973–985 Occurrence Handle1:CAS:528:DC%2BD3sXpsVWnsrk%3D

    CAS  Google Scholar 

  • G Neumann E Martinoia (2002) ArticleTitleCluster roots – An underground adaptation for survival in extreme environments Trends Plant Sci. 7 162–167 Occurrence Handle10.1016/S1360-1385(02)02241-0 Occurrence Handle1:CAS:528:DC%2BD38XjtVKnsbY%3D Occurrence Handle11950612

    Article  CAS  PubMed  Google Scholar 

  • C Nguyen (2003) ArticleTitleRhizodeposition of organic C by plants: Mechanisms and controls Agronomie 23 375–396 Occurrence Handle10.1051/agro:2003011 Occurrence Handle1:CAS:528:DC%2BD3sXot1yisbY%3D

    Article  CAS  Google Scholar 

  • K L Nielsen T J Bouma J P Lynch D M Eissenstat (1998) ArticleTitleEffects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris) New Phytol. 139 647–656 Occurrence Handle10.1046/j.1469-8137.1998.00242.x

    Article  Google Scholar 

  • K L Nielsen A Eshel J P Lynch (2001) ArticleTitleThe effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes J. Exp. Bot. 52 329–339 Occurrence Handle10.1093/jexbot/52.355.329 Occurrence Handle1:CAS:528:DC%2BD3MXjtVaju7w%3D Occurrence Handle11283178

    Article  CAS  PubMed  Google Scholar 

  • K Niklas (1994) Plant Allometry: The Scaling of Form and Process University of Chicago Press Chicago, IL

    Google Scholar 

  • S B Peng D M Eissenstat J H Graham K Williams N C Hodge (1993) ArticleTitleGrowth depression in mycorrhizal citrus at high-phosphorus supply – Analysis of carbon costs Plant Physiol. 101 1063–1071 Occurrence Handle1:CAS:528:DyaK3sXitlaqur0%3D Occurrence Handle12231758

    CAS  PubMed  Google Scholar 

  • J V Pothuluri D E Kissel D A Whitney S J Thien (1986) ArticleTitlePhosphorus uptake from soil layers having different soil test phosphorus levels Agron. J. 78 991–994 Occurrence Handle1:CAS:528:DyaL2sXjtF2gsQ%3D%3D

    CAS  Google Scholar 

  • K Raghothama (1999) ArticleTitlePhosphate acquisition Ann. Rev. Plant Physiol. Plant Mol. Biol. 50 665–693 Occurrence Handle1:CAS:528:DyaK1MXkt1yktrs%3D

    CAS  Google Scholar 

  • P B Reich (2002) Root–shoot Relations: Optimality in acclimation and adaptation or the ‘Emperor’s New Clothes’? Y Waisel A Eshel U Kafkafi (Eds) Plant Roots: The Hidden Half Marcel Dekker New York, NY 205–220

    Google Scholar 

  • G Rubio H Liao X L Yan J P Lynch (2003a) ArticleTitleTopsoil foraging and its role in plant competitiveness for phosphorus in common bean Crop Sci. 43 598–607

    Google Scholar 

  • G Rubio T Walk Z Y Ge X L Yan H Liao J P Lynch (2001) ArticleTitleRoot gravitropism and below-ground competition among neighbouring plants: A modeling approach Ann. Bot. 88 929–940 Occurrence Handle10.1006/anbo.2001.1530

    Article  Google Scholar 

  • G Rubio J Zhu J P Lynch (2003b) ArticleTitleA critical test of the two prevailing theories of plant response to nutrient availability Amer. J. Bot. 90 143–152 Occurrence Handle1:CAS:528:DC%2BD3sXht1Sks7g%3D

    CAS  Google Scholar 

  • M H Ryan J H Graham (2002) ArticleTitleIs there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244 263–271 Occurrence Handle10.1023/A:1020207631893 Occurrence Handle1:CAS:528:DC%2BD38XntFGrur8%3D

    Article  CAS  Google Scholar 

  • P R Ryan E Delhaize D L Jones (2001) ArticleTitleFunction and mechanism of organic anion exudation from plant roots Ann. Rev. Plant Physiol. Plant Mol. Biol. 52 527–560 Occurrence Handle1:CAS:528:DC%2BD3MXkslWgsbg%3D

    CAS  Google Scholar 

  • A M Rychter M Chauveau J L Bomsel C Lance (1992) ArticleTitleThe effect of phosphate deficiency on mitochondrial activity and adenylate levels in bean roots Physiol. Plant. 84 80–86 Occurrence Handle10.1034/j.1399-3054.1992.840113.x Occurrence Handle1:CAS:528:DyaK38XhsFSksbo%3D

    Article  CAS  Google Scholar 

  • A M Rychter M Mikulska (1990) ArticleTitleThe relationship between phosphate status and cyanide-resistant respiration in bean roots Physiol. Plant. 79 663–667 Occurrence Handle10.1034/j.1399-3054.1990.790413.x Occurrence Handle1:CAS:528:DyaK3cXlslWjsro%3D

    Article  CAS  Google Scholar 

  • F W Smith (2001) ArticleTitleSulphur and phosphorus transport systems in plants Plant Soil 232 109–118 Occurrence Handle10.1023/A:1010390120820 Occurrence Handle1:CAS:528:DC%2BD3MXlsVCks7c%3D

    Article  CAS  Google Scholar 

  • S E Smith D J Read (1997) Mycorrhizal Symbiosis Academic Press San Diego, CA 605

    Google Scholar 

  • S S Snapp R Koide J Lynch (1995) ArticleTitleExploitation of localized phosphorus patches by common bean roots Plant Soil 177 211–218 Occurrence Handle10.1007/BF00010127 Occurrence Handle1:CAS:528:DyaK28XhtlOhsbk%3D

    Article  CAS  Google Scholar 

  • S S Snapp J P Lynch (1996) ArticleTitlePhosphorus distribution and remobilization in bean plants as influenced by phosphorus nutrition Crop Sci. 36 929–935

    Google Scholar 

  • M E Theodorou W C Plaxton (1993) ArticleTitleMetabolic adaptations of plant respiration to nutritional phosphate deprivation Plant Physiol. 101 339–344 Occurrence Handle1:CAS:528:DyaK3sXhs1yhsLw%3D Occurrence Handle12231689

    CAS  PubMed  Google Scholar 

  • H Van der Berg (1998) ArticleTitleMultiple nutrient limitation in unicellulars: Reconstructing Liebig’s Law Math. Biosci. 149 1–22

    Google Scholar 

  • A Van der Werf R Welschen H Lambers (1992) Respiratory losses increase with decreasing inherent growth rate of a species and with decreasing nitrate supply: A search for explanations for these observations H Lambers L Van der Plas (Eds) Molecular, Biochemical, and Physiological Aspects of Plant Respiration SPB Academic Publishing The Hague

    Google Scholar 

  • C P Vance C Uhde-Stone D L Allan (2003) ArticleTitlePhosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource New Phytol. 157 423–447 Occurrence Handle10.1046/j.1469-8137.2003.00695.x Occurrence Handle1:CAS:528:DC%2BD3sXisF2gu70%3D

    Article  CAS  Google Scholar 

  • S Wahl P Ryser (2000) ArticleTitleRoot tissue structure is linked to ecological strategies of grasses New Phytol. 148 459–471 Occurrence Handle10.1046/j.1469-8137.2000.00775.x

    Article  Google Scholar 

  • M Wissuwa (2003) ArticleTitleHow do plants achieve tolerance to phosphorus deficiency? Small causes with big effects Plant Physiol. 133 1–12 Occurrence Handle10.1104/pp.103.029306

    Article  Google Scholar 

  • Yan X, Liao H, Becbe S E, Blair M W, Lynch J P 2004 QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil (in press)

  • R W Zobel (1992) ArticleTitleRoot morphology and development J. Plant Nutr. 15 677–684

    Google Scholar 

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  1. Intercollege Program in Plant Physiology, The Pennsylvania State University, University Park, PA, 16802, USA

    Jonathan P. Lynch, Melissa D. Ho & Low phosphorus

  2. Department of Horticulture, The Pennsylvania State University, PA, 16802, USA

    Jonathan P. Lynch

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  1. Jonathan P. Lynch
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Correspondence to Jonathan P. Lynch.

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Lynch, J.P., Ho, M.D. & phosphorus, L. Rhizoeconomics: Carbon costs of phosphorus acquisition. Plant Soil 269, 45–56 (2005). https://doi.org/10.1007/s11104-004-1096-4

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