Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems

Roots of the Second Green Revolution

Jonathan P. Lynch

Penn State, University Park, PA 16802, USA. Email:

Australian Journal of Botany 55(5) 493-512
Submitted: 8 June 2006  Accepted: 1 March 2007   Published: 17 August 2007


The Green Revolution boosted crop yields in developing nations by introducing dwarf genotypes of wheat and rice capable of responding to fertilisation without lodging. We now need a second Green Revolution, to improve the yield of crops grown in infertile soils by farmers with little access to fertiliser, who represent the majority of third-world farmers. Just as the Green Revolution was based on crops responsive to high soil fertility, the second Green Revolution will be based on crops tolerant of low soil fertility. Substantial genetic variation in the productivity of crops in infertile soil has been known for over a century. In recent years we have developed a better understanding of the traits responsible for this variation. Root architecture is critically important by determining soil exploration and therefore nutrient acquisition. Architectural traits under genetic control include basal-root gravitropism, adventitious-root formation and lateral branching. Architectural traits that enhance topsoil foraging are important for acquisition of phosphorus from infertile soils. Genetic variation in the length and density of root hairs is important for the acquisition of immobile nutrients such as phosphorus and potassium. Genetic variation in root cortical aerenchyma formation and secondary development (‘root etiolation’) are important in reducing the metabolic costs of root growth and soil exploration. Genetic variation in rhizosphere modification through the efflux of protons, organic acids and enzymes is important for the mobilisation of nutrients such as phosphorus and transition metals, and the avoidance of aluminum toxicity. Manipulation of ion transporters may be useful for improving the acquisition of nitrate and for enhancing salt tolerance. With the noteworthy exceptions of rhizosphere modification and ion transporters, most of these traits are under complex genetic control. Genetic variation in these traits is associated with substantial yield gains in low-fertility soils, as illustrated by the case of phosphorus efficiency in bean and soybean. In breeding crops for low-fertility soils, selection for specific root traits through direct phenotypic evaluation or molecular markers is likely to be more productive than conventional field screening. Crop genotypes with greater yield in infertile soils will substantially improve the productivity and sustainability of low-input agroecosystems, and in high-input agroecosystems will reduce the environmental impacts of intensive fertilisation. Although the development of crops with reduced fertiliser requirements has been successful in the few cases it has been attempted, the global scientific effort devoted to this enterprise is small, especially considering the magnitude of the humanitarian, environmental and economic benefits being forgone. Population growth, ongoing soil degradation and increasing costs of chemical fertiliser will make the second Green Revolution a priority for plant biology in the 21st century.


Abel S Ticconi CA Delatorre CA 2002 Phosphate sensing in higher plants. Physiologia Plantarum 115 1 8 doi:10.1034/j.1399-3054.2002.1150101.x

Abelson P 1999 A potential phosphate crisis. Science 283 2015 doi:10.1126/science.283.5410.2015

Ali MY Krishnamurthy L Saxena NP Rupela OP Kumar J Johansen C 2002 Scope for genetic manipulation of mineral acquisition in chickpea. Plant and Soil 245 123 134 doi:10.1023/A:1020616818106

Anonymous (1887) Report of the Pennsylvania State College Agricultural Experimental Station. Official Document Number 13, University Park, PA, USA.

Barber SA (1995) ‘Soil nutrient bioavailability: a mechanistic approach.’ (John Wiley & Sons Inc.: New York)

Bates TR Lynch JP 1996 Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19 529 538 doi:10.1111/j.1365-3040.1996.tb00386.x

Bates T Lynch JP 2000 a Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). American Journal of Botany 87 958 963 doi:10.2307/2656994

Bates T Lynch JP 2000 b The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. American Journal of Botany 87 964 970 doi:10.2307/2656995

Bates T Lynch JP 2001 Root hairs confer a competitive advantage under low phosphorus availability. Plant and Soil 236 243 250 doi:10.1023/A:1012791706800

Baumhardt RL Tolk JA Winter SR 2005 Seeding practices and cultivar maturity effects on simulated dryland grain sorghum yield. Agronomy Journal 97 935 942 doi:10.2134/agronj2004.0087

Bayuelo-Jimenez JS Craig R Lynch JP 2002 a Salinity tolerance of Phaseolus species during germination and early seedling growth. Crop Science 42 1584 1594

Bayuelo-Jimenez JS Debouck DG Lynch JP 2002 b Salinity tolerance in Phaseolus species during early vegetative growth. Crop Science 42 2184 2192

Bayuelo-Jimenez JS Debouck DG Lynch JP 2003 Growth, gas exchange, water relations, and ion composition of Phaseolus species grown under saline conditions. Field Crops Research 80 207 222

Beaver JS Rosas JC Myers J Acosta J Kelly JD Nchimbi-Msolla S Misangu R Bokosi J Temple S Arnaud-Santana E Coyne DP 2003 Contributions of the bean/cowpea CRSP to cultivar and germplasm development in common bean. Field Crops Research 82 87 102 doi:10.1016/S0378-4290(03)00032-7

Beebe S Lynch JP Galwey N Tohme J Ochoa I 1997 A geographical approach to identify phosphorus-efficient genotypes among landraces and wild ancestors of common bean. Euphytica 95 325 336 doi:10.1023/A:1003008617829

Bhat KKS Nye PH 1974 Diffusion of phosphate to plant roots in soil. III. Depletion around onion roots without root hairs. Plant and Soil 41 383 394 doi:10.1007/BF00017265

Bloom AJ Chapin FSI Mooney HA 1985 Resource limitation in plants—an economic analogy. Annual Review of Ecology and Systematics 16 363 392

Blumwald E Aharon GS Apse MP 2000 Sodium transport in plants. Biochimica et Biophysica Acta 1465 140 151

Bonser AM Lynch JP Snapp S 1996 Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytologist 132 281 288 doi:10.1111/j.1469-8137.1996.tb01847.x

Borch K Bouma TJ Lynch JP Brown KM 1999 Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant, Cell & Environment 22 425 431 doi:10.1046/j.1365-3040.1999.00405.x

Borlaug NE (1972) The green revolution, peace, and humanity. In ‘Speech delivered upon receipt of the 1970 Nobel Peace Prize’. (Centro Internacional de Mejoramiento de Maiz y Trigo: El Batan, Mexico)

Bouldin D 1961 Mathematical description of diffusion process in the soil. Soil Science Society of America Proceedings 25 476 480

Bouranis DL Chorianopoulou SN Siyiannis VF Protonotarios VE Hawkesford MJ 2003 Aerenchyma formation in roots of maize during sulphate starvation. Planta 217 382 391

Britto D Kronzucker H 2004 Bioengineering nitrogen acquisition in rice: can novel initiatives in rice genomics and physiology contribute to global food security? BioEssays 26 683 692 doi:10.1002/bies.20040

Britto D Kronzucker H 2006 Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends in Plant Science 11 529 534 doi:10.1016/j.tplants.2006.09.011

Broadley MR White PJ Hammond JP Zelko I Lux A 2007 Zinc in plants. New Phytologist 173 677 702 doi:10.1111/j.1469-8137.2007.01996.x

Caradus J 1981 Effect of root hair length on white clover growth over a range of soil phosphorus levels. New Zealand Journal of Agricultural Research 24 359 364

Chrispeels MJ Crawford NM Schroeder JI 1999 Proteins for transport of water and mineral nutrients across the membranes of plant cells. The Plant Cell 11 661 675

Clarkson DT 1985 Factors affecting mineral acquisition by plants. Annual Review of Plant Physiology 36 77 115 doi:10.1146/annurev.pp.36.060185.000453

Douds DD Johnson CR Koch KE 1988 Carbon cost of the fungal symbiont relative to net leaf-P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiology 86 491 496

Drew MC Saker LR 1978 Nutrient supply and the growth of the seminal root system in barley. Journal of Experimental Botany 29 435 451

Drew M He C Morgan P 1989 Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen-or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiology 91 266 271

Dunbabin V Diggle A Rengel Z 2003 Is there an optimal root architecture for nitrate capture in leaching environments? Plant, Cell & Environment 26 835 844

Eissenstat DM Graham JH Syvertsen JP Drouillard DL 1993 Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Annals of Botany 71 1 10 doi:10.1006/anbo.1993.1001

Elliott GC Lynch JP Lauchli A 1984 Influx and efflux of P in roots of intact maize plants. Double-labeling with 32P and 33P. Plant Physiology 76 336 341

Esau K (1977) ‘Anatomy of seed plants.’ (John Wiley and Sons: New York)

Eshel A , Nielsen K , Lynch JP (1995) Response of bean root systems to low level of P. In ‘Plant roots—from cells to systems. 14th Long Ashton international symposium’. p. 63. (IACR–Long Ashton Research Station: Bristol, England)

Fan MS Zhu JM Richards C Brown KM Lynch JP 2003 Physiological roles for aerenchyma in phosphorus-stressed roots. Functional Plant Biology 30 493 506

FAO (2002) ‘The state of food insecurity in the world 2002.’ (The Food and Agriculture Organisation of the United Nations: Rome)

Fitter A Williamson L Linkohr B Leyser O 2002 Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proceedings of the Royal Society of London. Series B. Biological Sciences 269 2017 2022 doi:10.1098/rspb.2002.2120

Foehse D Claassen N Jungk A 1991 Phosphorus efficiency of plants. II. Significance of root radius, root hairs and cation–anion balance for phosphorus influx in seven plant species. Plant and Soil 132 261 272

Forde BG 2000 Nitrate transporters in plants: structure, function, and regulation. Biochimica et Biophysica Acta 1465 219 235

Foy CD Chaney RL White MC 1978 The physiology of metal toxicity in plants. Annual Review of Plant Physiology 29 511 566 doi:10.1146/annurev.pp.29.060178.002455

Gahoonia TS Nielsen NE 1997 Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98 177 182 doi:10.1023/A:1003113131989

Gahoonia TS Nielsen NE 2003 Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils. Plant, Cell & Environment 26 1759 1766 doi:10.1046/j.1365-3040.2003.01093.x

Gahoonia TS Nielsen NE 2004 Root traits as tools for creating phosphorus efficient crop varieties. Plant and Soil 260 47 57 doi:10.1023/B:PLSO.0000030168.53340.bc

Gahoonia TS Care D Nielsen NE 1997 Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191 181 188 doi:10.1023/A:1004270201418

Gahoonia TS Nielsen NE Lyshede OB 1999 Phosphorus (P) acquisition of cereal cultivars in the field at three levels of P fertilization. Plant and Soil 211 269 281 doi:10.1023/A:1004742032367

Gahoonia TS Nielsen NE Joshi PA Jahoor A 2001 A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant and Soil 235 211 219 doi:10.1023/A:1011993322286

Ge ZY Rubio G Lynch JP 2000 The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant and Soil 218 159 171 doi:10.1023/A:1014987710937

George TS Simpson RJ Hadobas PA Richardson AE 2005 Expression of a fungal phytase gene in Nicotiana tabacum improves phosphorus nutrition of plants grown in amended soils. Plant Biotechnology Journal 3 129 140 doi:10.1111/j.1467-7652.2004.00116.x

Goldstein A (1992) Phosphate starvation inducible enzymes and proteins in higher plants. In ‘Inducible plant proteins’. (Ed. JL Wray) pp. 25–44. (Cambridge University Press: Cambridge, UK)

Gonzalez A Steffen KL Lynch JP 1998 Light and excess manganese—implications for oxidative stress in common bean. Plant Physiology 118 493 504 doi:10.1104/pp.118.2.493

Hackett C 1972 A method of applying nutrients locally to roots under controlled conditions, and some morphological effects of locally applied nitrate on the branching of wheat roots. Australian Journal of Biological Sciences 25 1169 1180

Halsted M Lynch JP 1996 Phosphorus responses of C-3 and C-4 species. Journal of Experimental Botany 47 497 505

Hardarson G , Broughton WJ (Eds) (2003) ‘Maximising the use of biological nitrogen fixation in agriculture.’ Developments in plant and soil sciences. (Kluwer Academic Publishers, Food and Agricultire Organisation of the United Nations, International Atomic Energy Agency: Dordrecht, The Netherlands)

Harris D , Paul E (1987) Carbon requirements of vesicular-arbuscular mycorrhizae. In ‘Ecophysiology of VA mycorrhizae’. (Ed. GR Safir) pp. 93–105. (CRC Press: Boca Raton, FL)

Hartemink AE (2003) ‘Soil fertility decline in the tropics.’ (CABI Publishing: Wageningen, The Netherlands)

Hinsinger P 2001 Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237 173 195 doi:10.1023/A:1013351617532

Hinsinger P Gobran GR Gregory PJ Wenzel WW 2005 Rhizosphere geometry and heterogeneity arising from root mediated physical and chemical processes. New Phytologist 168 293 303 doi:10.1111/j.1469-8137.2005.01512.x

Ho MD (2004) Effects of root architecture, plasticity, and tradeoffs on water and phosphorus acquisition in heterogenous environments. PhD Thesis, Penn State University, University Park, PA.

Ho M McCannon B Lynch JP 2004 Optimization modeling of plant root architecture for water and phosphorus acquisition. Journal of Theoretical Biology 226 331 340 doi:10.1016/j.jtbi.2003.09.011

Ho M Rosas J Brown K Lynch JP 2005 Root architectural tradeoffs for water and phosphorus acquisition. Functional Plant Biology 32 737 748 doi:10.1071/FP05043

Itoh S Barber S 1983 a A numerical solution of whole plant nutrient uptake for soil root systems with root hairs. Plant and Soil 70 403 413 doi:10.1007/BF02374895

Itoh S Barber S 1983 b Phosphorus uptake by six plant species as related to root hairs. Agronomy Journal 75 457 461

Jackson MB Armstrong W 1999 Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1 274 287

Jakobsen I Rosendahl L 1990 Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115 77 83

Jones DL Dennis PG Owen AG van Hees PAW 2003 Organic acid behavior in soils—misconceptions and knowledge gaps. Plant and Soil 248 31 41 doi:10.1023/A:1022304332313

Jungk A 2001 Root hairs and the acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164 121 129 doi:10.1002/1522-2624(200104)164:2<121::AID-JPLN121>3.0.CO;2-6

Kaeppler SM Parke JL Mueller SM Senior L Stuber C Tracy WF 2000 Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Science 40 358 364

Khush G 1999 Green revolution: preparing for the 21st century. Genome 42 646 655

Koch KE Johnson CR 1984 Photosynthate partitioning in split root citrus seedlings with mycorrhizal and non-mycorrhizal root systems. Plant Physiology 75 26 30

Kochian LV Piñeros MA Hoekenga OA 2005 The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant and Soil 274 175 195

Koide RT 2000 Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytologist 147 233235doi:10.1046/j.1469-8137.2000.00710.x

Konings H Verschuren G 1980 Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiologia Plantarum 49 265 279 doi:10.1111/j.1399-3054.1980.tb02661.x

Koyama H Kawamura A Kihara T Hara T Takita E Shibata D 2000 Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant & Cell Physiology 41 1030 1037 doi:10.1093/pcp/pcd029

Ladha JK Peoples MB (Eds) (1995) Management of biological nitrogen fixation for the development of more productive and sustainable agricultural systems. Plant and Soil 174, 1–286.

Lambers H , Atkin O , Millenaar FF (2002) Respiratory patterns in roots in relation to their functioning. In ‘Plant roots, the hidden half’. (Eds Y Waisel, A Eshel, K Kafkaki) pp. 521–552. (Marcel Dekker, Inc.: New York)

Lewis DG Quirk JP 1967 Phosphate diffusion in soil and uptake by plants. Plant and Soil 26 445 453 doi:10.1007/BF01379565

Li L Tang CX Rengel Z Zhang FS 2003 Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant and Soil 248 297 303 doi:10.1023/A:1022389707051

Li SM Li L Zhang FS Tang C 2004 Acid phosphatase role in chickpea/maize intercropping. Annals of Botany 94 297 303 doi:10.1093/aob/mch140

Liao H Rubio G Yan XL Cao AQ Brown KM Lynch JP 2001 Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil 232 69 79 doi:10.1023/A:1010381919003

Liao H Yan X Rubio G Beebe SE Blair MW Lynch JP 2004 Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Functional Plant Biology 31 959 970 doi:10.1071/FP03255

Lopez-Bucio J de la Vega OM Guevara-Garcia A Herrera-Estrella L 2000 a Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotechnology 18 450 453 doi:10.1038/74531

Lopez-Bucio J Nieto-Jacobo MF Ramirez-Rodriguez V Herrera-Estrella L 2000 b Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science 160 1 13 doi:10.1016/S0168-9452(00)00347-2

Lu Y Wassmann R Neue HU Huang C 1999 Impact of phosphorus supply on root exudation, aerenchyma formation and methane emission of rice plants. Biogeochemistry 47 203 218

Lynch JP (1998) The role of nutrient efficient crops in modern agriculture. In ‘Nutrient use in crop production’. (Ed. Z Rengel) (Food Products Press: New York)

Lynch JP (2005) Root architecture and nutrient acquisition. In ‘Nutrient acquisition by plants. An ecological perspective’. (Ed. H BassiriRad) (Springer-Verlag: Berlin)

Lynch JP Beebe SE 1995 Adaptation of beans to low soil phosphorus availability. HortScience 30 1165 1171

Lynch JP van Beem JJ 1993 Growth and architecture of seedling roots of common bean genotypes. Crop Science 33 1253 1257

Lynch JP , Brown K (1998) Root architecture and phosphorus acquisition efficiency in common bean. In ‘Phosphorus in plant biology: regulatory roles in ecosystem, organismic, cellular, and molecular processes’. (Eds JP Lynch, J Deikman) (American Society of Plant Physiologists: Rockville, MD)

Lynch JP Brown KM 2001 Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237 225 237

Lynch JP , Brown KM (2006) Whole plant adaptations to low phosphorus availability. In ‘Plant–environment interactions’. 3rd edn. (Ed. B Huang) (Taylor and Francis: New York)

Lynch JP , Deikman J (1998) ‘Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes.’ (American Society of Plant Physiologists: Rockville, MD)

Lynch JP Ho M 2005 Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269 45 56 doi:10.1007/s11104-004-1096-4

Lynch JP St Clair S 2004 Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crops Research 90 101 115 doi:10.1016/j.fcr.2004.07.008

Lynch JP Lauchli A Epstein E 1991 Vegetative growth of the common bean in response to phosphorus nutrition. Crop Science 31 380 387

Ma Z Bielenberg DG Brown KM Lynch JP 2001 a Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant, Cell & Environment 24 459 467

Ma Z Walk TC Marcus A Lynch JP 2001 b Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant and Soil 236 221 235 doi:10.1023/A:1012728819326

Mano Y Muraki M Fujimori M Takamizo T Kindiger B 2005 Identification of QTL controlling adventitious root formation during flooding conditions in teosinte (Zea mays ssp. huehuetenangensis) seedlings. Euphytica 142 33 42 doi:10.1007/s10681-005-0449-2

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London)

Martinez-Ballesta M Silva C Lopez-Berenguer C Cabanero F Carvajal M 2006 Plant aquaporins: New perspectives on water and nutrient uptake in saline environment. Plant Biology 8 535 546 doi:10.1055/s-2006-924172

Miguel M (2004) Genotypic variation in root hairs and phosphorus efficiency in common bean (Phaseolus vulgaris L.). MSc Thesis, Penn State, University Park, PA.

Miller CR Ochoa I Nielsen KL Beck D Lynch JP 2003 Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Functional Plant Biology 30 973 985 doi:10.1071/FP03078

Mollier A Pellerin S 1999 Maize root system growth and development as influenced by phosphorus deficiency. Journal of Experimental Botany 50 487 497 doi:10.1093/jexbot/50.333.487

Munns R Husain S Rivelli AR James RA Condon AGT Lindsay MP Lagudah ES Schachtman DP Hare RA 2002 Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant and Soil 247 93 105 doi:10.1023/A:1021119414799

Neumann G , Römheld V (2002) Root-induced changes in the availability of nutrients in the rhizosphere. In ‘Plant roots: the hidden half’. (Eds Y Waisel, A Eshel, U Kafkafi) pp. 617– 649. (Marcel Dekker: New York)

Newman E 1997 Phosphorus balance of contrasting farming systems, past and present. Can food production be sustainable? Journal of Applied Ecology 34 1334 1347 doi:10.2307/2405251

Nielsen KL Bouma TJ Lynch JP Eissenstat DM 1998 Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytologist 139 647 656 doi:10.1046/j.1469-8137.1998.00242.x

Nielsen KL Eshel A Lynch JP 2001 The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. Journal of Experimental Botany 52 329 339 doi:10.1093/jexbot/52.355.329

Ochoa I Blair M Lynch JP 2006 QTL Analysis of adventitious root formation in common bean (Phaseolus vulgaris L.) under contrasting phosphorus availability. Crop Science 46 1609 1621 doi:10.2135/cropsci2005.12-0446

van Oosterom EJ Bidinge FR Weltzien ER 2003 A yield architecture framework to explain adaptation of pearl millet to environmental stress. Field Crops Research 80 33 56 doi:10.1016/S0378-4290(02)00153-3

Owusu-Bennoah E Wild A 1979 Autoradiography of the depletion zone of phosphate around onion roots in the presence of vesicular-arbuscular mycorrhiza. New Phytologist 82 133 140 doi:10.1111/j.1469-8137.1979.tb07567.x

Palmgren MG 2001 Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52 817 845 doi:10.1146/annurev.arplant.52.1.817

Peng SB Eissenstat DM Graham JH Williams K Hodge NC 1993 Growth depression in mycorrhizal citrus at high-phosphorus supply—analysis of carbon costs. Plant Physiology 101 1063 1071

Peng S Cassman KG Virmani SS Sheehy J Khush GS 1999 Yield potential trends of tropical rice since the release of IR8 and the challenge of increasing rice yield potential. Crop Science 39 1552 1559

Peterson RL Farquhar ML 1996 Root hairs: specialized tubular cells extending root surfaces. Botanical Review 62 1 40

Piñeros MA Shaff JE Manslank HS Alves VMC Kochian LV 2005 Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiology 137 231 241

Rabalais NN Turner RE Wiseman WJJ 2002 Gulf of Mexico hypoxia, A.K.A. ‘The dead zone’. Annual Review of Ecology and Systematics 33 235 263 doi:10.1146/annurev.ecolsys.33.010802.150513

Radin J Eidenbock M 1984 Hydraulic conductance as a factor limiting leaf expansion of phosphorus-deficient cotton plants. Plant Physiology 75 372 377

Raghothama KG Karthikeyan AS 2005 Phosphate acquisition. Plant and Soil 274 37 49

Ramesh SA Choimes S Schachtman DP 2004 Over-expression of an Arabidopsis zinc transporter in Hordeum vulgare increases short-term zinc uptake after zinc deprivation and seed zinc content. Plant Molecular Biology 54 373 385 doi:10.1023/B:PLAN.0000036370.70912.34

Ray JD Kindiger B Sinclair TR 1999 Introgressing root aerenchyma into maize. Maydica 44 113 117

Rengel Z (1999) Physiological mechanisms underlying differential nutrient efficiency of crop genotypes. In ‘Mineral nutrition of crops: fundamental mechanisms and implications’. (Ed. Z Rengel) pp. 227–265. (Haworth Press, Inc.: New York)

Rengel Z 2001 Genotypic differences in micronutrient use efficiency in crops. Communications in Soil Science and Plant Analysis 32 1163 1186

Rengel Z 2002 Genetic control of root exudation. Plant and Soil 245 59 70 doi:10.1023/A:1020646011229

Robinson D (2005) Integrated root responses to variations in nutrient supply. In ‘Nutrient acquisition by plants. An ecological perspective’. (Ed. H BassiriRad) pp. 43–62. (Springer-Verlag: Berlin)

Rubio G Walk T Ge ZY Yan XL Liao H Lynch JP 2001 Root gravitropism and below-ground competition among neighbouring plants: a modelling approach. Annals of Botany 88 929 940 doi:10.1006/anbo.2001.1530

Rubio G Liao H Yan XL Lynch JP 2003 Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Science 43 598 607

Runge GF , Senauer B , Pardey P , Rosengrant M (2003) ‘Ending hunger in our lifetime: food security and globalization.’ (Johns Hopkins University Press: Baltimore, MD, USA)

Ryan MH Graham JH 2002 Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant and Soil 244 263 271

Ryan PR Delhaize E Jones DL 2001 Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52 527 560 doi:10.1146/annurev.arplant.52.1.527

Ryser P Lambers H 1995 Root and leaf attributes accounting for the performance of fast-growing and slow-growing grasses at different nutrient supply. Plant and Soil 170 251 265 doi:10.1007/BF00010478

Sanchez PA (1976) ‘Properties and management of soils in the tropics.’ (John Wiley: New York)

Sanchez PA 2002 Ecology—Soil fertility and hunger in Africa. Science 295 2019 2020 doi:10.1126/science.1065256

Sanchez PA Swaminathan MS 2005 Hunger in Africa: the link between unhealthy people and unhealthy soils. Lancet 365 442 444

Senior M Chin E Lee M Smith J Stuber C 1996 Simple sequence repeat markers developed from maize sequences found in GenBank database: map construction. Crop Science 36 1676 1683

Setter TL Waters I 2003 Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant and Soil 253 1 34

Shiva V 1991 The green revolution in the Punjab. The Ecologist 21 57 60

Singh SP Urrea CA Gutiérrez JA Garcia J 1989 Selection for yield at two fertilizer levels in small-seeded common bean. Canadian Journal of Plant Science 69 1011 1017

Smith SE , Read DJ (1997) ‘Mycorrhizal symbiosis.’ (Academic Press: San Diego, CA)

Sprent JI (2005) Biological nitrogen fixation associated with angiosperms in terrestrial systems. In ‘Nutrient acquisition by plants: an ecological perspective’. (Ed. H BassiriRad) pp. 89–116. (Springer-Verlag: Berlin)

Steen I 1998 Phosphorus availability in the 21st century management of a non-renewable resource. Phosphorus & Potassium 217 25 31

Tesfaye M Temple SJ Allan DL Vance CP Samac DA 2001 Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiology 127 1836 1844

Tollenaar M Lee EA 2002 Yield potential, yield stability and stress tolerance in maize. Field Crops Research 75 161 169 doi:10.1016/S0378-4290(02)00024-2

Tomscha J Trull M Deikman J Lynch JP Guiltinan M 2004 Phosphatase under-producing mutants have altered phosphorus relations. Plant Physiology 135 334 345 doi:10.1104/pp.103.036459

Tripathi SC Sayre KD Kaul JN Narang RS 2004 Lodging behaviour and yield potential of spring wheat (Triticum aestivum L.): effects of ethephon and genotypes. Field Crops Research 87 207 220 doi:10.1016/j.fcr.2003.11.003

Tuberosa R Salvi S Sanguineti MC Landi P Maccaferri M Conti S 2002 Mapping QTLs regulating morpho-physiological traits and yield: case studies, shortcomings and perspectives in drought-stressed maize. Annals of Botany 89 941 963 doi:10.1093/aob/mcf134 Spec. No.

USDA Soil Taxonomy (1999) ‘Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys.’ 2nd edn. Agricultural Handbook No. 436. Soil Survey Staff. United States Department of Agriculture, National Resources Conservation Service.

Vance CP 2001 Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiology 127 390 397 doi:10.1104/pp.127.2.390

Vance CP (2002) Root–bacteria interactions: symbiotic N2 fixation. In ‘Plant roots: the hidden half’. (Eds Y Waisel, A Eshel, U Kafkafi) pp. 839–868. (Marcel Dekker, Inc.: New York)

Vance CP , Graham PH , Allan DL (2000) Biological nitrogen fixation: phosphorus a critical future need? In ‘Nitrogen fixation: from molecules to crop productivity’. (Eds FO Pederosa, M Hungria, G Yates, WE Newton) pp. 509–514. (Kluwer Academic: Dordrecht, The Netherlands)

Vance CP Uhde-Stone C Allan DL 2003 Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157 423 447 doi:10.1046/j.1469-8137.2003.00695.x

Vartapetian BB Jackson MB 1997 Plant adaptations to anaerobic stress. Annals of Botany 79 3 20 doi:10.1006/anbo.1996.0295

Veneklaas EJ Stevens J Cawthray GR Turner S Grigg AM Lambers H 2003 Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant and Soil 248 187 197 doi:10.1023/A:1022367312851

Very A-A Sentenac H 2003 Molecular mechanisms and regulation of K+ transport in higher plants. Annual Review of Plant Biology 54 575 603 doi:10.1146/annurev.arplant.54.031902.134831

Vosti SA , Reardon T (1997) ‘Sustainability, growth, and poverty alleviation: a policy and agroecological perspective.’ (International Food Policy Research Institute: Washington, DC)

Walk T Jaramillo R Lynch JP 2006 Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant and Soil 279 347 366 doi:10.1007/s11104-005-0389-6

Welch RM Graham RD 2004 Breeding for micronutrients in staple food crops from a human nutrition perspective. Journal of Experimental Botany 55 353 364 doi:10.1093/jxb/erh064

White P 2000 Calcium channels in higher plants. Biochimica et Biophysica Acta 1465 171 189 doi:10.1016/S0005-2736(00)00137-1

Whiteaker G Gerloff GC Gabelman WH Lindgren D 1976 Intraspecific differences in growth of beans at stress levels of phosphorus. Journal of the American Society for Horticultural Science 101 472 475

World Bank (2004) ‘World development indicators.’ (The World Bank: Washington, DC)

Xie YJ Yu D 2003 The significance of lateral roots in phosphorus (P) acquisition of water hyacinth (Eichhornia crassipes). Aquatic Botany 75 311 321

Yan X (2005) The roots of P-efficient soybean: theories and practices. In ‘Plant nutrition for food security, human health and environmental protection’. (Ed. CJ Li) pp. 36–37. (Tsinghua University Press: Beijing)

Yan X Beebe SE Lynch JP 1995 a Genetic variation for phosphorus efficiency of common bean in contrasting soil types. II. Yield response. Crop Science 35 1094 1099

Yan X Lynch JP Beebe SE 1995 b Genetic variation for phosphorus efficiency of common bean in contrasting soil types. I. Vegetative response. Crop Science 35 1086 1093

Yan XL Lynch JP Beebe SE 1996 Utilization of phosphorus substrates by contrasting common bean genotypes. Crop Science 36 936 941

Yan X Liao H Beebe S Blair M Lynch JP 2004 QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil 265 17 29

Yan X Wu P Ling H Xu G Xu F Zhang Q 2006 Plant nutriomics in China—an overview. Annals of Botany 98 473 482 doi:10.1093/aob/mcl116

Yun SJ Kaeppler SM 2001 Induction of maize acid phosphatase activities under phosphorus starvation. Plant and Soil 237 109 115 doi:10.1023/A:1013329430212

Zhu J Lynch JP 2004 The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays L.) seedlings. Functional Plant Biology 31 949 958 doi:10.1071/FP04046

Zhu J Kaeppler S Lynch JP 2005 a Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant and Soil 270 299 310 doi:10.1007/s11104-004-1697-y

Zhu J Kaeppler S Lynch JP 2005 b Mapping of QTL for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theoretical and Applied Genetics 111 688 695 doi:10.1007/s00122-005-2051-3

Zhu J Kaeppler S Lynch JP 2005 c Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays L.). Functional Plant Biology 32 749 762 doi:10.1071/FP05005

Zhu J Mickelson S Kaeppler S Lynch JP 2006 Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theoretical and Applied Genetics 113 1 10 doi:10.1007/s00122-006-0260-z

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