Roots of the Second Green Revolution
Jonathan P. LynchAustralian Journal of Botany 55(5) 493-512 https://doi.org/10.1071/BT06118
Submitted: 8 June 2006 Accepted: 1 March 2007 Published: 17 August 2007
Abstract
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.
Acknowledgements
I thank my collaborators Kathleen Brown, Stephen Beebe, James Beaver and Xiaolong Yan for their insights and discussions. Financial support for the author’s research discussed here was provided by the McKnight Foundation, the National Science Foundation, the United States Department of Agriculture National Research Initiative, the United States Agency for International Development and the United States Department of Energy.
Abel S,
Ticconi CA, Delatorre CA
(2002) Phosphate sensing in higher plants. Physiologia Plantarum 115, 1–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Abelson P
(1999) A potential phosphate crisis. Science 283, 2015.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Bates TR, Lynch JP
(1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19, 529–538.
| Crossref | GoogleScholarGoogle Scholar |
Bates T, Lynch JP
(2000a) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). American Journal of Botany 87, 958–963.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bates T, Lynch JP
(2000b) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. American Journal of Botany 87, 964–970.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bates T, Lynch JP
(2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant and Soil 236, 243–250.
| Crossref | GoogleScholarGoogle Scholar |
Baumhardt RL,
Tolk JA, Winter SR
(2005) Seeding practices and cultivar maturity effects on simulated dryland grain sorghum yield. Agronomy Journal 97, 935–942.
| Crossref | GoogleScholarGoogle Scholar |
Bayuelo-Jimenez JS,
Craig R, Lynch JP
(2002a) Salinity tolerance of Phaseolus species during germination and early seedling growth. Crop Science 42, 1584–1594.
Bayuelo-Jimenez JS,
Debouck DG, Lynch JP
(2002b) 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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Broadley MR,
White PJ,
Hammond JP,
Zelko I, Lux A
(2007) Zinc in plants. New Phytologist 173, 677–702.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clarkson DT
(1985) Factors affecting mineral acquisition by plants. Annual Review of Plant Physiology 36, 77–115.
| Crossref | GoogleScholarGoogle Scholar |
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.
| PubMed |
Drew MC, Saker LR
(1978) Nutrient supply and the growth of the seminal root system in barley. Journal of Experimental Botany 29, 435–451.
| Crossref | GoogleScholarGoogle Scholar |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Foy CD,
Chaney RL, White MC
(1978) The physiology of metal toxicity in plants. Annual Review of Plant Physiology 29, 511–566.
| Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE
(1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177–182.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE
(2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant and Soil 260, 47–57.
| Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS,
Care D, Nielsen NE
(1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191, 181–188.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gonzalez A,
Steffen KL, Lynch JP
(1998) Light and excess manganese—implications for oxidative stress in common bean. Plant Physiology 118, 493–504.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ho M,
Rosas J,
Brown K, Lynch JP
(2005) Root architectural tradeoffs for water and phosphorus acquisition. Functional Plant Biology 32, 737–748.
| Crossref | GoogleScholarGoogle Scholar |
Itoh S, Barber S
(1983a) A numerical solution of whole plant nutrient uptake for soil root systems with root hairs. Plant and Soil 70, 403–413.
| Crossref | GoogleScholarGoogle Scholar |
Itoh S, Barber S
(1983b) 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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Jungk A
(2001) Root hairs and the acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164, 121–129.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koch KE, Johnson CR
(1984) Photosynthate partitioning in split root citrus seedlings with mycorrhizal and non-mycorrhizal root systems. Plant Physiology 75, 26–30.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Koide RT
(2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytologist 147, 233–235.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lewis DG, Quirk JP
(1967) Phosphate diffusion in soil and uptake by plants. Plant and Soil 26, 445–453.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Li SM,
Li L,
Zhang FS, Tang C
(2004) Acid phosphatase role in chickpea/maize intercropping. Annals of Botany 94, 297–303.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Lopez-Bucio J,
de la Vega OM,
Guevara-Garcia A, Herrera-Estrella L
(2000a) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotechnology 18, 450–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lopez-Bucio J,
Nieto-Jacobo MF,
Ramirez-Rodriguez V, Herrera-Estrella L
(2000b) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science 160, 1–13.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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, 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 KM
(2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237, 225–237.
| Crossref | GoogleScholarGoogle Scholar |
Lynch JP, Ho M
(2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269, 45–56.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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
(2001a) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant, Cell & Environment 24, 459–467.
| Crossref | GoogleScholarGoogle Scholar |
Ma Z,
Walk TC,
Marcus A, Lynch JP
(2001b) 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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Mollier A, Pellerin S
(1999) Maize root system growth and development as influenced by phosphorus deficiency. Journal of Experimental Botany 50, 487–497.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Newman E
(1997) Phosphorus balance of contrasting farming systems, past and present. Can food production be sustainable? Journal of Applied Ecology 34, 1334–1347.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Palmgren MG
(2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52, 817–845.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Radin J, Eidenbock M
(1984) Hydraulic conductance as a factor limiting leaf expansion of phosphorus-deficient cotton plants. Plant Physiology 75, 372–377.
| PubMed |
Raghothama KG, Karthikeyan AS
(2005) Phosphate acquisition. Plant and Soil 274, 37–49.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ray JD,
Kindiger B, Sinclair TR
(1999) Introgressing root aerenchyma into maize. Maydica 44, 113–117.
Rengel Z
(2001) Genotypic differences in micronutrient use efficiency in crops. Communications in Soil Science and Plant Analysis 32, 1163–1186.
| Crossref | GoogleScholarGoogle Scholar |
Rengel Z
(2002) Genetic control of root exudation. Plant and Soil 245, 59–70.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
Ryan MH, Graham JH
(2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant and Soil 244, 263–271.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Sanchez PA
(2002) Ecology—Soil fertility and hunger in Africa. Science 295, 2019–2020.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sanchez PA, Swaminathan MS
(2005) Hunger in Africa: the link between unhealthy people and unhealthy soils. Lancet 365, 442–444.
| PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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.
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tollenaar M, Lee EA
(2002) Yield potential, yield stability and stress tolerance in maize. Field Crops Research 75, 161–169.
| Crossref | GoogleScholarGoogle Scholar |
Tomscha J,
Trull M,
Deikman J,
Lynch JP, Guiltinan M
(2004) Phosphatase under-producing mutants have altered phosphorus relations. Plant Physiology 135, 334–345.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
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 Spec. No. 89, 941–963.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vance CP
(2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiology 127, 390–397.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Vartapetian BB, Jackson MB
(1997) Plant adaptations to anaerobic stress. Annals of Botany 79, 3–20.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Very A-A, Sentenac H
(2003) Molecular mechanisms and regulation of K+ transport in higher plants. Annual Review of Plant Biology 54, 575–603.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walk T,
Jaramillo R, Lynch JP
(2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant and Soil 279, 347–366.
| Crossref | GoogleScholarGoogle Scholar |
Welch RM, Graham RD
(2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. Journal of Experimental Botany 55, 353–364.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
White P
(2000) Calcium channels in higher plants. Biochimica et Biophysica Acta 1465, 171–189.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
Xie YJ, Yu D
(2003) The significance of lateral roots in phosphorus (P) acquisition of water hyacinth (Eichhornia crassipes). Aquatic Botany 75, 311–321.
| Crossref | GoogleScholarGoogle Scholar |
Yan X,
Beebe SE, Lynch JP
(1995a) 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
(1995b) 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.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yun SJ, Kaeppler SM
(2001) Induction of maize acid phosphatase activities under phosphorus starvation. Plant and Soil 237, 109–115.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Zhu J,
Kaeppler S, Lynch JP
(2005a) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant and Soil 270, 299–310.
| Crossref | GoogleScholarGoogle Scholar |
Zhu J,
Kaeppler S, Lynch JP
(2005b) 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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhu J,
Kaeppler S, Lynch JP
(2005c) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays L.). Functional Plant Biology 32, 749–762.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
