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Plant sciences, sustainable farming systems and food quality
FARRER REVIEW

The future of grain legumes in cropping systems

Thomas R. Sinclair A C and Vincent Vadez B
+ Author Affiliations
- Author Affiliations

A Crop Science Department, North Carolina State University, Raleigh, NC 27695, USA.

B ICRISAT (International Crops Research Institute for the Semiarid Tropics), Dryland Cereal Research Program, Patancheru 502324, Andhra Pradesh, India.

C Corresponding author. Email: trsincla@ncsu.edu

Crop and Pasture Science 63(6) 501-512 https://doi.org/10.1071/CP12128
Submitted: 3 April 2012  Accepted: 12 July 2012   Published: 14 September 2012

Abstract

Grain legume production is increasing worldwide due to their use directly as human food, feed for animals, and industrial demands. Further, grain legumes have the ability to enhance the levels of nitrogen and phosphorus in cropping systems. Considering the increasing needs for human consumption of plant products and the economic constraints of applying fertiliser on cereal crops, we envision a greater role for grain legumes in cropping systems, especially in regions where accessibility and affordability of fertiliser is an issue. However, for several reasons the role of grain legumes in cropping systems has often received less emphasis than cereals. In this review, we discuss four major issues in increasing grain legume productivity and their role in overall crop production: (i) increased symbiotic nitrogen fixation capacity, (ii) increased phosphorus recovery from the soil, (iii) overcoming grain legume yield limitations, and (iv) cropping systems to take advantage of the multi-dimensional benefits of grain legumes.


References

Abbo S, Berger J, Turner NC (2003) Evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation. Functional Plant Biology 30, 1081–1087.
Evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation.Crossref | GoogleScholarGoogle Scholar |

Ae N, Shen RF (2002) Root cell-wall properties are proposed to contribute to phosphorus (P) mobilization by groundnut and pigeonpea. Plant and Soil 245, 95–103.
Root cell-wall properties are proposed to contribute to phosphorus (P) mobilization by groundnut and pigeonpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCitr0%3D&md5=08bc457997a5341f438937ea2859fbc6CAS |

Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Science 248, 477–480.
Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslOitbw%3D&md5=1d5ae2eb29208b9bd86014dc13d079bdCAS |

Ali M, Gupta S (2012) Carrying capacity of Indian agriculture: pulse crops. Current Science 102, 874–881.

Belko N, Zaman MA, Diop NN, Cisse N, Ehlers JD, Ndoye O, Zombre G, Vadez V (2012) Lower soil moisture threshold for transpiration decline under water deficit correlates with lower canopy conductance and higher transpiration efficiency in drought tolerant cowpea. Functional Plant Biology 39, 306–322.

Berger JD, Buirchel BJ, Luckett DJ, Nelson MN (2012) Domestication bottlenecks limit genetic diversity and constrain adaptation in narrow-leafed lupin (Lupinus angustifolius L.). Theoretical and Applied Genetics 124, 637–652.
Domestication bottlenecks limit genetic diversity and constrain adaptation in narrow-leafed lupin (Lupinus angustifolius L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383it1Knug%3D%3D&md5=6822e62405df5555ca274340120f6b08CAS |

Bhadoria PS, El Dessougi H, Liebersbach H, Claassen N (2004) Phosphorus uptake kinetics, size of root system and growth of maize and groundnut in solution culture. Plant and Soil 262, 327–336.
Phosphorus uptake kinetics, size of root system and growth of maize and groundnut in solution culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlGgu7k%3D&md5=c7b133622eddce4a8dc69d6aaab052a2CAS |

Bieleski RL (1973) Phosphate pools, phosphate transport and phosphate availability. Annual Review of Plant Physiology 24, 225–252.
Phosphate pools, phosphate transport and phosphate availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXltFeitbY%3D&md5=d166384e3c862fb93fdeee6d9936dfa1CAS |

Blümmel M, Ratnakumar P, Vadez V (2012) Opportunities for exploiting variations in haulm fodder traits of intermittent drought tolerant lines in a reference collection of groundnut (Arachis hypogeae L.). Field Crops Research 126, 200–206.
Opportunities for exploiting variations in haulm fodder traits of intermittent drought tolerant lines in a reference collection of groundnut (Arachis hypogeae L.).Crossref | GoogleScholarGoogle Scholar |

Burkart MR, James DE (1999) Agricultural-nitrogen contributions to hypoxia in the Gulf of Mexico. Journal of Environmental Quality 28, 850–859.
Agricultural-nitrogen contributions to hypoxia in the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1yltL8%3D&md5=cba0311cc04cb463fd8d5a9034c75cffCAS |

Cadisch G, Giller KE (1997) ‘Driven by nature: plant residue quality and decomposition.’ (CAB International: Wallingford, UK)

Castellanos-Ramos JZ, Acosta-Gallegos JA, Orozco NR, Munoz-Ramos JJ (2009) Biological nitrogen fixation and tuber yield of yam bean in central Mexico. Agicultura Tecnica en Mexico 35, 277–283.

Chen P, Sneller CH, Purcell LC, Sinclair TR, King CA, Ishibashi T (2007) Registration of soybean germplasm lines R01-416F an R01-581F for improved yield and nitrogen fixation under drought stress. Journal of Plant Registrations 1, 166–167.
Registration of soybean germplasm lines R01-416F an R01-581F for improved yield and nitrogen fixation under drought stress.Crossref | GoogleScholarGoogle Scholar |

Choi HK, Mun JH, Kim DJ, Zhu H, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss JB, Young ND, Cook DR (2004) Estimating genome conservation between crop and model legume species. Proceedings of the National Academy of Sciences of the United States of America 101, 15 289–15 294.
Estimating genome conservation between crop and model legume species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKhsbzL&md5=fb3a0bded2aba5655724d8470970a56cCAS |

Chu Y, Holbrook C, Timper P, Ozias-Akins P (2007) Development of a PCR-based molecular marker to select for nematode resistance in peanut. Crop Science 47, 841–847.
Development of a PCR-based molecular marker to select for nematode resistance in peanut.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlShtbg%3D&md5=229c590fa6166e255c51d0263648f6c5CAS |

Clark EA, Francis CA (1985) Bean-maize intercrops: a comparison of bush and climbing bean growth habits. Field Crops Research 10, 151–166.
Bean-maize intercrops: a comparison of bush and climbing bean growth habits.Crossref | GoogleScholarGoogle Scholar |

Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156, 567–576.
Legume sanctions and the evolution of symbiotic cooperation by rhizobia.Crossref | GoogleScholarGoogle Scholar |

Denison RF, Sinclair TR (1985) Diurnal and seasonal variation in dinitrogen fixation (acetylene reduction) rates by field-grown soybeans. Agronomy Journal 77, 679–684.
Diurnal and seasonal variation in dinitrogen fixation (acetylene reduction) rates by field-grown soybeans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlslGnu7k%3D&md5=1d8e14372f1cbc3bc996d7cc9eed1539CAS |

Denison RF, Weisz PR, Sinclair TR (1985) Variability among plants in dinitrogen fixation (acetylene reduction) rates by field-grown soybean. Agronomy Journal 77, 947–950.
Variability among plants in dinitrogen fixation (acetylene reduction) rates by field-grown soybean.Crossref | GoogleScholarGoogle Scholar |

Devi MJ, Sinclair TR, Vadez V, Krishnamurthy L (2009) Peanut genotypic variation in transpiration efficiency and decreased transpiration during progressive soil drying. Field Crops Research 114, 280–285.
Peanut genotypic variation in transpiration efficiency and decreased transpiration during progressive soil drying.Crossref | GoogleScholarGoogle Scholar |

Devi MJ, Sinclair TR, Vadez V (2010) Genotypic variability among peanut (Arachis hypogea L.) in sensitivity of nitrogen fixation to soil drying. Plant and Soil 330, 139–148.
Genotypic variability among peanut (Arachis hypogea L.) in sensitivity of nitrogen fixation to soil drying.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktFequ7g%3D&md5=fd01defd337c9d81438861b1a14ba5adCAS |

Duan S, Bianchi TS, Satschi PH, Armon RMW (2010) Effects of tributary inputs on nutrient export from the Mississippi and Atchafalaya Rivers to the Gulf of Mexico. Marine and Freshwater Research 61, 1029–1038.
Effects of tributary inputs on nutrient export from the Mississippi and Atchafalaya Rivers to the Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Snt7jF&md5=e3aee5949f6eae23c7c31f6a27d93be8CAS |

Fredeen , AL , Rao , IM , Terry , N (1989) Influence of phosphorous nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89, 225–230.
Influence of phosphorous nutrition on growth and carbon partitioning in Glycine max.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtFelur0%3D&md5=62eec0f6534302a834c4a8a4f5e90755CAS |

Fujii K, Gatehouse AMR, Johnson CD, Mitchel R, Yoshida T (1989) Bruchids and legumes: economics, ecology and coevolution. In ‘Proceedings of the Second International Symposium on Bruchids and Legumes (ISBL-2)’. (Eds K Fujii, AMR Gatehouse, CD Johnson, R Mitchel, T Yoshida) pp. 303–315. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Furihata T, Suzki M, Sakurai H (1992) Kinetic characterization of two phosphate uptake systems with different affinities in suspension-cultured Catharanthus roseus protoplasts. Plant & Cell Physiology 33, 1151–1157.

Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant and Soil 198, 147–152.
Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFGis7g%3D&md5=31b05c1628bb1c2552cd4e48d1c951e6CAS |

Gan YT, Siddique KHM, MacLeod WJ, Jayakumar P (2006) Management options for minimizing the damage by ascochyta blight (Ascochyta rabiei) in chickpea (Cicer arietinum L.). Field Crops Research 97, 121–134.
Management options for minimizing the damage by ascochyta blight (Ascochyta rabiei) in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |

Gilbert GA, Knight JD, Vance CP, Allan DL (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant, Cell & Environment 22, 801–810.
Acid phosphatase activity in phosphorus-deficient white lupin roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFGnsr8%3D&md5=14e2572757afc4f8d441012c3bd9fe2fCAS |

Gowda C, Parthasarathy Rao P, Tripathi S, Gaur P, Deshmukh R (2009) Regional shift in chickpea production in India. In ‘Milestones in food legumes’. (Eds M Ali, S Kumar) pp. 21–35. (IIPR: Kanpur, India)

Graham PH, Temple SR (1984) Selection for improved nitrogen fixation in Glycine max (L.) Merr. and Phaseolus vulgaris L. Plant and Soil 82, 315–327.
Selection for improved nitrogen fixation in Glycine max (L.) Merr. and Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht1ykurw%3D&md5=c8d60813b8e40de29871d64966fea880CAS |

Hatayama R, Takahashi R, Ohshima M, Shibasaki B, Tokuyama T (2000) Ribulose-1,5-bisphosphate carboxylase/oxygenase from an ammonia-oxidizing bacterium, Nitrosomonas sp. K1: purification and properties. Journal of Bioscience and Bioengineering 90, 426–430.

Helal HM (1990) Varietal differences in root phosphatase activity as related to the utilization of organic phosphates. Plant and Soil 123, 161–163.
Varietal differences in root phosphatase activity as related to the utilization of organic phosphates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkvFKlsrg%3D&md5=de970a44e51f62ce6ac1c711146bf9ebCAS |

Hens M, Hocking P (2004) An evaluation of the phosphorus benefits from grain legumes in rotational cropping using 33P isotopic dilution. In ‘New directions for a diverse planet’. (Eds T Fischer, N Turner, J Angus, L McIntyre, M Robertson, A Borrell, D Lloyd) (The Regional Institute Ltd: Gosford, NSW) www.cropscience.org.au/icsc2004/poster/2/5/4/1190_hockingp.htm

Herridge DF, Pate JS (1977) Utilization of net photosynthate for nitrogen fixation and protein production in an annual legume. Plant Physiology 60, 759–764.
Utilization of net photosynthate for nitrogen fixation and protein production in an annual legume.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXkslKlsw%3D%3D&md5=67eb995c2f072bd4e080bfc715ade92dCAS |

Hinsinger H (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237, 173–195.
Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWlsQ%3D%3D&md5=a77ca3df64a9bbec83f05e7ae8cfcc56CAS |

Hufstetler EV, Boerma HR, Carter TE, Earl HJ (2007) Genotypic variation for three physiological traits affecting drought tolerance in soybean. Crop Science 47, 25–35.
Genotypic variation for three physiological traits affecting drought tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |

Hungria M, Neves MCP (1987) Cultivar and Rhizobium strain effect on nitrogen fixation and transport in Phaseolus vulgaris L. Plant and Soil 103, 111–121.
Cultivar and Rhizobium strain effect on nitrogen fixation and transport in Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXnt1WqsQ%3D%3D&md5=1554e0b181d0456724fef46130f214e7CAS |

Jackai LEN, Daoust RA (1986) Insect pests of cowpeas. Annual Review of Entomology 31, 95–119.
Insect pests of cowpeas.Crossref | GoogleScholarGoogle Scholar |

Jemo M, Abaidoo RC, Nolte C, Tchienkoua M, Sanginga N, Horst WJ (2006) Phosphorus benefits from grain-legume corps to subsequent maize grown on acid soils of southern Cameroon. Plant and Soil 284, 385–397.
Phosphorus benefits from grain-legume corps to subsequent maize grown on acid soils of southern Cameroon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntF2isbw%3D&md5=86c608302391c0132d344f4039dd2181CAS |

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.
Organic acid behavior in soils – misconceptions and knowledge gaps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqsro%3D&md5=3bb095819448cf15bea58317461997e8CAS |

Kerr RB, Snapp SS, Chirwa M, Shumba L, Msachi R (2007) Participatory research on legume diversification with Malawian smallholder farmers for improved human nutrition and soil fertility. Experimental Agriculture 43, 437–453.
Participatory research on legume diversification with Malawian smallholder farmers for improved human nutrition and soil fertility.Crossref | GoogleScholarGoogle Scholar |

Khan TN, Adhikari K, Siddique KHM, Garlinge J, Smith L, Morgan S, Boyd C (2009) Chickpea 2010 crop variety testing of germplasm developed by DAFWA/CLIMA/ICRISAT/COGGO alliance. Agribusiness Crop Updates 2010. Western Australian Agriculture Authority, Perth, Australia. pp. 9–12.

Klauer SF, Franceschi VR, Ku MSB, Zhang D (1996) Identification and localization of vegetative storage proteins in legume leaves. American Journal of Botany 83, 1–10.
Identification and localization of vegetative storage proteins in legume leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht1GisLg%3D&md5=a1553a533a95909bfa13b11649e9b1f9CAS |

Knights EJ, Southwell RJ, Schwinghamer MW, Harden S (2008) Resistance to Phytophthora medicaginis Hansen and Maxwell in wild Cicer species and its use in breeding root rot resistant chickpea (Cicer arietinum L.). Australian Journal of Agricultural Research 59, 383–387.
Resistance to Phytophthora medicaginis Hansen and Maxwell in wild Cicer species and its use in breeding root rot resistant chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |

Kornegay J, White JW, Ortiz Cruz O (1992) Growth habit and gene pool effects on inheritance of yield in common bean. Euphytica 62, 171–180.
Growth habit and gene pool effects on inheritance of yield in common bean.Crossref | GoogleScholarGoogle Scholar |

Krasilnikoff G, Gahoonia T, Nielsen NE (2003) Variation in phosphorus uptake efficiency by genotypes of cowpea (Vigna unguiculata) due to differences in root and root hair length and induced rhizosphere processes. Plant and Soil 251, 83–91.
Variation in phosphorus uptake efficiency by genotypes of cowpea (Vigna unguiculata) due to differences in root and root hair length and induced rhizosphere processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlKgtLY%3D&md5=ad0b5be0276bc215a5cd57bf5dcd37f4CAS |

Kueneman EA, Root WR, Dashiell KE, Hohenberg J (1984) Breeding soybeans for the tropics capable of nodulating effectively with indigenous Rhizobium spp. Plant and Soil 82, 387–396.
Breeding soybeans for the tropics capable of nodulating effectively with indigenous Rhizobium spp.Crossref | GoogleScholarGoogle Scholar |

Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693–713.
Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits.Crossref | GoogleScholarGoogle Scholar |

Lansing AJ, Franceschi VR (2000) The paraveinal mesophyll: a specialized path for intermediary transfer of assimilates in legume leaves. Australian Journal of Plant Physiology 17, 757–767.

Lauer MJ, Blevins DH, Sierzputowska-Gracz H (1989) 31P-nuclear magnetic resonance determinations of phosphate compartmentation in leaves of reproductive soybeans (Glycine max L.) as affected by phosphate nutrition. Plant Physiology 89, 1331–1336.
31P-nuclear magnetic resonance determinations of phosphate compartmentation in leaves of reproductive soybeans (Glycine max L.) as affected by phosphate nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXitFWmtLw%3D&md5=5bb7696af3b9f00c0af0ee619095fb6aCAS |

Lawn RJ (1989) Agronomic and physiological constraints to the productivity of tropical grain legumes and prospects for improvement. Experimental Agriculture 25, 509–528.
Agronomic and physiological constraints to the productivity of tropical grain legumes and prospects for improvement.Crossref | GoogleScholarGoogle Scholar |

Lawn RJ, Brun WA (1974) Symbiotic nitrogen fixation in soybean: I. Effect of photosynthetic source-sink manipulations. Crop Science 14, 11–16.
Symbiotic nitrogen fixation in soybean: I. Effect of photosynthetic source-sink manipulations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXkt1eis7k%3D&md5=fdfa4d3916d96085eb25f33636456351CAS |

Lee RB, Ratcliffe RG, Southon TE (1990) 31P NMR measurements of cytoplasmic and vacuolar Pi content of mature maize roots: relationships with phosphorus status and phosphate fluxes. Journal of Experimental Botany 41, 1063–1078.
31P NMR measurements of cytoplasmic and vacuolar Pi content of mature maize roots: relationships with phosphorus status and phosphate fluxes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVyns7s%3D&md5=b3212aa0a0e1515b933918595ef9cca1CAS |

Lemaire G, Jeuffroy M-H, Gastal F (2008) Diagnosis tool for plant and crop N status in vegetative stage. Theory and practices for crop N management. European Journal of Agronomy 28, 614–624.
Diagnosis tool for plant and crop N status in vegetative stage. Theory and practices for crop N management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktFClt70%3D&md5=e51df4444199c09e35075c7b79c0013bCAS |

Li H, Shen J, Zhang F, Marschner P, Cawthray G, Rengel Z (2010) Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil. Biology and Fertility of Soils 46, 79–91.
Phosphorus uptake and rhizosphere properties of intercropped and monocropped maize, faba bean, and white lupin in acidic soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktl2lsg%3D%3D&md5=d73f5037b646fc663c8f963c7cace419CAS |

Lugg DG, Sinclair TR (1981) Seasonal changes in photosynthesis of field grown soybean leaflets. 2. Relation to nitrogen content. Photosynthetica 15, 138–144.

Lynch JP (2007) Roots of the second Green Revolution. American Journal of Botany 55, 493–512.
Roots of the second Green Revolution.Crossref | GoogleScholarGoogle Scholar |

Lynch JP, Brown KM (2001) Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237, 225–237.
Topsoil foraging – an architectural adaptation of plants to low phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWltA%3D%3D&md5=d8d0e6a878c28e7632b50a5b4ad5275cCAS |

Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biology & Biochemistry 29, 881–888.
Regulation of oxygen diffusion in legume nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXks1WqsrY%3D&md5=1ae4d91ec19a92543069b0c442533f73CAS |

Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Romheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Annals of Botany 85, 909–919.
Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs12hu7o%3D&md5=ca9eec27a5cf1fb604f55dac0992f043CAS |

Nuruzzaman M, Lambers H, Bollard MDA, Veneklaas EJ (2005a) Phosphorus uptake by grain legumes and subsequently grown wheat at different levels of residual phosphorus fertiliser. Australian Journal of Agricultural Research 56, 1041–1047.
Phosphorus uptake by grain legumes and subsequently grown wheat at different levels of residual phosphorus fertiliser.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFChsLbE&md5=4a6366bb7db363550240fdbdc1c3777fCAS |

Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2005b) Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant and Soil 271, 175–187.
Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Ojt7g%3D&md5=3ce561cbc14aa5a035b1024a87d735bbCAS |

Nwoke OC, Diels J, Abaidoo R, Nziguheba G, Merckx R (2008) Organic acids in the rhizosphere and root characteristics of soybean (Glycine max) and cowpea (Vigna unguiculata) in relation to phosphorus uptake in poor savanna soils. African Journal of Biotechnology 7, 3620–3627.

Obaton M, Bouniols A, Piva G, Vadez V (2002) Are Bradyrhizobium japonicum stable during a long stay in soil. Plant and Soil 245, 315–326.
Are Bradyrhizobium japonicum stable during a long stay in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVGltrk%3D&md5=1a0a3020ee2779cfc371e635874371d8CAS |

Ohwaki Y, Hirata H (1992) Difference in the carboxylic acid exudation among P-starved leguminous crops in relation to carboxylic acid contents in plant tissues and phospholipid level in roots. Soil Science and Plant Nutrition 38, 235–243.
Difference in the carboxylic acid exudation among P-starved leguminous crops in relation to carboxylic acid contents in plant tissues and phospholipid level in roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvFSqsbY%3D&md5=5a4904ea5651cb4beb4a8e85f455a379CAS |

Pande S, Rao N (2001) Resistance of wild Arachis species to late leaf spot and rust in greenhouse trials. Plant Disease 85, 851–855.
Resistance of wild Arachis species to late leaf spot and rust in greenhouse trials.Crossref | GoogleScholarGoogle Scholar |

Perret X, Christian Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews 64, 180–201.
Molecular basis of symbiotic promiscuity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFygsr0%3D&md5=ffe8f03f6676b9082388574c0b0721a3CAS |

Piha MI, Munns DN (1987) Nitrogen fixation capacity of field-grown bean compared to other grain legumes. Agronomy Journal 79, 690–696.
Nitrogen fixation capacity of field-grown bean compared to other grain legumes.Crossref | GoogleScholarGoogle Scholar |

Purcell LC, Sinclair TR (1993) Soybean (Glycine max) nodule physical traits associated with permeability responses to oxygen. Plant Physiology 103, 149–156.

Purdue University (2012) Purdue Crop Cost & Return Guide. Purdue Extension ID-166-W. W. Lafayette, IN, USA

Rachie KO, Roberts LM (1974) Grain legumes of the lowland tropics. Advances in Agronomy 26, 1–132.
Grain legumes of the lowland tropics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXktVCrurY%3D&md5=f4113054eb0fe7631d29f3b8b2658e5fCAS |

Rao IM, Fredeen AL, Terry N (1993) Influence of phosphorus limitation on photosynthesis, carbon allocation and partitioning in sugar beet and soybean grown with a short photoperiod. Plant Physiology and Biochemistry 31, 223–231.

Robson RL, Postgate JR (1980) Oxygen and hydrogen in biological nitrogen fixation. Annual Review of Microbiology 34, 183–207.
Oxygen and hydrogen in biological nitrogen fixation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M%2FmtV2rsA%3D%3D&md5=6341ff79f5ab1ce3d406b1a2318b8fe7CAS |

Rodríguez-Navarro DN, Camacho M, Temprano F, Santamaria C, Leidi EO (2009) Assessment of nitrogen fixation potential in aphia (Pachyrhizus ahipa) and its effect on root and seed yield. Experimental Agriculture 45, 177–188.
Assessment of nitrogen fixation potential in aphia (Pachyrhizus ahipa) and its effect on root and seed yield.Crossref | GoogleScholarGoogle Scholar |

Roy MM, Singh KA (2008) The fodder situation in rural India: future outlook. International Forestry Review 10, 217–234.
The fodder situation in rural India: future outlook.Crossref | GoogleScholarGoogle Scholar |

Sanginga N, Okogun J, Vanlauwe B, Dashiell K (2002) The contribution of nitrogen by promiscuous soybeans to maize based cropping the moist savanna of Nigeria. Plant and Soil 241, 223–231.
The contribution of nitrogen by promiscuous soybeans to maize based cropping the moist savanna of Nigeria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltV2jsb4%3D&md5=be25b5024b757697f3619be0d7c9329fCAS |

Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447–453.
Phosphorus uptake by plants: from soil to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1ajtbc%3D&md5=a151c2da7fb1f0f25009a053e7756fb5CAS |

Serraj R, Sinclair TR, Purcell LC (1999a) Symbiotic N2 fixation response to drought. Journal of Experimental Botany 50, 143–155.

Serraj R, Vadez V, Purcell LC, Sinclair TR (1999b) Recent advances in the physiology of drought stress effects on symbiotic N2 fixation in soybean. In ‘Highlights of nitrogen fixation research’. (Eds F Matinez, G Hernandez) pp. 49–55. (Kluwer Academic/Plenum Publications: New York)

Shane MW, De Vos M, De Roock S, Lambers H (2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant, Cell & Environment 26, 265–273.
Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslOgur8%3D&md5=2deb34d1f5735f05b7a44696eede89e1CAS |

Shen H, Yan X, Zhao M, Zheng S, Wang X (2002) Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates. Environmental and Experimental Botany 48, 1–9.
Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVansrs%3D&md5=75ae0ab190091c04e56f5b9cb8f87376CAS |

Shiferaw BA, Kebede TA, You L (2008) Technology adoption under seed access constraints and the economic impacts of improved pigeonpea varieties in Tanzania. Agricultural Economics 39, 309–323.

Simpson CE, Starr JL (2001) Registration of ‘COAN’ peanut. Crop Science 41, 918
Registration of ‘COAN’ peanut.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR, deWit CT (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567.
Photosynthate and nitrogen requirements for seed production by various crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXltlSmurk%3D&md5=84d124ce49321e78ded9e4036242a000CAS |

Sinclair TR, Serraj R (1995) Legume nitrogen fixation and drought. Nature 378, 344
Legume nitrogen fixation and drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXps1anu70%3D&md5=566e34a89942c00a7176493f9f5a857aCAS |

Sinclair TR, Sinclair CJ (2010) ‘Bread, beer and the seeds of change: agriculture’s imprint on world history.’ (CAB International: Wallingford, UK)

Sinclair TR, Vadez V (2002) Physiological traits for crop yield improvement in low N and P environments. Plant and Soil 245, 1–15.
Physiological traits for crop yield improvement in low N and P environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCitro%3D&md5=87bb6b70e75af812d605a08d89e69e1bCAS |

Sinclair TR, Purcell LC, Vadez V, Serraj R, King CA, Nelson R (2000) Identification of soybean genotypes with N2 fixation tolerance to water deficits. Crop Science 40, 1803–1809.
Identification of soybean genotypes with N2 fixation tolerance to water deficits.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR, Zwieniecki MA, Nolbrook NM (2008) Low leaf hydraulic conductance associated with drought tolerance in soybean. Physiologia Plantarum 132, 446–451.
Low leaf hydraulic conductance associated with drought tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktb4%3D&md5=33d8bb93d04b9038b64012744a783c5cCAS |

Sinclair TR, Messina CD, Beatty A, Samples M (2010) Assessment across the United States of the benefits of altered soybean drought traits. Agronomy Journal 102, 475–482.
Assessment across the United States of the benefits of altered soybean drought traits.Crossref | GoogleScholarGoogle Scholar |

Singh KB, Robertson LD, Ocampo B (1998) Diversity for abiotic and biotic stress resistance in the wild annual Cicer species. Genetic Resources and Crop Evolution 45, 9–17.
Diversity for abiotic and biotic stress resistance in the wild annual Cicer species.Crossref | GoogleScholarGoogle Scholar |

Snapp SS, Silim SN (2002) Farmer preferences and legume intensification for low nutrient environments. Plant and Soil 245, 181–192.
Farmer preferences and legume intensification for low nutrient environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCit78%3D&md5=2ef83a25ef34bbd38537bb73132fda06CAS |

Snapp SS, Mafongoya PL, Waddington S (1998) Organic matter technologies to improve nutrient cycling in smallholder cropping systems of Southern Africa. Agriculture, Ecosystems & Environment 71, 185–200.
Organic matter technologies to improve nutrient cycling in smallholder cropping systems of Southern Africa.Crossref | GoogleScholarGoogle Scholar |

Snapp SS, Rohrback DD, Simtowe F, Freeman HA (2002) Sustainable soil management options for Malawi: can smallholder farmers grow more legumes? Agriculture, Ecosystems & Environment 91, 159–174.
Sustainable soil management options for Malawi: can smallholder farmers grow more legumes?Crossref | GoogleScholarGoogle Scholar |

Sperling L, Loevinsohn ME, Ntabomvura B (1993) Rethinking the farmer’s role in plant breeding: local bean experts and onstation selection in Rwanda. Experimental Agriculture 29, 509–519.
Rethinking the farmer’s role in plant breeding: local bean experts and onstation selection in Rwanda.Crossref | GoogleScholarGoogle Scholar |

Sundstøl F, Owen E (Eds) (1984) ‘Straw and other fibrous by-products as feed.’ (Elsevier: Amsterdam)

Tang C (1998) Factor affecting soil acidification under legumes. I. Effect of potassium supply. Plant and Soil 199, 275–282.
Factor affecting soil acidification under legumes. I. Effect of potassium supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjslOns7g%3D&md5=b3c8d879ef411191e52e6585c76490e5CAS |

Tanner CB, Sinclair TR (1983) Efficient water use in crop production: Research or re-search? In ‘Limitations to efficient water use in crop’. (Eds HM Taylor, WR Jordan, TR Sinclair) pp. 1–27. (American Society of Agronomy: Madison, WI)

Tjepkema JD, Yocum CS (1974) Measurement of oxygen partial pressure within soybean nodules by oxygen microelectrode. Planta 119, 351–360.
Measurement of oxygen partial pressure within soybean nodules by oxygen microelectrode.Crossref | GoogleScholarGoogle Scholar |

Tropical Legumes (1979) ‘Tropical legumes: resources for the future.’ (National Academy of Sciences: Washington, DC)

Upadhyaya HD, Ortiz R (2001) A mini-core subset for capturing diversity and promoting utilization of chickpea genetic resources in crop improvement. Theoretical and Applied Genetics 102, 1292–1298.
A mini-core subset for capturing diversity and promoting utilization of chickpea genetic resources in crop improvement.Crossref | GoogleScholarGoogle Scholar |

Vadez V, Sinclair TR, Serraj R (2000) Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean. Physiologia Plantarum 110, 215–223.
Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt1Cntbo%3D&md5=c02df021f9167c3b4c3fdb99a92b7564CAS |

Van Soest PJ (1994) ‘Nutritional ecology of the ruminant.’ 2nd edn. (Cornell University Press: Ithaca, NY)

Walsh KB, McCully ME, Canny MJ (1989) Vascular transport and soybean nodule function: nodule xylem is a blind alley, not a throughway. Plant, Cell & Environment 12, 395–405.
Vascular transport and soybean nodule function: nodule xylem is a blind alley, not a throughway.Crossref | GoogleScholarGoogle Scholar |

Wang L, Liao H, Yan X, Zhuang B, Dong Y (2004) Genetic variability for root hair traits as related to phosphorus status in soybean. Plant and Soil 261, 77–84.
Genetic variability for root hair traits as related to phosphorus status in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVehtLY%3D&md5=0846373e87e3597cf1f29935d38ba3feCAS |

Wittenbach VA, Ackerson RC, Giaquinta RT, Hebert RR (1980) Changes in photosynthesis, ribulose biosphosphate carboxylase, proteolytic activity, and ultrastructure of soybean leaves during senescence. Crop Science 20, 225–231.
Changes in photosynthesis, ribulose biosphosphate carboxylase, proteolytic activity, and ultrastructure of soybean leaves during senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWlu7w%3D&md5=fa44917a49d4cedae233c710d944c09dCAS |

Yan X, Liao H, Beebe SE, Blair MW, 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.
QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXns12ltg%3D%3D&md5=19747913fa3527ff9e456e1881c895abCAS |

Zaman-Allah M, Jenkinson D, Vadez V (2011a) Chickpea genotypes contrasting for seed yield under terminal drought stress in the field differ for traits related to the control of water use. Functional Plant Biology 38, 270–281.
Chickpea genotypes contrasting for seed yield under terminal drought stress in the field differ for traits related to the control of water use.Crossref | GoogleScholarGoogle Scholar |

Zaman-Allah M, Jenkinson D, Vadez V (2011b) A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea. Journal of Experimental Botany 62, 4239–4252.
A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVeit7jJ&md5=8b50735efc55be793b63081206a06fbdCAS |