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RESEARCH ARTICLE

Root exudation index: screening organic acid exudation and phosphorus acquisition efficiency in soybean genotypes

Vengavasi Krishnapriya A and Renu Pandey A B
+ Author Affiliations
- Author Affiliations

A Division of Plant Physiology, ICAR–Indian Agricultural Research Institute, New Delhi 110012, India.

B Corresponding author. Email: renu_iari@rediffmail.com

Crop and Pasture Science 67(10) 1096-1109 https://doi.org/10.1071/CP15329
Submitted: 28 September 2015  Accepted: 3 August 2016   Published: 13 September 2016

Abstract

High-molecular-weight secretory proteins and low-molecular-weight exudates (carboxylates, phenols, free amino acids and sugars) released from roots of soybean (Glycine max (L.) Merr.) differentially influence genotypic phosphorus (P) acquisition efficiency (PAE). We hypothesised that genotypes with higher root exudation potential would exhibit enhanced P acquisition, and screened 116 diverse soybean genotypes by labelling shoots with 14CO2. A root exudation index (REI) derived from total 14C in the root exudate at sufficient (250 μm) and low (4 μm) P levels was used to classify genotypes for PAE. Genotypes with REI >2.25 exhibited significantly higher exudation at low than at sufficient P, which in turn increased PAE. Under low P availability, efficient genotypes exude a greater quantity of organic compounds into the rhizosphere. This increases P availability to meet the crop requirement, enabling the crop to produce consistent biomass and seed yield with reduced fertiliser addition. Such maintenance of growth and yield potential by mining the inherent soil P is a favourable trait in genotypes, reducing dependence on P fertilisers. Measuring REI at seedling stage to select P-efficient plants accelerates the screening process by accommodating large numbers of genotypes.

Additional keywords: 14C labelling, cluster analysis, genotype × trait interaction, HPLC, hydroponic culture.


References

Adhya TP, Kumar N, Reddy G, Podile AR, Bee H, Samantaray B (2015) Microbial mobilization of soil phosphorus and sustainable P management in agricultural soils. Current Science 108, 1280–1287.

Ainsworth EA, Yendrek CR, Skoneczka JA, Long SP (2012) Accelerating yield potential in soybean: potential targets for biotechnological improvement. Plant, Cell & Environment 35, 38–52.
Accelerating yield potential in soybean: potential targets for biotechnological improvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvVWht78%3D&md5=3a2db6b071c633954dba2a1f6b4e5fadCAS |

Akhtar MS, Oki Y, Adachi T (2008) Genetic diversity of Brassica cultivars in relation to phosphorus uptake and utilization efficiency under P-stress environment. Archives of Agronomy and Soil Science 54, 93–108.
Genetic diversity of Brassica cultivars in relation to phosphorus uptake and utilization efficiency under P-stress environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovFGjtg%3D%3D&md5=1f209392e388d8f5bea5ae69a49d74dbCAS |

Assuero SG, Mollier A, Pellerin S (2004) The decrease in growth of phosphorus-deficient maize leaves is related to a lower cell production. Plant, Cell & Environment 27, 887–895.
The decrease in growth of phosphorus-deficient maize leaves is related to a lower cell production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1ygtbs%3D&md5=8f631bac19308a4f24d50e51bfcf1d43CAS |

Bayuelo-Jiménez JS, Gallardo-Valdez M, Perez-Decelis VA, Magdaleno-Armas L, Ochoa I, Lynch JP (2011) Genotypic variation for root traits of maize (Zea mays L.) from the Purhepecha Plateau under contrasting phosphorus availability. Field Crops Research 121, 350–362.
Genotypic variation for root traits of maize (Zea mays L.) from the Purhepecha Plateau under contrasting phosphorus availability.Crossref | GoogleScholarGoogle Scholar |

Bray HG, Thorpe WV (1954) Analysis of phenolic compounds of interest in metabolism. Methods of Biochemical Analysis 1, 27–52.
Analysis of phenolic compounds of interest in metabolism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2M%2FgsFWjsQ%3D%3D&md5=112fc4ef416116c6d63de958e61e6a4bCAS | 13193524PubMed |

Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M-R, Borriss R, von Wiren N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Journal of Plant Nutrition and Soil Science 174, 3–11.
Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFGrs7o%3D&md5=b616262ec96ad3830c1f180776418e8eCAS |

Chaudhary MI, Adu-Gyamfi JJ, Saneoka H, Nguyen NT, Suwa R, Kanai S, El-Shemy HA, Lightfoot DA, Fujita K (2008) The effect of phosphorus deficiency on nutrient uptake, nitrogen fixation and photosynthetic rate in mashbean, mungbean and soybean. Acta Physiologiae Plantarum 30, 537–544.
The effect of phosphorus deficiency on nutrient uptake, nitrogen fixation and photosynthetic rate in mashbean, mungbean and soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitV2jtrg%3D&md5=a54ec7c8c85ecc6dd2881c286ff4616fCAS |

Chen YL, Dunbabin VM, Diggle AJ, Siddique KHM, Rengel Z (2013) Phosphorus starvation boosts carboxylate secretion in P-deficient genotypes of Lupinus angustifolius with contrasting root structure. Crop & Pasture Science 64, 588–599.
Phosphorus starvation boosts carboxylate secretion in P-deficient genotypes of Lupinus angustifolius with contrasting root structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlyqurvP&md5=58c2346359e8709a16b14b2e61bb87cbCAS |

Cheng L, Tang X, Vance CP, White PJ, Zhang F, Shen J (2014) Interactions between light intensity and phosphorus nutrition affect the phosphate-mining capacity of white lupin (Lupinus albus L.). Journal of Experimental Botany 65, 2995–3003.
Interactions between light intensity and phosphorus nutrition affect the phosphate-mining capacity of white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar | 24723402PubMed |

Cordell D, White S (2011) Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus scarcity. Sustainability 3, 2027–2049.
Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus scarcity.Crossref | GoogleScholarGoogle Scholar |

Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245, 35–47.
Root exudates as mediators of mineral acquisition in low-nutrient environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCit70%3D&md5=1be19daccb1ee02a3ea77f33430631daCAS |

de Sousa SM, Clark RT, Mendes FF, de Oliveira AC, de Vasconcelos MJV, Parentoni SN, Kochian LV, Guimaraes CT, Magalhaes JV (2012) A role for root morphology and related candidate genes in P acquisition efficiency in maize. Functional Plant Biology 39, 925–935.
A role for root morphology and related candidate genes in P acquisition efficiency in maize.Crossref | GoogleScholarGoogle Scholar |

Dingkuhn M, Luquet D, Kim HK, Tambour L, Clement-Vidal A (2006) EcoMeristem, a model of morphogenesis and competition amog sinks in rice. 2. Simulating genotype responses to phosphorus deficiency. Functional Plant Biology 33, 325–337.
EcoMeristem, a model of morphogenesis and competition amog sinks in rice. 2. Simulating genotype responses to phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVOmu7o%3D&md5=273d48fdbbd6f2959aa98faa3b86f00fCAS |

Dong D, Peng X, Yan X (2004) Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiologia Plantarum 122, 190–199.
Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVyns7g%3D&md5=dd5f94dfb489088f9f9741cdff21e59bCAS |

Drouillon M, Merckx R (2003) The role of citric acid as a phosphorus mobilization mechanism in highly P-fixing soils. Gayana Botánica 60, 55–62.

Fageria NK, Baligar VC (1999) Phosphorus-use efficiency in wheat genotypes. Journal of Plant Nutrition 22, 331–340.
Phosphorus-use efficiency in wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlGhsL8%3D&md5=6c2a8360f2572bd8fc4d83f46e3b5869CAS |

FAO (2015) Production quantities by country. FAO STAT. Food and Agriculture Organization of the United Nations. Available at: http://faostat3.fao.org/browse/Q/QC/E (accessed 25 July 2015).

Fernández MC, Belinque H, Gutierrez Boem FH, Rubio G (2009) Compared phosphorus efficiency in soybean, sunflower and maize. Journal of Plant Nutrition 32, 2027–2043.
Compared phosphorus efficiency in soybean, sunflower and maize.Crossref | GoogleScholarGoogle Scholar |

Fess TL, Kotcon JB, Benedito VA (2011) Crop breeding for low input agriculture: a sustainable response to feed a growing world population. Sustainability 3, 1742–1772.
Crop breeding for low input agriculture: a sustainable response to feed a growing world population.Crossref | GoogleScholarGoogle Scholar |

Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89, 225–230.
Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtFelur0%3D&md5=f3fec2b7434373c9572c657772b27f97CAS | 16666518PubMed |

Gahoonia TS, Asmar F, Giese H, Gissel-Nielsen G, Nielsen NE (2000) Root-released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments. European Journal of Agronomy 12, 281–289.
Root-released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvFKnt7k%3D&md5=23b0bade966ed9c95e072ed25d6a34feCAS |

Gan Y, Stulen I, van Keulen H, Kuiper PJC (2002) Physiological changes in soybean (Glycine max) Wuyin9 in response to N and P nutrition. Annals of Applied Biology 140, 319–329.
Physiological changes in soybean (Glycine max) Wuyin9 in response to N and P nutrition.Crossref | GoogleScholarGoogle Scholar |

Gill HS, Singh A, Sethi SK, Behl RK (2004) Phosphorus uptake and use efficiency in different varieties of bread wheat (Triticum aestivum L.). Archives of Agronomy and Soil Science 50, 563–572.
Phosphorus uptake and use efficiency in different varieties of bread wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOmsrjO&md5=e0991b46f9f120e63c5e51a2134e7d8dCAS |

Goldsmith PD (2008) Economics of soybean production, marketing and utilization. In ‘Soybeans chemistry, production, processing and utilization’. (Eds LP Johnson, PA White, R Galloway) pp. 117–150. (AOCS Press: Urbana, IL, USA)

Guppy CN, Menzies NW, Moody PW, Blamey FPC (2005) Competitive sorption reactions between phosphorus and organic matter in soil: a review. Australian Journal of Soil Research 43, 189–202.
Competitive sorption reactions between phosphorus and organic matter in soil: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVOju78%3D&md5=cd17f131484f4457b3700f2b1f6b743dCAS |

Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, Hayden R, Meacham MC, Mead A, Overs T, Spracklen WP, Greenwood DJ (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. Journal of Experimental Botany 60, 1953–1968.
Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSjtbY%3D&md5=e2994b9189114782e4d4e926e9654900CAS | 19346243PubMed |

Hedge JE, Hofreiter BT (1962) Determination of total carbohydrate by anthrone method. In ‘Carbohydrates chemistry’. (Eds RL Whistler, JN BeMiller) p. 17. (Academic Press: New York)

Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant and Soil 248, 43–59.
Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqsr8%3D&md5=9850d141f87918055ebf244f72a76935CAS |

Hocking PJ, Randall PJ, Delhaize E, Keerthisinghe G (2000) The role of organic acids exuded from roots in phosphorus nutrition and aluminium tolerance in acidic soils. IAEA-TECDOC 1159, 61–70.

Hu H, Tang C, Rengel Z (2005) Role of phenolics and organic acids in phosphorus mobilization in calcareous and acidic soils. Journal of Plant Nutrition 28, 1427–1439.
Role of phenolics and organic acids in phosphorus mobilization in calcareous and acidic soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVSlsbrF&md5=d552180725aaf42ad3cbc9f3a8406088CAS |

Hu Y, Ye X, Shi L, Duan H, Xu F (2010) Genotypic differences in root morphology and phosphorus uptake kinetics in Brassica napus under low phosphorus supply. Journal of Plant Nutrition 33, 889–901.
Genotypic differences in root morphology and phosphorus uptake kinetics in Brassica napus under low phosphorus supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkt1Wqur0%3D&md5=1ddf4a7a145226e34d50e0000626a4adCAS |

Ishikawa S, Adu-Gyamfi JJ, Nakamura T, Yoshihara T, Watanabe T, Wagatsuma T (2002) Genotypic variability in phosphorus solubilizing activity of root exudates by pigeon pea grown in low-nutrient environments. Plant and Soil 245, 71–81.
Genotypic variability in phosphorus solubilizing activity of root exudates by pigeon pea grown in low-nutrient environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVCitrk%3D&md5=8a51e421ab35105e25b0e8c891f414dcCAS |

Juszczuk IM, Wiktorowska A, Malusa E, Rychter AM (2004) Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.). Plant and Soil 267, 41–49.
Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1WktLc%3D&md5=68ebddbb714cfefb8f00424f3f6eea94CAS |

Kochian LV (2012) Rooting for more phosphorus. Nature 488, 466–467.
Rooting for more phosphorus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1emtL3F&md5=8502fd251112db429cbca9956b931111CAS | 22914160PubMed |

Krishnappa R, Aftab Hussain IS (2014) Phosphorus acquisition form deficient soil: involvement of organic acids and acid phosphatase in pigeon pea (Cajanus cajan L. mill sp). Indian Journal of Plant Physiology / Official Publication of the Indian Society for Plant Physiology 19, 197–204.
Phosphorus acquisition form deficient soil: involvement of organic acids and acid phosphatase in pigeon pea (Cajanus cajan L. mill sp).Crossref | GoogleScholarGoogle Scholar |

Lauer MJ, Pallardy SG, Blevins DG, Randall DD (1989) Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.). Plant Physiology 91, 848–854.
Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlsVehtA%3D%3D&md5=c728b84025113ad3ee7c33369f4858adCAS | 16667147PubMed |

Li M, Osaki M, Rao IM, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant and Soil 195, 161–169.
Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions.Crossref | GoogleScholarGoogle Scholar |

Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminium interactions in soybean in relation to aluminium tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiology 141, 674–684.
Phosphorus and aluminium interactions in soybean in relation to aluminium tolerance. Exudation of specific organic acids from different regions of the intact root system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aktLg%3D&md5=e01579d26540a21541b8a66dfca7aa6fCAS | 16648222PubMed |

Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiology 85, 315–317.
Citrate, malate and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjs1Sk&md5=f3c4411be2bec9d1aa50ad919b228fe0CAS | 16665693PubMed |

López-Arrendondo DL, Levya-Gonzalez MA, Gonzalez-Morales SI, Lopez-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: Improving low-phosphate tolerance in crops. Annual Review of Plant Biology 65, 95–123.
Phosphate nutrition: Improving low-phosphate tolerance in crops.Crossref | GoogleScholarGoogle Scholar |

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. The Journal of Biological Chemistry 193, 265–275.

Moore S, Stein WH (1948) Polyphenol oxidase. In ‘Methods in enzymology’. (Eds SP Colowick, ND Kaplan) p. 468. (Academic Press: New York)

Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
A modified single solution method for the determination of phosphate in natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XksVyntr8%3D&md5=2c9787ac088fa6769fd44abefc9a362bCAS |

Ohwaki Y, Hirata H (1992) Differences in 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.
Differences in 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=1ee648a81e6987cbf3ac4fc64b8a7d9bCAS |

Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA circular. pp. 939.

Orf J (2010) Introduction. In ‘Genetics, genomics and breeding of soybean’. (Eds K Bilyeu, MB Ratnaparkhe, C Kole) pp. 1–18. (Science Publishers: New York)

Osborne LD, Rengel Z (2002) Screening cereals for genotypic variation in efficiency of phosphorus uptake and utilization. Crop & Pasture Science 53, 295–303.
Screening cereals for genotypic variation in efficiency of phosphorus uptake and utilization.Crossref | GoogleScholarGoogle Scholar |

Pandey R, Krishnapriya V, Kishora N, Singh SB, Singh B (2013) Shoot labelling with 14CO2: a technique for assessing total root carbon exudation under phosphorus stress. Indian Journal of Plant Physiology / Official Publication of the Indian Society for Plant Physiology 18, 250–262.
Shoot labelling with 14CO2: a technique for assessing total root carbon exudation under phosphorus stress.Crossref | GoogleScholarGoogle Scholar |

Qiu J, Israel DW (1994) Carbohydrate accumulation and utilization in soybean plants in response to altered phosphorus nutrition. Physiologia Plantarum 90, 722–728.
Carbohydrate accumulation and utilization in soybean plants in response to altered phosphorus nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFChurY%3D&md5=e0ac3b4d79e8e23cce95389035d70239CAS |

Rodríguez D, Pomar MC, Goudriaan J (1998) Leaf primordial initiation, leaf emergence and tillering in wheat (Triticum aestivum L.) grown under low-phosphorus conditions. Plant and Soil 202, 149–157.
Leaf primordial initiation, leaf emergence and tillering in wheat (Triticum aestivum L.) grown under low-phosphorus conditions.Crossref | GoogleScholarGoogle Scholar |

Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic acid exudation from plant roots. Annual Review of Plant Physiology and Molecular Biology 52, 527–560.
Function and mechanism of organic acid exudation from plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgsbg%3D&md5=04fa74c1f3e545175fc8cb97f1843f1fCAS |

Scaboo AM, Chen P, Sleper DA, Clark KM (2010) Classical breeding and genetics of soybean. In ‘Genetics, genomics and breeding of soybean’. (Eds K Bilyeu, MB Ratnaparkhe, C Kole) pp. 19–54. (Science Publishers: New York)

Singh B, Pandey R (2003) Differences in root exudation among phosphorus-starved genotypes of maize and green gram and its relationship with phosphorus uptake. Journal of Plant Nutrition 26, 2391–2401.
Differences in root exudation among phosphorus-starved genotypes of maize and green gram and its relationship with phosphorus uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotlSisLk%3D&md5=ef79595c55b823ef42249dbffc1226e2CAS |

Singh B, Ahuja S, Pandey R, Singhal RK (2014) 14CO2 labeling: a reliable technique for rapid measurement of total root exudation capacity and vascular sap flow in crop plants. Journal of Radioanalytical and Nuclear Chemistry 302, 1315–1320.
14CO2 labeling: a reliable technique for rapid measurement of total root exudation capacity and vascular sap flow in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVyrtLjN&md5=adefcff9494615cdbca926bde06b6b8bCAS |

Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environmental and Experimental Botany 67, 228–234.
Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.].Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2qs7vK&md5=f51965e1290dee1541e471244205bf88CAS |

Tsvetkova GE, Georgiev GI (2003) Effect of phosphorus nutrition on the nodulation, nitrogen fixation and nutrient use efficiency of Bradyrhizobium japonicum-soybean (Glycine max L. Merr.) symbiosis. Bulgarian Journal of Plant Physiology 2003, 331–335.

Valizadeh GR, Rengel Z, Rate AW (2002) Wheat genotypes differ in growth and phosphorus uptake when supplied with different sources and rates of phosphorus banded or mixed in soil in pots. Australian Journal of Experimental Agriculture 42, 1103–1111.
Wheat genotypes differ in growth and phosphorus uptake when supplied with different sources and rates of phosphorus banded or mixed in soil in pots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlt1amtQ%3D%3D&md5=c3676650af6c691ad723928ff633188fCAS |

Vandamme E, Renkens M, Pypers P, Smolders E, Vanlauwe B, Merckx R (2013) Root hairs explain P uptake efficiency in soybean genotypes grown in a P-deficient Ferralsol. Plant and Soil 369, 269–282.
Root hairs explain P uptake efficiency in soybean genotypes grown in a P-deficient Ferralsol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVyqtrzL&md5=eb247500f54c8dcb14eeaba8eb01cc81CAS |

Wang X, Wang Y, Tian J, Lim BL, Yan X, Liao H (2009) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiology 151, 233–240.
Overexpressing AtPAP15 enhances phosphorus efficiency in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOjsbzF&md5=d8dbe8b9949d57b747b0025053606ddfCAS | 19587103PubMed |

Wang X, Yan X, Liao H (2010) Genetic improvement for phosphorus efficiency in soybean: a radical approach. Annals of Botany 106, 215–222.
Genetic improvement for phosphorus efficiency in soybean: a radical approach.Crossref | GoogleScholarGoogle Scholar | 20228090PubMed |

Wissuwa M, Ae N (2001) Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breeding 120, 43–48.
Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitleqsbs%3D&md5=efbf2e5a1a86e0a3db0c6db164950304CAS |

Zhao J, Fu J, Liao H, He Y, Nian H, Hu Y, Qiu L, Dong Y, Yan X (2004) Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chinese Science Bulletin 49, 1611–1620.
Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFyhsb0%3D&md5=d92cc96eba36c2441e07f011dde70600CAS |