Skip to main content
SpringerLink
Log in

Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Incorporating soybean (Glycine max) genotypes with a high nitrogen fixation potential into cropping systems can sustainably improve the livelihoods of smallholder farmers in Western Kenya. Nitrogen fixation is, however, often constrained by low phosphorus (P) availability. The selection of soybean genotypes for increased P efficiency could help to overcome this problem. This study investigated the contribution of different root traits to variation in P efficiency among soybean genotypes.

Methods

Eight genotypes were grown in a Ferralsol amended with suboptimal (low P) and optimal (high P) amounts of soluble P. Root hair growth was visualized by growing plants in a novel agar system where P intensity was buffered by Al2O3 nanoparticles.

Results

In the pot trial, P uptake was unaffected among the genotypes at high P but differed about 2-fold at low P. The genotypes differed in P uptake efficiency but not in P utilization efficiency. Regression analysis and mechanistic modeling indicated that P uptake efficiencies were to a large extent related to root hair development (length and density) and, to a lower extent, to colonization by mycorrhizal fungi.

Conclusion

Breeding for improved root hair development is a promising way to increase P uptake efficiency in soybean.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AMF:

Arbuscular mycorrhizal fungi

DAP:

Days after planting

IITA:

International Institute of Tropical Agriculture

MP:

Maturity period

TSBF-CIAT:

Tropical Soil Biology and Fertility Institute of the International Center for Tropical Agriculture

References

  • Barber SA (1984) Soil nutrient bioavailability. John Wiley & Sons Inc, New York

    Google Scholar 

  • Barraclough PB, Tinker PB (1981) The determination of ionic diffusion coefficients in field soils I. Diffusion coefficients in sieved soils in relation to water content and bulk density. J Soil Sci 32:225–236

    Article  CAS  Google Scholar 

  • Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Soil 19:529–538

    CAS  Google Scholar 

  • Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132:281–288

    Article  PubMed  CAS  Google Scholar 

  • Brundrett MC, Piche Y, Peterson RL (1984) A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can J Bot 62:2128–2134

    Article  Google Scholar 

  • Cardoso IM, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agric Ecosyst Environ 116:72–84

    Article  Google Scholar 

  • Chhabra R, Pleysier J, Cremers A (1975) The measurement of cation exchange capacity and exchangeable cations in soil: a new method. In: Proceedings of the International Clay Conference. Applied publishing Ltd., Wilmette, Illinions, pp 433–499

  • Claassen N (1990) Nährstoffaufname höherer Pflanzen aus dem Boden als Ergebnis von Verfügbarkeit und Aneignungsvermögen. Severin-Verlag, Göttingen

    Google Scholar 

  • Claassen N, Steingrobe B (1999) Mechanistic simulation models for a better understanding of nutrient uptake from soil. In: Rengel Z, Binghamto NY (ed) Mineral Nutrition of Crops: Fundamental Mechanisms and Implications. The Haworth Press, Inc, pp 327–367

  • Day P (1965) Particle fractioning and particle size analysis. In: Black C et al (eds) Methods of Soil Analysis, Part 1. ASA, Madison, pp 545–562

    Google Scholar 

  • Dechassa N, Schenk MK, Claassen N, Steingrobe B (2003) Phosphorus Efficiency of Cabbage (Brassica oleraceae L. var. capitata), Carrot (Daucus carota L.), and Potato (Solanum tuberosum L.). Plant Soil 250:215–224

    Article  CAS  Google Scholar 

  • Edwards OW, Huffman EO (1959) Diffusion of aqueous solutions of phosphoric acid at 25°C. J Phys Chem 63:1830–1833

    Article  CAS  Google Scholar 

  • FAO-ISRIC-ISSS (1998) World reference base for soil resources. World Soil Resources Report 84. FAO, Rome

    Google Scholar 

  • Fernández MC, Belinque H, Boem FHG, Rubio G (2009) Compared Phosphorus Efficiency in soybean, sunflower and maize. J Plant Nutr 32:2027–2043

    Article  Google Scholar 

  • Föhse D, Jungk A (1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74:359–368

    Article  Google Scholar 

  • Föhse D, Claassen N, Jungk A (1988) Phosphorus efficiency of plants. I, External and internal P requirement and P uptake efficiency of different plant species. Plant Soil 110:101–109

    Article  Google Scholar 

  • Föhse 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 Soil 132:261–272

    Google Scholar 

  • Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68

    Article  CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant Soil 198:147–152

    Article  CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE (2004a) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant Soil 262:55–62

    Article  CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE (2004b) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260:47–57

    Article  Google Scholar 

  • Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant Soil 191:181–188

    Article  CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE, Lyshede OB (1999) Phosphorus (P) acquisition of cereal cultivars in the field at three levels of P fertilization. Plant Soil 211:269–281

    Article  CAS  Google Scholar 

  • Itoh S, Barber SA (1983) Phosphorus uptake by six plant species as related to root hairs. Agron J 75:457–461

    Article  Google Scholar 

  • Jungk A, Asher CJ, Edwards DG, Meyer D (1990) Influence of phosphate status on phosphate uptake kinetics of maize (Zea mays) and soybean (Glycine max). Plant Soil 124:175–182

    Article  CAS  Google Scholar 

  • Kirk GJD (2002) Use of modelling to understand nutrient acquisition by plants. Plant Soil 247:123–130

    Article  CAS  Google 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. Ann Bot 98:693–713

    Article  PubMed  Google Scholar 

  • Lynch JP (2007) Roots of the Second Green Revolution. Aust J Bot 55:493–512

    Article  Google Scholar 

  • Nwoko H, Sanginga N (1999) Dependence of promiscuous soybean and herbaceous legumes on arbuscular mycorrhizal fungi and their response to bradyrhizobial inoculation in low P soils. Appl Soil Ecol 13:251–258

    Google Scholar 

  • Nye PH, Mariott FC (1969) A theoretical study of the distribution of substances around roots resulting from simultaneous diffusion and mass flow. Plant Soil 30:459–472

    Article  Google Scholar 

  • Osborne L, Rengel Z (2002) Screening cereals for genotypic variation in efficiency of phosphorus uptake and utilisation. Aust J Agr Res 53:295–303

    Article  Google Scholar 

  • Ozanne PG, Shaw TC (1968) Advantages of the recently developed phosphate sorption test over older extractant methods for soil phosphate. Trans 9th Int Congr. Soil Sci 2:273–280

    CAS  Google Scholar 

  • Pan X, Li W, Zhang Q, Li Y, Liu M (2008) Assessment on Phosphorus Efficiency Characteristics of Soybean Genotypes in Phosphorus-Deficient Soils. Agr Sci China:958–969

  • Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331:241–255

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedure for cleaning roots and staining parasitic and Vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc 5:158–161

    Article  Google Scholar 

  • Pypers P (2006) Isotopic approaches to characterize P availability and P acquisition by maize and legumes in highly weathered soils. PhD dissertation, Katholieke Universiteit Leuven

  • Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crop Res 117:169–176

    Article  Google Scholar 

  • Rao IM, Borrero V, Ricaurte J, Garcia R, Ayarza MA (1996) Adaptive attributes of tropical forage species to acid soils. II. Differences in shoot and root growth responses to varying phosphorus supply and soil type. J Plant Nutr 19:323–352

    Article  CAS  Google Scholar 

  • Rao IM, Borrero V, Ricaurte J, Garcia R, Ayarza MA (1997) Adaptive attributes of tropical forage species to acid soils. III. Differences in phosphorus acquisition and utilization as influenced by varying phosphorus supply and soil type. J Plant Nutr 20:155–180

    Article  CAS  Google Scholar 

  • Sanginga N (2003) Role of biological nitrogen fixation in legume based cropping systems; a case study of West Africa farming systems. Plant Soil 252:25–39

    Article  CAS  Google Scholar 

  • Sanginga N, Okogun JA, Akobundu IO, Kang BT (1996) Phosphorus requirement and nodulation of herbaceous and shrub legumes in low P soils of a Guinean savanna in Nigeria. Appl Soil Ecol 3:247–255

    Article  Google Scholar 

  • Santner J, Smolders E, Wenzel W, Degryse F (2012) First observation of diffusion-limited plant root phosphorus uptake from nutrient. Plant Cell Environ 35:1558–1566

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute Inc (2012) SAS/STAT 9.3 User’s Guide, 2nd edn. SAS Institute Inc, Cary

    Google Scholar 

  • Schroeder MS, Janos DP (2005) Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density. Mycorrhiza 15:203–216

    Article  PubMed  CAS  Google Scholar 

  • Schwertmann U (1964) Differenzierung der eisen-oxide des bodens durch photochemische extraktion mit sauer ammonium oxalat-lösung. Z Pflanz Bodenkunde 105:194–202

    Article  CAS  Google Scholar 

  • Sibbesen E (1983) Phosphate soil tests and their suitability to assess the phosphate status of the soil. J Sci Food Agric 34:1368–1974

    Article  CAS  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  PubMed  CAS  Google Scholar 

  • Van Veldhoven PP, Mannaerts GP (1987) Inorganic and organic phosphate measurements in the nanomolar range. Anal Biochem 161:45–48

    Article  PubMed  Google Scholar 

  • Vanlauwe B, Bationo A, Chianu J, Giller KE, Merckx R, Mokwunye U, Ohiokpehai O, Pypers P, Tabo R, Shepherd KD, Smaling EMA, Woomer PL, Sanginga N (2010) Integrated soil fertility management. Operational definition and consequences for implementation and dissemination. Outlook Agr 39:17–24

    Article  Google 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 Soil 261:77–84

    Google Scholar 

  • Wang X, Yan X, Liao H (2010) Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann Bot 106:215–222

    Article  PubMed  Google Scholar 

  • Williams RF (1948) The effect of phosphorus supply on the rates of intake of phosphorus and nitrogen upon certain aspects of phosphorus metabolism in gramineous plants. Austr J Biol Sci 1:333–361

    Google Scholar 

  • Wissuwa M (2003) How do plants achieve tolerance to phosphorus deficiency? Small causes with Big effects. Plant Physiol 133:1947–1958

    Article  PubMed  CAS  Google Scholar 

  • 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 Soil 265:17–29

    Article  CAS  Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol R 63:968–989

    CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Philip Malala, Magdalene Mutia and Purity Nduku for their valuable help during greenhouse work and Nyawira Lukey for carrying out analyses on mycorrhizal colonization. We are also grateful to the team of the TSBF-CIAT Maseno for their assistance with soil sampling, and to Jan Diels for his expert advice on statistical analysis. Marian Renkens acknowledges a travel grant from the University Development Cooperation of the Flemish Interuniversity Council (VLIR-UDC). Elke Vandamme acknowledges a VLIR-UDC PhD scholarship.

Author information

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, Division Soil and Water Management, KU Leuven, Kasteelpark Arenberg 20, 3001, Leuven, Belgium

    E. Vandamme, M. Renkens, P. Pypers, E. Smolders & R. Merckx

  2. TSBF-CIAT (Tropical Soil Biology and Fertility Institute of CIAT), P.O. Box 30677, Nairobi, Kenya

    P. Pypers

  3. IITA (International Institute of Tropical Agriculture), P.O. Box 30772, Nairobi, Kenya

    B. Vanlauwe

Authors
  1. E. Vandamme
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Renkens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Pypers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Smolders
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Vanlauwe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. Merckx
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Vandamme.

Additional information

Responsible Editor: Tim Simon George.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vandamme, E., Renkens, M., Pypers, P. et al. Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol. Plant Soil 369, 269–282 (2013). https://doi.org/10.1007/s11104-012-1571-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-012-1571-2

Keywords

Search

Navigation