Abstract
Background and aims
The role of lateral roots in the acquisition of nutrients and contaminants from the soil may vary between mobile and immobile solutes. The aim of the present study was to quantify the contributions of lateral roots to growth and elemental uptake under different conditions.
Methods
A lateral rootless mutant of rice (Oryza sativa) with a gain-of-function mutation in OsIAA11 was compared with its wild-type (WT) in hydroponic, pot and field conditions. Three soils varying in the P availability were used in the pot experiment. Synchrotron fast X-ray fluorescence (XRF) was used to map the distribution of trace elements in fresh hydrated roots.
Results
The Osiaa11 mutant grew smaller compared with the WT in all three experiments, especially in the field. The difference was larger in a P-sufficient soil than in P-deficient soils in the pot experiment. Elemental concentrations in the roots and shoots were affected differently by the mutation, depending on the elements and the growth media. The apparent contributions of lateral roots to elemental uptake varied from 2.7 to 82.5% in the hydroponic experiment, from −19.8 to 76.4% in the pot experiment, and from 30 to 76% in the field experiment. In general, the apparent contributions to the uptake of P, Mn, Zn, Cu and As were larger than that for the biomass, whereas for N, S and K the apparent contributions were smaller than or similar to the effect on plant biomass. Synchrotron XRF revealed strong accumulation of Mn, Zn, Cu, As and Se in the lateral roots of the WT.
Conclusions
Lateral roots play an important role in the acquisition of less mobile elements such as P, Mn, Zn, Cu and As, but have relatively small effects on the acquisition of mobile elements such as N, S and K.
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References
Arth I, Frenzel P (2000) Nitrification and denitrification in the rhizosphere of rice: the detection of processes by a new multi-channel electrode. Biol Fertil Soils 31:427–435
Barber SA (1984) Soil nutrient bioavailability, a mechanistic approach. Wiley, New York
Clarkson DT (1984) Calcium transport between tissues and its distribution in the plant. Plant Cell Environ 7:449–456
De Smet I (2012) Lateral root initiation: one step at a time. New Phytol 193:867–873
Drew MC (1975) Comparison of effects of a localized supply of phosphate, nitrate, ammonium and potassium on growth of seminal root system, and shoot, in barley. New Phytol 75:479–490
Faiyue B, Vijayalakshmi C, Nawaz S, Nagato Y, Taketa S, Ichii M, Al-Azzawi MJ, Flowers TJ (2010) Studies on sodium bypass flow in lateral rootless mutants lrt1 and lrt2, and crown rootless mutant crl1 of rice (Oryza sativa L.). Plant Cell Environ 33:687–701
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. Proc R Soc London, Ser B 269:2017–2022
Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Inter Rev Cytol 256:111–137
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. J Exp Bot 60:1953–1968
Kawashima C (1988) The root system formation in rice plants. 3. Quantitative studies. Jap J Crop Sci 57:26–36
Kirkham R, Dunn PA, Kuczewski AJ, Siddons DP, Dodanwela R, Moorhead GF, Ryan CG, De Geronimo G, Beuttenmuller R, Pinelli D (2010) The Maia spectroscopy detector system: engineering for integrated pulse capture, low-latency scanning and real-time processing. AIP Conf Proc 1234:240–243
Kitomi Y, Inahashi H, Takehisa H, Sato Y, Inukai Y (2012) OsIAA13-mediated auxin signaling is involved in lateral root initiation in rice. Plant Sci 190:116–122
Kopittke PM, de Jonge M, Menzies NW, Wang P, Donner E, McKenna BA, Paterson D, Howard DL, Lombi E (2012) Examination of the distribution of arsenic in hydrated and fresh cowpea roots using two- and three-dimensional techniques. Plant Physiol 159:1149–1158
Krishnamurthy P, Ranathunge K, Nayak S, Schreiber L, Mathew MK (2011) Root apoplastic barriers block Na+ transport to shoots in rice (Oryza sativa L.). J Exp Bot 62:4215–4228
Lombi E, de Jonge MD, Donner E, Ryan CG, Paterson D (2011) Trends in hard X-ray fluorescence mapping: environmental applications in the age of fast detectors. Anal Bioanal Chem 400:1637–1644
Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37
Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13
Ma JF, Goto S, Tamai K, Ichii M (2001) Role of root hairs and lateral roots in silicon uptake by rice. Plant Physiol 127:1773–1780
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Nat Acad Sci USA 105:9931–9935
Moore KL, Schröder M, Wu ZC, Martin BGH, Hawes CR, McGrath SP, Hawkesford MJ, Ma JF, Zhao FJ, Grovenor CRM (2011) NanoSIMS analysis reveals contrasting patterns of arsenic and silicon localization in rice roots. Plant Physiol 156:913–924
Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–614
Paszkowski U, Boller T (2002) The growth defect of Irt1, a maize mutant lacking lateral roots, can be complemented by symbiotic fungi or high phosphate nutrition. Planta 214:584–590
Paterson DJ, Boldeman JW, Cohen DD, Ryan CG (2007) Microspectroscopy beamline at the Australian synchrotron. In: Choi JY, Rah S (eds) The ninth international conference on Synchrotron Radiation Instrumentation (SRI 2006), vol 879. AIP Conf Proc, Daegu, South Korea, pp 864–867
Robinson D, Hodge A, Griffiths BS, Fitter AH (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc R Soc London, Ser B 266:431–435
Ryan CG (2000) Quantitative trace element imaging using PIXE and the nuclear microprobe. Inter J Imaging System Technol 11:219–230
Ryan CG, Jamieson DN (1993) Dynamic analysis: on-line quantitative PIXE microanalysis and its use in overlap-resolved elemental mapping. Nucl Instr Meth Physics Res B 77:203–214
Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Ann Rev Plant Biol 59:709–733
Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New York
White PJ (2012) Ion uptake mechanisms of individual cells and roots: short-distance transport. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Elsevier, Amsterdam, pp 7–47
Williamson LC, Ribrioux S, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882
Yamaji N, Ma JF (2007) Spatial distribution and temporal variation of the rice silicon transporter Lsi1. Plant Physiol 143:1306–1313
Yeo AR, Yeo ME, Flowers TJ (1987) The contribution of an apoplastic pathway to sodium uptake by rice roots in saline conditions. J Exp Bot 38:1141–1153
Zhang HM, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food-chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Ann Rev Plant Biol 61:535–559
Zhu JM, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Func Plant Biol 31:949–958
Zhu ZX, Liu Y, Liu SJ, Mao CZ, Wu YR, Wu P (2012) A gain-of-function mutation in OsIAA11 affects lateral root development in rice. Mol Plant 5:154–161
Acknowledgments
This research was supported by the Ministry of Science and Technology of the People’s Republic of China (grant number 2010DFA31080), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and the 111 project (B12009). Part of this research was undertaken on the X-ray fluorescence microscopy beamline at the Australian Synchrotron, Victoria, Australia.
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Liu, Y., Donner, E., Lombi, E. et al. Assessing the contributions of lateral roots to element uptake in rice using an auxin-related lateral root mutant. Plant Soil 372, 125–136 (2013). https://doi.org/10.1007/s11104-012-1582-z
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DOI: https://doi.org/10.1007/s11104-012-1582-z