Estimating nitrogen uptake of individual roots in container- and field-grown plants using a 15N-depletion approach
Astrid Volder A B H , Laurel J. Anderson A C G , David R. Smart D , Arnold J. Bloom E , Alan N. Lakso F and David M. Eissenstat AA Department of Horticulture, The Pennsylvania State University, University Park, PA 16802, USA.
B Department of Horticultural Sciences, Texas A & M University, TAMU 2133, College Station, TX 77843, USA.
C Department of Botany/Microbiology, Ohio Wesleyan University, Delaware, OH 43015, USA.
D Department of Viticulture and Enology, University of California, Davis, CA 95616, USA.
E Department of Plant Science, University of California, Davis, CA 95616, USA.
F Department of Horticultural Sciences, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456, USA.
G Present address: Department of Botany/Microbiology, Ohio Wesleyan University, Delaware, OH 43015, USA.
H Corresponding author. Email: a-volder@tamu.edu
Functional Plant Biology 36(7) 621-628 https://doi.org/10.1071/FP08330
Submitted: 31 December 2008 Accepted: 6 May 2009 Published: 2 July 2009
Abstract
We only have a limited understanding of the nutrient uptake physiology of individual roots as they age. Despite this shortcoming, the importance of nutrient uptake processes to our understanding of plant nutrition and nutrient cycling cannot be underestimated. In this study, we used a 15N depletion method that allowed for the measurement of nitrate-N uptake rates on intact, individual, fine roots of known age. We expected that N uptake would decline rapidly as fine roots aged, regardless of the environmental conditions and species used. We compared age dependent uptake patterns of young grape cuttings with those of mature vines and with those of tomato. Although patterns of declining uptake with increasing root age were similar for all species and conditions tested, large differences in maximum N uptake rates existed between young cuttings and mature vines, and between woody and herbaceous species. Maximum rates were 10-fold higher for tomato and 3-fold higher for the grape cuttings, when compared with uptake rates of fine roots of mature vines. Coefficients of variation ranged from 43 to 122% within root age groups. The large variability in physiological characteristics of fine roots of the same age, diameter and order suggests that there is a functional diversity within fine roots that is still poorly understood.
Additional keywords: fine roots, nitrate uptake, nutrient uptake, root age, root diameter, root function.
Acknowledgements
We are indebted to David Harris (Stable Isotope Research facility for Environmental Research (SIRFER) at UC Davis) for performing the isotope analyses. This work was supported by USDA grant NRI 97–35107–4359 to DME, USDA/CSREES Special Research Grants Program 99–34360–7374 to DME and DRS and NSF IOS-08–18435 and USDA-NRI 2008–01029 to AJB.
Anderson LJ,
Comas LH,
Lakso AN, Eissenstat DM
(2003) Multiple risk factors in root survivorship: a 4 year study in Concord grape. New Phytologist 158, 489–501.
| Crossref | GoogleScholarGoogle Scholar |
Andriolo JL,
LeBot J,
Gary C,
Sappe G,
Orlando P,
Brunel B, Sarrouy C
(1996) An experimental set-up to study carbon, water and nitrate uptake rates by hydroponically grown plants. Journal of Plant Nutrition 19, 1441–1462.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Baddeley JA, Watson CA
(2005) Influences of root diameter, tree age, soil depth and season on fine root survivorship in Prunus avium. Plant and Soil 276, 15–22.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bhat KKS
(1982) Nutrient inflows into apple roots. 2. Nitrate uptake rates measured on intact roots of mature trees under field conditions. Plant, Cell & Environment 5, 461–469.
|
CAS |
Black KE,
Harbron CG,
Franklin M,
Atkinson D, Hooker JE
(1998) Differences in root longevity of some tree species. Tree Physiology 18, 259–264.
| PubMed |
Bloom AJ
(1985) Wild and cultivated barleys show similar affinities for mineral nitrogen. Oecologia 65, 555–557.
| Crossref | GoogleScholarGoogle Scholar |
Bouma TJ,
Yanai RD,
Elkin AD,
Hartmond U,
Flores-Alva DE, Eissenstat DM
(2001) Estimating age-dependent costs and benefits of roots with contrasting life span: comparing apples and oranges. New Phytologist 150, 685–695.
| Crossref | GoogleScholarGoogle Scholar |
Cardenas-Navarro R,
Adamowicz S, Robin P
(1998) Diurnal nitrate uptake in young tomato (Lycopersicon esculentum Mill.) plants: test of a feedback-based model. Journal of Experimental Botany 49, 721–730.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Clarkson DT, Scattergood CB
(1982) Growth and phosphate transport in barley and tomato plants during the development of, and recovery from, phosphate stress. Journal of Experimental Botany 33, 865–875.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Clarkson DT,
Sanderson J, Russell RS
(1968) Ion uptake and root age. Nature 220, 805–806.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Colmer TD, Bloom AJ
(1998) A comparison of NH4+ and NO3− net fluxes along roots of rice and maize. Plant, Cell & Environment 21, 240–246.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Comas LH,
Eissenstat DM, Lakso AN
(2000) Assessing root death and root system dynamics in a study of grape canopy pruning. New Phytologist 147, 171–178.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Eissenstat DM, Achor DS
(1999) Anatomical characteristics of roots of citrus rootstocks that vary in specific root length. New Phytologist 141, 309–321.
| Crossref | GoogleScholarGoogle Scholar |
Eissenstat DM, Yanai RD
(1997) The ecology of root lifespan. Advances in Ecological Research 27, 1–60.
| Crossref | GoogleScholarGoogle Scholar |
Eshel A, Waisel Y
(1972) Variations in sodium uptake along primary roots of corn seedlings. Plant Physiology 49, 585–589.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Eshel A, Waisel Y
(1973) Variations in uptake of sodium and rubidium along barley roots. Physiologia Plantarum 28, 557–560.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ferguson IB, Clarkson DT
(1975) Ion transport and endodermal suberization in roots of Zea mays. New Phytologist 75, 69–79.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Fitter AH
(1982) Morphometric analysis of root systems – application of the technique and influence of soil fertility on root system development in two herbaceous species. Plant, Cell & Environment 5, 313–322.
Gessler A,
Schneider S,
Von Sengbusch D,
Weber P,
Hanemann U,
Huber C,
Rothe A,
Kreutzer K, Rennenberg H
(1998) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytologist 138, 275–285.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Guo DL,
Mitchell RJ, Hendricks JJ
(2004) Fine root branch orders respond differentially to carbon source–sink manipulations in a longleaf pine forest. Oecologia 140, 450–457.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guo DL,
Li H,
Mitchell RJ,
Han WX,
Hendricks JJ,
Fahey TJ, Hendrick RL
(2008) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytologist 177, 443–456.
| Crossref |
PubMed |
Hansen GK
(1980) Diurnal-variation of root respiration rates and nitrate uptake as influenced by nitrogen supply. Physiologia Plantarum 48, 421–427.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Hendrick RL, Pregitzer KS
(1993a) The dynamics of fine root length, biomass, and nitrogen-content in two northern hardwood ecosystems. Canadian Journal of Forest Research 23, 2507–2520.
| Crossref | GoogleScholarGoogle Scholar |
Hendrick RL, Pregitzer KS
(1993b) Patterns of fine root mortality in two sugar maple forests. Nature 361, 59–61.
| Crossref | GoogleScholarGoogle Scholar |
Hendrick RL, Pregitzer KS
(1997) The relationship between fine root demography and the soil environment in northern hardwood forests. Ecoscience 4, 99–105.
Henriksen GH,
Bloom AJ, Spanswick RM
(1990) Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelectrodes. Plant Physiology 93, 271–280.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Henriksen GH,
Raman DR,
Walker LP, Spanswick RM
(1992) Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelectrodes. 2. Patterns of uptake along the root axis and evaluation of the microelectrode flux estimation technique. Plant Physiology 99, 734–747.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jensen G
(1962) Relationship between water and nitrate uptake in excised tomato root systems. Physiologia Plantarum 15, 791–803.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Joslin JD,
Gaudinski JB,
Torn MS,
Riley WJ, Hanson PJ
(2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a C-14-labeled hardwood forest. New Phytologist 172, 523–535.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kronzucker HJ,
Siddiqi MY, Glass ADM
(1995) Kinetics of NO3− influx in spruce. Plant Physiology 109, 319–326.
|
CAS |
PubMed |
Le Bot J, Kirkby EA
(1992) Diurnal uptake of nitrate and potassium during the vegetative growth of tomato plants. Journal of Plant Nutrition 15, 247–264.
| Crossref | GoogleScholarGoogle Scholar |
Lucash MS,
Joslin JD, Yanai RD
(2005) Temporal variation in nutrient uptake capacity by intact roots of mature loblolly pine. Plant and Soil 272, 253–262.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lucash MS,
Eissenstat DM,
Joslin JD,
McFarlane KJ, Yanai RD
(2007) Estimating nutrient uptake by mature tree roots under field conditions: challenges and opportunities. Trees – Structure and Function 21, 593–603.
|
CAS |
Macfall JS,
Johnson GA, Kramer PJ
(1991) Comparative water-uptake by roots of different ages in seedlings of loblolly pine (Pinus taeda L.). New Phytologist 119, 551–560.
| Crossref | GoogleScholarGoogle Scholar |
Marschner H,
Romheld V,
Horst WJ, Martin P
(1986) Root-induced changes in the rhizosphere – importance for the mineral nutrition of plants. Zeitschrift für Pflanzenernährung und Bodenkunde 149, 441–456.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Norby RJ, Jackson RB
(2000) Root dynamics and global change: seeking an ecosystem perspective. New Phytologist 147, 3–12.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Passioura JB
(1980) The transport of water from soil to shoot in wheat seedlings. Journal of Experimental Botany 31, 333–345.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Peek MS,
Leffler AJ,
Hipps L,
Ivans S,
Ryel RJ, Caldwell MM
(2006) Root turnover and relocation in the soil profile in response to seasonal soil water variation in a natural stand of Utah juniper (Juniperus osteosperma). Tree Physiology 26, 1469–1476.
| PubMed |
Peuke AD, Jeschke WD
(1998) The effects of light on induction, time courses, and kinetic patterns of net nitrate uptake in barley. Plant, Cell & Environment 21, 765–774.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Poorter H,
Remkes C, Lambers H
(1990) Carbon and nitrogen economy of 24 wild species differing in relative growth-rate. Plant Physiology 94, 621–627.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Raper CD,
Vessey JK, Henry LT
(1991) Increase in nitrate uptake by soybean plants during interruption of the dark period with low intensity light. Physiologia Plantarum 81, 183–189.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Resendes M,
Bryla D, Eissenstat D
(2008) Early events in the life of apple roots: variation in root growth rate is linked to mycorrhizal and nonmycorrhizal fungal colonization. Plant and Soil 313, 175–186.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Robinson D,
Linehan DJ, Caul S
(1991) What limits nitrate uptake from soil. Plant, Cell & Environment 14, 77–85.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Robinson D,
Hodge A,
Griffiths BS, Fitter AH
(1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 431–435.
| Crossref | GoogleScholarGoogle Scholar |
Russell RS, Sanderson J
(1967) Nutrient uptake by different parts of intact roots of plants. Journal of Experimental Botany 18, 491–508.
| Crossref | GoogleScholarGoogle Scholar |
Scheurwater I,
Clarkson DT,
Purves JV,
Van Rijt G,
Saker LR,
Welschen R, Lambers H
(1999) Relatively large nitrate efflux can account for the high specific respiratory costs for nitrate transport in slow-growing grass species. Plant and Soil 215, 123–134.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Siddiq MY,
Glass ADM, Ruth TJ
(1991) Studies of the uptake of nitrate in barley. 3. Compartmentation of NO3−. Journal of Experimental Botany 42, 1455–1463.
| Crossref | GoogleScholarGoogle Scholar |
Smart DR, Bloom AJ
(1988) Kinetics of ammonium and nitrate uptake among wild and cultivated tomatoes. Oecologia 76, 336–340.
Taylor AR, Bloom AJ
(1998) Ammonium, nitrate, and proton fluxes along the maize root. Plant, Cell & Environment 21, 1255–1263.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ter Steege MW,
Stulen I,
Wiersema PK,
Posthumus F, Vaalburg W
(1999) Efficiency of nitrate uptake in spinach: impact of external nitrate concentration and relative growth rate on nitrate influx and efflux. Plant and Soil 208, 125–134.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Valenzuela-Estrada LR,
Richards JH,
Diaz A, Eissenstat DM
(2009) Patterns of nocturnal rehydration in root tissues of Vaccinium corymbosum L. under severe drought conditions. Journal of Experimental Botany 60, 1241–1247.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Volder A,
Smart DR,
Bloom AJ, Eissenstat DM
(2005) Rapid decline in nitrate uptake and respiration with age in fine lateral roots of grape: implications for root efficiency and competitive effectiveness. New Phytologist 165, 493–502.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wang MY,
Siddiqi MY,
Ruth TJ, Glass ADM
(1993) Ammonium uptake by rice roots. 2. Kinetics of NH4+-N13 influx across the plasmalemma. Plant Physiology 103, 1259–1267.
|
CAS |
Crossref |
PubMed |
Wells CE, Eissenstat DM
(2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82, 882–892.
Wells CE, Eissenstat DM
(2003) Beyond the roots of young seedlings: the influence of age and order on fine root physiology. Journal of Plant Growth Regulation 21, 324–334.
| Crossref | GoogleScholarGoogle Scholar |
Wilson JB
(1988) A review of evidence on the control of shoot-root ratio, in relation to models. Annals of Botany 61, 433–449.