Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies

Burnett, Angela C.; Rogers, Alistair; Rees, Mark; Osborne, Colin P.

doi:10.1002/pld3.94

Title: Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies

Journal Article · 11 November 2018 · Plant Direct

DOI: https://doi.org/10.1002/pld3.94 · OSTI ID:1481803

Burnett, Angela C. ^[1]; Rogers, Alistair ^[2]; Rees, Mark ^[1]; Osborne, Colin P. ^[1]

Department of Animal and Plant Sciences University of Sheffield Sheffield UK
Environmental and Climate Sciences Department Brookhaven National Laboratory Upton New York

Abstract Mineral nutrients exert important limitations on plant growth. Growth is limited by the nutrient source when it is constrained by nutrient availability and uptake, which may simultaneously limit investment in photosynthetic proteins, leading to carbon source limitation. However, growth may also be limited by nutrient utilization in sink tissue. The relative importance of these processes is contested, with crop and vegetation models typically assuming source limitations of carbon and mineral nutrients (especially nitrogen). This study compared the importance of source and sink limitation on growth in a slower‐growing wild perennial barley ( Hordeum bulbosum ) and a faster‐growing domesticated annual barley ( Hordeum vulgare ), by applying a mineral nutrient treatment and measuring nitrogen uptake, growth, allocation, and carbon partitioning. We found that nitrogen uptake, growth, tillering, shoot allocation, and nitrogen storage were restricted by low nutrient treatments. Multiple lines of evidence suggest that low nutrient levels do not limit growth via carbon acquisition: (a) Carbohydrate storage does not increase at high nutrient levels. (b) Ratio of free amino acids to sucrose increases at high nutrient levels. (c) Shoot allocation increases at high nutrient levels. These data indicate that barley productivity is limited by the capacity for nutrient use in growth. Models must explicitly account for sink processes in order to properly simulate this mineral nutrient limitation of growth.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0012704

OSTI ID:: 1481803

Journal Information:: Plant Direct, Journal Name: Plant Direct Journal Issue: 11 Vol. 2; ISSN 2475-4455

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

References (54)

Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate Poorter, Hendrik; Remkes, Carlo Oecologia, Vol. 83, Issue 4 https://doi.org/10.1007/BF00317209	journal	July 1990
Responses of wild plants to nitrate availability: Relationships between growth rate and nitrate uptake parameters, a case study with two Bromus species, and a survey Garnier, E.; Koch, G. W.; Roy, J. Oecologia, Vol. 79, Issue 4 https://doi.org/10.1007/BF00378673	journal	June 1989
The Mineral Nutrition of Wild Plants Revisited: A Re-evaluation of Processes and Patterns Aerts, R.; Chapin III, F. S. Advances in Ecological Research https://doi.org/10.1016/S0065-2504(08)60016-1	book	January 1999
A comparison of the performance of the CSM-CERES-Maize and EPIC models using maize variety trial data Bao, Yawen; Hoogenboom, Gerrit; McClendon, Ron Agricultural Systems, Vol. 150 https://doi.org/10.1016/j.agsy.2016.10.006	journal	January 2017
Re-engineering of carbon fixation in plants – challenges for plant biotechnology to improve yields in a high-CO2 world Peterhansel, Christoph; Offermann, Sascha Current Opinion in Biotechnology, Vol. 23, Issue 2 https://doi.org/10.1016/j.copbio.2011.12.013	journal	April 2012
Grain weight, radiation interception and use efficiency as affected by sink-strength in Mediterranean wheats released from 1940 to 2005 Acreche, Martín M.; Slafer, Gustavo A. Field Crops Research, Vol. 110, Issue 2 https://doi.org/10.1016/j.fcr.2008.07.006	journal	February 2009
Paradigm shift in plant growth control Körner, Christian Current Opinion in Plant Biology, Vol. 25 https://doi.org/10.1016/j.pbi.2015.05.003	journal	June 2015
Next-generation strategies for understanding and influencing source–sink relations in crop plants Sonnewald, Uwe; Fernie, Alisdair R. Current Opinion in Plant Biology, Vol. 43 https://doi.org/10.1016/j.pbi.2018.01.004	journal	June 2018
Interactions between nitrogen and cytokinin in the regulation of metabolism and development Sakakibara, Hitoshi; Takei, Kentaro; Hirose, Naoya Trends in Plant Science, Vol. 11, Issue 9 https://doi.org/10.1016/j.tplants.2006.07.004	journal	September 2006
The global spectrum of plant form and function Díaz, Sandra; Kattge, Jens; Cornelissen, Johannes H. C. Nature, Vol. 529, Issue 7585 https://doi.org/10.1038/nature16489	journal	December 2015
How a century of ammonia synthesis changed the world Erisman, Jan Willem; Sutton, Mark A.; Galloway, James Nature Geoscience, Vol. 1, Issue 10 https://doi.org/10.1038/ngeo325	journal	September 2008
The environmental impact of fertilizer embodied in a wheat-to-bread supply chain Goucher, Liam; Bruce, Richard; Cameron, Duncan D. Nature Plants, Vol. 3, Issue 3 https://doi.org/10.1038/nplants.2017.12	journal	March 2017
Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen Taylor, Benton N.; Menge, Duncan N. L. Nature Plants, Vol. 4, Issue 9 https://doi.org/10.1038/s41477-018-0231-9	journal	August 2018
Photosynthetic nitrogen-use efficiency in leaves of woody and herbaceous species Hikosaka, K.; Hanba, Y. T.; Hirose, T. Functional Ecology, Vol. 12, Issue 6 https://doi.org/10.1046/j.1365-2435.1998.00272.x	journal	December 1998
Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance Paul, M. J.; Driscoll, S. P. Plant, Cell and Environment, Vol. 20, Issue 1 https://doi.org/10.1046/j.1365-3040.1997.d01-17.x	journal	January 1997
The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background Stitt, M.; Krapp, A. Plant, Cell and Environment, Vol. 22, Issue 6 https://doi.org/10.1046/j.1365-3040.1999.00386.x	journal	June 1999
Sucrose‐phosphate synthase responds differently to source‐sink relations and to photosynthetic rates: Lolium perenne L. growing at elevated p _CO2 in the field Isopp, H.; Frehner, M.; Long, S. P. Plant, Cell & Environment, Vol. 23, Issue 6 https://doi.org/10.1046/j.1365-3040.2000.00583.x	journal	June 2000
The Evolution of Plant Functional Variation: Traits, Spectra, and Strategies Reich, P. B.; Wright, I. J.; Cavender‐Bares, J. International Journal of Plant Sciences, Vol. 164, Issue S3 https://doi.org/10.1086/374368	journal	May 2003
Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture Masclaux-Daubresse, Céline; Daniel-Vedele, Françoise; Dechorgnat, Julie Annals of Botany, Vol. 105, Issue 7 https://doi.org/10.1093/aob/mcq028	journal	March 2010
Nitrate transport in intact wheat roots:II. Long-term effects of NO ₃ ⁻ concentration in the nutrient solution on NO ₃ ⁻ unidirectional fluxes and distribution within the tissues5 Devienne, F.; Mary, B.; Lamaze, T. Journal of Experimental Botany, Vol. 45, Issue 5 https://doi.org/10.1093/jxb/45.5.677	journal	January 1994
Nitrate transport and signalling Miller, A. J.; Fan, X.; Orsel, M. Journal of Experimental Botany, Vol. 58, Issue 9 https://doi.org/10.1093/jxb/erm066	journal	March 2007
Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin Kiba, Takatoshi; Kudo, Toru; Kojima, Mikiko Journal of Experimental Botany, Vol. 62, Issue 4 https://doi.org/10.1093/jxb/erq410	journal	December 2010
Manipulating resource allocation in plants Bennett, E.; Roberts, J. A.; Wagstaff, C. Journal of Experimental Botany, Vol. 63, Issue 9 https://doi.org/10.1093/jxb/err442	journal	January 2012
Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production Slewinski, T. L. Journal of Experimental Botany, Vol. 63, Issue 13 https://doi.org/10.1093/jxb/ers124	journal	June 2012
Internal efficiency of nutrient utilization: what is it and how to measure it during vegetative plant growth? Santa-Maria, G. E.; Moriconi, J. I.; Oliferuk, S. Journal of Experimental Botany, Vol. 66, Issue 11 https://doi.org/10.1093/jxb/erv162	journal	April 2015
How can we make plants grow faster? A source–sink perspective on growth rate White, Angela C.; Rogers, Alistair; Rees, Mark Journal of Experimental Botany, Vol. 67, Issue 1 https://doi.org/10.1093/jxb/erv447	journal	October 2015
Source–sink interaction: a century old concept under the light of modern molecular systems biology Chang, Tian-Gen; Zhu, Xin-Guang Journal of Experimental Botany, Vol. 68, Issue 16 https://doi.org/10.1093/jxb/erx002	journal	February 2017
Increasing crop yield and resilience with trehalose 6-phosphate: targeting a feast–famine mechanism in cereals for better source–sink optimization Paul, Matthew J.; Oszvald, Maria; Jesus, Claudia Journal of Experimental Botany, Vol. 68, Issue 16 https://doi.org/10.1093/jxb/erx083	journal	March 2017
Does seed mass drive the differences in relative growth rate between growth forms? Houghton, Jennie; Thompson, Ken; Rees, Mark Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1762 https://doi.org/10.1098/rspb.2013.0921	journal	July 2013
Leaf Amino Acid Supply Affects Photosynthetic and Plant Nitrogen Use Efficiency under Nitrogen Stress Perchlik, Molly; Tegeder, Mechthild Plant Physiology, Vol. 178, Issue 1 https://doi.org/10.1104/pp.18.00597	journal	August 2018
Allocating CSR plant functional types: the use of leaf economics and size traits to classify woody and herbaceous vascular plants Pierce, Simon; Brusa, Guido; Vagge, Ilda Functional Ecology, Vol. 27, Issue 4 https://doi.org/10.1111/1365-2435.12095	journal	April 2013
Host plants and butterfly biology. Do host-plant strategies drive butterfly status? Dennis, Roger L. H.; Hodgson, John G.; Grenyer, Richard Ecological Entomology, Vol. 29, Issue 1 https://doi.org/10.1111/j.1365-2311.2004.00572.x	journal	February 2004
The accumulation and storage of nitrogen by herbaceous plants Millard, P. Plant, Cell and Environment, Vol. 11, Issue 1 https://doi.org/10.1111/j.1365-3040.1988.tb01769.x	journal	January 1988
Effects of source-sink relations on photosynthetic acclimation to elevated CO2 Arp, W. J. Plant, Cell and Environment, Vol. 14, Issue 8 https://doi.org/10.1111/j.1365-3040.1991.tb01450.x	journal	October 1991
Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology Stitt, M.; Schulze, D. Plant, Cell and Environment, Vol. 17, Issue 5 https://doi.org/10.1111/j.1365-3040.1994.tb00144.x	journal	May 1994
Sink strength: Learning to measure, measuring to learn Geiger, D. R.; Shieh, W. -J. Plant, Cell and Environment, Vol. 16, Issue 9 https://doi.org/10.1111/j.1365-3040.1996.tb02048.x	journal	December 1993
Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis Tschoep, Hendrik; Gibon, Yves; Carillo, Petronia Plant, Cell & Environment, Vol. 32, Issue 3 https://doi.org/10.1111/j.1365-3040.2008.01921.x	journal	March 2009
Cultivar differences in the rate of nitrate uptake by intact wheat plants as related to growth rate Rodgers, C. O.; Barneix, A. J. Physiologia Plantarum, Vol. 72, Issue 1 https://doi.org/10.1111/j.1399-3054.1988.tb06632.x	journal	January 1988
Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species Garnier, E.; Laurent, G. New Phytologist, Vol. 128, Issue 4 https://doi.org/10.1111/j.1469-8137.1994.tb04036.x	journal	December 1994
Assessing the generality of global leaf trait relationships Wright, Ian J.; Reich, Peter B.; Cornelissen, Johannes H. C. New Phytologist, Vol. 166, Issue 2 https://doi.org/10.1111/j.1469-8137.2005.01349.x	journal	February 2005
Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling Fatichi, Simone; Leuzinger, Sebastian; Körner, Christian New Phytologist, Vol. 201, Issue 4 https://doi.org/10.1111/nph.12614	journal	November 2013
Evaluation of 11 terrestrial carbon-nitrogen cycle models against observations from two temperate Free-Air CO ₂ Enrichment studies Zaehle, Sönke; Medlyn, Belinda E.; De Kauwe, Martin G. New Phytologist, Vol. 202, Issue 3 https://doi.org/10.1111/nph.12697	journal	January 2014
Source and sink mechanisms of nitrogen transport and use Tegeder, Mechthild; Masclaux-Daubresse, Céline New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14876	journal	November 2017
Physiological mechanisms in plant growth models: do we need a supra-cellular systems biology approach?: Physiological mechanisms in plant growth models Poorter, Hendrik; Anten, Niels P. R.; Marcelis, Leo F. M. Plant, Cell & Environment, Vol. 36, Issue 9 https://doi.org/10.1111/pce.12123	journal	June 2013
Carbon source-sink limitations differ between two species with contrasting growth strategies: Source-sink limitations vary with growth strategy Burnett, Angela C.; Rogers, Alistair; Rees, Mark Plant, Cell & Environment, Vol. 39, Issue 11 https://doi.org/10.1111/pce.12801	journal	September 2016
Gulf of Mexico Hypoxia, A.K.A. “The Dead Zone” Rabalais, Nancy N.; Turner, R. Eugene; Wiseman, William J. Annual Review of Ecology and Systematics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.ecolsys.33.010802.150513	journal	November 2002
Post-Flowering Nitrate Uptake in Wheat Is Controlled by N Status at Flowering, with a Putative Major Role of Root Nitrate Transporter NRT2.1 Taulemesse, François; Le Gouis, Jacques; Gouache, David PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0120291	journal	March 2015
Grain Filling and Dry Matter Translocation Responses to Source–Sink Modifications in a Historical Series of Durum Wheat Álvaro, F.; Royo, C.; García del Moral, L. F. Crop Science, Vol. 48, Issue 4 https://doi.org/10.2135/cropsci2007.10.0545	journal	January 2008
Photosynthetic Responses in Annual Rye, Perennial Wheat, and Perennial Rye Subjected to Modest Source:Sink Ratio Changes Jaikumar, Nikhil S.; Snapp, Sieglinde S.; Flore, James A. Crop Science, Vol. 54, Issue 1 https://doi.org/10.2135/cropsci2013.04.0280	journal	January 2014
An Experimental Test of Plant Strategy Theory Campbell, Bruce D.; Grime, J. Philip Ecology, Vol. 73, Issue 1 https://doi.org/10.2307/1938717	journal	February 1992
Relative Growth-Rate: Its Range and Adaptive Significance in a Local Flora Grime, J. P.; Hunt, Roderick The Journal of Ecology, Vol. 63, Issue 2 https://doi.org/10.2307/2258728	journal	July 1975
Growth Analysis of Congeneric Annual and Perennial Grass Species Garnier, E. The Journal of Ecology, Vol. 80, Issue 4 https://doi.org/10.2307/2260858	journal	December 1992
The Role of Sink Strength and Nitrogen Availability in the Down-Regulation of Photosynthetic Capacity in Field-Grown Nicotiana tabacum L. at Elevated CO2 Concentration Ruiz-Vera, Ursula M.; De Souza, Amanda P.; Long, Stephen P. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00998	journal	June 2017
Nitrogen feedbacks increase future terrestrial ecosystem carbon uptake in an individual-based dynamic vegetation model Wårlind, D.; Smith, B.; Hickler, T. Biogeosciences, Vol. 11, Issue 21 https://doi.org/10.5194/bg-11-6131-2014	journal	January 2014

Similar Records

Carbon source-sink limitations differ between two species with contrasting growth strategies: Source-sink limitations vary with growth strategy

Journal Article · 2016 · Plant, Cell and Environment · OSTI ID:1336088

Burnett, Angela C.; Rogers, A.; Rees, M.; +1 more

Photoassimilate partitioning of main shoot leaves in field-grown spring barley. [Hordeum vulgare L]

Journal Article · · Crop Sci.; (United States) · OSTI ID:6035208

Lauer, J G; Simmons, S R

Effect of nitrogen nutrition on endosperm protein synthesis in wild and cultivated barley grown in spike culture

Journal Article · 1988 · Plant Physiology; (USA) · OSTI ID:5400105

Corke, H; Atsmon, D

Title: Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies

Citation Formats

References (54)

Similar Records

Related Subjects