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

Burnett, Angela C.; Rogers, A.; Rees, M.; Osborne, Colin P.

doi:10.1111/pce.12801

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

Journal Article · Thu Sep 22 00:00:00 EDT 2016 · Plant, Cell and Environment

DOI:https://doi.org/10.1111/pce.12801· OSTI ID:1336088

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

Univ. of Sheffield (United Kingdom). Dept. of Animal and Plant Sciences
Brookhaven National Lab. (BNL), Upton, NY (United States). Environmental and Climate Sciences Dept.

When we understand how carbon source and sink strengths limit plant growth we realized how critical the knowledge gap is in hindering efforts to maximize crop yield. Here, we investigated how differences in growth rate arise from source–sink limitations, using a model system comparing a fast-growing domesticated annual barley (Hordeum vulgare cv. NFC Tipple) with a slow-growing wild perennial relative (Hordeum bulbosum). Source strength was manipulated by growing plants at sub-ambient and elevated CO₂ concentrations ([CO₂]). Limitations on vegetative growth imposed by source and sink were diagnosed by measuring relative growth rate, developmental plasticity, photosynthesis and major carbon and nitrogen metabolite pools. Growth was sink limited in the annual but source limited in the perennial. RGR and carbon acquisition were higher in the annual, but photosynthesis responded weakly to elevated [CO₂] indicating that source strength was near maximal at current [CO₂]. In contrast, photosynthetic rate and sink development responded strongly to elevated [CO₂] in the perennial, indicating significant source limitation. Sink limitation was avoided in the perennial by high sink plasticity: a marked increase in tillering and root:shoot ratio at elevated [CO₂], and lower non-structural carbohydrate accumulation. Finally, by alleviating sink limitation during vegetative development could be important for maximizing growth of elite cereals under future elevated [CO₂].

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC00112704

OSTI ID:: 1336088

Report Number(s):: BNL-112493-2016-JA; R&D Project: 2016-BNL-EE630EECA-Budg; KP1701000

Journal Information:: Plant, Cell and Environment, Vol. 39, Issue 11; ISSN 0140-7791

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 39 works

Citation information provided by
Web of Science

References (56)

Temporal Changes in Allocation and Partitioning of New Carbon as ¹¹ C Elicited by Simulated Herbivory Suggest that Roots Shape Aboveground Responses in Arabidopsis Ferrieri, Abigail P.; Agtuca, Beverly; Appel, Heidi M. Plant Physiology, Vol. 161, Issue 2 https://doi.org/10.1104/pp.112.208868	journal	December 2012
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
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
Is stimulation of leaf photosynthesis by elevated carbon dioxide concentration maintained in the long term? A test with Lolium perenne grown for 10 years at two nitrogen fertilization levels under Free Air CO2Enrichment (FACE) Ainsworth, E. A.; Davey, P. A.; Hymus, G. J. Plant, Cell and Environment, Vol. 26, Issue 5 https://doi.org/10.1046/j.1365-3040.2003.01007.x	journal	May 2003
Does elevated atmospheric [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves? Ainsworth, E. A.; Rogers, A.; Leakey, A. D. B. Journal of Experimental Botany, Vol. 58, Issue 3 https://doi.org/10.1093/jxb/erl233	journal	December 2006
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
Acclimation of Photosynthesis to Elevated CO ₂ under Low-Nitrogen Nutrition Is Affected by the Capacity for Assimilate Utilization. Perennial Ryegrass under Free-Air CO ₂ Enrichment Rogers, Alistair; Fischer, Bernt U.; Bryant, Jonathan Plant Physiology, Vol. 118, Issue 2 https://doi.org/10.1104/pp.118.2.683	journal	October 1998
Solutions for a cultivated planet Foley, Jonathan A.; Ramankutty, Navin; Brauman, Kate A. Nature, Vol. 478, Issue 7369 https://doi.org/10.1038/nature10452	journal	October 2011
Increasing Sucrose Uptake Capacity of Wheat Grains Stimulates Storage Protein Synthesis Weichert, Nicola; Saalbach, Isolde; Weichert, Heiko Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.150854	journal	December 2009
Architectural Evolution and its Implications for Domestication in Grasses Doust, A. Annals of Botany, Vol. 100, Issue 5 https://doi.org/10.1093/aob/mcm040	journal	July 2007
FACE-ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO ₂ ] impacts on crop yield and food supply Ainsworth, Elizabeth A.; Leakey, Andrew D. B.; Ort, Donald R. New Phytologist, Vol. 179, Issue 1 https://doi.org/10.1111/j.1469-8137.2008.02500.x	journal	July 2008
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
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
Targets for Crop Biotechnology in a Future High-CO ₂ and High-O ₃ World Ainsworth, Elizabeth A.; Rogers, Alistair; Leakey, Andrew D. B. Plant Physiology, Vol. 147, Issue 1 https://doi.org/10.1104/pp.108.117101	journal	April 2008
Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments Serrago, Román A.; Alzueta, Ignacio; Savin, Roxana Field Crops Research, Vol. 150 https://doi.org/10.1016/j.fcr.2013.05.016	journal	August 2013
Prediction of the growth response to elevated CO2: a search for physiological criteria in closely related grass species Roumet, C.; Roy, J. New Phytologist, Vol. 134, Issue 4 https://doi.org/10.1111/j.1469-8137.1996.tb04926.x	journal	December 1996
Redesigning photosynthesis to sustainably meet global food and bioenergy demand Ort, Donald R.; Merchant, Sabeeha S.; Alric, Jean Proceedings of the National Academy of Sciences, Vol. 112, Issue 28 https://doi.org/10.1073/pnas.1424031112	journal	June 2015
Enhanced leaf photosynthesis as a target to increase grain yield: insights from transgenic rice lines with variable Rieske FeS protein content in the cytochrome b ₆ / f complex Yamori, Wataru; Kondo, Eri; Sugiura, Daisuke Plant, Cell & Environment, Vol. 39, Issue 1 https://doi.org/10.1111/pce.12594	journal	November 2015
Evidence against sink limitation by the sucrose-to-starch route in potato plants expressing fructosyltransferases Zuther, Ellen; Hoermiller, Imke I.; Heyer, Arnd G. Physiologia Plantarum, Vol. 143, Issue 2 https://doi.org/10.1111/j.1399-3054.2011.01495.x	journal	July 2011
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
Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction Freschet, Grégoire T.; Swart, Elferra M.; Cornelissen, Johannes H. C. New Phytologist, Vol. 206, Issue 4 https://doi.org/10.1111/nph.13352	journal	March 2015
Coordination of carbon supply and plant growth Smith, Alison M.; Stitt, Mark Plant, Cell & Environment, Vol. 30, Issue 9 https://doi.org/10.1111/j.1365-3040.2007.01708.x	journal	September 2007
Photosynthetic acclimation to elevated CO2 is modified by source:sink balance in three component species of chalk grassland swards grown in a free air carbon dioxide enrichment (FACE) experiment Bryant, J.; Taylor, G.; Frehner, M. Plant, Cell and Environment, Vol. 21, Issue 2 https://doi.org/10.1046/j.1365-3040.1998.00265.x	journal	February 1998
Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE Leakey, Andrew D. B.; Ainsworth, Elizabeth A.; Bernacchi, Carl J. Journal of Experimental Botany, Vol. 60, Issue 10 https://doi.org/10.1093/jxb/erp096	journal	April 2009
Is barley yield in the UK sink limited? Bingham, Ian J.; Blake, Jonathan; Foulkes, M. John Field Crops Research, Vol. 101, Issue 2 https://doi.org/10.1016/j.fcr.2006.11.005	journal	March 2007
Is barley yield in the UK sink limited? Bingham, Ian J.; Blake, Jonathan; Foulkes, M. John Field Crops Research, Vol. 101, Issue 2 https://doi.org/10.1016/j.fcr.2006.11.004	journal	March 2007
Food for Thought: Lower-Than-Expected Crop Yield Stimulation with Rising CO2 Concentrations Long, S. P. Science, Vol. 312, Issue 5782 https://doi.org/10.1126/science.1114722	journal	June 2006
Whole-plant versus leaf-level regulation of photosynthetic responses after partial defoliation in Eucalyptus globulus saplings Eyles, Alieta; Pinkard, Elizabeth A.; Davies, Noel W. Journal of Experimental Botany, Vol. 64, Issue 6 https://doi.org/10.1093/jxb/ert017	journal	February 2013
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
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
Effects of partial defoliation, changes of irradiance during growth, short-term water stress and growth at enhanced p(CO2) on the photosynthetic capacity of leaves of Phaseolus vulgaris L. von Caemmerer, S.; Farquhar, G. D. Planta, Vol. 160, Issue 4 https://doi.org/10.1007/BF00393413	journal	March 1984
Genes and Mutations Underlying Domestication Transitions in Grasses: Figure 1. Sang, Tao Plant Physiology, Vol. 149, Issue 1 https://doi.org/10.1104/pp.108.128827	journal	January 2009
The dynamics of recovery and growth: how defoliation affects stored resources Atkinson, R. R. L.; Burrell, M. M.; Rose, K. E. Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1783 https://doi.org/10.1098/rspb.2013.3355	journal	May 2014
Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume Rogers, Alistair; Gibon, Yves; Stitt, Mark Plant, Cell and Environment, Vol. 29, Issue 8 https://doi.org/10.1111/j.1365-3040.2006.01549.x	journal	August 2006
Testing the “source–sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max Ainsworth, Elizabeth A.; Rogers, Alistair; Nelson, Randall Agricultural and Forest Meteorology, Vol. 122, Issue 1-2 https://doi.org/10.1016/j.agrformet.2003.09.002	journal	March 2004
Recommendations for Reporting Metabolite Data Fernie, Alisdair R.; Aharoni, Asaph; Willmitzer, Lothar The Plant Cell, Vol. 23, Issue 7 https://doi.org/10.1105/tpc.111.086272	journal	July 2011
Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1. Ainsworth, Elizabeth A.; Bush, Daniel R. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.167684	journal	October 2010
Source/sink interactions underpin crop yield: the case for trehalose 6-phosphate/SnRK1 in improvement of wheat Lawlor, David W.; Paul, Matthew J. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00418	journal	August 2014
Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration Poorter, Hendrik Vegetatio, Vol. 104-105, Issue 1 https://doi.org/10.1007/BF00048146	journal	January 1993
Elevated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata Kinsman, E. A.; Lewis, C.; Davies, M. S. Plant, Cell and Environment, Vol. 20, Issue 10 https://doi.org/10.1046/j.1365-3040.1997.d01-21.x	journal	October 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
Starch as a major integrator in the regulation of plant growth Sulpice, R.; Pyl, E. -T.; Ishihara, H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 25 https://doi.org/10.1073/pnas.0903478106	journal	June 2009
A simple and rapid method for the analysis of water-soluble carbohydrates from small segments of cereal leaf tissue Harrison, J.; Gallagher, J. A.; Pollock, C. J. Journal of Plant Physiology, Vol. 151, Issue 6 https://doi.org/10.1016/S0176-1617(97)80061-2	journal	January 1997
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
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
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
The Effects of Elevated CO ₂ Concentrations on Cell Division Rates, Growth Patterns, and Blade Anatomy in Young Wheat Plants Are Modulated by Factors Related to Leaf Position, Vernalization, and Genotype Masle, Josette Plant Physiology, Vol. 122, Issue 4 https://doi.org/10.1104/pp.122.4.1399	journal	April 2000
A non-targeted metabolomics approach to quantifying differences in root storage between fast- and slow-growing plants Atkinson, Rebecca R. L.; Burrell, Mike M.; Osborne, Colin P. New Phytologist, Vol. 196, Issue 1 https://doi.org/10.1111/j.1469-8137.2012.04274.x	journal	August 2012
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
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species Farquhar, G. D.; von Caemmerer, S.; Berry, J. A. Planta, Vol. 149, Issue 1 https://doi.org/10.1007/BF00386231	journal	June 1980
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
Achieving yield gains in wheat: Achieving yield gains in wheat Reynolds, Matthew; Foulkes, John; Furbank, Robert Plant, Cell & Environment, Vol. 35, Issue 10 https://doi.org/10.1111/j.1365-3040.2012.02588.x	journal	August 2012
Food Security: The Challenge of Feeding 9 Billion People Godfray, H. C. J.; Beddington, J. R.; Crute, I. R. Science, Vol. 327, Issue 5967 https://doi.org/10.1126/science.1185383	journal	January 2010
The Development of C ₄ Rice: Current Progress and Future Challenges von Caemmerer, Susanne; Quick, W. Paul; Furbank, Robert T. Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1220177	journal	June 2012
The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling - a review Schnyder, Hans New Phytologist, Vol. 123, Issue 2 https://doi.org/10.1111/j.1469-8137.1993.tb03731.x	journal	February 1993
Protein Measurement with the Folin Phenol Reagent Lowry, OliverH.; Rosebrough, NiraJ.; Farr, A. Lewis Journal of Biological Chemistry, Vol. 193, Issue 1 https://doi.org/10.1016/S0021-9258(19)52451-6	journal	November 1951

Cited By (11)

Spectroscopy can predict key leaf traits associated with source–sink balance and carbon–nitrogen status Ely, Kim S.; Burnett, Angela C.; Lieberman-Cribbin, Wil Journal of Experimental Botany, Vol. 70, Issue 6 https://doi.org/10.1093/jxb/erz061	journal	February 2019
Stress-induced senescence and plant tolerance to abiotic stress Sade, Nir; del Mar Rubio-Wilhelmi, María; Umnajkitikorn, Kamolchanok Journal of Experimental Botany, Vol. 69, Issue 4 https://doi.org/10.1093/jxb/erx235	journal	July 2017
Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies Burnett, Angela C.; Rogers, Alistair; Rees, Mark Plant Direct, Vol. 2, Issue 11 https://doi.org/10.1002/pld3.94	journal	November 2018
Sucrose promotes etiolated stem branching through activation of cytokinin accumulation followed by vacuolar invertase activity Salam, Bolaji Babajide; Barbier, Francois; Danieli, Raz https://doi.org/10.1101/2020.01.08.897009	posted_content	January 2020
Genotypic variation in source and sink traits affects the response of photosynthesis and growth to elevated atmospheric CO ₂ Fabre, Denis; Dingkuhn, Michael; Yin, Xinyou Plant, Cell & Environment, Vol. 43, Issue 3 https://doi.org/10.1111/pce.13693	journal	December 2019
Hydraulic Traits Emerge as Relevant Determinants of Growth Patterns in Wild Olive Genotypes Under Water Stress Hernandez-Santana, Virginia; Diaz-Rueda, Pablo; Diaz-Espejo, Antonio Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00291	journal	March 2019
Effects of Elevated CO2 on Wheat Yield: Non-Linear Response and Relation to Site Productivity Broberg, Malin C.; Högy, Petra; Feng, Zhaozhong Agronomy, Vol. 9, Issue 5 https://doi.org/10.3390/agronomy9050243	journal	May 2019
Increased biomass accumulation in maize grown in mixed nitrogen supply is mediated by auxin synthesis Wang, Peng; Wang, Zhangkui; Pan, Qingchun Journal of Experimental Botany, Vol. 70, Issue 6 https://doi.org/10.1093/jxb/erz047	journal	February 2019
Is triose phosphate utilization involved in the feedback inhibition of photosynthesis in rice under conditions of sink limitation? Fabre, Denis; Yin, Xinyou; Dingkuhn, Michael Journal of Experimental Botany, Vol. 70, Issue 20 https://doi.org/10.1093/jxb/erz318	journal	July 2019
The potential role of sucrose transport gene expression in the photosynthetic and yield response of rice cultivars to future CO ₂ concentration Zhang, Jishuang; Li, Danfeng; Xu, Xi Physiologia Plantarum, Vol. 168, Issue 1 https://doi.org/10.1111/ppl.12973	journal	May 2019
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

Similar Records

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

Journal Article · Mon Nov 12 00:00:00 EST 2018 · Plant Direct · OSTI ID:1336088

Burnett, Angela C.; Rogers, Alistair; Rees, Mark; +1 more

Seasonal decline in leaf photosynthesis in perennial switchgrass explained by sink limitations and water deficit

Journal Article · Wed Jan 04 00:00:00 EST 2023 · Frontiers in Plant Science · OSTI ID:1336088

Tejera-Nieves, Mauricio; Abraha, Michael; Chen, Jiquan; +3 more

Doubling the CO{sub 2} concentration enhanced the activity of carbohydrate-metabolism enzymes, source carbohydrate production, photoassimilate transport, and sink strength for Opuntia ficus-indica

Journal Article · Fri Mar 01 00:00:00 EST 1996 · Plant Physiology (Bethesda) · OSTI ID:1336088

Wang, Ning; Nobel, P S

Related Subjects

54 ENVIRONMENTAL SCIENCES

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

Citation Formats

References (56)

Cited By (11)

Similar Records

Related Subjects