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

Abstract

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 maximizingmore » growth of elite cereals under future elevated [CO2].« less

Authors:
 [1];  [2];  [1];  [1]
  1. Univ. of Sheffield (United Kingdom). Dept. of Animal and Plant Sciences
  2. Brookhaven National Lab. (BNL), Upton, NY (United States). Environmental and Climate Sciences Dept.
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1336088
Report Number(s):
BNL-112493-2016-JA
Journal ID: ISSN 0140-7791; R&D Project: 2016-BNL-EE630EECA-Budg; KP1701000
Grant/Contract Number:  
SC00112704
Resource Type:
Accepted Manuscript
Journal Name:
Plant, Cell and Environment
Additional Journal Information:
Journal Volume: 39; Journal Issue: 11; Journal ID: ISSN 0140-7791
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Burnett, Angela C., Rogers, A., Rees, M., and Osborne, Colin P. Carbon source-sink limitations differ between two species with contrasting growth strategies: Source-sink limitations vary with growth strategy. United States: N. p., 2016. Web. doi:10.1111/pce.12801.
Burnett, Angela C., Rogers, A., Rees, M., & Osborne, Colin P. Carbon source-sink limitations differ between two species with contrasting growth strategies: Source-sink limitations vary with growth strategy. United States. https://doi.org/10.1111/pce.12801
Burnett, Angela C., Rogers, A., Rees, M., and Osborne, Colin P. Thu . "Carbon source-sink limitations differ between two species with contrasting growth strategies: Source-sink limitations vary with growth strategy". United States. https://doi.org/10.1111/pce.12801. https://www.osti.gov/servlets/purl/1336088.
@article{osti_1336088,
title = {Carbon source-sink limitations differ between two species with contrasting growth strategies: Source-sink limitations vary with growth strategy},
author = {Burnett, Angela C. and Rogers, A. and Rees, M. and Osborne, Colin P.},
abstractNote = {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].},
doi = {10.1111/pce.12801},
journal = {Plant, Cell and Environment},
number = 11,
volume = 39,
place = {United States},
year = {Thu Sep 22 00:00:00 EDT 2016},
month = {Thu Sep 22 00:00:00 EDT 2016}
}

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Works referenced in this record:

Temporal Changes in Allocation and Partitioning of New Carbon as 11 C Elicited by Simulated Herbivory Suggest that Roots Shape Aboveground Responses in Arabidopsis
journal, December 2012

  • Ferrieri, Abigail P.; Agtuca, Beverly; Appel, Heidi M.
  • Plant Physiology, Vol. 161, Issue 2
  • DOI: 10.1104/pp.112.208868

Sink strength: Learning to measure, measuring to learn
journal, December 1993


Re-engineering of carbon fixation in plants – challenges for plant biotechnology to improve yields in a high-CO2 world
journal, April 2012


Does elevated atmospheric [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves?
journal, December 2006

  • Ainsworth, E. A.; Rogers, A.; Leakey, A. D. B.
  • Journal of Experimental Botany, Vol. 58, Issue 3
  • DOI: 10.1093/jxb/erl233

Grain Filling and Dry Matter Translocation Responses to Source–Sink Modifications in a Historical Series of Durum Wheat
journal, January 2008


Solutions for a cultivated planet
journal, October 2011

  • Foley, Jonathan A.; Ramankutty, Navin; Brauman, Kate A.
  • Nature, Vol. 478, Issue 7369
  • DOI: 10.1038/nature10452

Increasing Sucrose Uptake Capacity of Wheat Grains Stimulates Storage Protein Synthesis
journal, December 2009

  • Weichert, Nicola; Saalbach, Isolde; Weichert, Heiko
  • Plant Physiology, Vol. 152, Issue 2
  • DOI: 10.1104/pp.109.150854

Architectural Evolution and its Implications for Domestication in Grasses
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
journal, July 2008


Grain weight, radiation interception and use efficiency as affected by sink-strength in Mediterranean wheats released from 1940 to 2005
journal, February 2009


Effects of source-sink relations on photosynthetic acclimation to elevated CO2
journal, October 1991


Targets for Crop Biotechnology in a Future High-CO 2 and High-O 3 World
journal, April 2008

  • Ainsworth, Elizabeth A.; Rogers, Alistair; Leakey, Andrew D. B.
  • Plant Physiology, Vol. 147, Issue 1
  • DOI: 10.1104/pp.108.117101

Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments
journal, August 2013


Redesigning photosynthesis to sustainably meet global food and bioenergy demand
journal, June 2015

  • Ort, Donald R.; Merchant, Sabeeha S.; Alric, Jean
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 28
  • DOI: 10.1073/pnas.1424031112

Evidence against sink limitation by the sucrose-to-starch route in potato plants expressing fructosyltransferases
journal, July 2011


Growth Analysis of Congeneric Annual and Perennial Grass Species
journal, December 1992

  • Garnier, E.
  • The Journal of Ecology, Vol. 80, Issue 4
  • DOI: 10.2307/2260858

Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction
journal, March 2015

  • Freschet, Grégoire T.; Swart, Elferra M.; Cornelissen, Johannes H. C.
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13352

Coordination of carbon supply and plant growth
journal, September 2007


Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE
journal, April 2009

  • Leakey, Andrew D. B.; Ainsworth, Elizabeth A.; Bernacchi, Carl J.
  • Journal of Experimental Botany, Vol. 60, Issue 10
  • DOI: 10.1093/jxb/erp096

Is barley yield in the UK sink limited?
journal, March 2007


Is barley yield in the UK sink limited?
journal, March 2007


Whole-plant versus leaf-level regulation of photosynthetic responses after partial defoliation in Eucalyptus globulus saplings
journal, February 2013

  • Eyles, Alieta; Pinkard, Elizabeth A.; Davies, Noel W.
  • Journal of Experimental Botany, Vol. 64, Issue 6
  • DOI: 10.1093/jxb/ert017

Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance
journal, January 1997


Genes and Mutations Underlying Domestication Transitions in Grasses: Figure 1.
journal, January 2009


The dynamics of recovery and growth: how defoliation affects stored resources
journal, May 2014

  • Atkinson, R. R. L.; Burrell, M. M.; Rose, K. E.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1783
  • DOI: 10.1098/rspb.2013.3355

Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume
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
journal, March 2004


Recommendations for Reporting Metabolite Data
journal, July 2011

  • Fernie, Alisdair R.; Aharoni, Asaph; Willmitzer, Lothar
  • The Plant Cell, Vol. 23, Issue 7
  • DOI: 10.1105/tpc.111.086272

Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1.
journal, October 2010

  • Ainsworth, Elizabeth A.; Bush, Daniel R.
  • Plant Physiology, Vol. 155, Issue 1
  • DOI: 10.1104/pp.110.167684

Source/sink interactions underpin crop yield: the case for trehalose 6-phosphate/SnRK1 in improvement of wheat
journal, August 2014


Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration
journal, January 1993


Elevated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata
journal, October 1997


Starch as a major integrator in the regulation of plant growth
journal, June 2009

  • Sulpice, R.; Pyl, E. -T.; Ishihara, H.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 25
  • DOI: 10.1073/pnas.0903478106

A simple and rapid method for the analysis of water-soluble carbohydrates from small segments of cereal leaf tissue
journal, January 1997


How can we make plants grow faster? A source–sink perspective on growth rate
journal, October 2015

  • White, Angela C.; Rogers, Alistair; Rees, Mark
  • Journal of Experimental Botany, Vol. 67, Issue 1
  • DOI: 10.1093/jxb/erv447

Manipulating resource allocation in plants
journal, January 2012

  • Bennett, E.; Roberts, J. A.; Wagstaff, C.
  • Journal of Experimental Botany, Vol. 63, Issue 9
  • DOI: 10.1093/jxb/err442

Relative Growth-Rate: Its Range and Adaptive Significance in a Local Flora
journal, July 1975

  • Grime, J. P.; Hunt, Roderick
  • The Journal of Ecology, Vol. 63, Issue 2
  • DOI: 10.2307/2258728

A non-targeted metabolomics approach to quantifying differences in root storage between fast- and slow-growing plants
journal, August 2012


Photosynthetic Responses in Annual Rye, Perennial Wheat, and Perennial Rye Subjected to Modest Source:Sink Ratio Changes
journal, January 2014


A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
journal, June 1980

  • Farquhar, G. D.; von Caemmerer, S.; Berry, J. A.
  • Planta, Vol. 149, Issue 1
  • DOI: 10.1007/BF00386231

Achieving yield gains in wheat: Achieving yield gains in wheat
journal, August 2012


Food Security: The Challenge of Feeding 9 Billion People
journal, January 2010


The Development of C 4 Rice: Current Progress and Future Challenges
journal, June 2012

  • von Caemmerer, Susanne; Quick, W. Paul; Furbank, Robert T.
  • Science, Vol. 336, Issue 6089
  • DOI: 10.1126/science.1220177

Protein Measurement with the Folin Phenol Reagent
journal, November 1951


Works referencing / citing this record:

Spectroscopy can predict key leaf traits associated with source–sink balance and carbon–nitrogen status
journal, February 2019

  • Ely, Kim S.; Burnett, Angela C.; Lieberman-Cribbin, Wil
  • Journal of Experimental Botany, Vol. 70, Issue 6
  • DOI: 10.1093/jxb/erz061

Stress-induced senescence and plant tolerance to abiotic stress
journal, July 2017

  • Sade, Nir; del Mar Rubio-Wilhelmi, María; Umnajkitikorn, Kamolchanok
  • Journal of Experimental Botany, Vol. 69, Issue 4
  • DOI: 10.1093/jxb/erx235

Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies
journal, November 2018

  • Burnett, Angela C.; Rogers, Alistair; Rees, Mark
  • Plant Direct, Vol. 2, Issue 11
  • DOI: 10.1002/pld3.94

Genotypic variation in source and sink traits affects the response of photosynthesis and growth to elevated atmospheric CO 2
journal, December 2019

  • Fabre, Denis; Dingkuhn, Michael; Yin, Xinyou
  • Plant, Cell & Environment, Vol. 43, Issue 3
  • DOI: 10.1111/pce.13693

Hydraulic Traits Emerge as Relevant Determinants of Growth Patterns in Wild Olive Genotypes Under Water Stress
journal, March 2019

  • Hernandez-Santana, Virginia; Diaz-Rueda, Pablo; Diaz-Espejo, Antonio
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.00291

Effects of Elevated CO2 on Wheat Yield: Non-Linear Response and Relation to Site Productivity
journal, May 2019


Increased biomass accumulation in maize grown in mixed nitrogen supply is mediated by auxin synthesis
journal, February 2019

  • Wang, Peng; Wang, Zhangkui; Pan, Qingchun
  • Journal of Experimental Botany, Vol. 70, Issue 6
  • DOI: 10.1093/jxb/erz047

Is triose phosphate utilization involved in the feedback inhibition of photosynthesis in rice under conditions of sink limitation?
journal, July 2019

  • Fabre, Denis; Yin, Xinyou; Dingkuhn, Michael
  • Journal of Experimental Botany, Vol. 70, Issue 20
  • DOI: 10.1093/jxb/erz318