skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: How can we make plants grow faster? A source–sink perspective on growth rate

Abstract

Growth is a major component of fitness in all organisms, an important mediator of competitive interactions in plant communities, and a central determinant of yield in crops. Understanding what limits plant growth is therefore of fundamental importance to plant evolution, ecology, and crop science, but each discipline views the process from a different perspective. This review highlights the importance of source–sink interactions as determinants of growth. The evidence for source- and sink-limitation of growth, and the ways in which regulatory molecular feedback systems act to maintain an appropriate source:sink balance, are first discussed. Evidence clearly shows that future increases in crop productivity depend crucially on a quantitative understanding of the extent to which sources or sinks limit growth, and how this changes during development. In addition, to identify bottlenecks limiting growth and yield, a holistic view of growth is required at the whole-plant scale, incorporating mechanistic interactions between physiology, resource allocation, and plant development. Such a holistic perspective on source–sink interactions will allow the development of a more integrated, whole-system level understanding of growth, with benefits across multiple disciplines.

Authors:
 [1];  [2];  [1];  [1]
  1. Univ. of Sheffield (United Kingdom). Department of Animal and Plant Sciences
  2. Brookhaven National Lab. (BNL), Upton, NY (United States). Biological, Environmental and Climate Sciences Department
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1336061
Report Number(s):
BNL-112417-2016-JA
Journal ID: ISSN 0022-0957; R&D Project: 2016-BNL-EE630EECA-Budg; KP1701000
Grant/Contract Number:  
SC0012704
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 67; Journal Issue: 1; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; carbon; crops; models; nitrogen; plant growth; regulation; sink; source

Citation Formats

White, Angela C., Rogers, Alistair, Rees, Mark, and Osborne, Colin P. How can we make plants grow faster? A source–sink perspective on growth rate. United States: N. p., 2015. Web. doi:10.1093/jxb/erv447.
White, Angela C., Rogers, Alistair, Rees, Mark, & Osborne, Colin P. How can we make plants grow faster? A source–sink perspective on growth rate. United States. doi:10.1093/jxb/erv447.
White, Angela C., Rogers, Alistair, Rees, Mark, and Osborne, Colin P. Wed . "How can we make plants grow faster? A source–sink perspective on growth rate". United States. doi:10.1093/jxb/erv447. https://www.osti.gov/servlets/purl/1336061.
@article{osti_1336061,
title = {How can we make plants grow faster? A source–sink perspective on growth rate},
author = {White, Angela C. and Rogers, Alistair and Rees, Mark and Osborne, Colin P.},
abstractNote = {Growth is a major component of fitness in all organisms, an important mediator of competitive interactions in plant communities, and a central determinant of yield in crops. Understanding what limits plant growth is therefore of fundamental importance to plant evolution, ecology, and crop science, but each discipline views the process from a different perspective. This review highlights the importance of source–sink interactions as determinants of growth. The evidence for source- and sink-limitation of growth, and the ways in which regulatory molecular feedback systems act to maintain an appropriate source:sink balance, are first discussed. Evidence clearly shows that future increases in crop productivity depend crucially on a quantitative understanding of the extent to which sources or sinks limit growth, and how this changes during development. In addition, to identify bottlenecks limiting growth and yield, a holistic view of growth is required at the whole-plant scale, incorporating mechanistic interactions between physiology, resource allocation, and plant development. Such a holistic perspective on source–sink interactions will allow the development of a more integrated, whole-system level understanding of growth, with benefits across multiple disciplines.},
doi = {10.1093/jxb/erv447},
journal = {Journal of Experimental Botany},
number = 1,
volume = 67,
place = {United States},
year = {2015},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 13 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

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


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


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


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

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


The McCree–de Wit–Penning de Vries–Thornley Respiration Paradigms: 30 Years Later
journal, July 2000


Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2
journal, April 2013

  • Aranjuelo, Iker; Sanz-Sáez, Álvaro; Jauregui, Iván
  • Journal of Experimental Botany, Vol. 64, Issue 7
  • DOI: 10.1093/jxb/ert081

Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues: TCA control and regulation in plant tissues
journal, June 2011


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


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


Regulation and function of root exudates
journal, June 2009


Decoupled leaf and stem economics in rain forest trees: Decoupled leaf and stem economics spectra
journal, August 2010


Allocating Resources to Reproduction and Defense
journal, January 1987

  • Bazzaz, Fakhri A.; Chiariello, Nona R.; Coley, Phyllis D.
  • BioScience, Vol. 37, Issue 1
  • DOI: 10.2307/1310178

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

Resource Limitation in Plants-An Economic Analogy
journal, November 1985


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

Mycorrhiza-induced resistance: more than the sum of its parts?
journal, October 2013


Multiscale digital Arabidopsis predicts individual organ and whole-organism growth
journal, September 2014

  • Chew, Yin Hoon; Wenden, Bénédicte; Flis, Anna
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 39
  • DOI: 10.1073/pnas.1410238111

Responses of shoot and root gas exchange, leaf blade expansion and biomass production to pulses of elevated C0 2 in hydroponic wheat
journal, January 1995

  • Christ, Rudolf A.; Körner, Christian
  • Journal of Experimental Botany, Vol. 46, Issue 11
  • DOI: 10.1093/jxb/46.11.1661

Resource Availability and Plant Antiherbivore Defense
journal, November 1985


Environmental Constraints on a Global Relationship Among leaf and root Traits of Grasses
journal, January 2005

  • Craine, Joseph M.; Lee, William G.; Bond, William J.
  • Ecology, Vol. 86, Issue 1
  • DOI: 10.1890/04-1075

The plant traits that drive ecosystems: Evidence from three continents
journal, January 2004


Phylogenetic Analysis of Trait Evolution and Species Diversity Variation among Angiosperm Families
journal, June 1999

  • Dodd, Michael E.; Silvertown, Jonathan; Chase, Mark W.
  • Evolution, Vol. 53, Issue 3
  • DOI: 10.2307/2640713

Sink strength: Dynamic with source strength
journal, December 1993


The most abundant protein in the world
journal, November 1979


Photosynthesis and nitrogen relationships in leaves of C3 plants
journal, January 1989


Sugars, signalling, and plant development
journal, December 2011

  • Eveland, A. L.; Jackson, D. P.
  • Journal of Experimental Botany, Vol. 63, Issue 9
  • DOI: 10.1093/jxb/err379

Simulation of wheat growth and development based on organ-level photosynthesis and assimilate allocation
journal, March 2010

  • Evers, J. B.; Vos, J.; Yin, X.
  • Journal of Experimental Botany, Vol. 61, Issue 8
  • DOI: 10.1093/jxb/erq025

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

Does a Low Nitrogen Supply Necessarily Lead to Acclimation of Photosynthesis to Elevated CO 2 ?
journal, October 1998

  • Farage, Peter K.; McKee, Ian F.; Long, Steve P.
  • Plant Physiology, Vol. 118, Issue 2
  • DOI: 10.1104/pp.118.2.573

Physiological control of metabolic flux: the requirement for multisite modulation
journal, October 1995

  • Fell, D. A.; Thomas, S.
  • Biochemical Journal, Vol. 311, Issue 1
  • DOI: 10.1042/bj3110035

A Strong Nucleotypic Effect on the Cell Cycle Regardless of Ploidy Level
journal, March 2008

  • Francis, D.; Davies, M. S.; Barlow, P. W.
  • Annals of Botany, Vol. 101, Issue 6
  • DOI: 10.1093/aob/mcn038

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

Uncertainties in CMIP5 Climate Projections due to Carbon Cycle Feedbacks
journal, January 2014

  • Friedlingstein, Pierre; Meinshausen, Malte; Arora, Vivek K.
  • Journal of Climate, Vol. 27, Issue 2
  • DOI: 10.1175/JCLI-D-12-00579.1

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


Evidence for the Existence of Three Primary Strategies in Plants and Its Relevance to Ecological and Evolutionary Theory
journal, November 1977

  • Grime, J. P.
  • The American Naturalist, Vol. 111, Issue 982
  • DOI: 10.1086/283244

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

Genome Size Is a Strong Predictor of Root Meristem Growth Rate
journal, May 2010

  • Gruner, Adam; Hoverter, Nathan; Smith, Tylia
  • Journal of Botany, Vol. 2010
  • DOI: 10.1155/2010/390414

Is ‘peak N’ key to understanding the timing of flowering in annual plants?
journal, October 2014

  • Guilbaud, Camille S. E.; Dalchau, Neil; Purves, Drew W.
  • New Phytologist, Vol. 205, Issue 2
  • DOI: 10.1111/nph.13095

The Dilemma of Plants: To Grow or Defend
journal, September 1992

  • Herms, Daniel A.; Mattson, William J.
  • The Quarterly Review of Biology, Vol. 67, Issue 3
  • DOI: 10.1086/417659

Atmospheric CO2 forces abrupt vegetation shifts locally, but not globally
journal, June 2012


Short-Term Dynamics of a Neotropical Forest: Why Ecological Research Matters to Tropical Conservation and Management
journal, February 1992

  • Hubbell, Stephen P.; Foster, Robin B.
  • Oikos, Vol. 63, Issue 1
  • DOI: 10.2307/3545515

Sirius: a mechanistic model of wheat response to environmental variation
journal, April 1998


Modulation of nitrate reductase: some new insights, an unusual case and a potentially important side reaction
journal, April 2002

  • Kaiser, Werner M.; Weiner, Hendrik; Kandlbinder, Andrea
  • Journal of Experimental Botany, Vol. 53, Issue 370
  • DOI: 10.1093/jexbot/53.370.875

Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance
journal, March 2008

  • Kawakami, A.; Sato, Y.; Yoshida, M.
  • Journal of Experimental Botany, Vol. 59, Issue 4
  • DOI: 10.1093/jxb/erm367

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


Tree carbon allocation dynamics determined using a carbon mass balance approach
journal, August 2014

  • Klein, Tamir; Hoch, Günter
  • New Phytologist, Vol. 205, Issue 1
  • DOI: 10.1111/nph.12993

Some Often Overlooked Plant Characteristics as Determinants of Plant Growth: A Reconsideration
journal, January 1991


When growth controls photosynthesis
conference, October 2012

  • Korner, Christian
  • 2012 IEEE 4th International Symposium on Plant Growth Modeling, Simulation, Visualization and Applications (PMA)
  • DOI: 10.1109/PMA.2012.6524804

CO2 responsiveness of plants: a possible link to phloem loading
journal, May 1995


Sugar signals and the control of plant growth and development
journal, January 2014

  • Lastdrager, Jeroen; Hanson, Johannes; Smeekens, Sjef
  • Journal of Experimental Botany, Vol. 65, Issue 3
  • DOI: 10.1093/jxb/ert474

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


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

Arabidopsis Vegetative Storage Protein Is an Anti-Insect Acid Phosphatase
journal, October 2005


Can improvement in photosynthesis increase crop yields?
journal, March 2006


A simulation and mechanism analysis of long-term variations at land surface over arid/semi-arid area in north China
journal, January 2006

  • Lu, Jianhua; Ji, Jinjun
  • Journal of Geophysical Research, Vol. 111, Issue D9
  • DOI: 10.1029/2005JD006252

Substrate flow in the rhizosphere
journal, December 1990


Limitations to CO2-induced growth enhancement in pot studies
journal, July 1993

  • McConnaughay, K. D. M.; Berntson, G. M.; Bazzaz, F. A.
  • Oecologia, Vol. 94, Issue 4
  • DOI: 10.1007/BF00566971

Biomass Allocation in Plants: Ontogeny or Optimality? A Test along Three Resource Gradients
journal, December 1999

  • McConnaughay, K. D. M.; Coleman, J. S.
  • Ecology, Vol. 80, Issue 8
  • DOI: 10.2307/177242

Growth-survival trade-offs and allometries in rosette-forming perennials
journal, April 2006


The accumulation and storage of nitrogen by herbaceous plants
journal, January 1988


Agriculture and the new challenges for photosynthesis research
journal, December 2008


The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf: A review of the hypothesis
journal, April 1968

  • Neales, T. F.; Incoll, L. D.
  • The Botanical Review, Vol. 34, Issue 2
  • DOI: 10.1007/BF02872604

The Trehalose 6-Phosphate/SnRK1 Signaling Pathway Primes Growth Recovery following Relief of Sink Limitation
journal, June 2013

  • Nunes, C.; O'Hara, L. E.; Primavesi, L. F.
  • PLANT PHYSIOLOGY, Vol. 162, Issue 3
  • DOI: 10.1104/pp.113.220657

Metabolic and Signaling Aspects Underpinning the Regulation of Plant Carbon Nitrogen Interactions
journal, November 2010

  • Nunes-Nesi, Adriano; Fernie, Alisdair R.; Stitt, Mark
  • Molecular Plant, Vol. 3, Issue 6
  • DOI: 10.1093/mp/ssq049

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

Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny
journal, August 2012


Quantifying how winter wheat crops accumulate and use nitrogen reserves during growth
journal, February 2012


Sink strength: Whole plant considerations
journal, December 1993


Sink regulation of photosynthesis
journal, July 2001


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


Fructan Metabolism in Grasses and Cereals
journal, June 1991


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


Pot size matters: a meta-analysis of the effects of rooting volume on plant growth
journal, January 2012

  • Poorter, Hendrik; Bühler, Jonas; van Dusschoten, Dagmar
  • Functional Plant Biology, Vol. 39, Issue 11
  • DOI: 10.1071/FP12049

Elevated CO2 and plant structure: a review
journal, October 1999


Control of bud activation by an auxin transport switch
journal, September 2009

  • Prusinkiewicz, P.; Crawford, S.; Smith, R. S.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 41
  • DOI: 10.1073/pnas.0906696106

Mechanism for increased leaf growth in elevated CO 2
journal, January 1996

  • Ranasinghe, Sanathanie; Taylor, Gail
  • Journal of Experimental Botany, Vol. 47, Issue 3
  • DOI: 10.1093/jxb/47.3.349

Mycorrhizas in ecosystems
journal, April 1991


Effect of sink size on growth response to elevated atmospheric CO2 within the genus Brassica
journal, January 1998

  • Reekie, Edward G.; MacDougall, Glenn; Wong, Ivan
  • Canadian Journal of Botany, Vol. 76, Issue 5
  • DOI: 10.1139/cjb-76-5-829

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


Will Elevated Carbon Dioxide Concentration Amplify the Benefits of Nitrogen Fixation in Legumes?
journal, September 2009

  • Rogers, Alistair; Ainsworth, Elizabeth A.; Leakey, Andrew D. B.
  • Plant Physiology, Vol. 151, Issue 3
  • DOI: 10.1104/pp.109.144113

The costs and benefits of fast living: The costs and benefits of fast living
journal, October 2009


Genotypic variation in water-soluble carbohydrate accumulation in wheat
journal, January 2006

  • Ruuska, Sari A.; Rebetzke, Greg J.; van Herwaarden, Anthony F.
  • Functional Plant Biology, Vol. 33, Issue 9
  • DOI: 10.1071/FP06062

The Nitrogen Use Efficiency of C 3 and C 4 Plants : III. Leaf Nitrogen Effects on the Activity of Carboxylating Enzymes in
journal, October 1987

  • Sage, Rowan F.; Pearcy, Robert W.; Seemann, Jeffrey R.
  • Plant Physiology, Vol. 85, Issue 2
  • DOI: 10.1104/pp.85.2.355

Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates
journal, January 2011


Starch storage in the stems of wheat plants: localization and temporal changes
journal, February 2009

  • Scofield, Graham N.; Ruuska, Sari A.; Aoki, Naohiro
  • Annals of Botany, Vol. 103, Issue 6
  • DOI: 10.1093/aob/mcp010

Metabolic repression of transcription in higher plants.
journal, October 1990


Plant Storage Proteins
journal, August 1995


Determinate Root Growth and Meristem Maintenance in Angiosperms
journal, December 2007

  • Shishkova, S.; Rost, T. L.; Dubrovsky, J. G.
  • Annals of Botany, Vol. 101, Issue 3
  • DOI: 10.1093/aob/mcm251

Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model
journal, February 2003


Coordination of carbon supply and plant growth
journal, September 2007


Starch in the Arabidopsis plant
journal, February 2012


A genetic playground for enhancing grain number in cereals
journal, February 2012


Novel Regulation of Vegetative Storage Protein Genes.
journal, January 1990


Starch turnover: pathways, regulation and role in growth
journal, June 2012


Interplay between Sucrose and Folate Modulates Auxin Signaling in Arabidopsis
journal, May 2013

  • Stokes, M. E.; Chattopadhyay, A.; Wilkins, O.
  • PLANT PHYSIOLOGY, Vol. 162, Issue 3
  • DOI: 10.1104/pp.113.215095

Auxin–Cytokinin Interaction Regulates Meristem Development
journal, July 2011

  • Su, Ying-Hua; Liu, Yu-Bo; Zhang, Xian-Sheng
  • Molecular Plant, Vol. 4, Issue 4
  • DOI: 10.1093/mp/ssr007

Elevated CO2 and plant growth: cellular mechanisms and responses of whole plants
journal, November 1994


Plant growth rates and seed size: a re-evaluation
journal, June 2012

  • Turnbull, Lindsay A.; Philipson, Christopher D.; Purves, Drew W.
  • Ecology, Vol. 93, Issue 6
  • DOI: 10.1890/11-0261.1

Functional–structural plant modelling: a new versatile tool in crop science
journal, December 2009

  • Vos, J.; Evers, J. B.; Buck-Sorlin, G. H.
  • Journal of Experimental Botany, Vol. 61, Issue 8
  • DOI: 10.1093/jxb/erp345

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

A winter wheat crop simulation model without water or nutrient limitations
journal, April 1984

  • Weir, A. H.; Bragg, P. L.; Porter, J. R.
  • The Journal of Agricultural Science, Vol. 102, Issue 2
  • DOI: 10.1017/S0021859600042702

Optimal acclimation of the C3 photosynthetic system under enhanced CO2
journal, March 1994


Functional traits and the growth–mortality trade‐off in tropical trees
journal, December 2010

  • Wright, S. Joseph; Kitajima, Kaoru; Kraft, Nathan J. B.
  • Ecology, Vol. 91, Issue 12
  • DOI: 10.1890/09-2335.1

Modelling plant resource allocation and growth partitioning in response to environmental heterogeneity
journal, January 2005


Starch: Its Metabolism, Evolution, and Biotechnological Modification in Plants
journal, June 2010


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


    Works referencing / citing this record:

    Heat stress effects on source–sink relationships and metabolome dynamics in wheat
    journal, June 2019

    • Abdelrahman, Mostafa; Burritt, David J.; Gupta, Aarti
    • Journal of Experimental Botany, Vol. 71, Issue 2
    • DOI: 10.1093/jxb/erz296