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

Journal Article · · Journal of Experimental Botany
DOI: https://doi.org/10.1093/jxb/erv447 · OSTI ID:1336061
 [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

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.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0012704
OSTI ID:
1336061
Report Number(s):
BNL-112417-2016-JA; R&D Project: 2016-BNL-EE630EECA-Budg; KP1701000
Journal Information:
Journal of Experimental Botany, Vol. 67, Issue 1; ISSN 0022-0957
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 181 works
Citation information provided by
Web of Science

References (137)

Grain weight, radiation interception and use efficiency as affected by sink-strength in Mediterranean wheats released from 1940 to 2005 journal February 2009
The Mineral Nutrition of Wild Plants Revisited: A Re-evaluation of Processes and Patterns book January 1999
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) journal May 2003
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
The response of photosynthesis and stomatal conductance to rising [CO 2 ]: mechanisms and environmental interactions : Photosynthesis and stomatal conductance responses to rising [CO journal January 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
Carbohydrate Export from the Leaf: A Highly Regulated Process and Target to Enhance Photosynthesis and Productivity: Figure 1. journal October 2010
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
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
Manipulating resource allocation in plants journal January 2012
Resource Limitation in Plants-An Economic Analogy journal November 1985
STICS: a generic model for the simulation of crops and their water and nitrogen balances. I. Theory and parameterization applied to wheat and corn journal January 1998
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 journal February 1998
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. journal March 1984
The Development of C 4 Rice: Current Progress and Future Challenges journal June 2012
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
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
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
Darwinian Agriculture journal July 2012
Phylogenetic Analysis of Trait Evolution and Species Diversity Variation among Angiosperm Families journal June 1999
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
Simulation of wheat growth and development based on organ-level photosynthesis and assimilate allocation journal March 2010
Whole-plant versus leaf-level regulation of photosynthetic responses after partial defoliation in Eucalyptus globulus saplings journal February 2013
Does a Low Nitrogen Supply Necessarily Lead to Acclimation of Photosynthesis to Elevated CO 2 ? journal October 1998
Physiological control of metabolic flux: the requirement for multisite modulation journal October 1995
A Strong Nucleotypic Effect on the Cell Cycle Regardless of Ploidy Level journal March 2008
Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction journal March 2015
Uncertainties in CMIP5 Climate Projections due to Carbon Cycle Feedbacks journal January 2014
Sink strength: Learning to measure, measuring to learn journal December 1993
Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods journal July 2009
Evidence for the Existence of Three Primary Strategies in Plants and Its Relevance to Ecological and Evolutionary Theory journal November 1977
Relative Growth-Rate: Its Range and Adaptive Significance in a Local Flora journal July 1975
Genome Size Is a Strong Predictor of Root Meristem Growth Rate journal May 2010
Is ‘peak N’ key to understanding the timing of flowering in annual plants? journal October 2014
The Dilemma of Plants: To Grow or Defend journal September 1992
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
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
Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance journal March 2008
Elevated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata journal October 1997
Regulation of nitrate reductase expression in leaves by nitrate and nitrogen metabolism is completely overridden when sugars fall below a critical level journal August 2000
Tree carbon allocation dynamics determined using a carbon mass balance approach journal August 2014
Annual and interannual CO2 exchanges of the terrestrial biosphere: process-based simulations and uncertainties journal June 2000
Some Often Overlooked Plant Characteristics as Determinants of Plant Growth: A Reconsideration journal January 1991
When growth controls photosynthesis conference October 2012
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
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
Arabidopsis Vegetative Storage Protein Is an Anti-Insect Acid Phosphatase journal October 2005
Food for Thought: Lower-Than-Expected Crop Yield Stimulation with Rising CO2 Concentrations journal June 2006
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
Substrate flow in the rhizosphere journal December 1990
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 journal April 2000
Limitations to CO2-induced growth enhancement in pot studies journal July 1993
Biomass Allocation in Plants: Ontogeny or Optimality? A Test along Three Resource Gradients journal December 1999
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
Inhibition of the ADP-glucose pyrophosphorylase in transgenic potatoes leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes. journal April 1992
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
The Trehalose 6-Phosphate/SnRK1 Signaling Pathway Primes Growth Recovery following Relief of Sink Limitation journal June 2013
Metabolic and Signaling Aspects Underpinning the Regulation of Plant Carbon Nitrogen Interactions journal November 2010
Redesigning photosynthesis to sustainably meet global food and bioenergy demand journal June 2015
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
Relationship between starch degradation and carbon demand for maintenance and growth in A rabidopsis thaliana in different irradiance and temperature regimes : Starch degradation and carbon demand journal July 2014
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
Elevated CO2 and plant structure: a review journal October 1999
Control of bud activation by an auxin transport switch journal September 2009
The Calvin cycle revisited journal January 2003
Mechanism for increased leaf growth in elevated CO 2 journal January 1996
Mycorrhizas in ecosystems journal April 1991
Response of nitrate reductase activity and NIA genes expression in roots of Arabidopsis hxk1 mutant treated with selected carbon and nitrogen metabolites journal January 2015
Effect of sink size on growth response to elevated atmospheric CO2 within the genus Brassica journal January 1998
Achieving yield gains in wheat: Achieving yield gains in wheat journal August 2012
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 journal October 1998
Will Elevated Carbon Dioxide Concentration Amplify the Benefits of Nitrogen Fixation in Legumes? journal September 2009
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
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
Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates journal January 2011
The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling - a review journal February 1993
Starch storage in the stems of wheat plants: localization and temporal changes journal February 2009
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
Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model journal February 2003
Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production journal June 2012
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
The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background journal June 1999
Starch turnover: pathways, regulation and role in growth journal June 2012
Interplay between Sucrose and Folate Modulates Auxin Signaling in Arabidopsis journal May 2013
Auxin–Cytokinin Interaction Regulates Meristem Development journal July 2011
Elevated CO2 and plant growth: cellular mechanisms and responses of whole plants journal November 1994
The Arabidopsis GSQ5/DOG1 Cvi allele is induced by the ABA-mediated sugar signalling pathway, and enhances sugar sensitivity by stimulating ABI4 expression journal August 2008
Plant growth rates and seed size: a re-evaluation journal June 2012
Functional–structural plant modelling: a new versatile tool in crop science journal December 2009
Increasing Sucrose Uptake Capacity of Wheat Grains Stimulates Storage Protein Synthesis journal December 2009
A winter wheat crop simulation model without water or nutrient limitations journal April 1984
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
Modelling plant resource allocation and growth partitioning in response to environmental heterogeneity journal January 2005
Carbon and nitrogen cycle dynamics in the O-CN land surface model: 2. Role of the nitrogen cycle in the historical terrestrial carbon balance: NITROGEN EFFECTS ON GLOBAL C CYCLING journal February 2010
Starch: Its Metabolism, Evolution, and Biotechnological Modification in Plants journal June 2010
Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm journal August 2007
Evidence against sink limitation by the sucrose-to-starch route in potato plants expressing fructosyltransferases journal July 2011
Regulation and function of root exudates journal December 2008
The plant traits that drive ecosystems: Evidence from three continents journal February 2004
Novel Regulation of Vegetative Storage Protein Genes journal January 1990
Plant growth rates and seed size: a re-evaluation text January 2012
Phylogenetic Analysis of Trait Evolution and Species Diversity Variation Among Angiosperm Families journal June 1999
Metabolic Repression of Transcription in Higher Plants journal October 1990
The costs and benefits of fast living text January 2009
Cell Cycle and Environmental Stresses journal April 2018

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