DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana

Abstract

Leaf area growth determines the light interception capacity of a crop and is often used as a surrogate for plant growth in high-throughput phenotyping systems. The relationship between leaf area growth and growth in terms of mass will depend on how carbon is partitioned among new leaf area, leaf mass, root mass, reproduction, and respiration. A model of leaf area growth in terms of photosynthetic rate and carbon partitioning to different plant organs was developed and tested with Arabidopsis thaliana L. Heynh. ecotype Columbia (Col-0) and a mutant line, gigantea-2 (gi-2), which develops very large rosettes. Data obtained from growth analysis and gas exchange measurements was used to train a genetic programming algorithm to parameterize and test the above model. The relationship between leaf area and plant biomass was found to be non-linear and variable depending on carbon partitioning. The model output was sensitive to the rate of photosynthesis but more sensitive to the amount of carbon partitioned to growing thicker leaves. The large rosette size of gi-2 relative to that of Col-0 resulted from relatively small differences in partitioning to new leaf area vs. leaf thickness.

Authors:
 [1];  [2];  [1];  [3];  [1];  [1]
  1. Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
  2. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab., Dept. of Computer Science
  3. Wageningen Univ., Wageningen (Netherlands). Center for Crop Systems Analysis
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1184839
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
carbon partitioning; photosynthesis; leaf area; leaf thickening; growth; specific leaf area

Citation Formats

Weraduwage, Sarathi M., Chen, Jin, Anozie, Fransisca C., Morales, Alejandro, Weise, Sean E., and Sharkey, Thomas D. The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. United States: N. p., 2015. Web. doi:10.3389/fpls.2015.00167.
Weraduwage, Sarathi M., Chen, Jin, Anozie, Fransisca C., Morales, Alejandro, Weise, Sean E., & Sharkey, Thomas D. The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. United States. https://doi.org/10.3389/fpls.2015.00167
Weraduwage, Sarathi M., Chen, Jin, Anozie, Fransisca C., Morales, Alejandro, Weise, Sean E., and Sharkey, Thomas D. Thu . "The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana". United States. https://doi.org/10.3389/fpls.2015.00167. https://www.osti.gov/servlets/purl/1184839.
@article{osti_1184839,
title = {The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana},
author = {Weraduwage, Sarathi M. and Chen, Jin and Anozie, Fransisca C. and Morales, Alejandro and Weise, Sean E. and Sharkey, Thomas D.},
abstractNote = {Leaf area growth determines the light interception capacity of a crop and is often used as a surrogate for plant growth in high-throughput phenotyping systems. The relationship between leaf area growth and growth in terms of mass will depend on how carbon is partitioned among new leaf area, leaf mass, root mass, reproduction, and respiration. A model of leaf area growth in terms of photosynthetic rate and carbon partitioning to different plant organs was developed and tested with Arabidopsis thaliana L. Heynh. ecotype Columbia (Col-0) and a mutant line, gigantea-2 (gi-2), which develops very large rosettes. Data obtained from growth analysis and gas exchange measurements was used to train a genetic programming algorithm to parameterize and test the above model. The relationship between leaf area and plant biomass was found to be non-linear and variable depending on carbon partitioning. The model output was sensitive to the rate of photosynthesis but more sensitive to the amount of carbon partitioned to growing thicker leaves. The large rosette size of gi-2 relative to that of Col-0 resulted from relatively small differences in partitioning to new leaf area vs. leaf thickness.},
doi = {10.3389/fpls.2015.00167},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {Thu Apr 09 00:00:00 EDT 2015},
month = {Thu Apr 09 00:00:00 EDT 2015}
}

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

Citation Metrics:
Cited by: 195 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Model-Based Analysis of Arabidopsis Leaf Epidermal Cells Reveals Distinct Division and Expansion Patterns for Pavement and Guard Cells
journal, June 2011

  • Kheibarshekan Asl, Leila; Dhondt, Stijn; Boudolf, Véronique
  • Plant Physiology, Vol. 156, Issue 4
  • DOI: 10.1104/pp.111.181180

MassFlowDyn I: A Carbon Transport and Partitioning Model for Root System Architecture
journal, June 2000


Nighttime Stomatal Conductance and Transpiration in C 3 and C 4 Plants
journal, January 2007

  • Caird, Mairgareth A.; Richards, James H.; Donovan, Lisa A.
  • Plant Physiology, Vol. 143, Issue 1
  • DOI: 10.1104/pp.106.092940

Influence of Instantaneous and Integrated Light-Flux Density on Leaf Anatomy and Photosynthesis
journal, September 1979

  • Chabot, Brian F.; Jurik, Thomas W.; Chabot, Jean F.
  • American Journal of Botany, Vol. 66, Issue 8
  • DOI: 10.2307/2442235

Magnitude of nighttime transpiration does not affect plant growth or nutrition in well-watered Arabidopsis
journal, July 2009


A fast and elitist multiobjective genetic algorithm: NSGA-II
journal, April 2002

  • Deb, K.; Pratap, A.; Agarwal, S.
  • IEEE Transactions on Evolutionary Computation, Vol. 6, Issue 2
  • DOI: 10.1109/4235.996017

Variational Gaussian process classifiers
journal, January 2000

  • Mackay, D. J. C.; Gibbs, M. N.
  • IEEE Transactions on Neural Networks, Vol. 11, Issue 6
  • DOI: 10.1109/72.883477

Crop Productivity and Photoassimilate Partitioning
journal, August 1984


Adaptation to Sun and Shade: a Whole-Plant Perspective
journal, January 1988


Accurate inference of shoot biomass from high-throughput images of cereal plants
journal, January 2011

  • Golzarian, Mahmood R.; Frick, Ross A.; Rajendran, Karthika
  • Plant Methods, Vol. 7, Issue 1
  • DOI: 10.1186/1746-4811-7-2

Tree Branch Angle: Maximizing Effective Leaf Area
journal, February 1978


Multiple Objective Decision Making — Methods and Applications
book, January 1979


Variations in leaf mass per area according to N nutrition, plant age, and leaf position reflect ontogenetic plasticity in winter oilseed rape (Brassica napus L.)
journal, November 2009

  • Jullien, Alexandra; Allirand, Jean-Michel; Mathieu, Amélie
  • Field Crops Research, Vol. 114, Issue 2
  • DOI: 10.1016/j.fcr.2009.07.015

Effects of leaf and plant age on specific leaf area in deciduous tree species Quercus cerris L. var. Cerris
journal, February 2014


Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis
journal, June 2012

  • Kircher, S.; Schopfer, P.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 28
  • DOI: 10.1073/pnas.1203746109

Historical gains in soybean (Glycine max Merr.) seed yield are driven by linear increases in light interception, energy conversion, and partitioning efficiencies
journal, April 2014

  • Koester, Robert P.; Skoneczka, Jeffrey A.; Cary, Troy R.
  • Journal of Experimental Botany, Vol. 65, Issue 12
  • DOI: 10.1093/jxb/eru187

Plant Physiological Ecology
book, January 2008


Process-based simple model for simulating sugarcane growth and production
journal, February 2014


Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species
journal, November 1999


Quantitative Modeling of Arabidopsis Development
journal, September 2005

  • Mündermann, Lars; Erasmus, Yvette; Lane, Brendan
  • Plant Physiology, Vol. 139, Issue 2
  • DOI: 10.1104/pp.105.060483

Products, requirements and efficiency of biosynthesis a quantitative approach
journal, June 1974

  • De Vries, F. W. T. Penning; Brunsting, A. H. M.; Van Laar, H. H.
  • Journal of Theoretical Biology, Vol. 45, Issue 2
  • DOI: 10.1016/0022-5193(74)90119-2

Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean plants
journal, December 1994


Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis
journal, April 2009


Leaf carbohydrate controls over Arabidopsis growth and response to elevated CO 2 : an experimentally based model
journal, November 2006


Functional dynamics of plant growth and photosynthesis - from steady-state to dynamics - from homogeneity to heterogeneity
journal, March 2006


Starch and Sucrose Synthesis in Phaseolus vulgaris as Affected by Light, CO 2 , and Abscisic Acid
journal, March 1985

  • Sharkey, Thomas D.; Berry, Joseph A.; Raschke, Klaus
  • Plant Physiology, Vol. 77, Issue 3
  • DOI: 10.1104/pp.77.3.617

Does hydraulic lift or nighttime transpiration facilitate nitrogen acquisition?
journal, February 2008

  • Snyder, Keirith A.; James, Jeremy J.; Richards, James H.
  • Plant and Soil, Vol. 306, Issue 1-2
  • DOI: 10.1007/s11104-008-9567-7

Night-time conductance in C3 and C4 species: do plants lose water at night?
journal, February 2003

  • Snyder, K. A.
  • Journal of Experimental Botany, Vol. 54, Issue 383
  • DOI: 10.1093/jxb/erg082

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


Arabidopsis Coordinates the Diurnal Regulation of Carbon Allocation and Growth across a Wide Range of Photoperiods
journal, January 2014

  • Sulpice, Ronan; Flis, Anna; Ivakov, Alexander A.
  • Molecular Plant, Vol. 7, Issue 1
  • DOI: 10.1093/mp/sst127

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

Functional approach to high-throughput plant growth analysis
journal, January 2013


Growth and maintenance components of leaf respiration of cotton grown in elevated carbon dioxide partial pressure
journal, June 1993


Environmental Effects on Spatial and Temporal Patterns of Leaf and Root Growth
journal, June 2009


Specific leaf area and nitrogen distribution in New Zealand forests: Species independently respond to intercepted light
journal, May 2006


Variation in parameters related to leaf thickness in common bean (Phaseolus vulgaris L.)
journal, January 2005


Natural Genetic Variation for Growth and Development Revealed by High-Throughput Phenotyping in Arabidopsis thaliana
journal, January 2012

  • Zhang, Xu; Hause, Ronald J.; Borevitz, Justin O.
  • G3: Genes|Genomes|Genetics, Vol. 2, Issue 1
  • DOI: 10.1534/g3.111.001487

Plant Physiological Ecology
book, January 1998


Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean plants
journal, December 1994


Influence of Instantaneous and Integrated Light-Flux Density on leaf Anatomy and Photosynthesis
journal, September 1979


Monogenic Recessive Mutations Causing Both Late Floral Initiation and Excess Starch Accumulation in Arabidopsis
journal, October 1995

  • Eimert, Klaus; Wang, Shue-Mei; Lue, Wei-ling
  • The Plant Cell, Vol. 7, Issue 10
  • DOI: 10.2307/3870031

Influence of Instantaneous and Integrated Light-Flux Density on leaf Anatomy and Photosynthesis
journal, September 1979


MassFlowDyn I: A Carbon Transport and Partitioning Model for Root System Architecture
journal, June 2000


Maintenance and constructive respiration in various organs ofHelianthus annuus L. andZinnia elegans L.
journal, March 1988


Does hydraulic lift or nighttime transpiration facilitate nitrogen acquisition?
journal, February 2008

  • Snyder, Keirith A.; James, Jeremy J.; Richards, James H.
  • Plant and Soil, Vol. 306, Issue 1-2
  • DOI: 10.1007/s11104-008-9567-7

Products, requirements and efficiency of biosynthesis a quantitative approach
journal, June 1974

  • De Vries, F. W. T. Penning; Brunsting, A. H. M.; Van Laar, H. H.
  • Journal of Theoretical Biology, Vol. 45, Issue 2
  • DOI: 10.1016/0022-5193(74)90119-2

Variation in parameters related to leaf thickness in common bean (Phaseolus vulgaris L.)
journal, January 2005


Variations in leaf mass per area according to N nutrition, plant age, and leaf position reflect ontogenetic plasticity in winter oilseed rape (Brassica napus L.)
journal, November 2009

  • Jullien, Alexandra; Allirand, Jean-Michel; Mathieu, Amélie
  • Field Crops Research, Vol. 114, Issue 2
  • DOI: 10.1016/j.fcr.2009.07.015

Specific leaf area and nitrogen distribution in New Zealand forests: Species independently respond to intercepted light
journal, May 2006


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


Nitrogen reallocation and photosynthetic acclimation in response to partial shading in soybean plants
journal, December 1994


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

Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis
journal, June 2012

  • Kircher, S.; Schopfer, P.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 28
  • DOI: 10.1073/pnas.1203746109

Night-time conductance in C3 and C4 species: do plants lose water at night?
journal, February 2003

  • Snyder, K. A.
  • Journal of Experimental Botany, Vol. 54, Issue 383
  • DOI: 10.1093/jxb/erg082

Historical gains in soybean (Glycine max Merr.) seed yield are driven by linear increases in light interception, energy conversion, and partitioning efficiencies
journal, April 2014

  • Koester, Robert P.; Skoneczka, Jeffrey A.; Cary, Troy R.
  • Journal of Experimental Botany, Vol. 65, Issue 12
  • DOI: 10.1093/jxb/eru187

Arabidopsis Coordinates the Diurnal Regulation of Carbon Allocation and Growth across a Wide Range of Photoperiods
journal, January 2014

  • Sulpice, Ronan; Flis, Anna; Ivakov, Alexander A.
  • Molecular Plant, Vol. 7, Issue 1
  • DOI: 10.1093/mp/sst127

Quantitative Modeling of Arabidopsis Development
journal, September 2005

  • Mündermann, Lars; Erasmus, Yvette; Lane, Brendan
  • Plant Physiology, Vol. 139, Issue 2
  • DOI: 10.1104/pp.105.060483

Nighttime Stomatal Conductance and Transpiration in C 3 and C 4 Plants
journal, January 2007

  • Caird, Mairgareth A.; Richards, James H.; Donovan, Lisa A.
  • Plant Physiology, Vol. 143, Issue 1
  • DOI: 10.1104/pp.106.092940

Variational Gaussian process classifiers
journal, January 2000

  • Mackay, D. J. C.; Gibbs, M. N.
  • IEEE Transactions on Neural Networks, Vol. 11, Issue 6
  • DOI: 10.1109/72.883477

Effect of Topological and Phenological Changes on Biomass Partitioning in Arabidopsis thaliana Inflorescence: A Preliminary Model-Based Study
conference, November 2006

  • Letort, V.; Cournede, Paul-Henry; Lecoeur, J.
  • 2006 Second International Symposium on Plant Growth Modeling and Applications
  • DOI: 10.1109/pma.2006.56

Growth and maintenance components of leaf respiration of cotton grown in elevated carbon dioxide partial pressure
journal, June 1993


Functional dynamics of plant growth and photosynthesis - from steady-state to dynamics - from homogeneity to heterogeneity
journal, March 2006


Magnitude of nighttime transpiration does not affect plant growth or nutrition in well-watered Arabidopsis
journal, July 2009


Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis
journal, April 2009


Tree Branch Angle: Maximizing Effective Leaf Area
journal, February 1978


Crop Productivity and Photoassimilate Partitioning
journal, August 1984


Environmental Effects on Spatial and Temporal Patterns of Leaf and Root Growth
journal, June 2009


Accurate inference of shoot biomass from high-throughput images of cereal plants
journal, January 2011

  • Golzarian, Mahmood R.; Frick, Ross A.; Rajendran, Karthika
  • Plant Methods, Vol. 7, Issue 1
  • DOI: 10.1186/1746-4811-7-2

Natural Genetic Variation for Growth and Development Revealed by High-Throughput Phenotyping in Arabidopsis thaliana
journal, January 2012

  • Zhang, Xu; Hause, Ronald J.; Borevitz, Justin O.
  • G3: Genes|Genomes|Genetics, Vol. 2, Issue 1
  • DOI: 10.1534/g3.111.001487

Effects of leaf and plant age on specific leaf area in deciduous tree species Quercus cerris L. var. Cerris
journal, February 2014


Works referencing / citing this record:

Semisynthetic Triterpenes Derived from Euphorbia officinarum as Plant Growth Promoters and Inducers of Disease Resistance
journal, August 2018

  • Smaili, Amal; Rifai, Lalla Aicha; Mazoir, Noureddine
  • Journal of Plant Growth Regulation, Vol. 38, Issue 1
  • DOI: 10.1007/s00344-018-9838-3

Carbon source–sink relationship in Arabidopsis thaliana: the role of sucrose transporters
journal, November 2017


Effect of density and neighbours on interactions between invasive plants of similar growth form
journal, January 2020


Field Performance of Saccharum × Miscanthus Intergeneric Hybrids (Miscanes) Under Cool Climatic Conditions of Northern Japan
journal, November 2019


Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs
journal, August 2016

  • Campos, Marcelo L.; Yoshida, Yuki; Major, Ian T.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12570

Mathematical modeling of diurnal patterns of carbon allocation to shoot and root in Arabidopsis thaliana
journal, January 2019

  • Küstner, Lisa; Nägele, Thomas; Heyer, Arnd G.
  • npj Systems Biology and Applications, Vol. 5, Issue 1
  • DOI: 10.1038/s41540-018-0080-1

Improved chloroplast energy balance during water deficit enhances plant growth: more crop per drop
journal, December 2017

  • Dahal, Keshav; Vanlerberghe, Greg C.
  • Journal of Experimental Botany, Vol. 69, Issue 5
  • DOI: 10.1093/jxb/erx474

Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology
journal, December 2018

  • Ren, Tao; Weraduwage, Sarathi M.; Sharkey, Thomas D.
  • Journal of Experimental Botany, Vol. 70, Issue 4
  • DOI: 10.1093/jxb/ery448

Antagonistic pleiotropy can maintain fitness variation in annual plants
journal, November 2017

  • Brown, K. E.; Kelly, J. K.
  • Journal of Evolutionary Biology, Vol. 31, Issue 1
  • DOI: 10.1111/jeb.13192

The genetic control of leaf allometry in the common bean, Phaseolus vulgaris
journal, March 2020


A “Do-It-Yourself” phenotyping system: measuring growth and morphology throughout the diel cycle in rosette shaped plants
journal, November 2017

  • Dobrescu, Andrei; Scorza, Livia C. T.; Tsaftaris, Sotirios A.
  • Plant Methods, Vol. 13, Issue 1
  • DOI: 10.1186/s13007-017-0247-6

Genome-wide association mapping of leaf mass traits in a Vietnamese rice landrace panel
journal, July 2019


In-field High Throughput Phenotyping and Cotton Plant Growth Analysis Using LiDAR
journal, January 2018

  • Sun, Shangpeng; Li, Changying; Paterson, Andrew H.
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00016

Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology
posted_content, July 2018

  • Ren, Tao; Weraduwage, Sarathi M.; Sharkey, Thomas D.
  • bioRxiv
  • DOI: 10.1101/379065

Mathematical modeling of diurnal patterns of carbon allocation to shoot and root in Arabidopsis thaliana
collection, January 2019

  • Küstner, Lisa; Nägele, Thomas; Heyer, Arnd G.
  • Universität Stuttgart
  • DOI: 10.18419/opus-10274

Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs
journal, August 2016

  • Campos, Marcelo L.; Yoshida, Yuki; Major, Ian T.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms12570

The genetic control of leaf allometry in the common bean, Phaseolus vulgaris
journal, March 2020


Mathematical modeling of diurnal patterns of carbon allocation to shoot and root in Arabidopsis thaliana
collection, January 2019

  • Küstner, Lisa; Nägele, Thomas; Heyer, Arnd G.
  • Universität Stuttgart
  • DOI: 10.18419/opus-10274

Mechanisms Underlying the Environmentally Induced Plasticity of Leaf Morphology
journal, October 2018


Control of Carbon Assimilation and Partitioning by Jasmonate: An Accounting of Growth–Defense Tradeoffs
journal, January 2016