Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP08099
RESEARCH ARTICLE
Contents Vol 35(11)

A model-based analysis of the dynamics of carbon balance at the whole-plant level in Arabidopsis thaliana

Angélique Christophe A E , Véronique Letort B , Irène Hummel A , Paul-Henry Cournède B , Philippe de Reffye C and Jérémie Lecœur D
+ Author Affiliations
- Author Affiliations

A INRA, UMR759 LEPSE, 2 place Viala, F-34060 Montpellier, France.

B Ecole Centrale Paris, Applied Mathematics Laboratory, 2 Grande Voie des Vignes, F-92295 Châtenay-Malabry, France.

C Cirad-Amis, TA 40/01 Avenue Agropolis, 34398 Montpellier cedex 5 France and INRIA-Rocquencourt, BP 105, 78153 Le Chesnay cedex, France.

D SupAgro, UMR759 LEPSE, 2 place Viala, F-34060 Montpellier, France.

E Corresponding author. Email: christop@supagro.inra.fr

Functional Plant Biology 35(11) 1147-1162 https://doi.org/10.1071/FP08099
Submitted: 27 March 2008  Accepted: 11 August 2008   Published: 28 November 2008

Abstract

Arabidopsis thaliana (L.) Heynh. is used as a model plant in many research projects. However, few models simulate its growth at the whole-plant scale. The present study describes the first model of Arabidopsis growth integrating organogenesis, morphogenesis and carbon-partitioning processes for aerial and subterranean parts of the plant throughout its development. The objective was to analyse competition among sinks as they emerge from patterns of plant structural development. The model was adapted from the GreenLab model and was used to estimate organ sink strengths by optimisation against biomass measurements. Dry biomass production was calculated by a radiation use efficiency-based approach. Organogenesis processes were parameterised based on experimental data. The potential of this model for growth analysis was assessed using the Columbia ecotype, which was grown in standard environmental conditions. Three phases were observed in the overall time course of trophic competition within the plant. In the vegetative phase, no competition was observed. In the reproductive phase, competition increased with a strong increase when lateral inflorescences developed. Roots and internodes and structures bearing siliques were strong sinks and had a similar impact on competition. The application of the GreenLab model to the growth analysis of A. thaliana provides new insights into source–sink relationships as functions of phenology and morphogenesis.

Additional keywords: functional–structural models, GreenLab model, plant development, source–sink relationships.


Acknowledgements

The authors thank Zhan Zhigang for his help in designing the flower symbol for the 3D simulations of Arabidopsis plants, and Benoît Pallas and Julie Sappa for valuable discussions.


References


Allen MT, Prusinkiewicz P, DeJong TM (2005) Using L-systems for modeling source–sink interactions, architecture and physiology of growing trees: the L-PEACH model. The New Phytologist 166(3), 869–880.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Asch F, Sow A, Dingkuhn M (1999) Reserve mobilization, dry matter partitioning and specific leaf area in seedlings of African rice cultivars differing in early vigor. Field Crops Research 62, 191–202.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Baille A, Gutierrez Colomer RP, Gonzalez-Real MM (2006) Analysis of intercepted radiation and dry matter accumulation in rose flower shoots. Agricultural and Forest Meteorology 137, 68–80.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of Botany 99, 375–407.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Barthélémy D , Caraglio Y , Costes E (1997) Architecture, gradients morphogénétiques et âge physiologique chez les végétaux. In ‘Modélisation et simulation de l’architecture des végétaux’. (Eds. Barthélémy D, Bouchon J, de Reffye P) pp. 89–136. (INRA Editions science Update: Paris, France).

Bleecker AB, Patterson SE (1997) Last exist: senescence, abscission, and meristem arrest in Arabidopsis. The Plant Cell 9, 1169–1179.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell 13, 1499–1510.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Chenu K, Franck N, Dauzat J, Barczi JF, Rey H, Lecoeur J (2005) Integrated responses of rosette organogenesis, morphogenesis and architecture to reduced incident light in Arabidopsis thaliana results in higher efficiency of light interception. Functional Plant Biology 32(12), 1123–1134.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Chenu K, Franck N, Lecoeur J (2007) Simulations of virtual plants reveal a role for SERRATE in the response of leaf development to light in Arabidopsis thaliana. The New Phytologist 175(3), 472–481.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Christophe A, Moulia B, Varlet-Grancher C (2006) Quantitative contributions of blue light and PAR to the photocontrol of plant morphogenesis in Trifolium repens (L.) Journal of Experimental Botany 57, 2379–2390.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cline MG (1997) Concepts and terminology of apical dominance. American Journal of Botany 84(8), 1064–1069.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Cookson SJ, van Lijsebettens M, Granier C (2005) Correlation between leaf growth variables suggests intrinsic and early controls of leaf size in Arabidopsis thaliana. Plant, Cell & Environment 28, 1355–1366.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Cournède P-H, Kang M, Mathieu A, Yan H, Hu B, de Reffye P (2006) Structural factorization of plants to compute their functional and architectural growth. Simulation 82(7), 427–438.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Cox CM, Swain S (2006) Localised and non-localised promotion of fruit development by seeds in Arabidopsis. Functional Plant Biology 33, 1–8.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dauzat J , Franck N , Rapidel B , Luquet D , Vaast P (2008) Simulation of ecophysiological processes on 3D virtual stands with the ARCHIMED simulation platform. In ‘Plant growth modeling and applications (Proceedings PMA06: The second international symposium on plant growth modeling, simulation, visualization and their applications)’. (Eds. Fourcaud T, Zhang X-P) )’. pp. 101–108. (IEEE Computer Society: Beijing, Chine)

De Visser PHB , Marcelis LFM , van der Heijden GWAM , Angenent GC (2003) 3D digitization and modeling of flower mutants of Arabidopsis thaliana. In ‘Plant growth modeling and applications (Proceedings PMA03: 2003’ International symposium on plant growth modeling, simulation, visualization and their applications)’. (Eds M Jaeger, BG Hu) pp. 218–226. (Tsinghua University Press and Springer-Verlag: Beijing, China)

Dingkuhn M, Luquet D, Quilot B, Reffye PD (2005) Environmental and genetic control of morphogenesis in crops: towards models simulating phenotypic plasticity. Australian Journal of Agricultural Research 56, 1289–1302.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Dingkuhn M, Luquet D, Kim HK, Tambour L, Clément-Vidal A (2006) EcoMeristem, a model of morphogenesis and competition among sinks in rice: 2. Simulating genotype responses to phosphorus deficiency. Functional Plant Biology 33, 325–337.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Doerner D (2001) Plant meristems: a ménage à-trois to end it all. Current Biology 11(19), R785–R787.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dong Q, Louarn G, Wang Y, Barczi JF, de Reffye P (2008) Does the structure–function model GREENLAB deal with crop phenotypic plasticity induced by plant spacing? A case study on tomato. Annals of Botany 108, 1195–1206. open url image1

Drouet J-L, Pagès L (2003) GRAAL: a model of growth, architecture and carbon allocation during the vegetative phase of the whole maize plant. Model description and parametrisation. Ecological Modelling 165, 147–173.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gallagher HN, Biscoe V (1978) Radiation absorption, growth and yield of cereals. The Journal of Agricultural Science 91, 47–60. open url image1

Gigon A, Matos A-R, Lafray D, Zuily-Fodil Y, Pham-Thi A-T (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (Ecotype Columbia). Annals of Botany 94, 345–351.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Granier C, Massonet C, Turc O, Muller B, Chenu K, Tardieu F (2002) Individual leaf development in Arabidopsis thaliana: a stable thermal-time-based programme. Annals of Botany 89, 595–604.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guo Y, Ma YT, Zhan ZG, Li BG, Dingkuhn M, Luquet D, de Reffye P (2006) Parameter optimization and field validation of the functional–structural model GREENLAB for maize. Annals of Botany 97, 217–230.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hammer G, Sinclair TR, Chapman S, van Oosterom E (2004) On systems thinking, systems biology, and the in silico plant. Plant Physiology 134, 909–911.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hammer G, Cooper M, Tardieu F, Welch S, Walsh B, Van Eeuwijk F, Chapman S, Podlich D (2006) Models for navigating biological complexity in breeding improved crop plants. Trends in Plant Science 11(12), 587–593.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hensel L, Grbic V, Baumgarten DB, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. The Plant Cell 5, 553–564.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kang MZ , de Reffye P , Barczi J-F , Hu BG , Houllier F (2003) Stochastic 3D tree simulation using substructure instancing. In ‘Plant growth modeling and applications (Proceedings PMA03 : 2003’ International symposium on plant growth modeling, simulation, visualization and their applications)’. (Eds M Jaeger, BG Hu) pp. 154–168. (Tsinghua University Press and Springer-Verlag: Beijing, China)

Kang MZ, Heuvelink E, de Reffye P (2006) Building virtual chrysanthemum based on sink–source relationships: preliminary results. Acta Horticulturae 718, 129–136. open url image1

Ko J-H, Han K-H, Park S, Yang J (2004) Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole transcriptome profiling. Plant Physiology 135, 1069–1083.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lacointe A (2000) Carbon allocation among tree organs: a review of basic processes and representation in functional–structural tree models. Annals of Forest Science 57, 521–533.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Lancashire PD, Bleiholder H, van der Boom T, Langeluddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth stages of crops and weeds. Annals of Applied Biology 119, 561–601.
| Crossref |
open url image1

Lecoeur J, Ney B (2003) Change with time in potential radiation-use efficiency in field pea. European Journal of Agronomy 19, 91–105.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Li Y, Roycewicz P, Smith E, Borevitz JO (2006) Genetics of local adaptation in the laboratory: flowering time quantitative trait loci under geographic and seasonal conditions in Arabidopsis. PLoS ONE 1(1), e105.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Louarn G, Lecoeur J, Lebon E (2008) A three-dimensional statistical reconstruction model of grapevine (Vitis vinifera) simulating canopy structure variability within and between cultivar/training system pairs. Annals of Botany 101(8), 1167–1184.
| Crossref | PubMed |
open url image1

Luquet D, Dingkuhn M, Kim H, Tambour L, Clément-Vidal A (2006) EcoMeristem, a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis. Functional Plant Biology 33, 309–323.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Luquet D, Song YH, Elbet S, This D, Clément-Vidal A, Périn C, Fabre D, Dingkuhn M (2007) Model assisted physiological analysis of Phyllo, a rice architectural mutant. Functional Plant Biology 34, 11–23.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ma Y, Li B, Zhan Z, Guo Y, Luquet D, de Reffye P, Dingkuhn M (2007) Parameter stability of the structural–functional plant model GREENLAB as affected by variation within populations, among seasons and among growth stages. Annals of Botany 99, 61–73.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Marcelis LFM (1994) A simulation model for dry matter partitioning in cucumber. Annals of Botany 74(1), 43–52.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Marcelis LFM, Heuvelink E, Goudriaan J (1998) Modeling biomass production and yield of horticultural crops: a review. Scientia Horticulturae 74, 83–111.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Mathieu A, Cournède P-H, de Reffye P (2004) A dynamical model of plant growth with full retroaction between organogenesis and photosynthesis. ARIMA 4, 101–107. open url image1

Mathieu A, Cournède P-H, Barthélémy D, de Reffye P (2008) Rhythms and alternating patterns in plants as emergent properties of a model of interaction between development and functioning. Annals of Botany 101, 1233–1242.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Medford JI, Behringer FJ, Callos JD, Feldmann KA (1992) Normal and abnormal development in the Arabidopsis vegetative shoot apex. The Plant Cell 4(6), 631–643.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Monteith JL (1977) Climate and the efficiency of crop production in Britain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 281, 277–294.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Mündermann L, Erasmus Y, Lane B, Cohen E, Prusinkiewicz P (2005) Quantitative modeling of Arabidopsis development. Plant Physiology 139, 960–968.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Netzer MH, Tittonnel ED, Merrien A (1989) Evènements liés au passage du méristème de l’état végétatif à l’état reproducteur, chez le colza Brassica napus L. var. oleifera Metzg. Agronomie 9, 151–159.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Penning de Vries FWT , van Laar HH , Chardon MCM (1983) Bioenergetics of growth of seeds, fruits and storage organs. In ‘Symposium on potential productivity of field crops under different environments’. (Eds WH Smith, SJ Banta) pp. 37–59. (International Rice Research Institute: Manila)

Planchais I, Sinoquet H (1998) Foliage determinants of light interception in sunny and shaded branches of Fagus sylvatica L. Agricultural and Forest Meteorology 89, 241–253.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ratcliffe OJ, Bradley DJ, Coen ES (1999) Separation of shoot and floral identity in Arabidopsis. Development 126, 1109–1120.
|  CAS | PubMed |
open url image1

Renton M, Kaitaniemi P, Hanan J (2005) Functional–structural plant modelling using a combination of architectural analysis, L-systems and a canonical model of function. Ecological Modelling 184, 277–298.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Reymond M, Muller B, Leonardi A, Charcosset A, Tardieu F (2003) Combining QTL analysis and an ecophysiological model to analyse the genetic variability of the responses of maize leaf growth to temperature and water deficit. Plant Physiology 131, 664–675.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sinclair TR, Muchow RC (1999) Radiation use efficiency. Advances in Agronomy 65, 215–263.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Welch SM, Roe JL, Dong Z (2003) A genetic neural network model of flowering time control in Arabidopsis thaliana. Agronomy Journal 95, 71–81. open url image1

White WJ, Hoogenboom G (2003) Gene-based approaches to crop simulation: past experiences and future opportunities. Agronomy Journal 95, 52–64. open url image1

Yan H-P, Kang MZ, de Reffye P, Dingkuhn M (2004) A dynamic, architectural plant model simulating resource-dependent growth. Annals of Botany 93, 591–602.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yin X, Goudriaan J, Lantinga EA, Vos J, Spiertz HJ (2003) A flexible sigmoid function of determinate growth. Annals of Botany 91, 361–371.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yin X, Struik PC, Kropff MJ (2004) Role of crop physiology in predicting gene-to-phenotype relationships. Trends in Plant Science 9, 426–432.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zhan ZG , de Reffye P , Houllier F , Hu BG (2003) Fitting a structural–functional model with plant architectural data. In ‘Plant growth modeling and applications (Proceedings PMA03: 2003’ International symposium on plant growth modeling, simulation, visualization and their applications)’. (Eds M Jaeger, BG Hu) pp. 236–249. (Tsinghua University Press and Springer-Verlag: Beijing, Chine)