Plant systems biology: Network matters

Plant, Cell and Environment

Volumn 34, Issue 4, 2011, Pages 535-553

  Lucas, Mikaël ^a,b   Laplaze, Laurent ^b   Bennett, Malcolm J ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Auxin; Bottom up modelling; Crop model; Functional structural plant model; Molecular networks; Sub cellular model; Systems biology; Tissue model; Top down modelling; Whole plant model

Indexed keywords

CROP; GENE EXPRESSION; HORMONE; MOLECULAR ANALYSIS; NETWORK ANALYSIS; NUMERICAL MODEL; PROTEIN;

BIOLOGICAL MODEL; GENE REGULATORY NETWORK; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR BIOLOGY; PLANT; PLANT ROOT; PROTEIN DOMAIN; REVIEW; SYSTEMS BIOLOGY; ULTRASTRUCTURE;

GENE REGULATORY NETWORKS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; MOLECULAR BIOLOGY; PLANT ROOTS; PLANTS; PROTEIN INTERACTION DOMAINS AND MOTIFS; SYSTEMS BIOLOGY;

EID: 79952494097     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02273.x     Document Type: Review

References (225)

1. Ahn Y., Bagrow J.P. & Lehmann S. (2010) Link communities reveal multiscale complexity in networks. Nature 466, 761-764.
2. Ainsworth E.A., Rogers A., Vodkin L.O., Walter A. & Schurr U. (2006) The effects of elevated CO2 Concentration on soybean gene expression. An analysis of growing and mature leaves. Plant Physiology 142, 135-147.
3. Allen M.T., Prusinkiewicz P. & DeJong T.M. (2005) Using L-systems for modeling source-sink interactions, architecture and physiology of growing trees: the L-PEACH model. The New Phytologist 166, 869-880.
4. Alon U. (2007a) An Introduction to Systems Biology: Design Principles of Biological Circuits. CRC Press, London, UK.
5. Alon U. (2007b) Network motifs: theory and experimental approaches. Nature Review of Genetics 8, 450-461.
6. Alvarez-Buylla E.R., Benitez M., Davila E.B., Chaos A., Espinosa-Soto C. & Padilla-Longoria P. (2007) Gene regulatory network models for plant development. Current Opinion in Plant Biology 10, 83-91.
7. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
8. Baginsky S. & Fernie A.R. (2007) Plant Systems Biology. Birhäuser, Basel, Switzerland.
9. Bajic V.B., Veronika M., Veladandi P.S., Meka A., Heng M.W., Rajaraman K., Pan H. & Swarup S. (2005) Dragon Plant Biology Explorer. A text-mining tool for integrating associations between genetic and biochemical entities with genome annotation and biochemical terms lists. Plant Physiology 138, 1914-1925.
10. Balázsi G., Barabási A. & Oltvai Z.N. (2005) Topological units of environmental signal processing in the transcriptional regulatory network of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 102, 7841-7846.
11. Barczi J., Rey H., Caraglio Y., de Reffye P., Barthélémy D., Dong Q.X. & Fourcaud T. (2008) AmapSim: a structural whole-plant simulator based on botanical knowledge and designed to host external functional models. Annals of Botany 101, 1125-1138.
12. Barthelemy D. & Caraglio Y. (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of Botany 99, 375-407.
13. Batagelj V. & Mrvar A. (1998) PAJEK - program for large network analysis. Connections 21, 47-57.
14. Bayer E.M., Smith R.S., Mandel T., Nakayama N., Sauer M., Prusinkiewicz P. & Kuhlemeier C. (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes & Development 23, 373-384.
15. Benfey P.N. & Brady S.M. (2006) A systems approach to understanding root development. Canadian Journal of Botany 84, 695-701.
16. Bennett M. & Monk N. (2008) The flowering of systems approaches in plant and crop biology. The New Phytologist 179, 567-568.
17. von Bertallanfy L. (1950) An outline of general systems theory. The British Journal of Philosophical Science 1, 139-164.
18. von Bertallanfy L. (1968) General System Theory. Brazillier, New York, NY, USA.
19. Bhalla U.S. & Iyengar R. (1999) Emergent properties of networks of biological signaling pathways. Science 283, 381-387.
20. Bhalla U.S. & Iyengar R. (2001) Robustness of the bistable behavior of a biological signaling feedback loop. Chaos: An Interdisciplinary Journal of Nonlinear Science 11, 221.
21. Bhalla U.S., Ram P.T. & Iyengar R. (2002) MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297, 1018-1023.
22. Bornholdt S. (2005) SYSTEMS BIOLOGY: less is more in modeling large genetic networks. Science 310, 449-451.
23. Bothwell J.H.F. (2006) The long past of systems biology. The New Phytologist 170, 6-10.
24. Bouman B.A.M., Ven Keulen H., Van Laar H.H. & Rabbinge R. (1996) The 'School of de Wit' crop growth simulation models: a pedigree and historical overview. Agricultural Systems 52, 171-198.
25. Brandman O. & Meyer T. (2008) Feedback loops shape cellular signals in space and time. Science 322, 390-395.
26. Brandman O., Ferrell J.E. Jr, Li R. & Meyer T. (2005) Interlinked fast and slow positive feedback loops drive reliable cell decisions. Science 310, 496-498.
27. Bruggeman F.J. & Westerhoff H.V. (2007) The nature of systems biology. Trends in Microbiology 15, 45-50.
28. Buck-Sorlin G.H., Burela B.S., Evers J.B., ven der Heijden G.W.A.M., Heuvelink E., Marcelis L.F.M., Struik P.C., de Visser P.H.B., Damen T.H.J. & Vos J. (2007) Virtual rose: a new tool to optimize plant architecture in glasshouse rose production systems. In Proceedings of the 5th International Workshop on Functional-Structural Plant Models. 5th International Workshop on Functional-Structural Plant Model. Napier.
29. Bumgarner R.E. & Yeung K.Y. (2009) Methods for the inference of biological pathways and networks. Methods in Molecular Biology (Clifton, N.J.) 541, 225-245.
30. Burrell M., Earnshaw C. & Clench M. (2007) Imaging Matrix Assisted Laser Desorption Ionization Mass Spectrometry: a technique to map plant metabolites within tissues at high spatial resolution. Journal of Experimental Botany 58, 757-763.
31. Carrera J., Rodrigo G., Jaramillo A. & Elena S.F. (2009) Reverse-engineering the Arabidopsis thaliana transcriptional network under changing environmental conditions. Genome Biology 10, R96.
32. Carvunis A., Gomez E., Thierry-Mieg N., Trilling L. & Vidal M. (2009) [Systems biology: from yesterday's concepts to tomorrow's discoveries]. Médecine 25, 578-584.
33. Chang D., Leung S., Atkinson M.R., Reifler A., Forger D. & Ninfa A.J. (2010) Building biological memory by linking positive feedback loops. Proceedings of the National Academy of Sciences of the United States of America 107, 175-180.
34. Chang W., Li C. & Chen B. (2005) Quantitative inference of dynamic regulatory pathways via microarray data. BMC Bioinformatics 6, 44.
35. Charles-Edwards D.A. & Fisher M.J. (1980) A physiological approach to the analysis of crop growth data. I. Theoretical considerations. Annals of Botany 46, 413-423.
36. Cheeseman J.M. (1993) Plant growth modelling without integrating mechanisms. Plant, Cell & Environment 16, 137-147.
37. Chickarmane V., Roeder A.H., Tarr P.T., Cunha A., Tobin C. & Meyerowitz E.M. (2010) Computational morphodynamics: a modeling framework to understand plant growth. Annual Review of Plant Biology 61, 65-87.
38. Choi S. (2007) Introduction to Systems Biology. Humana Press, Totowa, NJ, USA.
39. Connor D.J. & Fereres E. (1999) A dynamic model of crop growth and partitioning of biomass. Field Crops Research 63, 139-157.
40. Corson F., Hamant O., Bohn S., Traas J., Boudaoud A. & Couder Y. (2009) Turning a plant tissue into a living cell froth through isotropic growth. Proceedings of the National Academy of Sciences of the United States of America 106, 8453-8458.
41. Coruzzi G. & Gutiérrez R.A. (2009) Plant Systems Biology. Blackwell Publishing Ltd., Chichester, West Sussex, UK.
42. Coveney P.V. & Fowler P.W. (2005) Modelling biological complexity: a physical scientist's perspective. Journal of the Royal Society Interface 2, 267-280.
43. Cui J., Li P., Li G., Xu F., Zhao C., Li Y., Yang Z., Wang G., Yu Q., Li Y. & Shi T. (2008) AtPID: Arabidopsis thaliana protein interactome database an integrative platform for plant systems biology. Nucleic Acids Research 36 (Suppl 1), D999-1008.
44. Danjon F. & Reubens B. (2008) Assessing and analyzing 3D architecture of woody root systems, a review of methods and applications in tree and soil stability, resource acquisition and allocation. Plant Soil 303, 1-34.
45. Davidich M.I. & Bornholdt S. (2008) Boolean network model predicts cell cycle sequence of fission yeast. PLoS ONE 3, e1672.
46. Davuluri R.V., Sun H., Palaniswamy S.K., Matthews N., Molina C., Kurtz M. & Grotewold E. (2003) AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics 4, 25.
47. de Dorlodot S., Forster B., Pagès L., Price A., Tuberosa R. & Draye X. (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends in Plant Science 12, 474-481.
48. De Schepper V. & Steppe K. (2010) Development and verification of a water and sugar transport model using measured stem diameter variations. Journal of Experimental Botany 61, 2083-2099.
49. Drack M., Apfalter W. & Pouvreau D. (2007) On the making of a system theory of life: Paul A. Weiss and Ludwig von Bertalanffy's conceptual connection. The Quarterly Review of Biology 82, 349-373.
50. Draye X., Kim Y., Lobet G. & Javaux M. (2010) Model-assisted integration of physiological and environmental constraints affecting the dynamic and spatial patterns of root water uptake from soils. Journal of Experimental Botany 61, 2145-2155.
51. Duncan W.G., Loomis R.S., Williams W.A. & Hanau R. (1967) A model for simulating photosynthesis in plant communities. Hilgardia 38, 181-205.
52. Dupuy L., Fourcaud T. & Stokes A. (2005) A numerical investigation into the influence of soil type and root architecture on tree anchorage. Plant and Soil 278, 119-134.
53. Dupuy L., McKenzie J., Rudge T. & Haseloff J. (2008) A system for modelling cell-cell interactions during plant morphogenesis. Annals of Botany 101, 1255-1265.
54. Dupuy L., Vignes M., McKenzie B.M. & White P.J. (2010a) The dynamics of root meristem distribution in the soil. Plant, Cell & Environment 33, 358-369.
55. Dupuy L., Mackenzie J. & Haseloff J. (2010b) Coordination of plant cell division and expansion in a simple morphogenetic system. Proceedings of the National Academy of Sciences of the United States of America 107, 2711-2716.
56. Ehrenberg M., Elf J. & Hohmann S. (2009) Systems biology: Nobel symposium 146. FEBS Letters 583, 3881.
57. Eschenbach C. (2005) Emergent properties modelled with the functional structural tree growth model ALMIS: computer experiments on resource gain and use. Ecological Modelling 186, 470-488.
58. Espinosa-Soto C., Padilla-Longoria P. & Alvarez-Buylla E.R. (2004) A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. The Plant Cell 16, 2923-2939.
59. Evers J.B., Vos J., Chelle M., Andrieu B., Fournier C. & Struik P.C. (2007) Simulating the effects of localized red:far-red ratio on tillering in spring wheat (Triticum aestivum) using a three-dimensional virtual plant model. The New Phytologist 176, 325-336.
60. Evers J.B., Vos J., Yin X., Romero P., van der Putten P.E. & Struik P.C. (2010) Simulation of wheat growth and development based on organ-level photosynthesis and assimilate allocation. Journal of Experimental Botany 61, 2203-2216.
61. Fernandez R., Das P., Mirabet V., Moscardi E., Traas J., Verdeil J.L., Malandain G. & Godin C. (2010) Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution. Nature Methods 7, 547-553.
62. de Folter S., Immink R.G., Kieffer M. etal. (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17, 1424-1433.
63. Fox J.J. & Hill C.C. (2001) From topology to dynamics in biochemical networks. Chaos (Woodbury, N.Y.) 11, 809-815.
64. Fukushima A., Kusano M., Nakamichi N., Kusano M., Nakamichi N., Kobayashi M., Hayashi N., Sakakibara H., Mizuno T. & Saito K. (2009a) Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proceedings of the National Academy of Sciences of the United States of America 106, 7251-7256.
65. Fukushima A., Kusano M., Redestig H., Kusano M., Redestig H., Arita M. & Saito K. (2009b) Integrated omics approaches in plant systems biology. Current Opinion in Chemical Biology 13, 532-538.
66. Garcia-Hernandez M., Berardini T.Z., Chen G. etal. (2002) TAIR: a resource for integrated Arabidopsis data. Functional & Integrative Genomics 2, 239-253.
67. Garnett P., Steinacher A., Stepney S., Clayton R. & Leyser O. (2010) Computer simulation: the imaginary friend of auxin transport biology. Bioessays 32, 828-835.
68. Gatherer D. (2010) So what do we really mean when we say that systems biology is holistic? BMC Systems Biology 4, 22-22.
69. Geisler-Lee J., O'Toole N., Ammar R., Provart N.J., Millar A.H. & Geisler M. (2007) A predicted interactome for Arabidopsis. Plant Physiology 145, 317-329.
70. Genoud T., Trevino Santa Cruz M.B. & Metraux J. (2001) Numeric simulation of plant signaling networks. Plant Physiology 126, 1430-1437.
71. Giavitto J.L. & Olivier M. (2003) Modeling the topological organization of cellular processes. Bio Systems 70, 149-163.
72. Gifford R.M. (1995) Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long-term vs. short-term distinctions for modelling. Global Change Biology 1, 385-396.
73. Giot L., Bader J.S., Brouwer C. etal. (2003) A protein interaction map of drosophila melanogaster. Science 302, 1727-1736.
74. Godin C. (2000) Representing and encoding plant architecture: a review. Annals of Forest Science 57, 413-438.
75. Godin C. & Caraglio Y. (1998) A multiscale model of plant topological structures. Journal of Theoretical Biology 191, 1-46.
76. Godin C., Costes E. & Caraglio Y. (1997) Exploring plant topological structure with the AMAPmod software: an outline. Silva Fennica 31, 357-368.
77. Grandjean O., Vernoux T., Laufs P., Belcram K., Mizukami Y. & Traas J. (2004) In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. The Plant Cell 16, 74-87.
78. Granier C., Massonnet 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.
79. Green P.B. (1962) Mechanism for plant cellular morphogenesis. Science 138, 1404-1405.
80. Green P.B. (1968) Growth physics in nitella: a method for continuous in vivo analysis of extensibility based on a micro-manometer technique for turgor pressure. Plant Physiology 43, 1169-1184.
81. Green P.B. (1980) Organogenesis-a biophysical view. Annual Review of Plant Physiology 31, 51-82.
82. Grieneisen V.A. & Scheres B. (2009) Back to the future: evolution of computational models in plant morphogenesis. Current Opinion in Plant Biology 12, 606-614.
83. Grieneisen V.A., Xu J., Marée A.F., Hogeweg P. & Scheres B. (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008-1013.
84. Guédon Y., Barthélémy D., Caraglio Y. & Costes E. (2001) Pattern analysis in branching and axillary flowering sequences. Journal of Theoretical Biology 212, 481-520.
85. Hall R., BEale M., Fiehn O., Hardy N., Sumner L. & Bino R. (2002) Plant metabolomics: the missing link in functional genomics strategies. Plant Cell 14, 1437-1440.
86. Hallé F. (1978) Architectural variation at specific level of tropical trees. In Tropical Trees As Living Systems, pp. 209-221. Cambridge University Press, Cambridge, UK.
87. Hamant O. & Traas J. (2010) The mechanics behind plant development. The New Phytologist 185, 369-385.
88. Hamant O., Heisler M.G., Jönsson H. etal. (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650-1655.
89. Hammer G.L., Sinclair T.R., Chapman S.C. & van Oosterom E. (2004) On systems thinking, systems biology, and the in silico plant. Plant Physiology 134, 909-911.
90. 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, 587-593.
91. Hecker M., Lambeck S., Toepfer S., van Someren E. & Guthke R. (2009) Gene regulatory network inference: data integration in dynamic models - a review. Bio Systems 96, 86-103.
92. van der Heijden G., de Visser P. & Heuvelink E. (2007) Measurements for functional-structural plant models. In Functional-Structural Plant Modelling in Crop Production Wageningen UR Frontis Series. pp. 13-25. Springer, Berlin.
93. Heisler M.G. & Jönsson H. (2007) Modelling meristem development in plants. Current Opinion in Plant Biology 10, 92-97.
94. Hickman G.J. & Hodgman T.C. (2009) Inference of gene regulatory networks using Boolean-network inference methods. Journal of Bioinformatics and Computational Biology 7, 1013-1029.
95. Ho Q.T., Verboven P., Verlinden B.E. & Nicolaï B.M. (2010) A model for gas transport in pear fruit at multiple scales. Journal of Experimental Botany 61, 2071-2081.
96. Hofmeister W.F.B. (1868) Allgemeine Morphologie Der Gewachse. W. Engelmann, Hofmeister, Leipzig.
97. Hu Z., Hung J.H., Wang Y., Chang Y.C., Huang C.L., Huyck M. & DeLisi C. (2009) VisANT 3.5: multi-scale network visualization, analysis and inference based on the gene ontology. Nucleic Acids Research 37, (Web Server issue), W115-W121.
98. Ideker T., Galitski T. & Hood L. (2001) A new approach to decoding life: systems biology. Annual Review of Genomics and Human Genetics 2, 343-372.
99. Ihmels J., Bergmann S. & Barkai N. (2004) Defining transcription modules using large-scale gene expression data. Bioinformatics 20, 1993-2003.
100. Jacob F. (1974) The Logic of Living Systems: A History of Heredity. Allen Lane, London, UK.
101. Jaeger J., Irons D. & Monk N. (2008) Regulative feedback in pattern formation: towards a general relativistic theory of positional information. Development 135, 3175-3183.
102. de Jong H. (2002) Modeling and simulation of genetic regulatory systems: a literature review. Journal of Computational Biology: A Journal of Computational Molecular Cell Biology 9, 67-103.
103. de Jong H. & Ropers D. (2006) Strategies for dealing with incomplete information in the modeling of molecular interaction networks. Briefings in bioinformatics 7, 354-363.
104. Jönsson H., Heisler M., Reddy G.V., Agrawal V., Gor V., Shapiro B.E., Mjolsness E. & Meyerowitz E.M. (2005) Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem. Bioinformatics 21, i232-i240.
105. Jönsson H., Heisler M.G., Shapiro B.E., Meyerowitz E.M. & Mjolsness E. (2006) An auxin-driven polarized transport model for phyllotaxis. Proceedings of the National Academy of Sciences of the United States of America 103, 1633-1638.
106. Joung J., Corbett A.M., Fellman S.M., Tieman D.M., Klee H.J., Giovannoni J.J. & Fei Z. (2009) Plant MetGenMAP: an integrative analysis system for plant systems biology. Plant Physiology 151, 1758-1768. pp.109.145169.
107. Kauffman S.A. (1969) Metabolic stability and epigenesis in randomly constructed genetic nets. Journal of Theoretical Biology 22, 437-467.
108. Kauffman S.A. (1993) The Origins of Order: Self Organization and Selection in Evolution. Oxford University Press, New York, USA.
109. van Keulen H. & Penning de Vries F.W.T. (1993) Farming under uncertainty: terminology and techniques. In International Crop Science pp. 139-144. Crop Science Society of America, Honolulu, HI, USA.
110. van Keulen H., Penning de Vries F.W.T. & Drees E.M. (1982) A summary model for crop growth. In Simulation of Plant Growth and Crop Production, pp. 87-97. Simulation Monographs, Wageningen, The Netherlands.
111. van Keulen H., van Laar H.H. & Rabbinge R. (2008) 40 Years Theory and Model at Wageningen UR (eds H. Van Keulen, H.H. Van Laar & R. Rabbinge), Wageningen University and Research Centre, The Netherlands.
112. Kim J., Shin D., Jung S.H., Heslop-Harrison P. & Cho K.H. (2010) A design principle underlying the synchronization of oscillations in cellular systems. Journal of Cell Science 123, 537-543.
113. Kim T. & Park P.J. (2010) Advances in analysis of transcriptional regulatory networks. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 3, 21-35.
114. Kitano H. (2002) Systems biology: a brief overview. Science 295, 1662-1664.
115. Kohl P., Crampin E. & Noble D. (2010) Systems biology: an approach. Clinical Pharmacology and Therapeutics 88, 25-33.
116. Konopka A.K. (2007) Systems Biology: Principles, Methods and Concepts (ed. A.K. Konopka), CRC Press, New York, NY, USA.
117. Kramer E.M. (2009) Computer models of auxin transport: a review and commentary. Journal of Experimental Botany 59, 45-53.
118. Krouk G., Tranchina D., Lejay L., Cruikshank A.A., Shasha D., Coruzzi G.M. & Gutiérrez R.A. (2009) A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLoS Computational Biology 5, e1000326.
119. Krupinski P. & Jönsson H. (2010) Modeling auxin-regulated development. Cold Spring Harbor Perspectives in Biology 2, a001560.
120. Laskowski M., Grieneisen V.A., Hofhuis H., Hove C.A., Hogeweg P., Marée A.F. & Scheres B. (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biology 6, e307.
121. Le Roux X., Lacointe A., Escobar-Gutiérrez A. & Le Dizès S. (2001) Carbon-based models of individual tree growth: a critical appraisal. Annals of Forest Science 58, 38.
122. Li H., Xuan J., Wang Y. & Zhan M. (2008) Inferring regulatory networks. Frontiers in Bioscience: A Journal and Virtual Library 13, 263-275.
123. Li S., Assmann S.M. & Albert R. (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biology 4, e312.
124. Lindenmayer A. (1968) Mathematical models for cellular interactions in development. I. Filaments with one-sided inputs. Journal of Theoretical Biology 18, 280-299.
125. Lindenmayer A. (1975) Developmental algorithms for multicellular organisms: a survey of L-systems. Journal of Theoretical Biology 54, 3-22.
126. Locke J.C.W., Millar A. & Turner M. (2005) Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. Journal of Theoretical Biology 234, 383-393.
127. Locke J.C.W., Southern M.M., Kozma-Bognär L., Hibberd V., Brown P.E., Turner M.S. & Millar A.J. (2005) Extension of a genetic network model by iterative experimentation and mathematical analysis. Molecular Systems Biology 1, 1-9.
128. Locke J.C.W., Kozma-Bognär L., Gould P.D., Fehér B., Kevei E., Nagy F., Turner M.S., Hall A. & Millae A.J. (2006) Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Molecular Systems Biology 2, 59-59.
129. Lontoc-Roy M., Dutilleul P., Prasher S.O., Han L. & Smith D.L. (2005) Computed tomography scanning for three-dimensional imaging and complexity analysis of developing rootsystems. Canadian Journal of Botany 83, 1434-1442.
130. Loomis R.S., Rabbinge R. & Ng E. (1979) Explanatory models in crop physiology. Annual Review of Plant Physiology 30, 339-367.
131. Lough T.J. & Lucas W.J. (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annual Review of Plant Biology 57, 203-232.
132. Lucas M., Guédon Y., Jay-Allemand C., Godin C. & Laplaze L. (2008) An auxin transport-based model of root branching in Arabidopsis thaliana. PLoS ONE 3, e3673.
133. Lucas W.J. & Lee J. (2004) Plasmodesmata as a supracellular control network in plants. Nature Reviews Molecular Cell Biology 5, 712-726.
134. Ma'ayan A., Cecchi G.A., Wagner J., Rao A.R., Iyengar R. & Stolovitzky G. (2008) Ordered cyclic motifs contribute to dynamic stability in biological and engineered networks. Proceedings of the National Academy of Sciences of the United States of America 105, 19235-19240.
135. Ma'ayan A., Jenkins S.L., Webb R.L., Berger S.I., Purushothaman S.P., Abul-Husn N.S., Posner J.M., Flores T. & Iyengar R. (2009) SNAVI: desktop application for analysis and visualization of large-scale signaling networks. BMC Systems Biology 3, 10.
136. Marbach D., Prill R.J., Schaffter T., Mattiussi C., Floreano D. & Stolovitzky G. (2010) Revealing strengths and weaknesses of methods for gene network inference. Proceedings of the National Academy of Sciences of the United States of America 107, 6286-6291.
137. Martin M.H., Goldsmith M.H.M. & Goldsmith T.H. (1990) On polar auxin transport in plant cells. Journal of Mathematical Biology 28, 197-223.
138. 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.
139. Mathieu A., Cournède P.H., Letort V., Barthélémy D. & de Reffye P. (2009) A dynamic model of plant growth with interactions between development and functional mechanisms to study plant structural plasticity related to trophic competition. Annals of Botany 103, 1173-1186.
140. Matthews D.E., Lazo G.R. & Anderson O.D. (2009) Plant and crop databases. Methods in Molecular Biology (Clifton, N.J.) 513, 243-262.
141. McDermott J. (2009) Computational systems biology. Humana.
142. Měch R. & Prusinkiewicz P. (1996) Visual models of plants interacting with their environment. Computer Graphics (SIGGRAPH '96 Conference Proceedings), 397-410.
143. Mendoza L. & Alvarez-Buylla E.R. (2000) Genetic regulation of root hair development in Arabidopsis thaliana: a network model. Journal of Theoretical Biology 204, 311-326.
144. Middleton A.M., King J.R., Bennett M.J. & Owen M.R. (2010) Mathematical modelling of the Aux/IAA negative feedback loop. Bulletin of Mathematical Biology 72, 1383-1407.
145. Milenković T., Lai J. & Przulj N. (2008) GraphCrunch: a tool for large network analyses. BMC Bioinformatics 9, 70.
146. Millar A.J., Short S.R., Hiratsuka K., Chua N.H. & Kay S.A. (1992) Firefly luciferase as a reporter of regulated gene expression in higher plants. Plant Molecular Biology Reporter 10, 324-337.
147. Millar A., Carré I.A., Strayer C.A., Chua N.H. & Kay S.A. (1995) Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267, 1161-1163.
148. Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D. & Alon U. (2002) Network motifs: simple building blocks of complex networks. Science 298, 824-827.
149. Mironova V.V., Omelyanchuk N.A., Yosiphon G., Fadeev S.I., Kolchanov N.A., Mjolsness E. & Likhoshvai V.A. (2010) A plausible mechanism for auxin patterning along the developing root. BMC Systems Biology 4, 98.
150. Morris M.K., Saez-Rodriguez J., Sorger P.K. & Lauffenburger D.A. (2010) Logic-based models for the analysis of cell signaling networks. Biochemistry 49, 3216-3224.
151. Nakamichi N., Ito S., Oyama T., Yamashino T., Kondo T. & Mizuno T. (2004) Characterization of plant circadian rhythms by employing Arabidopsis cultured cells with bioluminescence reporters. Plant Cell Physiology 45, 57-67.
152. Nakielski J. (2008) The tensor-based model for growth and cell divisions of the root apex. I. The significance of principal directions. Planta 228, 179-189.
153. Nakielski J. & Hejnowicz Z. (2003) The description of growth of plant organs: a continuous approach based on the growth tensor. In Formal Descriptions of Developing Systems pp. 119-136. Kluwer Academuc Publishers, Dordrecht, The Netherlands. Available at: [Accessed August 19, 2010].
154. Niklas K.J. (1992) Plant Biomechanics: An Engineering Approach to Plant Form and Function. University of Chicago Press, Chicago, IL, USA.
155. Niklas K.J. (2007) Maximum plant height and the biophysical factors that limit it. Tree Physiology 27, 433-440.
156. van Noordwijk M. & Wadman W.P. (1992) Effects of spatial variability of nitrogen supply on environmental acceptable nitrogen fertilizer application rates to arable crops. The Netherlands Journal of Agriculture Science 40, 51-72.
157. Paananen J. & Wong G. (2009) FORG3D: force-directed 3D graph editor for visualization of integrated genome scale data. BMC Systems Biology 3, 26.
158. Palaniswamy S.K., James S., Sun H., Lamb R.S., Davuluri R.V. & Grotewold E. (2006) AGRIS and AtRegNet. a platform to link cis-regulatory elements and transcription factors into regulatory networks. Plant Physiology 140, 818-829.
159. Pan D., Sun N., Cheung K.H., Guan Z., Ma L., Holford M., Deng X. & Zhao H. (2003) PathMAPA: a tool for displaying gene expression and performing statistical tests on metabolic pathways at multiple levels for Arabidopsis. BMC Bioinformatics 4, 56.
160. Parent B., Turc O., Gibon Y., Stitt M. & Tarfieu F. (2010) Modelling temperature-compensated physiological rates, based on the co-ordination of responses to temperature of developmental processes. Journal of Experimental Botany 61, 2057-2069.
161. Parizot B., De Rybel B. & Beeckman T. (2010) VisuaLRTC: a new view on lateral root initiation by combining specific transcriptome data sets. Plant Physiology 153, 34-40.
162. Paul M.J. & Pellny T.K. (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany. 54, 539-547.
163. Perrine-Walker F., Doumas P., Lucas M. etal. (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by frankia in casuarina glauca actinorhizal nodules. Plant Physiology 154, 1372-1380.
164. Pesch M. & Hülskamp M. (2009) One, two, three...models for trichome patterning in Arabidopsis? Current Opinion in Plant Biology 12, 587-592.
165. Poorter H., Niinemets U., Walter A., Fiorani F. & Schurr U. (2010) A method to construct dose-response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data. Journal of Experimental Botany 61, 2043-2055.
166. Popescu S.C., Popescu G.V., Bachan S., Zhang Z., Seay M., Gerstein M., Snyder M. & Dinesh-Kumar S.P. (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proceedings of the National Academy of Sciences of the United States of America 104, 4730-4735.
167. Pradal C., Dufour-Kowalski S., Boudon F., Fournier C. & Godin C. (2008) OpenAlea: a visual programming and component-based software platform for plant modelling. Functional Plant Biology 35, 751-760.
168. Prusinkiewicz P. (2004) Modeling plant growth and development. Current Opinion in Plant Biology 7, 79-83.
169. Prusinkiewicz P. & Lindenmayer A. (1990) The Algorithmic Beauty of Plants. Springer-Verlag New York, Inc., New York, USA. Available at: [Accessed July 12, 2010].
170. Prusinkiewicz P., Crawford S., Smith R.S., Ljung K., Bennett T., Ongaro V. & Leyser O. (2009) Control of bud activation by an auxin transport switch. Proceedings of the National Academy of Sciences of the United States of America 106, 17431-17436.
171. Pu L. & Brady S. (2010) Systems biology update: cell type-specific transcriptional regulatory networks. Plant Physiology 152, 411-419.
172. Rao C.V. & Arkin A.P. (2001) Control motifs for intracellular regulatory networks. Annual Review of Biomedical Engineering 3, 391-419.
173. de Reffye P., Heuvelink E., Barthélémy D. & Cournède P.H. (2008) Plant growth models. In Encyclopedia of Ecology, pp. 2824-2838. Elsevier, Amsterdam.
174. de Reuille P.B., Bohn-Courseau I., Ljung K., Morin H., Carraro N., Godin C. & Traas J. (2006) Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 1627-1632.
175. Rigoutsos I. & Stephanopoulos G. (2007) Systems Biology: Volume I - Genomics & Volume II - Networks, Models, and Applications. Oxford University Press US, New York, USA.
176. Robertson J.B., Stowers C.C., Boczko E. & Johnson C.H. (2008) Real-time luminescence monitoring of cell-cycle and respiratory oscillations in yeast. Proceedings of the National Academy of Sciences of the United States of America 105, 17988-17993.
177. Rolland-Lagan A. & Prusinkiewicz P. (2005) Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. The Plant Journal 44, 854-865.
178. Sakai H., Hasegawa T. & Kobayashi K. (2006) Enhancement of rice canopy carbon gain by elevated CO(2) is sensitive to growth stage and leaf nitrogen concentration. The New Phytologist 170, 321-332.
179. Savage N.S., Walker T., Wieckowski Y., Schiefelbein J., Dolan L. & Monk N.A. (2008) A Mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biology 6, e235.
180. Schauer N. & Fernie A. (2006) Plant metabolomics: towards biological function and mechanism. Trends in Plant Science 11, 508-516.
181. Schellmann S., Hulskamp M. & Uhrig J. (2007) Epidermal pattern formation in the root and shoot of Arabidopsis. Biochemical Society Transactions 35, 146-148.
182. Shapiro B.E., Levchenko A., Meyerowitz E.M., Wold B.J. & Mjolsness E.D. (2003) Cellerator: extending a computer algebra system to include biochemical arrows for signal transduction simulations. Bioinformatics 19, 677-678.
183. Sievänen R., Nikinmaa E., Nygren P., Ozier-Lafontaine H., Perttunen J. & Hakula H. (2000) Components of functional-structural tree models. Annals of Forest Science 57, 14.
184. Smith R.S., Guyomarc'h S. & Mandel T. (2006) A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences of the United States of America 103, 1301-1306.
185. Snow M. & Snow R. (1962) A theory of the regulation of phyllotaxis based on lupinus albus. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 244, 483-513.
186. Soussana J., Graux A. & Tubiello F.N. (2010) Improving the use of modelling for projections of climate change impacts on crops and pastures. Journal of Experimental Botany 61, 2217-2228.
187. Stolovitzky G., Monroe D. & Califano A. (2007) Dialogue on reverse-engineering assessment and methods: the DREAM of high-throughput pathway inference. Annals of the New York Academy of Sciences 1115, 1-22.
188. Stolovitzky G., Prill R.J. & Califano A. (2009) Lessons from the DREAM2 Challenges. Annals of the New York Academy of Sciences 1158, 159-195.
189. Stoma S., Lucas M., Chopard J., Schaedel M., Traas J. & Godin C. (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Computational Biology 4, e1000207.
190. Struik P.C., Cassman K.G. & Koornneef M. (2007) A dialogue on interdisciplinary collaboration to bridge the gap between plant genomics and crop sciences. In Proceedings of the Frontis Workshop on Scale and Complexity in Plant Systems Research: Gene-Plant-Crop Relations Wageningen UR Frontis 21. Frontis Workshop on Scale and complexity in plant systems research: gene-plant-crop relations. pp. 319-328. Springer, Wageningen, The Netherlands.
191. Suderman M. & Hallett M. (2007) Tools for visually exploring biological networks. Bioinformatics (Oxford, England) 23, 2651-2659.
192. Szallasi Z., Stelling J. & Periwal V. (2010) System Modeling in Cellular Biology: From Concepts to Nuts and Bolts. The MIT Press, Boston, MA, USA.
193. Szymanowska-Pułka J. & Nakielski J. (2010) The tensor-based model for growth and cell divisions of the root apex. II. Lateral root formation. Planta 232, 1207-1218. Available at: [Accessed August 19, 2010].
194. Tardieu F. (2010) Why work and discuss the basic principles of plant modelling 50 years after the first plant models? Journal of Experimental Botany 61, 2039-2041.
195. Taylor R. & Singhal M. (2009) Biological network inference and analysis using SEBINI and CABIN. Methods in Molecular Biology (Clifton, N.J.) 541, 551-576.
196. Thomas R. (1973) Boolean formalization of genetic control circuits. Journal of Theoretical Biology 42, 563-585.
197. Thornley J.H.M. (1972) A Balanced quantitative model for root: shoot ratios in vegetative plants. Annals of Botany 36, 431-441.
198. Tobin B., Cermak J., Chiatante D. etal. (2007) Towards developmental modelling of tree root systems. Plant Biosystems 141, 481-501.
199. Trewavas A. (2006) A brief history of systems biology: 'every object that biology studies is a system of systems.' Francois Jacob (1974). The Plant Cell 18, 2420-2430.
200. Triboi E. & Triboi-Blondel A. (2002) Productivity and grain or seed composition: a new approach to an old problem invited paper. European journal of Agronomy 16, 163-186.
201. Turing A.M. (1952) The chemical basis of morphogenesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 237, 37-72.
202. Twycross J., Band L.R., Bennett M.J., King J.R. & Krasnogor N. (2010) Stochastic and deterministic multiscale models for systems biology: an auxin-transport case study. BMC Systems Biology 4, 34.
203. Uyttewaal M., Traas J. & Hamant O. (2010) Integrating physical stress, growth, and development. Current Opinion in Plant Biology 13, 46-52.
204. Van Norman J.M. & Benfey P.N. (2009) Arabidopsis thaliana as a model organism in systems biology. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 1, 372-379.
205. Vidal M. (2009) A unifying view of 21st century systems biology. FEBS Letters 583, 3891-3894.
206. Vidal E.A. & Gutiérrez R.A. (2008) A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Current Opinion in Plant Biology 11, 521-529.
207. Vos J., Marcelis L.F.M., Visser P.H.B., Struik P.C. & Evers J.B. (2007) Functional-Structural Plant Modelling in Crop Production (eds J. Vos, L.F.M. Marcelis, P.H.B. De Visser, P.C. Struik & J.B. Evers), Springer, Dordrecht, Holland.
208. Vos J., Evers J.B., Buck-Sorlin G.H., Andrieu B., Chelle M. & de Visser P.H. (2010) Functional-structural plant modelling: a new versatile tool in crop science. Journal of Experimental Botany 61, 2101-2115.
209. Walker D.C. & Southgate J. (2009) The virtual cell - a candidate co-ordinator for 'middle-out' modelling of biological systems. Briefings in Bioinform 10, 450-461.
210. Weckwerth W. (2003) Metabolomics in systems biology. Annual Review of Plant Biology 54, 669-689.
211. Wei H., Persson S., Mehta T., Srinivasasainagendra V., Chen L., Page P.G., Somerville C. & Loraine A. (2006) Transcriptional coordination of the metabolic network in Arabidopsis. Plant Physiology 142, 762-774.
212. Werhli A.V., Grzegorczyk M. & Husmeier D. (2006) Comparative evaluation of reverse engineering gene regulatory networks with relevance networks, graphical Gaussian models and Bayesian networks. Bioinformatics (Oxford, England) 22, 2523-2531.
213. Westerhoff H.V., Winder C., Messiha H., Simeonidis E., Adamczyk M., Verma M., Bruggeman F.J. & Dunn W. (2009) Systems biology: the elements and principles of life. FEBS Letters 583, 3882-3890.
214. de Wit A. (1982) Simulation of living systems. In Simulation of Plant Growth and Crop Production pp. 3-8. Simulation Monographs, Wageningen, The Netherlands.
215. de Wit A. & van Diepen C. (2008) Crop growth modelling and crop yield forecasting using satellite-derived meteorological inputs. International Journal of Applied Earth Observation and Geoinformation 10, 414-425.
216. Wymer C.L., Wymer S.A., Cosgrove D.J. & Cyr R.J. (1996) Plant cell growth responds to external forces and the response requires intact microtubules. Plant Physiology 110, 425-430.
217. Xu D.Q., Gifford R.M. & Chow W.S. (1994) Photosynthetic acclimation in pea and soybean to high atmospheric CO2 partial pressure. Plant Physiology 106, 661-671.
218. Yin X. & van Laar H.H. (2005) Crop Systems Dynamics: An Ecophysiological Simulation Model for Genotype-by-Environment Interactions (eds X. Yin & H.H. Van Laar), Wageningen Academic Publishers, Wageningen, The Netherlands.
219. Yin X. & Struik P.C. (2010) Modelling the crop: from system dynamics to systems biology. Journal of Experimental Botany 61, 2171-2183.
220. Yin X., Struik P. & Kropff M. (2004) Role of crop physiology in predicting gene-to-phenotype relationships. Trends in Plant Science 9, 426-432.
221. Yip K.Y., Yu H., Schultz M. & Gerstein M. (2006) The tYNA platform for comparative interactomics: a web tool for managing, comparing and mining multiple networks. Bioinformatics (Oxford, England) 22, 2968-2970.
222. Yook S., Oltvai Z.N. & Barabási A. (2004) Functional and topological characterization of protein interaction networks. Proteomics 4, 928-942.
223. Yu H., Luscombe N.M., Lu H.X., Zhu X., Xia Y., Han J.D., Bertin N., CHung S., Vidal M. & Gerstein M. (2004) Annotation transfer between genomes: protein-protein interologs and protein-DNA regulogs. Genome Research 14, 1107-1118.
224. Yuan J.S., Galbraith D.W., Dai S.Y., Griffin P. & Stewart C.N. Jr. (2008) Plant systems biology comes of age. Trends in Plant Science 13, 165-171.
225. Zeilinger M.N., Farré E.M., Taylor S.R., Kay S.A. & Doyle F.J. 3rd (2006) A novel computational model of the circadian clock in Arabidopsis that incorporates PRR7 and PRR9. Molecular Systems Biology 2, 58-58.