Programmable and Self-Organised Processes in Plant Morphogenesis: The Architectural Development of Ryegrass

The morphology of forage grass, in particular ryegrass, emerges from the combination of many entangled dynamical processes. Although a plant seems to possess an intrinsic (i.e., genetically determined) architecture, its morphogenesis also displays very high plasticity with respect to environmental conditions. This plasticity could be partly mediated by a self-regulatory process. Indeed, the architecture of a shoot can affect subsequent architectural development recursively. For instance, leaf length is directly influenced by the length of the preceding leaves. We present a functional-structural 3D model of ryegrass shoots based on the hypothesis that their morphogenesis obeys such self-regulatory processes. The behaviour and emergent properties of the model are highly compatible with observations regarding plant morphology development, genetic variability and plasticity. Experimental and simulation results therefore suggest that the architectural development of ryegrass could emerge from the collaborative association between genetic programmability and self-organisation, instead of resulting from a centralised control of each architectural trait.

[1]  P. Barre,et al.  Morphological characteristics of perennial ryegrass leaves that influence short-term intake in dairy cows , 2006 .

[2]  Jochem B. Evers,et al.  Functional-Structural Plant Modelling in Crop Production: Adding a dimension , 2007 .

[3]  L. Hazard,et al.  Productivity under contrasting cutting regimes of perennial ryegrass selected for short and long leaves , 1997, Euphytica.

[4]  Abraham J. Escobar-Gutiérrez,et al.  A study of ryegrass architecture as a self-regulated system, using functional-structural plant modelling. , 2008, Functional plant biology : FPB.

[5]  Matthew,et al.  Tiller size/density compensation in perennial ryegrass miniature swards subject to differing defoliation heights and a proposed productivity index , 1999 .

[6]  Alban Verdenal,et al.  De la simulation de la morphogénèse de l'appareil aérien du ray-grass anglais (Lolium perenne L. ) : exploration d'un schéma cybernétique inspiré du concept d'auto-organisation et applications , 2009 .

[7]  M. Agnusdei,et al.  A comparative analysis of the temperature response of leaf elongation in Bromus stamineus and Lolium perenne plants in the field: intrinsic and size-mediated effects. , 2007, Annals of botany.

[8]  Gilles Lemaire,et al.  Tillering and leaf area index in grasses in the vegetative phase , 1987 .

[9]  P. Barre,et al.  QTLs of lamina length in Lolium perenne. , 2002 .

[10]  T. Lafarge,et al.  A model co-ordinating the elongation of all leaves of a sorghum cultivar was applied to both Mediterranean and Sahelian conditions. , 2002, Journal of experimental botany.

[11]  J. Casal,et al.  Effects of Light Quality on Tiller Production in Lolium spp. , 1983, Plant physiology.

[12]  James White,et al.  THE PLANT AS A METAPOPULATION , 1979 .

[13]  A. Laidlaw,et al.  The role of the sheath tube in the development of expanding leaves in perennial ryegrass , 1985 .

[14]  C. Ghersa,et al.  Intraspecific changes in plant morphology, associated with grazing, and effects on litter quality, carbon and nutrient dynamics during decomposition , 2006 .

[15]  C. J. Nelson,et al.  Epidermal cell division and the coordination of leaf and tiller development. , 1994, Annals of botany.

[16]  A. Elgersma,et al.  Sward characteristics important for intake in six Lolium perenne varieties , 2005 .

[17]  M. Dingkuhn,et al.  Leaf Blade Dimensions of Rice (Oryza sativa L. and Oryza glaberrima Steud.). Relationships between Tillers and the Main Stem , 2001 .

[18]  Paul C. Struik,et al.  Functional-Structural Plant Modelling in Crop Production , 2007 .

[19]  C. J. Nelson,et al.  Effects of nitrogen on mesophyll cell division and epidermal cell elongation in tall fescue leaf blades. , 1989, Plant physiology.

[20]  H. Gautier,et al.  Tillering Responses to the Light Environment and to Defoliation in Populations of Perennial Ryegrass (Lolium perenneL.) Selected for Contrasting Leaf Length , 1999 .

[21]  B. Forde.  Effect of Various Environments on the Anatomy and Growth of Perennial Ryegrass and Cocksfoot , 1966 .

[22]  J. Peyraud,et al.  Herbage intake and milk yield of dairy cows grazing perennial ryegrass swards or white clover/perennial ryegrass swards at low- and medium-herbage allowances , 2005 .

[23]  Isaac Asimov,et al.  Adding a Dimension , 1964 .

[24]  E. Thom,et al.  Differences in Tillering of Long‐ and Short‐Leaved Perennial Ryegrass Genetic Lines under Full Light and Shade Treatments , 2000 .

[25]  A. Beddows.  Biological Flora of the British Isles. Lolium perenne L. , 1967 .

[26]  Kevin F. Smith,et al.  QTL Analysis of Morphological, Developmental, and Winter Hardiness-Associated Traits in Perennial Ryegrass , 2004 .

[27]  I. Casey,et al.  Effects of sheath tube length on leaf development in perennial ryegrass (Lolium perenne L.) , 1999 .

[28]  L. Torvell,et al.  Components of regrowth in grazed and cut Lolium perenne swards , 1981 .

[29]  S. Prache,et al.  Préhensibilité de l'herbe pâturée chez les bovins et les ovins , 1997 .

[30]  A. Davies,et al.  Regrowth of perennial ryegrass as affected by simulated leaf sheaths , 1983, The Journal of Agricultural Science.

[31]  M. Duru,et al.  Growth and Senescence of the Successive Leaves on a Cocksfoot Tiller. Effect of Nitrogen and Cutting Regime , 2000 .

[32]  H. Schnyder,et al.  Components of leaf elongation rate and their relationship to specific leaf area in contrasting grasses , 2003 .

[33]  Bruno Andrieu,et al.  Onset of sheath extension and duration of lamina extension are major determinants of the response of maize lamina length to plant density. , 2006, Annals of botany.

[34]  J. Emile,et al.  Differences in sward structure of ryegrass cultivars and impact on milk production of grazing dairy cows , 2006 .

[35]  H. Schnyder,et al.  Phosphorus nutrition and mycorrhiza effects on grass leaf growth. P status- and size-mediated effects on growth zone kinematics. , 2006, Plant, cell & environment.

[36]  Lars Olof Björn,et al.  Plants as light traps , 1986 .

[37]  Przemyslaw Prusinkiewicz,et al.  Design and Implementation of the L+C Modeling Language , 2003, RULE@RDP.

[38]  B. Andrieu,et al.  Towards a generic architectural model of tillering in Gramineae, as exemplified by spring wheat (Triticum aestivum). , 2005, The New phytologist.

[39]  Jan Vos,et al.  A flexible sigmoid function of determinate growth. , 2003, Annals of botany.

[40]  B. Forde.  Effect of various environments on the anatomy and growth of Perennial Ryegrass and Cocksfoot: I. Leaf Growth , 1966 .

[41]  Przemyslaw Prusinkiewicz,et al.  The Algorithmic Beauty of Plants , 1990, The Virtual Laboratory.

[42]  C. J. Nelson,et al.  Interrelationships between Rates of Leaf Appearance and Tillering in Selected Tall Fescue Populations1 , 1984 .

[43]  G. McMaster,et al.  Phytomers, phyllochrons, phenology and temperate cereal development , 2005, The Journal of Agricultural Science.

[44]  A. Davies,et al.  Rates of Leaf and Tiller Production in Young Spaced Perennial Ryegrass Plants in Relation to Soil Temperature and Solar Radiation , 1983 .