Understanding the effect of carbon status on stem diameter variations.

BACKGROUND Carbon assimilation and leaf-to-fruit sugar transport are, along with plant water status, the driving mechanisms for fruit growth. An integrated comprehension of the plant water and carbon relationships is therefore essential to better understand water and dry matter accumulation. Variations in stem diameter result from an integrated response to plant water and carbon status and are as such a valuable source of information. METHODS A mechanistic water flow and storage model was used to relate variations in stem diameter to phloem sugar loading and sugar concentration dynamics in tomato. The simulation results were compared with an independent model, simulating phloem sucrose loading at the leaf level based on photosynthesis and sugar metabolism kinetics and enabled a mechanistic interpretation of the 'one common assimilate pool' concept for tomato. KEY RESULTS Combining stem diameter variation measurements and mechanistic modelling allowed us to distinguish instantaneous dynamics in the plant water relations and gradual variations in plant carbon status. Additionally, the model combined with stem diameter measurements enabled prediction of dynamic variables which are difficult to measure in a continuous and non-destructive way, such as xylem water potential and phloem hydrostatic potential. Finally, dynamics in phloem sugar loading and sugar concentration were distilled from stem diameter variations. CONCLUSIONS Stem diameter variations, when used in mechanistic models, have great potential to continuously monitor and interpret plant water and carbon relations under natural growing conditions.

[1]  A. Bel,et al.  Strategies of Phloem Loading , 1993 .

[2]  D. Intrigliolo,et al.  Crop load affects maximum daily trunk shrinkage of plum trees. , 2007, Tree physiology.

[3]  J. Boyer,et al.  Separating growth from elastic deformation during cell enlargement , 1999, Plant physiology.

[4]  N. Holbrook,et al.  Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. , 2011, Plant, cell & environment.

[5]  André Lacointe,et al.  Modelling phloem and xylem transport within a complex architecture. , 2008, Functional plant biology : FPB.

[6]  Kathy Steppe,et al.  A step towards new irrigation scheduling strategies using plant-based measurements and mathematical modelling , 2008, Irrigation Science.

[7]  J. Ortega.  Augmented growth equation for cell wall expansion. , 1985, Plant physiology.

[8]  Joan Bonany,et al.  Could trunk diameter sensors be used in woody crops for irrigation scheduling? A review of current knowledge and future perspectives. , 2010 .

[9]  John A. Nelder,et al.  A Simplex Method for Function Minimization , 1965, Comput. J..

[10]  J. Grace,et al.  Continuous measurements of water tensions in the xylem of trees based on the elastic properties of wood , 1997, Planta.

[11]  L. Ho.  The Regulation of Carbon Transport and the Carbon Balance of Mature Tomato Leaves , 1978 .

[12]  L. Ho.  The Relationship Between the Rates of Carbon Transport and of Photosynthesis in Tomato Leaves , 1976 .

[13]  H. Jones.  Plants and Microclimate: Other environmental factors: wind, altitude, climate change and atmospheric pollutants , 2013 .

[14]  E. Nikinmaa,et al.  Sugar transport together with environmental conditions controls time lags between xylem and stem diameter changes , 2003 .

[15]  K. Steppe,et al.  Could rapid diameter changes be facilitated by a variable hydraulic conductance? , 2012, Plant, cell & environment.

[16]  Kathy Steppe,et al.  Development and verification of a water and sugar transport model using measured stem diameter variations. , 2010, Journal of experimental botany.

[17]  Kathy Steppe,et al.  A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth. , 2006, Tree physiology.

[18]  C. Gary,et al.  Un modèle simple de simulation des relations microclimat -- bilan carboné chez la tomate en phase végétative , 1988 .

[19]  M. Génard,et al.  Model-assisted analysis of tomato fruit growth in relation to carbon and water fluxes. , 2007, Journal of experimental botany.

[20]  B. Brunel,et al.  Relation entre température, teneur en glucides et respiration de la plante entière chez la tomate en phase végétative , 1988 .

[21]  M. Dixon,et al.  Water relations of the tomato during fruit growth , 1992 .

[22]  E. Heuvelink,et al.  Dry matter distribution in tomato and cucumber. , 1989 .

[23]  Ep Heuvelink,et al.  Dry matter partitioning in a tomato plant: one common assimilate pool? , 1995 .

[24]  Park S. Nobel,et al.  Physicochemical and Environmental Plant Physiology , 1991 .

[25]  M. Génard,et al.  A biophysical model of fruit growth: simulation of seasonal and diurnal dynamics of mass , 1998 .

[26]  J G Huguet,et al.  A biophysical analysis of stem and root diameter variations in woody plants. , 2001, Plant physiology.

[27]  C. Pollock,et al.  Soluble acid invertase activity in leaves is independent of species differences in leaf carbohydrates, diurnal sugar profiles and paths of phloem loading , 1998 .

[28]  Kathy Steppe,et al.  MRI links stem water content to stem diameter variations in transpiring trees. , 2012, Journal of experimental botany.

[29]  Kathy Steppe,et al.  Determining reference values for stem water potential and maximum daily trunk shrinkage in young apple trees based on plant responses to water deficit , 2009 .

[30]  Ep Heuvelink,et al.  Dry-matter production in a tomato crop: comparison of two simulation models , 1993 .

[31]  J. Lockhart.  An analysis of irreversible plant cell elongation. , 1965, Journal of theoretical biology.

[32]  Wolf B. Frommer,et al.  Phloem loading and unloading of sugars and amino acids , 2003 .

[33]  M. Monsi,et al.  On the factor light in plant communities and its importance for matter production. 1953. , 2004, Annals of botany.

[34]  T. Dejong,et al.  Water stress and crop load effects on fruit fresh and dry weights in peach (Prunus persica). , 1996, Tree physiology.

[35]  R. Lemeur,et al.  Detailed analysis of double girdling effects on stem diameter variations and sap flow in young oak trees , 2010 .

[36]  H. Challa,et al.  A dynamic tomato growth and yield model (TOMGRO) , 1991 .

[37]  K. Burton,et al.  Source—sink Relationships and Carbon Metabolism in Tomato Leaves 1. 14C Assimilate Compartmentation , 1983 .

[38]  Tom De Swaef.  Measuring, modelling and understanding sap flow and stem diameter variations in tomato , 2011 .

[39]  W. Cornelis,et al.  Tomato sap flow, stem and fruit growth in relation to water availability in rockwool growing medium , 2011, Plant and Soil.

[40]  D. Geiger,et al.  Role of starch in carbon translocation and partitioning at the plant level , 2000 .

[41]  Kris Villez,et al.  Use of Unfold PCA for on-line plant stress monitoring and sensor failure detection , 2009 .

[42]  Nathan G. McDowell,et al.  Update on Mechanisms of Vegetation Mortality Mechanisms Linking Drought , Hydraulics , Carbon Metabolism , and Vegetation Mortality 1 [ W ] , 2011 .

[43]  D. J. Fitter,et al.  The Contribution of Leaves from Different Levels within a Tomato Crop to Canopy Net Photosynthesis: An Experimental Examination of Two Canopy Models , 1978 .

[44]  H. Jones.  Irrigation scheduling: advantages and pitfalls of plant-based methods. , 2004, Journal of experimental botany.

[45]  K. Steppe,et al.  Linking stem diameter variations to sap flow, turgor and water potential in tomato , 2010 .

[46]  N. Bertin,et al.  Time-course of tomato whole-plant respiration and fruit and stem growth during prolonged darkness in relation to carbohydrate reserves. , 2003, Annals of botany.

[47]  J. Hewitt,et al.  Remobilization of Nonstructural Carbohydrates from Vegetative Tissues to Fruits in Tomato , 1986, Journal of the American Society for Horticultural Science.

[48]  G. Vercambre,et al.  An analysis of elastic and plastic fruit growth of mango in response to various assimilate supplies. , 2007, Tree physiology.

[49]  Kathy Steppe,et al.  Tree girdling responses simulated by a water and carbon transport model. , 2011, Annals of botany.

[50]  H. Gautier,et al.  Towards a virtual fruit focusing on quality: modelling features and potential uses. , 2007, Journal of experimental botany.

[51]  D. Geiger,et al.  Evidence for active Phloem loading in the minor veins of sugar beet. , 1974, Plant physiology.

[52]  Mª Victoria Cuevas Sánchez,et al.  Irrigation scheduling from stem diameter variations: A review , 2010 .

[53]  P. D. de Visser,et al.  Exploring the spatial distribution of light interception and photosynthesis of canopies by means of a functional-structural plant model. , 2011, Annals of botany.

[54]  A. Gosselin,et al.  Photosynthesis in leaves, fruits, stem and petioles of greenhouse-grown tomato plants , 1998, Photosynthetica.

[55]  D J W De Pauw,et al.  Identifiability analysis and improvement of a tree water flow and storage model. , 2008, Mathematical biosciences.

[56]  P. Lootens,et al.  Low night temperature acclimation of Phalaenopsis , 2011, Plant Cell Reports.

[57]  H. Cochard,et al.  Experimental analysis of the role of water and carbon in tree stem diameter variations. , 2004, Journal of experimental botany.

[58]  G. Vercambre,et al.  Improvement of the enhanced phloem exudation technique to estimate phloem concentration and turgor pressure in tomato , 2010 .

[59]  E. Komor.  Source physiology and assimilate transport: the interaction of sucrose metabolism, starch storage and phloem export in source leaves and the effects on sugar status in phloem , 2000 .