The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model

We have observed that low soil phosphorus availability alters the gravitropic response of basal roots in common bean (Phaseolus vulgaris L.), resulting in a shallower root system. In this study we use a geometric model to test the hypotheses that a shallower root system is a positive adaptive response to low soil P availability by (1) concentrating root foraging in surface soil horizons, which generally have the highest P availability, and (2) reducing spatial competition for P among roots of the same plant. The growth of nine root systems contrasting in gravitropic response over 320 h was simulated in SimRoot, a dynamic three-dimensional geometric model of root growth and architecture. Phosphorus acquisition and inter-root competition were estimated with Depzone, a program that dynamically models nutrient diffusion to roots. Shallower root systems had greater P acquisition per unit carbon cost than deeper root systems, especially in older root systems. This was due to greater inter-root competition in deeper root systems, as measured by the volume of overlapping P depletion zones. Inter-root competition for P was a significant fraction of total soil P depletion, and increased with increasing values of the P diffusion coefficient (De), with root age, and with increasing root gravitropism. In heterogenous soil having greater P availability in surface horizons, shallower root systems had greater P acquisition than deeper root systems, because of less inter-root competition as well as increased root foraging in the topsoil. Root P acquisition predicted by SimRoot was validated against values for bean P uptake in the field, with an r2 between observed and predicted values of 0.75. Our results support the hypothesis that altered gravitropic sensitivity in P-stressed roots, resulting in a shallower root system, is a positive adaptive response to low P availability by reducing inter-root competition within the same plant and by concentrating root activity in soil domains with the greatest P availability.

[1]  P. Nye,et al.  A model to calculate the uptake by a developing root system or root hair system of solutes with concentration variable diffusion coefficients , 1974, Plant and Soil.

[2]  P. J. Smethurst,et al.  SIMULATING NUTRIENT UPTAKE BY SINGLE OR COMPETING AND CONTRASTING ROOT SYSTEMS , 1993 .

[3]  J. Lynch,et al.  Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. , 1996, The New phytologist.

[4]  G. Berntson.  Modelling root architecture: are there tradeoffs between efficiency and potential of resource acquisition? , 1994 .

[5]  P. B. Tinker,et al.  Solute Movement in the Soil-Root System. , 1978 .

[6]  Andrei G. Jablokow,et al.  Carbon cost of root systems: an architectural approach , 1994, Plant and Soil.

[7]  E. J. Kamprath,et al.  Soil Nutrient Bioavailability—A Mechanistic Approach , 1985 .

[8]  C. Hackett,et al.  A model of the Extension and Branching of a Seminal Root of Barley, and Its Use in Studying Relations Between Root Dimensions II. Results and Inferences From Manipulation of the Model , 1972 .

[9]  Alastair H. Fitter,et al.  Characteristics and Functions of Root Systems , 2002 .

[10]  J. Lynch.  Root Architecture and Plant Productivity , 1995, Plant physiology.

[11]  S. A. Barber,et al.  Phosphate Uptake by Corn as Affected by Soil Characteristics and Root Morphology 1 , 1979 .

[12]  P. Ahn,et al.  Profile characteristics, and form and surface activity of inorganic phosphorus in a deep red Kenya coffee soil (Nitosol) , 1986 .

[13]  S. A. Barber,et al.  Simulation Model for Nutrient Uptake from Soil by a Growing Plant Root System1 , 1976 .

[14]  N. Claassen,et al.  Ion Diffusion in the Soil–Root System , 1997 .

[15]  P. Nye,et al.  The relative uptake of phosphorus by crops and natural fallow from different parts of their root zone , 1961, Journal of Agricultural Sciences.

[16]  C. Hackett,et al.  A Model of the Extension and Branching of a Seminal Root of Barley, and Its Use in Studying Relations Between Root Dimensions I the Model , 1972 .

[17]  A. J. Diggle,et al.  ROOTMAP—a model in three-dimensional coordinates of the growth and structure of fibrous root systems , 1988, Plant and Soil.

[18]  Loïc Pagès,et al.  MODELLING OF THE HYDRAULIC ARCHITECTURE OF ROOT SYSTEMS : AN INTEGRATED APPROACH TO WATER ABSORPTION : MODEL DESCRIPTION , 1998 .

[19]  S. Thien,et al.  Phosphorus Uptake from Soil Layers Having Different Soil Test Phosphorus Levels1 , 1986 .

[20]  R. Zobel,et al.  Root Characteristics of Black Beans. II. Morphological Differences Among Genotypes 1 , 1979 .

[21]  J. Lynch,et al.  Growth and architecture of seedling roots of common bean genotypes , 1993 .

[22]  Andrei G. Jablokow,et al.  Carbon cost of root systems: an architectural approach , 1994 .

[23]  D. Eissenstat.  6 – Trade-offs in Root Form and Function , 1997 .

[24]  D. Eissenstat,et al.  Responses of citrus fine roots to localized soil drying: a comparison of seedlings with adult fruiting trees. , 1998, Tree physiology.

[25]  S. A. Barber,et al.  Soil Nutrient Bioavailability: A Mechanistic Approach , 1984 .

[26]  D. Lungley,et al.  The growth of root systems — A numerical computer simulation model , 1973, Plant and Soil.

[27]  J. Hopmans,et al.  Transient three-dimensional modeling of soil water and solute transport with simultaneous root growth, root water and nutrient uptake , 1998, Plant and Soil.

[28]  A. Oyanagi,et al.  Varietal Differences in Geotropic Response of Primary Seminal Root in Japanese Wheat , 1991 .

[29]  C. Gourley,et al.  Plant nutrient efficiency: A comparison of definitions and suggested improvement , 2004, Plant and Soil.

[30]  Alastair H. Fitter,et al.  Architectural analysis of plant root systems , 1992 .

[31]  J. Lynch,et al.  An automated greenhouse sand culture system suitable for studies of P nutrition , 1990 .

[32]  M. Evans,et al.  Gravitropism: interaction of sensitivity modulation and effector redistribution. , 1991, Plant physiology.

[33]  L. Pagès,et al.  A simulation model of the three-dimensional architecture of the maize root system , 1989, Plant and Soil.

[34]  K. L. Nielsen,et al.  Effects of phosphorus availability and vesicular–arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris) , 1998 .

[35]  J. Lynch,et al.  Adaptation of beans (Phaseolus vulgaris L.) to low phosphorus availability , 1995 .

[36]  Robert D. Davis,et al.  SimRoot: Modelling and visualization of root systems , 2004, Plant and Soil.

[37]  J. Hopmans,et al.  Simultaneous modeling of transient three-dimensional root growth and soil water flow , 1994, Plant and Soil.