Regulation of Root Elongation under Phosphorus Stress Involves Changes in Ethylene Responsiveness1

We characterized the growth of the primary root of Arabidopsis under phosphorus sufficiency (1 mm phosphate) and deficiency (1 μm phosphate), focusing on the role of ethylene. We quantified the spatial profile of relative elongation with a novel method based on image processing, as well as the production rates of cortical cells, trichoblasts, and atrichoblasts. Phosphorus deficiency moderately decreased the maximal rate of relative elongation, shortened the growth zone, and decreased the production rate of both epidermal cell types but not of cortical cells. Inhibiting ethylene production (with aminoethoxyvinyl-glycine) or action (with 1-methylcyclopropene) increased elongation in high phosphorus and decreased it in low phosphorus. That these effects were specific to ethylene was confirmed by negating the effect of inhibited ethylene production with simultaneous treatment with an ethylene precursor (1-aminocyclopropane-1-carboxylic acid). Under both phosphorus regimes, ethylene regulated the maximal rate of relative elongation rather than the size of the growth zone. In addition, inhibiting ethylene action in high versus low phosphorus elicited opposite responses for the position of root hair initiation and for the production rates of cortex cells and atrichoblasts. We conclude that the root system acclimates to phosphorus deficiency by changing the signal transduction pathway connecting ethylene levels to growth and division.

[1]  Kristian Borch,et al.  Ethylene: a regulator of root architectural responses to soil phosphorus availability , 1999 .

[2]  Luis Herrera-Estrella,et al.  Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System1 , 2002, Plant Physiology.

[3]  M. Serek,et al.  Effect of 1-methylcyclopropene and methylenecyclopropane on ethylene binding and ethylene action on cut carnations , 1996, Plant Growth Regulation.

[4]  H. Leyser,et al.  Phosphate availability regulates root system architecture in Arabidopsis. , 2001, Plant physiology.

[5]  P. Nye,et al.  Diffusion of phosphate to plant roots in soil , 1976, Plant and Soil.

[6]  J. Lynch,et al.  Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). , 2000, American journal of botany.

[7]  R. E. Sharp,et al.  Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. , 2000, Journal of experimental botany.

[8]  T. Baskin,et al.  Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. , 1998, Plant physiology.

[9]  J. Lynch,et al.  Regulation of root hair density by phosphorus availability in Arabidopsis thaliana , 2001 .

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

[11]  J. Lynch,et al.  The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. , 2000, American journal of botany.

[12]  M. Evans,et al.  Specialized Zones of Development in Roots , 1995, Plant physiology.

[13]  J. Lynch,et al.  Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: A modeling approach , 2001, Plant and Soil.

[14]  R. E. Sharp,et al.  Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. , 2000, Plant physiology.

[15]  J. H. Manwaring,et al.  Temporal dynamics of soil spatial heterogeneity in sagebrush-wheatgrass steppe during a growing season , 1996, Plant and Soil.

[16]  P. Nye,et al.  Diffusion of phosphate to plant roots in soil , 1974, Plant and Soil.

[17]  P. Green.  Growth and Cell Pattern Formation on an Axis: Critique of Concepts, Terminology, and Modes of Study , 1976, Botanical Gazette.

[18]  J. Schiefelbein,et al.  The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process , 1994, Plant physiology.

[19]  R. E. Sharp,et al.  Growth of the maize primary root at low water potentials : I. Spatial distribution of expansive growth. , 1988, Plant physiology.

[20]  F. Tardieu,et al.  Spatial distributions of tissue expansion and cell division rates are related to irradiance and to sugar content in the growing zone of maize roots , 1998 .

[21]  M. Drew,et al.  Enhanced Sensitivity to Ethylene in Nitrogen- or Phosphate-Starved Roots of Zea mays L. during Aerenchyma Formation. , 1992, Plant physiology.

[22]  T. Baskin,et al.  The impact of mannose and other carbon sources on the elongation and diameter of the primary root of Arabidopsis thaliana , 2001 .

[23]  L. Dolan,et al.  Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. , 1995, The Plant journal : for cell and molecular biology.

[24]  B. Jähne,et al.  Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis , 1998 .

[25]  S. R. Olsen,et al.  Test of an Ascorbic Acid Method for Determining Phosphorus in Water and NaHCO3 Extracts from Soil , 1965 .

[26]  Jack L. Mullen,et al.  Analysis of changes in relative elemental growth rate patterns in the elongation zone of Arabidopsis roots upon gravistimulation , 1998, Planta.

[27]  J. Lynch,et al.  Topsoil foraging – an architectural adaptation of plants to low phosphorus availability , 2001, Plant and Soil.

[28]  W. R. Jordan,et al.  Ethylene Evolution from Maize (Zea mays L.) Seedling Roots and Shoots in Response to Mechanical Impedance. , 1991, Plant physiology.

[29]  J. Lynch,et al.  Ethylene and plant responses to nutritional stress , 1997 .

[30]  Pattern in the Root Epidermis: An Interplay of Diffusible Signals and Cellular Geometry , 1996 .

[31]  M. Evans,et al.  Cellular specifiCity of the gravitropic motor response in roots , 1997, Planta.

[32]  D. G. Lewis,et al.  Phosphate diffusion in soil and uptake by plants , 1967, Plant and Soil.

[33]  M. Evans,et al.  The Role of the Distal Elongation Zone in the Response of Maize Roots to Auxin and Gravity , 1993, Plant physiology.

[34]  N. E. Nielsen,et al.  Variation in root hairs of barley cultivars doubled soil phosphorus uptake , 1997, Euphytica.

[35]  J. Lynch,et al.  Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability , 1996 .