Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: A modeling approach

Zhong Ma, Thomas C. Walk, Andrew Marcus, Jonathan P. Lynch

Research output: Contribution to journalArticle

74 Citations (Scopus)

Abstract

Low phosphorus availability regulates root hair growth in Arabidopsis by (1) increasing root hair length, (2) increasing root hair density, (3) decreasing the distance between the root tip and the point at which root hairs begin to emerge, and (4) increasing the number of epidermal cell files that bear hairs (trichoblasts). The coordinated regulation of these traits by phosphorus availability prompted us to speculate that they are synergistic, that is, that they have greater adaptive value in combination than they do in isolation. In this study, we explored this concept using a geometric model to evaluate the effect of varying root hair length (short, medium, and long), density (0, 24, 48, 72, 96, and 120 root hairs per mm of root length), tip to first root hair distance (0.5, 1, 2, and 4 mm), and number of trichoblast files (8 vs. 12) on phosphorus acquisition efficiency (PAE) in Arabidopsis. SimRoot, a dynamic threedimensional geometric model of root growth and architecture, was used to simulate the growth of Arabidopsis roots with contrasting root hair parameters at three values of phosphorus diffusion coefficient (De=1 × 10-7, 1 × 10-8, and 1 × 10-9 cm2 s-1) over time (20, 40, and 60 h). Depzone, a program that dynamically models nutrient diffusion to roots, was employed to estimate PAE and competition among root hairs. As De decreased from 1 × 10-7 to 1 × 10-9 cm2 s-1, roots with longer root hairs and higher root hair densities had greater PAE than those with shorter and less dense root hairs. At De=1 × 10-9 cm2 s-1, the PAE of root hairs at any given density was in the order of long hairs > medium length hairs > short hairs, and the maximum PAE occurred at density = 96 hairs mm-1 for both long and medium length hairs. This was due to greater competition among root hairs when they were short and dense. Competition over time decreased differences in PAE due to density, but the effect of length was maintained, as there was less competition among long hairs than short hairs. At high De(1 × 10-7 cm2 s-1), competition among root hairs was greatest among long hairs and lowest among short hairs, and competition increased with increasing root hair densities. This led to a decrease in PAE as root hair length and density increased. PAE was also affected by the tip to first root hair distance. At low De values, decreasing tip to first root hair distance increased PAE of long hairs more than that of short hairs, whereas at high De values, decreasing tip to first root hair distance increased PAE of root hairs at low density but decreased PAE of long hairs at very high density. Our models confirmed the benefits of increasing root hair density by increasing the number of trichoblast files rather than decreasing the trichoblast length. The combined effects of all four root hair traits on phosphorus acquisition was 371% greater than their additive effects, demonstrating substantial morphological synergy. In conclusion, our data support the hypothesis that the responses of root hairs to low phosphorus availability are synergistic, which may account for their coordinated regulation.

Original languageEnglish (US)
Pages (from-to)221-235
Number of pages15
JournalPlant and Soil
Volume236
Issue number2
DOIs
StatePublished - Dec 1 2001
Externally publishedYes

Fingerprint

synergism
root hairs
hair
Arabidopsis thaliana
phosphorus
geometry
trichomes
modeling
root competition
Arabidopsis

Keywords

  • Arabidopsis thaliana
  • Competition
  • Modeling
  • Phosphorus acquisition efficiency
  • Root hair density
  • Root hair length

ASJC Scopus subject areas

  • Soil Science
  • Plant Science

Cite this

Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana : A modeling approach. / Ma, Zhong; Walk, Thomas C.; Marcus, Andrew; Lynch, Jonathan P.

In: Plant and Soil, Vol. 236, No. 2, 01.12.2001, p. 221-235.

Research output: Contribution to journalArticle

@article{96cb622a1d194f4d891b8cb585fd7231,
title = "Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: A modeling approach",
abstract = "Low phosphorus availability regulates root hair growth in Arabidopsis by (1) increasing root hair length, (2) increasing root hair density, (3) decreasing the distance between the root tip and the point at which root hairs begin to emerge, and (4) increasing the number of epidermal cell files that bear hairs (trichoblasts). The coordinated regulation of these traits by phosphorus availability prompted us to speculate that they are synergistic, that is, that they have greater adaptive value in combination than they do in isolation. In this study, we explored this concept using a geometric model to evaluate the effect of varying root hair length (short, medium, and long), density (0, 24, 48, 72, 96, and 120 root hairs per mm of root length), tip to first root hair distance (0.5, 1, 2, and 4 mm), and number of trichoblast files (8 vs. 12) on phosphorus acquisition efficiency (PAE) in Arabidopsis. SimRoot, a dynamic threedimensional geometric model of root growth and architecture, was used to simulate the growth of Arabidopsis roots with contrasting root hair parameters at three values of phosphorus diffusion coefficient (De=1 × 10-7, 1 × 10-8, and 1 × 10-9 cm2 s-1) over time (20, 40, and 60 h). Depzone, a program that dynamically models nutrient diffusion to roots, was employed to estimate PAE and competition among root hairs. As De decreased from 1 × 10-7 to 1 × 10-9 cm2 s-1, roots with longer root hairs and higher root hair densities had greater PAE than those with shorter and less dense root hairs. At De=1 × 10-9 cm2 s-1, the PAE of root hairs at any given density was in the order of long hairs > medium length hairs > short hairs, and the maximum PAE occurred at density = 96 hairs mm-1 for both long and medium length hairs. This was due to greater competition among root hairs when they were short and dense. Competition over time decreased differences in PAE due to density, but the effect of length was maintained, as there was less competition among long hairs than short hairs. At high De(1 × 10-7 cm2 s-1), competition among root hairs was greatest among long hairs and lowest among short hairs, and competition increased with increasing root hair densities. This led to a decrease in PAE as root hair length and density increased. PAE was also affected by the tip to first root hair distance. At low De values, decreasing tip to first root hair distance increased PAE of long hairs more than that of short hairs, whereas at high De values, decreasing tip to first root hair distance increased PAE of root hairs at low density but decreased PAE of long hairs at very high density. Our models confirmed the benefits of increasing root hair density by increasing the number of trichoblast files rather than decreasing the trichoblast length. The combined effects of all four root hair traits on phosphorus acquisition was 371{\%} greater than their additive effects, demonstrating substantial morphological synergy. In conclusion, our data support the hypothesis that the responses of root hairs to low phosphorus availability are synergistic, which may account for their coordinated regulation.",
keywords = "Arabidopsis thaliana, Competition, Modeling, Phosphorus acquisition efficiency, Root hair density, Root hair length",
author = "Zhong Ma and Walk, {Thomas C.} and Andrew Marcus and Lynch, {Jonathan P.}",
year = "2001",
month = "12",
day = "1",
doi = "10.1023/A:1012728819326",
language = "English (US)",
volume = "236",
pages = "221--235",
journal = "Plant and Soil",
issn = "0032-079X",
publisher = "Springer Netherlands",
number = "2",

}

TY - JOUR

T1 - Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana

T2 - A modeling approach

AU - Ma, Zhong

AU - Walk, Thomas C.

AU - Marcus, Andrew

AU - Lynch, Jonathan P.

PY - 2001/12/1

Y1 - 2001/12/1

N2 - Low phosphorus availability regulates root hair growth in Arabidopsis by (1) increasing root hair length, (2) increasing root hair density, (3) decreasing the distance between the root tip and the point at which root hairs begin to emerge, and (4) increasing the number of epidermal cell files that bear hairs (trichoblasts). The coordinated regulation of these traits by phosphorus availability prompted us to speculate that they are synergistic, that is, that they have greater adaptive value in combination than they do in isolation. In this study, we explored this concept using a geometric model to evaluate the effect of varying root hair length (short, medium, and long), density (0, 24, 48, 72, 96, and 120 root hairs per mm of root length), tip to first root hair distance (0.5, 1, 2, and 4 mm), and number of trichoblast files (8 vs. 12) on phosphorus acquisition efficiency (PAE) in Arabidopsis. SimRoot, a dynamic threedimensional geometric model of root growth and architecture, was used to simulate the growth of Arabidopsis roots with contrasting root hair parameters at three values of phosphorus diffusion coefficient (De=1 × 10-7, 1 × 10-8, and 1 × 10-9 cm2 s-1) over time (20, 40, and 60 h). Depzone, a program that dynamically models nutrient diffusion to roots, was employed to estimate PAE and competition among root hairs. As De decreased from 1 × 10-7 to 1 × 10-9 cm2 s-1, roots with longer root hairs and higher root hair densities had greater PAE than those with shorter and less dense root hairs. At De=1 × 10-9 cm2 s-1, the PAE of root hairs at any given density was in the order of long hairs > medium length hairs > short hairs, and the maximum PAE occurred at density = 96 hairs mm-1 for both long and medium length hairs. This was due to greater competition among root hairs when they were short and dense. Competition over time decreased differences in PAE due to density, but the effect of length was maintained, as there was less competition among long hairs than short hairs. At high De(1 × 10-7 cm2 s-1), competition among root hairs was greatest among long hairs and lowest among short hairs, and competition increased with increasing root hair densities. This led to a decrease in PAE as root hair length and density increased. PAE was also affected by the tip to first root hair distance. At low De values, decreasing tip to first root hair distance increased PAE of long hairs more than that of short hairs, whereas at high De values, decreasing tip to first root hair distance increased PAE of root hairs at low density but decreased PAE of long hairs at very high density. Our models confirmed the benefits of increasing root hair density by increasing the number of trichoblast files rather than decreasing the trichoblast length. The combined effects of all four root hair traits on phosphorus acquisition was 371% greater than their additive effects, demonstrating substantial morphological synergy. In conclusion, our data support the hypothesis that the responses of root hairs to low phosphorus availability are synergistic, which may account for their coordinated regulation.

AB - Low phosphorus availability regulates root hair growth in Arabidopsis by (1) increasing root hair length, (2) increasing root hair density, (3) decreasing the distance between the root tip and the point at which root hairs begin to emerge, and (4) increasing the number of epidermal cell files that bear hairs (trichoblasts). The coordinated regulation of these traits by phosphorus availability prompted us to speculate that they are synergistic, that is, that they have greater adaptive value in combination than they do in isolation. In this study, we explored this concept using a geometric model to evaluate the effect of varying root hair length (short, medium, and long), density (0, 24, 48, 72, 96, and 120 root hairs per mm of root length), tip to first root hair distance (0.5, 1, 2, and 4 mm), and number of trichoblast files (8 vs. 12) on phosphorus acquisition efficiency (PAE) in Arabidopsis. SimRoot, a dynamic threedimensional geometric model of root growth and architecture, was used to simulate the growth of Arabidopsis roots with contrasting root hair parameters at three values of phosphorus diffusion coefficient (De=1 × 10-7, 1 × 10-8, and 1 × 10-9 cm2 s-1) over time (20, 40, and 60 h). Depzone, a program that dynamically models nutrient diffusion to roots, was employed to estimate PAE and competition among root hairs. As De decreased from 1 × 10-7 to 1 × 10-9 cm2 s-1, roots with longer root hairs and higher root hair densities had greater PAE than those with shorter and less dense root hairs. At De=1 × 10-9 cm2 s-1, the PAE of root hairs at any given density was in the order of long hairs > medium length hairs > short hairs, and the maximum PAE occurred at density = 96 hairs mm-1 for both long and medium length hairs. This was due to greater competition among root hairs when they were short and dense. Competition over time decreased differences in PAE due to density, but the effect of length was maintained, as there was less competition among long hairs than short hairs. At high De(1 × 10-7 cm2 s-1), competition among root hairs was greatest among long hairs and lowest among short hairs, and competition increased with increasing root hair densities. This led to a decrease in PAE as root hair length and density increased. PAE was also affected by the tip to first root hair distance. At low De values, decreasing tip to first root hair distance increased PAE of long hairs more than that of short hairs, whereas at high De values, decreasing tip to first root hair distance increased PAE of root hairs at low density but decreased PAE of long hairs at very high density. Our models confirmed the benefits of increasing root hair density by increasing the number of trichoblast files rather than decreasing the trichoblast length. The combined effects of all four root hair traits on phosphorus acquisition was 371% greater than their additive effects, demonstrating substantial morphological synergy. In conclusion, our data support the hypothesis that the responses of root hairs to low phosphorus availability are synergistic, which may account for their coordinated regulation.

KW - Arabidopsis thaliana

KW - Competition

KW - Modeling

KW - Phosphorus acquisition efficiency

KW - Root hair density

KW - Root hair length

UR - http://www.scopus.com/inward/record.url?scp=0035664364&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0035664364&partnerID=8YFLogxK

U2 - 10.1023/A:1012728819326

DO - 10.1023/A:1012728819326

M3 - Article

AN - SCOPUS:0035664364

VL - 236

SP - 221

EP - 235

JO - Plant and Soil

JF - Plant and Soil

SN - 0032-079X

IS - 2

ER -