Plant and Soil

, Volume 353, Issue 1–2, pp 231–247 | Cite as

Rare earth elements lanthanum and gadolinium induce phosphate-deficiency responses in Arabidopsis thaliana seedlings

  • León F. Ruíz-Herrera
  • Lenin Sánchez-Calderón
  • Luis Herrera-Estrella
  • José López-Bucio
Regular Article
First Online:
Received:
Accepted:

Abstract

Aims

The aim of this work was to investigate the effects of rare earth elements lanthanum (La3+) and gadolinium (Gd3+) on root system architecture and interactions with low phosphate signaling in Arabidopsis thaliana.

Methods

Detailed analysis of root system architecture was performed in Arabidopsis WT seedlings and in low phosphorus insensitive mutants lpi1-3 and lpr1-1 lpr2-1 in response to REEs. Expression studies of P-deficiency regulated phosphate transporters AtPT1, AtPT2 and AtMGD2 were also conducted. The role of auxin as a mediator of root morphogenetic changes by Gd3+ was evaluated by using the auxin-inducible marker gene DR5:uidA and auxin-signaling mutants tir1, tir1 afb2 afb3, arf7, arf19 and arf7 arf19.

Results

We found that increasing concentrations of REEs inhibited primary root growth and increased root hair and lateral root development in WT seedlings. These effects were reduced in low phosphorus insensitive mutants lpi1-3 and lpr1-1 lpr2-1. Gd3+ activated the expression of AtPT1, AtPT2 and AtMGD2 markers. Lateral root formation by Gd3+ decreased in tir1 afb2 afb3 and arf7 arf19 mutants.

Conclusions

Our results suggest that REEs affect RSA in Arabidopsis by inducing low-P adaptive responses by creating P deficiency conditions in the growth medium by precipitating phosphate.

Keywords

Lanthanum Gadolinium Phosphate deficiency Arabidopsis thaliana Auxin mutants 

Abbreviations

ABA

Abscisic acid

AR

Adventitious root

IAA

Indole-3-acetic acid

LR

Lateral roots

LRD

Lateral root density

P

Phosphorus

PLD

Phospholipase D

PRL

Primary root length

RAM

Root apical meristem

RSA

Root system architecture

REEs

Rare earth elements

ROS

Reactive oxygen species

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Notes

Acknowledgments

This work was supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, grant no. 43978) and the Consejo de la Investigación Científica (UMSNH, México, grant no. CIC 2.26). We thank Drs Peter Doerner, Tom Guilfoyle, Mark A. Estelle, Thierry Desnos and Hiroyuki Ohta for kindly providing us with Arabidopsis transgenic and mutant seeds.

Supplementary material

11104_2011_1026_Fig1_ESM.gif (165 kb)
Supplementary Fig. 1

Effects of Gd3+ on Arabidopsis root system architecture. Arabidopsis WT (Col-0) seedlings were grown for 12 days in medium supplemented with the solvent (left plate) or with 200 μM GdCl3 (right plate). Microscope photographs (b) of root tips from seedlings supplemented with increasing concentrations of Gd3+. Photographs in (a) are representative of 9 independent plates analyzed (GIF 165 kb)

11104_2011_1026_Fig1_ESM.tif (8.6 mb)
High resolution image file (TIF 8.62 mb)
11104_2011_1026_Fig2_ESM.gif (166 kb)
Supplementary Fig. 2

Effects of Gd3+ on Arabidopsis root system architecture in WT and low phosphate resistant mutants. Arabidopsis WT (Col-0) seedlings and lpi1-3 and lpr1-1 lpr2-1 mutants were grown for 12 days in medium supplemented with the solvent (upper plates) or with 150 μM GdCl3 (lower plates). Photographs are representative of 9 independent plates analyzed. The experiment was repeated three times with similar results (GIF 166 kb)

11104_2011_1026_Fig2_ESM.tif (8.8 mb)
High resolution image file (TIF 8.76 mb)
11104_2011_1026_Fig3_ESM.gif (185 kb)
Supplementary Fig. 3

Effect of Gd3+ on AtMGD2::GUS expression. GUS staining was performed overnight in WT plants grown for 12 days in medium with solvent (controls) or with two increasing concentrations of GdCl3 (120 and 150 μM). Gd3+ induced expression of AtMGD2 in leaves (f and k), cotyledons (g and l), shoot meristem (h and m), lateral roots (i and n), but not in the root meristem (j and o), despite the clear effect of gadolinium in this zone. Photographs are representative of 20 stained plants (GIF 184 kb)

11104_2011_1026_Fig3_ESM.tif (9.7 mb)
High resolution image file (TIF 9.68 mb)
11104_2011_1026_Fig4_ESM.gif (136 kb)
Supplementary Fig. 4

Effect of phosphate in root tip structure of WT and low phosphate resistant mutants treated with Gd3+. WT and mutant seedlings lpi1-3 and lpr1-1 lpr2-1 were grown side by side for 12 days on medium with different P treatments supplied or not with Gd3+ and the primary root tip photographed. Notice that a 4 mM P treatment completely reverts the effect of Gd3+ on differentiation in root tips (GIF 135 kb)

11104_2011_1026_Fig4_ESM.tif (8 mb)
High resolution image file (TIF 8.01 mb)
11104_2011_1026_Fig5_ESM.gif (125 kb)
Supplementary Fig. 5

Effect of La3+ on AtPT2:GUS expression. AtPT2:GUS expressing seedlings were grown for 12 days in medium supplied with DMSO (Control) or with the indicated LaCl3 concentrations. Photographs are representative of 20 stained plants. Arrow in 300 μM LaCl3 treatment indicates the primary root. The experiment was repeated three times with similar results (GIF 124 kb)

11104_2011_1026_Fig5_ESM.tif (7.2 mb)
High resolution image file (TIF 7.15 mb)

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Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • León F. Ruíz-Herrera
    • 1
  • Lenin Sánchez-Calderón
    • 2
  • Luis Herrera-Estrella
    • 2
  • José López-Bucio
    • 1
  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMexico
  2. 2.Laboratorio Nacional de Genómica para la Biodiversidad, CINVESTAV IrapuatoIrapuatoMexico

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