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Aluminum induces low phosphate adaptive responses and modulates primary and lateral root growth by differentially affecting auxin signaling in Arabidopsis seedlings

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Abstract

Aims

The aims of this work were to investigate the aluminum (Al) and phosphate (P) interactions in the regulation of root system architecture of Arabidopsis thaliana seedlings and the contribution of auxin signaling in primary and lateral root growth in response to Al toxicity.

Methods

Detailed analyses of root system architecture and cell division were performed in Arabidopsis WT seedlings and in low phosphorus insensitive mutants lpi1-3 and lpr1-1 lpr2-1 in response to Al. Expression studies of P-deficiency regulated phosphate transporter AtPT2 were also conducted. The role of auxin as a mediator of root morphogenetic changes by Al was evaluated by using the auxin-signaling mutants tir1, tir1 afb2 afb3, and arf7 arf19.

Results

Al inhibited primary root growth by affecting cell cycle progression and causing differentiation of cells in the root meristem. These effects were reduced in low phosphorus insensitive lpi1-3 and low phosphate resistant lpr1-1 lpr2-1 Arabidopsis mutants. Al also activated the expression of the low phosphate-induced P transporter AtPT2 in roots. Lateral root formation by Al decreased in tir1 afb2 afb3 while arf7 arf19 mutants were highly resistant to Al in both primary root inhibition and lateral root induction.

Conclusions

Our results suggest that lateral root formation in response to Al toxicity and P deficiency may involve common signaling mechanisms, while a pathway involving ARF7 and ARF19 is important for primary root growth inhibition by Al.

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Abbreviations

Al:

Aluminum

LR:

Lateral roots

LRD:

Lateral root density

NPA:

Naphthylphthalamic acid

P:

Phosphorus

Pi:

Phosphate

PRL:

Primary root length

RSA:

Root system architecture

ROS:

Reactive oxygen species

WT:

Wild-type

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Acknowledgments

We thank Drs. Peter Doerner, Tom Guilfoyle, Kaschandra Raghothama, Mark Estelle and Thierry Desnos for kindly providing us with seeds of Arabidopsis transgenic and mutant lines. This work was supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, grants Nos. 43978 and 60999), and Consejo de la Investigación Científica (UMSNH, México, grant no. CIC 2.26).

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Authors and Affiliations

  1. Instituto de Investigaciones Químico-Biológicas, Universidad Michoacana de San Nicolás de Hidalgo, Edificio B3, Ciudad Universitaria, 58030, Morelia, Michoacán, Mexico

    León Francisco Ruíz-Herrera & José López-Bucio

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  1. León Francisco Ruíz-Herrera
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  2. José López-Bucio
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Correspondence to José López-Bucio.

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Responsible Editor: Yong Chao Liang.

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Figure S1

Arabidopsis root system architecture as affected by AlCl3 and low pH. Arabidopsis WT (Col-0), lpi1-3 and lpr1-1 lpr1-2 seedlings were grown for 12 days in medium supplemented with 125 or 150 μM AlCl3 in acidified (a–f) or neutral medium (g–l). Photographs are representative of 9 independent plates analyzed (JPEG 537 kb)

Figure S2

Root architecture in WT and lpi1-3 and lpr1-1 lpr2-1 mutants in response to Al and P. 150 μM AlCl3 (d) and/or a KH2PO4 excess (b) were supplied in the growth medium of plants. Notice that increasing P supply resumes PR growth in Al-treated seedlings (JPEG 686 kb)

Figure S3

Effect of phosphate (d–f) and aluminum (g–i) in primary root meristem in wild type and low phosphate insensitive mutants. A small increase in the concentration of phosphate restores the structure of primary root meristem in Col-0 (j) compared with control (a). Photographs are representative individuals of 45 seedlings (JPEG 633 kb)

Figure S4

Root system architecture development in WT (Col-0) and auxin related Arabidopsis mutants. Seedlings were treated with water (a), 125, 150 and 175 μM AlCl3 (b–c). Notice how double mutant arf7-1 arf19-1 is resistant to all AlCl3 concentrations tested. Photographs in a are representative of 9 independent plates analyzed (JPEG 715 kb)

Figure S5

Root waving and lateral root formation in response to aluminum in WT (Col-0) and arf7-1 arf19-1 double mutants. Note that the arf7-1 arf19-1 double mutant is not only resistant to lateral rot formation but also to primary root waving. Photographs are representative individuals of 45 seedlings (JPEG 412 kb)

Figure S6

Effect of aluminum on pH of the medium and primary root growth (a). Effect of Al on the pH of the media. b Inhibition of the primary root is similar adjusting the pH to 7.0 after addition of Al (black line) or after addition of Al (gray line) (b) in WT plants. Values shown represent the mean ± SD of 45 seedlings analyzed per treatment. Different letters are used to indicated means that differ significantly (P < 0.05) (JPEG 198 kb)

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Ruíz-Herrera, L.F., López-Bucio, J. Aluminum induces low phosphate adaptive responses and modulates primary and lateral root growth by differentially affecting auxin signaling in Arabidopsis seedlings. Plant Soil 371, 593–609 (2013). https://doi.org/10.1007/s11104-013-1722-0

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