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Root tip contact with low-phosphate media reprograms plant root architecture

Nature Genetics volume 39, pages 792–796 (2007)Cite this article

Abstract

Plant roots are able to sense soil nutrient availability. In order to acquire heterogeneously distributed water and minerals1,2,3, they optimize their root architecture. One poorly understood plant response to soil phosphate (Pi) deficiency is a reduction in primary root growth with an increase in the number and length of lateral roots4,5,6,7,8,9,10,11,12. Here we show that physical contact of the Arabidopsis thaliana primary root tip with low-Pi medium is necessary and sufficient to arrest root growth. We further show that loss-of-function mutations in Low Phosphate Root1 (LPR1) and its close paralog LPR2 strongly reduce this inhibition. LPR1 was previously mapped as a major quantitative trait locus (QTL)12; the molecular origin of this QTL is explained by the differential allelic expression of LPR1 in the root cap. These results provide strong evidence for the involvement of the root cap in sensing nutrient deficiency, responding to it, or both. LPR1 and LPR2 encode multicopper oxidases (MCOs), highlighting the essential role of MCOs for plant development.

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Figure 1: LPR1 is necessary for root growth inhibition by low Pi.
Figure 2: LPR1 and LPR2 have similar and additive functions.
Figure 3: LPR1 is a multicopper oxidase.
Figure 4: In the root tip, less LPR1Bay0 than LPR1Sha is expressed.
Figure 5: Root growth on low-Pi medium is inhibited through the root tip.

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Protein Data Bank

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Acknowledgements

We gratefully thank the Nottingham Arabidopsis Stock Centre for providing SALK insertion lines; J. Vicente for the γ-ray irradiation; L. Martins (Instituto de Tecnologia Química e Biológica, Oeiras) for the CotA antibody; L. Noël (CEA Cadarache) for the pXCSG-GFP vector; F. Parcy (CNRS, Grenoble) for the pFP100 vector; T. Tron (CNRS, Marseille) for the yeast vectors; N. Leonhardt for helping with QRT-PCR; C. Sallaud for the 96-well DNA extraction protocol; A. Caroff for helping with laser microdissection; C. Sarrobert for her early involvement on Fe studies; the Groupement de Recherches Appliquées en Phytotechnologie team for taking care of plants; J.-L. Montillet for helpful discussions; and M. Crespi, M. Koornneef, G. Kunze, E. Marin-Nussaume, L. Noël and M.-C. Thibaud for critical reading and suggestions on an early version of the manuscript. We thank R. Carol for correcting the English on an early version of the manuscript. S.S. was supported by the French Ministère de la Recherche and by the CEA; C.S.-C., M.R. and L.R. were supported by the CEA.

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Author notes

  1. Sergio Svistoonoff

    Present address: Present address: Equipe Rhizogenese, Unité Mixte de Recherche Diversité et Adaptation des Plantes Cultivées, Institut de Recherche pour le Développement, 911, Avenue Agropolis, 34394 Montpellier Cedex 5, France.,

  2. Matthieu Reymond

    Present address: Present address: Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, D-50829 Cologne, Germany.,

  3. Aline Blanchet

    Present address: Present address: Monsanto, Route de Crest, 26740 Sauzet, France.,

Authors and Affiliations

  1. Département d'Écophysiologie Végétale et de Microbiologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Commissariat à l'Énergie Atomique (CEA), Centre National de la Recherche Scientifique (CNRS), Université Aix-Marseille-II, CEA Cadarache, St. Paul-lez-Durance Cedex, 13108, France

    Sergio Svistoonoff, Audrey Creff, Matthieu Reymond, Cécile Sigoillot-Claude, Lilian Ricaud, Aline Blanchet, Laurent Nussaume & Thierry Desnos

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Contributions

S.S., A.C. and T.D. performed most of the experiments. M.R. contributed to the fine mapping of LPR1 and performed statistical analysis; C.S.-C. performed enzymatic analysis of LPR1; L.R. complemented the 194Bay0 line; A.B. isolated the lpr2 mutants. S.S. and T.D. analyzed the data and wrote the manuscript with input from L.N. T.D. conceived and supervised the project.

Corresponding author

Correspondence to Thierry Desnos.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

pH and Fe affect low Pi–induced Arabidopsis primary root growth inhibition. (PDF 565 kb)

Supplementary Fig. 2

Details of the γ-ray–induced lpr1 mutations. (PDF 257 kb)

Supplementary Fig. 3

Molecular analysis of the lpr mutants. (PDF 701 kb)

Supplementary Fig. 4

Genetic complementation tests between lpr1-1 and 194Bay0 and between lpr1-1 and lpr1-2. (PDF 1946 kb)

Supplementary Fig. 5

Genetic complementation of the 194Bay0 line with the pLPR1Sha:LPR1Bay0 transgene. (PDF 314 kb)

Supplementary Fig. 6

Expression analysis of the LPR1Sha and LPR1Bay0 promoters and of the cyclin B1;1. (PDF 2199 kb)

Supplementary Fig. 7

Root tip contact with low-Pi medium stops root growth. (PDF 896 kb)

Supplementary Table 1

Fine mapping of LPR1. (PDF 871 kb)

Supplementary Table 2

Pi content of seedling roots grown for 10 d on low- or high-Pi medium. (PDF 72 kb)

Supplementary Table 3

List of PCR primers. (PDF 63 kb)

Supplementary Methods (PDF 153 kb)

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Svistoonoff, S., Creff, A., Reymond, M. et al. Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39, 792–796 (2007). https://doi.org/10.1038/ng2041

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