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A phosphate transporter expressed in arbuscule-containing cells in potato

Nature volume 414, pages 462–465 (2001)Cite this article

Abstract

Arbuscular mycorrhizas are the most common non-pathogenic symbioses in the roots of plants. It is generally assumed that this symbiosis facilitated the colonization of land by plants1. In arbuscular mycorrhizas, fungal hyphae often extend between the root cells and tuft-like branched structures (arbuscules) form within the cell lumina that act as the functional interface for nutrient exchange. In the mutualistic arbuscular-mycorrhizal symbiosis the host plant derives mainly phosphorus from the fungus, which in turn benefits from plant-based glucose2. The molecular basis of the establishment and functioning of the arbuscular-mycorrhizal symbiosis is largely not understood. Here we identify the phosphate transporter gene StPT3 in potato (Solanum tuberosum). Functionality of the encoded protein was confirmed by yeast complementation. RNA localization and reporter gene expression indicated expression of StPT3 in root sectors where mycorrhizal structures are formed. A sequence motif in the StPT3 promoter is similar to transposon-like elements, suggesting that the mutualistic symbiosis evolved by genetic rearrangements in the StPT3 promoter.

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Figure 1: Phylogenetic relationship of StPT3 with other Pi transporters.
Figure 2: Complementation of Pi uptake-deficient yeast and kinetics of Pi uptake.
Figure 3: StPT3 transcript abundance in mycorrhizas.
Figure 4: Localization of StPT3 transcripts and reporter gene activity in arbuscule-containing root sectors.

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Acknowledgements

We thank R. Ruh for support with microscopic analysis; B. Regierer and J. Kossmann for the potato genomic library; and T. Mandel and C. Kuhlemeier for the 35S minimal promoter. This work was supported by the Swiss National Science Foundation, and Hoffmann-La Roche, Switzerland.

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Author notes

  1. Nikolaus Amrhein

    Present address: Federal Institute of Technology (ETH) Zurich, Institute of Plant Sciences, Universitätsstrasse 2, Zurich, 8092, Switzerland

  2. Maryse Laloi

    Present address: Nestlé Research Center, Lausanne, PO Box 44, Vers-chez-les-Blanc, 1000, Lausanne, 26, Switzerland

  3. Christine Rausch, Pierre Daram and Georg Leggewie: These authors contributed equally to the work

Authors and Affiliations

  1. Federal Institute of Technology (ETH) Zurich, Institute of Plant Sciences, Experimental Station Eschikon 33, Lindau, 8315, Switzerland

    Christine Rausch, Pierre Daram, Silvia Brunner, Jan Jansa & Marcel Bucher

  2. Max Planck Institute of Plant Molecular Physiology, Potsdam, 14424, Germany

    Georg Leggewie

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Corresponding author

Correspondence to Marcel Bucher.

Supplementary information

StPT3 gene structure and predicted topology of the encoded protein.

Figure A

(GIF 17.2 KB)

a, The structure of the StPT3 gene is presented. The diagram depicts the intron-less open reading frame (open box) which is terminated by a TAA in-frame stop codon and 5’ upstream and 3’ non-translated regions (thin lines). TATA box, putative binding site for HD-ZIP transcription factors, and MRR element are indicated in the 5’ upstream region. Sizes are given in base pairs with 1 indicating the first nucleotide of the intitiation codon ATG. Distances are drawn to scale. b, Predicted topology of the StPT3 polypeptide with encircled numbers specifying the 12 transmembrane domains embedded in the membrane bilayer. Putative sites for posttranslational modifications are indicated with P for phosphorylation and a schematic oligosaccharide moiety for N-linked glycosylation.

Alignment of the deduced amino acid sequence of StPT3 with that of plant Pht1 proteins.

Figure B

(GIF 29.5 KB)

Alignment of the deduced amino acid sequence of StPT3 with the Pht1 transporters from potato and tomato (see Fig. 1). Identical amino acids are shaded in black, similar amino acids are shaded in grey. The membrane spanning domains are underlined in the StPT3 sequence (-). (*) Consensus site for N-linked glycosylation, and (+) sites for phosphorylation conserved in all proteins aligned in Figure 1.

A MITE-like element in the StPT3 promoter region exhibits homology to resistance (R) genes.

Figure C

(GIF 17.5 KB)

a, Sequence of a 431 base pairs MITE-like transposable element in the StPT3 upstream genic region. Shaded regions designate TIRs. The MRR element is underlined. b, alignment of StPT3 MRR element with sequences from solanaceous resistance (R) genes as obtained by a BLAST search. The highly conserved boxes MRR1 and MRR2 are designated by thin lines. Gene or cluster names are followed by GenBank accession numbers: rclust-a and rclust-b from the S. tuberosum resistance gene cluster (AF265664); VFNT-Pto from the L. esculentum VFNT Cherry Pto locus (AF220603); rx from the S. tuberosum rx gene (AJ011801); Pto-a and Pto-b from the L. pimpinellifolium Rio Grande 76R Pto locus (AF220602); Mi-copy2 from the L. esculentum disease resistance gene homologue Mi-copy2 (U81378). c, alignment of MRR1 and MRR2 elements from the genomic regions specified at left. Identities between different elements are listed at the bottom of the different alignments. HCR9-4A and HCR9-9A specify genes from the L. pimpinellifolium Cf-9 resistance gene cluster (AJ002236) or the L. hirsutum Cf-4 resistance gene cluster (AJ002235), respectively.

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Rausch, C., Daram, P., Brunner, S. et al. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414, 462–465 (2001). https://doi.org/10.1038/35106601

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