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The evolution of the plastid phosphate translocator family

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Abstract

Main conclusion

The plastid phosphate translocators evolved in algae but diversified into several groups, which adopted different physiological functions by extensive gene duplications and losses in Streptophyta.

The plastid phosphate translocators (pPT) are a family of transporters involved in the exchange of metabolites and inorganic phosphate between stroma and cytosol. Based on their substrate specificities, they were divided into four subfamilies named TPT, PPT, GPT and XPT. To analyse the occurrence of these transporters in different algae and land plant species, we identified 652 pPT genes in 101 sequenced genomes for phylogenetic analysis. The first three subfamilies are found in all species and evolved before the split of red and green algae while the XPTs were derived from the duplication of a GPT gene at the base of Streptophyta. The analysis of the intron–exon structures of the pPTs corroborated these findings. While the number and positions of introns are conserved within each subfamily, they differ between the subfamilies suggesting an insertion of the introns shortly after the three subfamilies evolved. During angiosperm evolution, the subfamilies further split into different groups (TPT1-2, PPT1-3, GPT1-6). Angiosperm species differ significantly in the total number of pPTs, with many species having only a few, while several plants, especially crops, have a higher number, pointing to the importance of these transporters for improved source–sink strength and yield. The differences in the number of pPTs can be explained by several small-scale gene duplications and losses in plant families or single species, but also by whole genome duplications, for example, in grasses. This work could be the basis for a comprehensive analysis of the molecular and physiological functions of this important family of transporters.

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Abbreviations

Glc6P:

Glucose-6-phosphate

GPT:

Glucose-6-phosphate/phosphate translocator

MRCA:

Most recent common ancestor

OPPP:

Oxidative pentose phosphate pathway

PEP:

Phosphoenolpyruvate

pPT:

Plastid phosphate translocators

PPT:

Phosphoenolpyruvate/phosphate translocator

TPT:

Triose phosphate/phosphate translocator

WGD:

Whole genome duplication

XPT:

Xylulose-5-phosphate/phosphate translocators

Xul5P:

Xylulose-5-phosphate

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Acknowledgements

We thank Toni I. Gossmann for helpful comments on this manuscript. The computations were performed on resources provided by UNINETT Sigma2—the National Infrastructure for High Performance Computing and Data Storage in Norway.

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  1. Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Biologibygget, Framstredet 39, 9037, Tromsø, Norway

    Mathias Bockwoldt, Ines Heiland & Karsten Fischer

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425_2019_3161_MOESM1_ESM.pdf

Detailed view of the TPT phylogeny in Streptophyta. Subfamilies as mentioned in the text are written in bold. The scale bar shows the evolutionary distance 1 (PDF 949 kb)

425_2019_3161_MOESM2_ESM.pdf

Detailed view of the PPT phylogeny in Streptophyta. Subfamilies as mentioned in the text are written in bold. The scale bar shows the evolutionary distance 2 (PDF 1117 kb)

425_2019_3161_MOESM3_ESM.pdf

Detailed view of the GPT phylogeny in Streptophyta. Subfamilies as mentioned in the text are written in bold. The scale bar shows the evolutionary distance 3 (PDF 1469 kb)

Detailed view of the XPT phylogeny. The scale bar shows the evolutionary distance 4 (PDF 441 kb)

425_2019_3161_MOESM5_ESM.pdf

Multiple sequence alignment of pPT sequences of Viridiplantae with intron positions indicated by blue background 5 (PDF 845 kb)

425_2019_3161_MOESM6_ESM.xlsx

Complete list of protein sequences. Given are the NCBI accessions, the plant species, the pPT subfamilies and groups. A letter is indicating the specific gene, if necessary 6 (XLSX 30 kb)

425_2019_3161_MOESM7_ESM.xlsx

Comprehensive list of the number of pPTs in each species. Proteins which could not be assigned to a particular group are shown with a grey background 7 (XLSX 14 kb)

425_2019_3161_MOESM8_ESM.zip

Python scripts used for determining the intron/exon borders and for visualizing the multiple sequence alignments. The individual scripts and workflows are explained in the readme file 8 (ZIP 17 kb)

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Bockwoldt, M., Heiland, I. & Fischer, K. The evolution of the plastid phosphate translocator family. Planta 250, 245–261 (2019). https://doi.org/10.1007/s00425-019-03161-y

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