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A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching

Abstract

Strigolactones were originally identified as stimulators of the germination of root-parasitic weeds1 that pose a serious threat to resource-limited agriculture2. They are mostly exuded from roots and function as signalling compounds in the initiation of arbuscular mycorrhizae3, which are plant–fungus symbionts with a global effect on carbon and phosphate cycling4. Recently, strigolactones were established to be phytohormones that regulate plant shoot architecture by inhibiting the outgrowth of axillary buds5,6. Despite their importance, it is not known how strigolactones are transported. ATP-binding cassette (ABC) transporters, however, are known to have functions in phytohormone translocation7,8,9. Here we show that the Petunia hybrida ABC transporter PDR1 has a key role in regulating the development of arbuscular mycorrhizae and axillary branches, by functioning as a cellular strigolactone exporter. P. hybrida pdr1 mutants are defective in strigolactone exudation from their roots, resulting in reduced symbiotic interactions. Above ground, pdr1 mutants have an enhanced branching phenotype, which is indicative of impaired strigolactone allocation. Overexpression of Petunia axillaris PDR1 in Arabidopsis thaliana results in increased tolerance to high concentrations of a synthetic strigolactone, consistent with increased export of strigolactones from the roots. PDR1 is the first known component in strigolactone transport, providing new opportunities for investigating and manipulating strigolactone-dependent processes.

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Figure 1: Below-ground PDR1 expression and PDR1 localization.
Figure 2: Below-ground pdr1 phenotypes.
Figure 3: Orobanchol content and PDR1-dependent GR24 tolerance and transport.
Figure 4: Above-ground PDR1 expression and pdr1 -related branching phenotypes.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Sequences for P. hybrida PDR1, a 1.8-kb element upstream of PDR1 and the P. axillaris orthologue of PDR1 have been deposited in the GenBank database under accession numbers JQ292813, JQ292814 and JQ292812.

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Acknowledgements

We kindly thank the following: C. Gübeli for technical assistance; and T. Gerats, S. Hörtensteiner, A. Osbourne, P. Schläpfer and C. Beveridge for comments. This study was funded by the Swiss National Foundation within the NCCR-Plant Survival (project ‘ABC transporters involved in signaling’) and by The Netherlands Organization for Scientific Research (NWO; VICI grant 865.06.002 and Equipment grant 834.08.001to H.J.B.). H.J.B. was co-financed by the Centre for BioSystems Genomics (CBSG).

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Contributions

T.K. wrote the manuscript, designed the project and carried out most of the experiments. W.K. and R.B. carried out the P. hybrida strigolactone analysis and the P. ramosa biossays. J.S. performed the quantitative PCR with reverse transcription assays and the transport assays. J.S. and M.S. performed branching and GUS trials. L.B. analysed the PDR1-OE lines. J.B.B. sectioned material. D.R. investigated arbuscular mycorrhizal morphology. H.J.B. supervised the analytical part of the project. E.M. conceived and supervised the project. D.R., E.M., J.S., W.K. and H.J.B. assisted in editing the manuscript.

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Correspondence to Tobias Kretzschmar.

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The authors declare no competing financial interests.

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Kretzschmar, T., Kohlen, W., Sasse, J. et al. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483, 341–344 (2012). https://doi.org/10.1038/nature10873

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