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Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis

Abstract

The plant hormone gibberellin (GA) regulates multiple developmental processes. It accumulates in the root elongating endodermis, but how it moves into this cell file and the significance of this accumulation are unclear. Here we identify three NITRATE TRANSPORTER1/PEPTIDE TRANSPORTER (NPF) transporters required for GA and abscisic acid (ABA) translocation. We demonstrate that NPF2.14 is a subcellular GA/ABA transporter, presumably the first to be identified in plants, facilitating GA and ABA accumulation in the root endodermis to regulate suberization. Further, NPF2.12 and NPF2.13, closely related proteins, are plasma membrane-localized GA and ABA importers that facilitate shoot-to-root GA12 translocation, regulating endodermal hormone accumulation. This work reveals that GA is required for root suberization and that GA and ABA can act non-antagonistically. We demonstrate how the clade of transporters mediates hormone flow with cell-file-specific vacuolar storage at the phloem unloading zone, and slow release of hormone to induce suberin formation in the maturation zone.

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Fig. 1: NPF2.14 is a vacuolar GA and ABA transporter.
Fig. 2: NPF2.14 expression in differentiated pericycle is required for endodermal root suberization.
Fig. 3: NPF2.12 and NPF2.13 are plasma membrane-localized GA and ABA importers that facilitate endodermal hormone accumulation.
Fig. 4: NPF2.12 and NPF2.13 regulate root endodermis suberization.
Fig. 5: NPF2.12 and NPF2.13 facilitate long-distance shoot-to-root GA transport.
Fig. 6: NPF transporters mediate pericycle-specific hormone uptake into the vacuoles at the phloem unloading zone to facilitate a hormone slow-release mechanism that allows suberization at the maturation zone.
Fig. 7: Proposed model illustrating that NPF2.12, NPF2.13, NPF2.14 and NPF3.1 function in regulating endodermal suberin formation.

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Data availability

All the data supporting the findings of this study are available within the Article and its Supplementary Information. Source data are provided with this paper. The python code used to produce the model results is available at: https://gitlab.com/leahband/ga_aba_transport_rootcrosssection_model.

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Acknowledgements

We thank D. Binenbaum for the illustrations and P. Hedden (Rothamsted Research) for sharing pGA3ox1-4:GUS seeds. This work was supported by grants from the Israel Science Foundation (2378/19 and 3419/20 to E.S.), the Human Frontier Science Program (HFSP—RGY0075/2015 and HFSP—LIY000540/2020 to E.S., H.H.N.-E. and L.R.B.), Danmarks Grundforskningsfond (DNRF99 to H.H.N.-E.), the European Research Council (757683-RobustHormoneTrans to E.S.), the Constantiner Travel Fellowship (to J.B.), the Centre National de la Recherche Scientifique (to L.S-A. J-M.D. and P.A.) and the French Ministry of Research and Higher Education studentship (to L.C.).

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Contributions

J.B. performed the research and wrote the manuscript. N.W. performed the oocyte transporter assays. L.C., L.S-A., J-M.D. and P.A. carried out long-distance transport assays. K.K. performed the mathematical modelling. I.T. assisted in cloning overexpression and reporter lines. H.V. and A.A. quantified root GA and ABA content. M.A. helped with genotyping T-DNA mutant lines and profiling suberin patterning. Y.Z. helped with npf mutant identification. D.R. and L.R. assisted in cross-sectioning and staining. E.C. quantified hormone content in the phloem sap. E.M. and H.C. performed suberin monomer quantifications. S.L. and R.W. synthesized fluorescently tagged hormones. S.B.Y. carried out the qPCR and created hormone-treated reporter lines. V.N. and C.C. helped with nitrate and hormone quantification in oocyte assays, respectively. C.H. carried out hormone competition transport assays. L.R.B., P.A., H.H.N.-E. and ES designed and supervised the work and edited the manuscript. All authors discussed the results and commented on the manuscript.

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Correspondence to Leah R. Band, Patrick Achard, Hussam Hassan Nour-Eldin or Eilon Shani.

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Binenbaum, J., Wulff, N., Camut, L. et al. Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis. Nat. Plants 9, 785–802 (2023). https://doi.org/10.1038/s41477-023-01391-3

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