Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis

Jenia Binenbaum; Nikolai Wulff; Lucie Camut; Kristian Kiradjiev; Moran Anfang; Iris Tal; Himabindu Vasuki; Yuqin Zhang; Lali Sakvarelidze-Achard; Jean Michel Davière; Dagmar Ripper; Esther Carrera; Ekaterina Manasherova; Shir Ben Yaakov; Shani Lazary; Chengyao Hua; Vlastimil Novak; Christoph Crocoll; Roy Weinstain; Hagai Cohen; Laura Ragni; Asaph Aharoni; Leah R. Band; Patrick Achard; Hussam Hassan Nour-Eldin; Eilon Shani

doi:10.1038/s41477-023-01391-3

Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis

Jenia Binenbaum, Nikolai Wulff, Lucie Camut, Kristian Kiradjiev, Moran Anfang, Iris Tal, Himabindu Vasuki, Yuqin Zhang, Lali Sakvarelidze-Achard, Jean Michel Davière, Dagmar Ripper, Esther Carrera, Ekaterina Manasherova, Shir Ben Yaakov, Shani Lazary, Chengyao Hua, Vlastimil Novak, Christoph Crocoll, Roy Weinstain, Hagai CohenLaura Ragni, Asaph Aharoni, Leah R. Band, Patrick Achard, Hussam Hassan Nour-Eldin, Eilon Shani^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

13 Citationer (Scopus)

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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.

Originalsprog	Engelsk
Tidsskrift	Nature Plants
Vol/bind	9
Udgave nummer	5
Sider (fra-til)	785-802
Antal sider	18
ISSN	2055-026X
DOI	https://doi.org/10.1038/s41477-023-01391-3
Status	Udgivet - 2023

Bibliografisk note

Funding Information:
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.).

Funding Information:
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.).

Publisher Copyright:
© 2023, The Author(s), under exclusive licence to Springer Nature Limited.

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10.1038/s41477-023-01391-3

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Citationsformater

Binenbaum, J., Wulff, N., Camut, L., Kiradjiev, K., Anfang, M., Tal, I., Vasuki, H., Zhang, Y., Sakvarelidze-Achard, L., Davière, J. M., Ripper, D., Carrera, E., Manasherova, E., Ben Yaakov, S., Lazary, S., Hua, C., Novak, V., Crocoll, C., Weinstain, R., ... Shani, E. (2023). Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis. Nature Plants, 9(5), 785-802. https://doi.org/10.1038/s41477-023-01391-3

Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis. / Binenbaum, Jenia; Wulff, Nikolai; Camut, Lucie; Kiradjiev, Kristian; Anfang, Moran; Tal, Iris; Vasuki, Himabindu; Zhang, Yuqin; Sakvarelidze-Achard, Lali; Davière, Jean Michel; Ripper, Dagmar; Carrera, Esther; Manasherova, Ekaterina; Ben Yaakov, Shir; Lazary, Shani; Hua, Chengyao; Novak, Vlastimil; Crocoll, Christoph; Weinstain, Roy; Cohen, Hagai; Ragni, Laura; Aharoni, Asaph; Band, Leah R.; Achard, Patrick; Nour-Eldin, Hussam Hassan; Shani, Eilon.

I: Nature Plants, Bind 9, Nr. 5, 2023, s. 785-802.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Binenbaum, J, Wulff, N, Camut, L, Kiradjiev, K, Anfang, M, Tal, I, Vasuki, H, Zhang, Y, Sakvarelidze-Achard, L, Davière, JM, Ripper, D, Carrera, E, Manasherova, E, Ben Yaakov, S, Lazary, S, Hua, C, Novak, V, Crocoll, C, Weinstain, R, Cohen, H, Ragni, L, Aharoni, A, Band, LR, Achard, P, Nour-Eldin, HH & Shani, E 2023, 'Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis', Nature Plants, bind 9, nr. 5, s. 785-802. https://doi.org/10.1038/s41477-023-01391-3

Binenbaum, Jenia ; Wulff, Nikolai ; Camut, Lucie ; Kiradjiev, Kristian ; Anfang, Moran ; Tal, Iris ; Vasuki, Himabindu ; Zhang, Yuqin ; Sakvarelidze-Achard, Lali ; Davière, Jean Michel ; Ripper, Dagmar ; Carrera, Esther ; Manasherova, Ekaterina ; Ben Yaakov, Shir ; Lazary, Shani ; Hua, Chengyao ; Novak, Vlastimil ; Crocoll, Christoph ; Weinstain, Roy ; Cohen, Hagai ; Ragni, Laura ; Aharoni, Asaph ; Band, Leah R. ; Achard, Patrick ; Nour-Eldin, Hussam Hassan ; Shani, Eilon. / Gibberellin and abscisic acid transporters facilitate endodermal suberin formation in Arabidopsis. I: Nature Plants. 2023 ; Bind 9, Nr. 5. s. 785-802.

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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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AU - Anfang, Moran

AU - Tal, Iris

AU - Vasuki, Himabindu

AU - Zhang, Yuqin

AU - Sakvarelidze-Achard, Lali

AU - Davière, Jean Michel

AU - Ripper, Dagmar

AU - Carrera, Esther

AU - Manasherova, Ekaterina

AU - Ben Yaakov, Shir

AU - Lazary, Shani

AU - Hua, Chengyao

AU - Novak, Vlastimil

AU - Crocoll, Christoph

AU - Weinstain, Roy

AU - Cohen, Hagai

AU - Ragni, Laura

AU - Aharoni, Asaph

AU - Band, Leah R.

AU - Achard, Patrick

AU - Nour-Eldin, Hussam Hassan

AU - Shani, Eilon

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N2 - 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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