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 for this work

Research output: Contribution to journal › Journal article › Research › peer-review

13 Citations (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.

Original language	English
Journal	Nature Plants
Volume	9
Issue number	5
Pages (from-to)	785-802
Number of pages	18
ISSN	2055-026X
DOIs	https://doi.org/10.1038/s41477-023-01391-3
Publication status	Published - 2023

Bibliographical note

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

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Cite this

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.

In: Nature Plants, Vol. 9, No. 5, 2023, p. 785-802.

Research output: Contribution to journal › Journal article › Research › 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, vol. 9, no. 5, pp. 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. In: Nature Plants. 2023 ; Vol. 9, No. 5. pp. 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

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AU - Davière, Jean Michel

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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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