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The Glucose-Related Decrease in Polar Auxin Transport During Ripening and its Possible Role in Grapevine Berry Coloring

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Abstract

Auxin is a hormone that delays ripening in part by reducing anthocyanin content and impairing color development. Auxin content declines during the ripening process, whereas sugars accumulate from pre-veraison onwards. The spatio-temporal distribution of this hormone depends in part on polar auxin transport. On the other hand, sugar, acting as a signal molecule, modulates auxin distribution in model organisms; however, its effect on polar auxin transport during the coloring process in grapevine berries has not been investigated. To address this issue, we characterized auxin transport and sugar variations during the ripening process and performed treatments intended to alter auxin homeostasis in grape fruits. We found that polar auxin transport declines in concert with increasing sugar content prior to and at veraison. Moreover, N-1-napthylphthalamic acid (NPA; a polar auxin transport inhibitor) and glucose treatment increased berry coloration, reduced polar auxin transport and VvPIN1 transcript abundance at pre-veraison, and combined NPA and glucose treatment further increased berry color compared to glucose and NPA alone. Indole-3-acetic acid (IAA) treatment prevented the negative effect of glucose on auxin transport, suggesting that auxin homeostasis might be relevant for glucose modulation of berry ripening in grapevine. Impaired auxin transport is associated with increased ethylene sensitivity in several plant processes, including fruit abscission. For exploring a potential involvement of the ethylene pathway during the coloring process, we analyzed the transcript abundance of the putative ethylene receptor, VvETR2, a possible negative regulator of the ethylene pathway. We found that glucose plus NPA treatment reduced VvETR2 transcript abundance, whose expression is reported to decline from veraison onwards. Our results suggest a possible mechanism in which a rise in glucose contributes to auxin transport inhibition in coloring berries. As glucose has been reported to promote ripening and IAA inhibits berry coloring, our results further support an antagonistic switch between IAA and glucose, that could also involve changes in the expression of the VvETR2 gene.

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Abbreviations

NCED:

9-Cis-epoxy-carotenoid dioxygenase

ABA:

Abscisic acid

E-L:

Eichhorn-Lorenz

ETR:

Ethylene receptor

ERS:

Ethylene response sensor

NPA:

N-1-napthylphthalamic acid

PIN:

PIN-FORMED

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Funding

This work was supported by Proyecto Postdoctorado FONDECYT-CONICYT Nº 3150608 and Nº 3150259, ICM-MINECON, Proyecto NC130030, NM BSBSV, and FONDECYT 1150220.

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Author notes

  1. Alejandra Serrano and Nathalie Kuhn contributed equally to this work.

Authors and Affiliations

  1. Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Av. Libertador Bernardo O´Higgins 340, 8331150, Santiago, Chile

    Alejandra Serrano, Franko Restovic, Carlos Meyer-Regueiro & Patricio Arce-Johnson

  2. Facultad de Ciencias Agronómicas y de los Alimentos, Pontificia Universidad Católica de Valparaíso, 2340025, Valparaíso, Chile

    Nathalie Kuhn & Mónica Madariaga

  3. Instituto de Investigaciones Agropecuarias, INIA-La Platina, 8831314, Santiago, Chile

    Alejandra Serrano

  4. Center for Systems Biotechnology, Fraunhofer Chile Research Foundation, 8580704, Santiago, Huechuraba, Chile

    Franko Restovic

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  1. Alejandra Serrano
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Contributions

AS and NK conceived, design, and conducted research. AS, NK FR, and CM-R wrote the manuscript. AS, FR, MM, and PAJ were involved in revising the manuscript critically for important intellectual content. All authors read and approved the final manuscript. We thank Alyssa Grube for assistance in language support.

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Correspondence to Patricio Arce-Johnson.

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Serrano, A., Kuhn, N., Restovic, F. et al. The Glucose-Related Decrease in Polar Auxin Transport During Ripening and its Possible Role in Grapevine Berry Coloring. J Plant Growth Regul 42, 365–375 (2023). https://doi.org/10.1007/s00344-021-10553-6

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