Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW

This work provides insight into several mechanisms involved in boron (B) regulation pathway in response to high B conditions in Citrus. The study was carried out in Citrus macrophylla W. (Cm) seedlings cultured “in vitro” in media with 50 or 400 μMH3BO3 (control, Ct, and B-excess, +B, plants, res...

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Autores principales: Martínez-Cuenca, Mary-Rus, Martínez-Alcántara, Belén, Quinones, Ana, Ruiz, Marta, Iglesias, Domingo J., Primo-Millo, Eduardo, Forner-Giner, María A.
Formato: Artículo
Lenguaje:Inglés
Publicado: PLOS 2020
Materias:
Acceso en línea:http://hdl.handle.net/20.500.11939/6417
https://doi.org/10.1371/journal.pone.0137941
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0134372
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author Martínez-Cuenca, Mary-Rus
Martínez-Alcántara, Belén
Quinones, Ana
Ruiz, Marta
Iglesias, Domingo J.
Primo-Millo, Eduardo
Forner-Giner, María A.
author_browse Forner-Giner, María A.
Iglesias, Domingo J.
Martínez-Alcántara, Belén
Martínez-Cuenca, Mary-Rus
Primo-Millo, Eduardo
Quinones, Ana
Ruiz, Marta
author_facet Martínez-Cuenca, Mary-Rus
Martínez-Alcántara, Belén
Quinones, Ana
Ruiz, Marta
Iglesias, Domingo J.
Primo-Millo, Eduardo
Forner-Giner, María A.
author_sort Martínez-Cuenca, Mary-Rus
collection ReDivia
description This work provides insight into several mechanisms involved in boron (B) regulation pathway in response to high B conditions in Citrus. The study was carried out in Citrus macrophylla W. (Cm) seedlings cultured “in vitro” in media with 50 or 400 μMH3BO3 (control, Ct, and B-excess, +B, plants, respectively). Growth parameters, B concentration, leaf chlorophyll (Chl) concentration, the expression of the main putative genes involved in B transport and distribution, and leaf and root proline and malonaldehyde (MDA) concentrations, were assessed. Excess B led to high B concentration in +B plants (3.8- and 1.4-fold in leaves and roots, respectively) when compared with Ct ones. However, a minor effect was recorded in the plant (incipient visual symptoms, less than 27% reduction in root growth and 26% decrease in Chl b concentration). B toxicity down-regulated by half the expression level of putative B transporter genes NIP5 and PIP1. CmBOR1 gene was not repressed in +B plants and B accumulated in the shoots. High B level increased the transcripts of putative gene TIP5, involved in B transport across the tonoplast, by 3.3- and 2.4-fold in leaves and roots, respectively. The activity of V-PPiase proton pump, related with the electrochemical gradient in the vacuole, was also enhanced in +B organs. B toxicity up-regulated putative BOR4 gene (2.1- and 2.7-fold in roots and leaves, respectively), which codifies for an active efflux B transporter. Accordingly, B was located in +B plants preferently in an insoluble form on cell walls. Finally, excess B caused a significant rise in proline concentration (51% and 34% in roots and leaves, respectively), while the MDA level did not exceed 20%. In conclusion, Cm tolerance to a high B level is likely based on the synergism of several specific mechanisms against B toxicity, including: 1/ down-regulation of NIP5 and PIP1 boron transporters; 2/ activation of B efflux from cells due to the up-regulation of putative BOR4 gene; 3/ compartmentation of B in the vacuole through TIP5 transporter activation and the acidification of the organelle; 4/ insolubilisation of B and deposition in cell walls preventing from cytoplasm damage; and, 5/ induction of an efficient antioxidant system through proline accumulation.
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spelling ReDivia64172025-04-25T14:47:01Z Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW Martínez-Cuenca, Mary-Rus Martínez-Alcántara, Belén Quinones, Ana Ruiz, Marta Iglesias, Domingo J. Primo-Millo, Eduardo Forner-Giner, María A. F61 Plant physiology - Nutrition This work provides insight into several mechanisms involved in boron (B) regulation pathway in response to high B conditions in Citrus. The study was carried out in Citrus macrophylla W. (Cm) seedlings cultured “in vitro” in media with 50 or 400 μMH3BO3 (control, Ct, and B-excess, +B, plants, respectively). Growth parameters, B concentration, leaf chlorophyll (Chl) concentration, the expression of the main putative genes involved in B transport and distribution, and leaf and root proline and malonaldehyde (MDA) concentrations, were assessed. Excess B led to high B concentration in +B plants (3.8- and 1.4-fold in leaves and roots, respectively) when compared with Ct ones. However, a minor effect was recorded in the plant (incipient visual symptoms, less than 27% reduction in root growth and 26% decrease in Chl b concentration). B toxicity down-regulated by half the expression level of putative B transporter genes NIP5 and PIP1. CmBOR1 gene was not repressed in +B plants and B accumulated in the shoots. High B level increased the transcripts of putative gene TIP5, involved in B transport across the tonoplast, by 3.3- and 2.4-fold in leaves and roots, respectively. The activity of V-PPiase proton pump, related with the electrochemical gradient in the vacuole, was also enhanced in +B organs. B toxicity up-regulated putative BOR4 gene (2.1- and 2.7-fold in roots and leaves, respectively), which codifies for an active efflux B transporter. Accordingly, B was located in +B plants preferently in an insoluble form on cell walls. Finally, excess B caused a significant rise in proline concentration (51% and 34% in roots and leaves, respectively), while the MDA level did not exceed 20%. In conclusion, Cm tolerance to a high B level is likely based on the synergism of several specific mechanisms against B toxicity, including: 1/ down-regulation of NIP5 and PIP1 boron transporters; 2/ activation of B efflux from cells due to the up-regulation of putative BOR4 gene; 3/ compartmentation of B in the vacuole through TIP5 transporter activation and the acidification of the organelle; 4/ insolubilisation of B and deposition in cell walls preventing from cytoplasm damage; and, 5/ induction of an efficient antioxidant system through proline accumulation. 2020-05-04T14:48:18Z 2020-05-04T14:48:18Z 2015 article publishedVersion Martinez-Cuenca, M. R., Martinez-Alcantara, B., Quiñones, A., Ruiz, M., Iglesias, D. J., Primo-Millo, E., & Forner-Giner, M. A. (2015). Physiological and molecular responses to excess boron in Citrus macrophylla W. PloS one, 10(7). 1932-6203 http://hdl.handle.net/20.500.11939/6417 https://doi.org/10.1371/journal.pone.0137941 https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0134372 en Atribución-NoComercial-SinDerivadas 3.0 España http://creativecommons.org/licenses/by-nc-nd/3.0/es/ PLOS electronico
spellingShingle F61 Plant physiology - Nutrition
Martínez-Cuenca, Mary-Rus
Martínez-Alcántara, Belén
Quinones, Ana
Ruiz, Marta
Iglesias, Domingo J.
Primo-Millo, Eduardo
Forner-Giner, María A.
Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW
title Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW
title_full Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW
title_fullStr Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW
title_full_unstemmed Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW
title_short Physiological and Molecular Responses to Excess Boron in Citrus macrophyllaW
title_sort physiological and molecular responses to excess boron in citrus macrophyllaw
topic F61 Plant physiology - Nutrition
url http://hdl.handle.net/20.500.11939/6417
https://doi.org/10.1371/journal.pone.0137941
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0134372
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