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A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato

Intracellular vesicular trafficking ensures the exchange of lipids and proteins between endomembrane compartments. This is relevant under high salinity conditions, since both the removal of transporters and ion channels from the plasma membrane and the compartmentalization of toxic ions require the...

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Autores principales: Salinas-Cornejo, Josselyn, Madrid-Espinoza, José, Verdugo, Isabel, Norambuena, Lorena, Ruiz-Lara, Simón
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10431929/
https://www.ncbi.nlm.nih.gov/pubmed/37593042
http://dx.doi.org/10.3389/fpls.2023.1212806
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author Salinas-Cornejo, Josselyn
Madrid-Espinoza, José
Verdugo, Isabel
Norambuena, Lorena
Ruiz-Lara, Simón
author_facet Salinas-Cornejo, Josselyn
Madrid-Espinoza, José
Verdugo, Isabel
Norambuena, Lorena
Ruiz-Lara, Simón
author_sort Salinas-Cornejo, Josselyn
collection PubMed
description Intracellular vesicular trafficking ensures the exchange of lipids and proteins between endomembrane compartments. This is relevant under high salinity conditions, since both the removal of transporters and ion channels from the plasma membrane and the compartmentalization of toxic ions require the formation of vesicles, which can be maintained as multivesicular bodies or be fused to the central vacuole. SNARE proteins (Soluble N-ethylmaleimide-sensitive factor attachment receptor) participate in the vesicle fusion process and give specificity to their destination. Plant genome studies have revealed a superfamily of genes that encode for proteins called SNARE-like. These proteins appear to be participating in vesicular trafficking with similar functions to those of SNARE proteins. A SNARE-like, named SlSLSP6, in Solanum lycopersicum plants has been shown to be induced under high salinity conditions. A phylogenetic relationship of SlSLSP6 with SNARE-like proteins of salinity-tolerant plants, including Salicornia brachiata, Zostera marina and Solanum pennelli, was determined. Considering its amino acid sequence, a putative clathrin adapter complex domain and palmitoylation site was predicted. Subcellular localization analysis evidenced that SlSLSP6 is mostly localized in the plasma membrane. Using transgenic tomato plants, we identified that overexpression of SlSLSP6 increased tolerance to salt stress. This tolerance was evident when we quantified an improvement in physiological and biochemical parameters, such as higher chlorophyll content, performance index, efficiency of photosystem II and relative water content, and lower malondialdehyde content, compared to control plants. At the subcellular level, the overexpression of SlSLSP6 reduced the presence of H(2)O(2) in roots and increased the compartmentalization of sodium in vacuoles during salt stress. These effects appear to be associated with the higher endocytic rate of FM4-64, determined in the plant root cells. Taken together, these results indicate that SlSLSP6 increases tolerance to salt stress by modulating vesicular trafficking through over-induction of the endocytic pathway. This work contributes to understanding the role of this type of SNARE-like protein during salt stress and could be a potential candidate in breeding programs for tolerance to salt stress in tomato plants.
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spelling pubmed-104319292023-08-17 A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato Salinas-Cornejo, Josselyn Madrid-Espinoza, José Verdugo, Isabel Norambuena, Lorena Ruiz-Lara, Simón Front Plant Sci Plant Science Intracellular vesicular trafficking ensures the exchange of lipids and proteins between endomembrane compartments. This is relevant under high salinity conditions, since both the removal of transporters and ion channels from the plasma membrane and the compartmentalization of toxic ions require the formation of vesicles, which can be maintained as multivesicular bodies or be fused to the central vacuole. SNARE proteins (Soluble N-ethylmaleimide-sensitive factor attachment receptor) participate in the vesicle fusion process and give specificity to their destination. Plant genome studies have revealed a superfamily of genes that encode for proteins called SNARE-like. These proteins appear to be participating in vesicular trafficking with similar functions to those of SNARE proteins. A SNARE-like, named SlSLSP6, in Solanum lycopersicum plants has been shown to be induced under high salinity conditions. A phylogenetic relationship of SlSLSP6 with SNARE-like proteins of salinity-tolerant plants, including Salicornia brachiata, Zostera marina and Solanum pennelli, was determined. Considering its amino acid sequence, a putative clathrin adapter complex domain and palmitoylation site was predicted. Subcellular localization analysis evidenced that SlSLSP6 is mostly localized in the plasma membrane. Using transgenic tomato plants, we identified that overexpression of SlSLSP6 increased tolerance to salt stress. This tolerance was evident when we quantified an improvement in physiological and biochemical parameters, such as higher chlorophyll content, performance index, efficiency of photosystem II and relative water content, and lower malondialdehyde content, compared to control plants. At the subcellular level, the overexpression of SlSLSP6 reduced the presence of H(2)O(2) in roots and increased the compartmentalization of sodium in vacuoles during salt stress. These effects appear to be associated with the higher endocytic rate of FM4-64, determined in the plant root cells. Taken together, these results indicate that SlSLSP6 increases tolerance to salt stress by modulating vesicular trafficking through over-induction of the endocytic pathway. This work contributes to understanding the role of this type of SNARE-like protein during salt stress and could be a potential candidate in breeding programs for tolerance to salt stress in tomato plants. Frontiers Media S.A. 2023-08-01 /pmc/articles/PMC10431929/ /pubmed/37593042 http://dx.doi.org/10.3389/fpls.2023.1212806 Text en Copyright © 2023 Salinas-Cornejo, Madrid-Espinoza, Verdugo, Norambuena and Ruiz-Lara https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Salinas-Cornejo, Josselyn
Madrid-Espinoza, José
Verdugo, Isabel
Norambuena, Lorena
Ruiz-Lara, Simón
A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
title A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
title_full A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
title_fullStr A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
title_full_unstemmed A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
title_short A SNARE-like protein from Solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
title_sort snare-like protein from solanum lycopersicum increases salt tolerance by modulating vesicular trafficking in tomato
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10431929/
https://www.ncbi.nlm.nih.gov/pubmed/37593042
http://dx.doi.org/10.3389/fpls.2023.1212806
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