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New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean

BACKGROUND: SPX-containing proteins have been known as key players in phosphate signaling and homeostasis. In Arabidopsis and rice, functions of some SPXs have been characterized, but little is known about their function in other plants, especially in the legumes. RESULTS: We analyzed SPX gene famil...

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Autores principales: Nezamivand-Chegini, Mahnaz, Ebrahimie, Esmaeil, Tahmasebi, Ahmad, Moghadam, Ali, Eshghi, Saeid, Mohammadi-Dehchesmeh, Manijeh, Kopriva, Stanislav, Niazi, Ali
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8717665/
https://www.ncbi.nlm.nih.gov/pubmed/34969367
http://dx.doi.org/10.1186/s12864-021-08242-5
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author Nezamivand-Chegini, Mahnaz
Ebrahimie, Esmaeil
Tahmasebi, Ahmad
Moghadam, Ali
Eshghi, Saeid
Mohammadi-Dehchesmeh, Manijeh
Kopriva, Stanislav
Niazi, Ali
author_facet Nezamivand-Chegini, Mahnaz
Ebrahimie, Esmaeil
Tahmasebi, Ahmad
Moghadam, Ali
Eshghi, Saeid
Mohammadi-Dehchesmeh, Manijeh
Kopriva, Stanislav
Niazi, Ali
author_sort Nezamivand-Chegini, Mahnaz
collection PubMed
description BACKGROUND: SPX-containing proteins have been known as key players in phosphate signaling and homeostasis. In Arabidopsis and rice, functions of some SPXs have been characterized, but little is known about their function in other plants, especially in the legumes. RESULTS: We analyzed SPX gene family evolution in legumes and in a number of key species from algae to angiosperms. We found that SPX harboring proteins showed fluctuations in domain fusions from algae to the angiosperms with, finally, four classes appearing and being retained in the land plants. Despite these fluctuations, Lysine Surface Cluster (KSC), and the third residue of Phosphate Binding Sites (PBS) showed complete conservation in almost all of SPXs except few proteins in Selaginella moellendorffii and Papaver sumniferum, suggesting they might have different ligand preferences. In addition, we found that the WGD/segmentally or dispersed duplication types were the most frequent contributors to the SPX expansion, and that there is a positive correlation between the amount of WGD contribution to the SPX expansion in individual species and its number of EXS genes. We could also reveal that except SPX class genes, other classes lost the collinearity relationships among Arabidopsis and legume genomes. The sub- or neo-functionalization of the duplicated genes in the legumes makes it difficult to find the functional orthologous genes. Therefore, we used two different methods to identify functional orthologs in soybean and Medicago. High variance in the dynamic and spatial expression pattern of GmSPXs proved the new or sub-functionalization in the paralogs. CONCLUSION: This comprehensive analysis revealed how SPX gene family evolved from algae to legumes and also discovered several new domains fused to SPX domain in algae. In addition, we hypothesized that there different phosphate sensing mechanisms might occur in S. moellendorffii and P. sumniferum. Finally, we predicted putative functional orthologs of AtSPXs in the legumes, especially, orthologs of AtPHO1, involved in long-distance Pi transportation. These findings help to understand evolution of phosphate signaling and might underpin development of new legume varieties with improved phosphate use efficiency. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-08242-5.
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spelling pubmed-87176652022-01-05 New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean Nezamivand-Chegini, Mahnaz Ebrahimie, Esmaeil Tahmasebi, Ahmad Moghadam, Ali Eshghi, Saeid Mohammadi-Dehchesmeh, Manijeh Kopriva, Stanislav Niazi, Ali BMC Genomics Research BACKGROUND: SPX-containing proteins have been known as key players in phosphate signaling and homeostasis. In Arabidopsis and rice, functions of some SPXs have been characterized, but little is known about their function in other plants, especially in the legumes. RESULTS: We analyzed SPX gene family evolution in legumes and in a number of key species from algae to angiosperms. We found that SPX harboring proteins showed fluctuations in domain fusions from algae to the angiosperms with, finally, four classes appearing and being retained in the land plants. Despite these fluctuations, Lysine Surface Cluster (KSC), and the third residue of Phosphate Binding Sites (PBS) showed complete conservation in almost all of SPXs except few proteins in Selaginella moellendorffii and Papaver sumniferum, suggesting they might have different ligand preferences. In addition, we found that the WGD/segmentally or dispersed duplication types were the most frequent contributors to the SPX expansion, and that there is a positive correlation between the amount of WGD contribution to the SPX expansion in individual species and its number of EXS genes. We could also reveal that except SPX class genes, other classes lost the collinearity relationships among Arabidopsis and legume genomes. The sub- or neo-functionalization of the duplicated genes in the legumes makes it difficult to find the functional orthologous genes. Therefore, we used two different methods to identify functional orthologs in soybean and Medicago. High variance in the dynamic and spatial expression pattern of GmSPXs proved the new or sub-functionalization in the paralogs. CONCLUSION: This comprehensive analysis revealed how SPX gene family evolved from algae to legumes and also discovered several new domains fused to SPX domain in algae. In addition, we hypothesized that there different phosphate sensing mechanisms might occur in S. moellendorffii and P. sumniferum. Finally, we predicted putative functional orthologs of AtSPXs in the legumes, especially, orthologs of AtPHO1, involved in long-distance Pi transportation. These findings help to understand evolution of phosphate signaling and might underpin development of new legume varieties with improved phosphate use efficiency. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-08242-5. BioMed Central 2021-12-30 /pmc/articles/PMC8717665/ /pubmed/34969367 http://dx.doi.org/10.1186/s12864-021-08242-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Nezamivand-Chegini, Mahnaz
Ebrahimie, Esmaeil
Tahmasebi, Ahmad
Moghadam, Ali
Eshghi, Saeid
Mohammadi-Dehchesmeh, Manijeh
Kopriva, Stanislav
Niazi, Ali
New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean
title New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean
title_full New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean
title_fullStr New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean
title_full_unstemmed New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean
title_short New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean
title_sort new insights into the evolution of spx gene family from algae to legumes; a focus on soybean
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8717665/
https://www.ncbi.nlm.nih.gov/pubmed/34969367
http://dx.doi.org/10.1186/s12864-021-08242-5
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