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Evolution and functional diversification of catalase genes in the green lineage

BACKGROUND: Catalases (CATs) break down hydrogen peroxide into water and oxygen to prevent cellular oxidative damage, and play key roles in the development, biotic and abiotic stresses of plants. However, the evolutionary relationships of the plant CAT gene family have not been systematically report...

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Autores principales: Pan, Luzhao, Luo, Yin, Wang, Jin, Li, Xiumin, Tang, Bingqian, Yang, Huiping, Hou, Xilin, Liu, Feng, Zou, Xuexiao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9158360/
https://www.ncbi.nlm.nih.gov/pubmed/35650553
http://dx.doi.org/10.1186/s12864-022-08621-6
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author Pan, Luzhao
Luo, Yin
Wang, Jin
Li, Xiumin
Tang, Bingqian
Yang, Huiping
Hou, Xilin
Liu, Feng
Zou, Xuexiao
author_facet Pan, Luzhao
Luo, Yin
Wang, Jin
Li, Xiumin
Tang, Bingqian
Yang, Huiping
Hou, Xilin
Liu, Feng
Zou, Xuexiao
author_sort Pan, Luzhao
collection PubMed
description BACKGROUND: Catalases (CATs) break down hydrogen peroxide into water and oxygen to prevent cellular oxidative damage, and play key roles in the development, biotic and abiotic stresses of plants. However, the evolutionary relationships of the plant CAT gene family have not been systematically reported. RESULTS: Here, we conducted genome-wide comparative, phylogenetic, and structural analyses of CAT orthologs from 29 out of 31 representative green lineage species to characterize the evolution and functional diversity of CATs. We found that CAT genes in land plants were derived from core chlorophytes and detected a lineage-specific loss of CAT genes in Fabaceae, suggesting that the CAT genes in this group possess divergent functions. All CAT genes were split into three major groups (group α, β1, and β2) based on the phylogeny. CAT genes were transferred from bacteria to core chlorophytes and charophytes by lateral gene transfer, and this led to the independent evolution of two types of CAT genes: α and β types. Ten common motifs were detected in both α and β groups, and β CAT genes had five unique motifs, respectively. The findings of our study are inconsistent with two previous hypotheses proposing that (i) new CAT genes are acquired through intron loss and that (ii) the Cys-343 residue is highly conserved in plants. We found that new CAT genes in most higher plants were produced through intron acquisition and that the Cys-343 residue was only present in monocots, Brassicaceae and Pp_CatX7 in P. patens, which indicates the functional specificity of the CATs in these three lineages. Finally, our finding that CAT genes show high overall sequence identity but that individual CAT genes showed developmental stage and organ-specific expression patterns suggests that CAT genes have functionally diverged independently. CONCLUSIONS: Overall, our analyses of the CAT gene family provide new insights into their evolution and functional diversification in green lineage species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08621-6.
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spelling pubmed-91583602022-06-02 Evolution and functional diversification of catalase genes in the green lineage Pan, Luzhao Luo, Yin Wang, Jin Li, Xiumin Tang, Bingqian Yang, Huiping Hou, Xilin Liu, Feng Zou, Xuexiao BMC Genomics Research BACKGROUND: Catalases (CATs) break down hydrogen peroxide into water and oxygen to prevent cellular oxidative damage, and play key roles in the development, biotic and abiotic stresses of plants. However, the evolutionary relationships of the plant CAT gene family have not been systematically reported. RESULTS: Here, we conducted genome-wide comparative, phylogenetic, and structural analyses of CAT orthologs from 29 out of 31 representative green lineage species to characterize the evolution and functional diversity of CATs. We found that CAT genes in land plants were derived from core chlorophytes and detected a lineage-specific loss of CAT genes in Fabaceae, suggesting that the CAT genes in this group possess divergent functions. All CAT genes were split into three major groups (group α, β1, and β2) based on the phylogeny. CAT genes were transferred from bacteria to core chlorophytes and charophytes by lateral gene transfer, and this led to the independent evolution of two types of CAT genes: α and β types. Ten common motifs were detected in both α and β groups, and β CAT genes had five unique motifs, respectively. The findings of our study are inconsistent with two previous hypotheses proposing that (i) new CAT genes are acquired through intron loss and that (ii) the Cys-343 residue is highly conserved in plants. We found that new CAT genes in most higher plants were produced through intron acquisition and that the Cys-343 residue was only present in monocots, Brassicaceae and Pp_CatX7 in P. patens, which indicates the functional specificity of the CATs in these three lineages. Finally, our finding that CAT genes show high overall sequence identity but that individual CAT genes showed developmental stage and organ-specific expression patterns suggests that CAT genes have functionally diverged independently. CONCLUSIONS: Overall, our analyses of the CAT gene family provide new insights into their evolution and functional diversification in green lineage species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08621-6. BioMed Central 2022-06-01 /pmc/articles/PMC9158360/ /pubmed/35650553 http://dx.doi.org/10.1186/s12864-022-08621-6 Text en © The Author(s) 2022 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
Pan, Luzhao
Luo, Yin
Wang, Jin
Li, Xiumin
Tang, Bingqian
Yang, Huiping
Hou, Xilin
Liu, Feng
Zou, Xuexiao
Evolution and functional diversification of catalase genes in the green lineage
title Evolution and functional diversification of catalase genes in the green lineage
title_full Evolution and functional diversification of catalase genes in the green lineage
title_fullStr Evolution and functional diversification of catalase genes in the green lineage
title_full_unstemmed Evolution and functional diversification of catalase genes in the green lineage
title_short Evolution and functional diversification of catalase genes in the green lineage
title_sort evolution and functional diversification of catalase genes in the green lineage
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9158360/
https://www.ncbi.nlm.nih.gov/pubmed/35650553
http://dx.doi.org/10.1186/s12864-022-08621-6
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