Origin, evolution and functional characterization of the land plant glycoside hydrolase subfamily GH5_11
Copyright © 2019 Elsevier Inc. All rights reserved..
Colonization of the land by plants was a critical event in the establishment of modern terrestrial ecosystems, and many characteristics of land plants originated during this process, including the emergence of rosette terminal cellulose-synthesizing complexes. Cellulases are non-homologous isofunctional enzymes, encoded by glycosyl hydrolase (GH) gene families. Although the plant GH5_11 gene subfamily is presumed to encode a cell-wall degrading enzyme, its evolutionary and functional characteristics remain unclear. In the present study, we report the evolution of the land plant GH5_11 subfamily, and the functions of its members in terms of cellulase activity, through comprehensive phylogenetic analyses and observation of Arabidopsis mutants. Phylogenetic and sequence similarity analyses reveal that the ancestor of land plants acquired the GH5_11 gene from fungi through a horizontal gene transfer (HGT) event. Subsequently, positive selection with massive gene duplication and loss events contributed to the evolution of this subfamily in land plants. In Arabidopsis and rice, expression of GH5_11 genes are regulated by multiple abiotic stresses, the duplicated genes showing different patterns of expression. The Arabidopsis mutants atgh5_11a and atgh5_11c display low levels of cellulase and endoglucanase activities, with correspondingly high levels of cellulose, implying that the encoded proteins may function as endoglucanases. However, atgh5_11a and atgh5_11c also display an enlarged rosette leaf phenotype, and atgh5_11c is late-flowering under short photoperiods. These observations suggest that plant GH5_11s possess more functions beyond being endonucleases. To summarize, we demonstrate that the ancestor of land plants has acquired GH5_11 gene through HGT, which extends the cellulose degradation complexity. Our investigations illuminate features of part of the molecular framework underlying the origin of land plants and provide a focus on the cellulose degradation pathway.
| Medienart: |
E-Artikel |
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| Erscheinungsjahr: |
2019 |
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| Erschienen: |
2019 |
| Enthalten in: |
Zur Gesamtaufnahme - volume:138 |
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| Enthalten in: |
Molecular phylogenetics and evolution - 138(2019) vom: 15. Sept., Seite 205-218 |
| Sprache: |
Englisch |
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| Beteiligte Personen: |
Chen, Rujia [VerfasserIn] |
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| Links: |
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| Themen: |
9004-34-6 |
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| Anmerkungen: |
Date Completed 29.11.2019 Date Revised 29.11.2019 published: Print-Electronic Citation Status MEDLINE |
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| doi: |
10.1016/j.ympev.2019.05.031 |
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| funding: |
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| Förderinstitution / Projekttitel: |
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| PPN (Katalog-ID): |
NLM297506080 |
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| 100 | 1 | |a Chen, Rujia |e verfasserin |4 aut | |
| 245 | 1 | 0 | |a Origin, evolution and functional characterization of the land plant glycoside hydrolase subfamily GH5_11 |
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| 500 | |a Citation Status MEDLINE | ||
| 520 | |a Copyright © 2019 Elsevier Inc. All rights reserved. | ||
| 520 | |a Colonization of the land by plants was a critical event in the establishment of modern terrestrial ecosystems, and many characteristics of land plants originated during this process, including the emergence of rosette terminal cellulose-synthesizing complexes. Cellulases are non-homologous isofunctional enzymes, encoded by glycosyl hydrolase (GH) gene families. Although the plant GH5_11 gene subfamily is presumed to encode a cell-wall degrading enzyme, its evolutionary and functional characteristics remain unclear. In the present study, we report the evolution of the land plant GH5_11 subfamily, and the functions of its members in terms of cellulase activity, through comprehensive phylogenetic analyses and observation of Arabidopsis mutants. Phylogenetic and sequence similarity analyses reveal that the ancestor of land plants acquired the GH5_11 gene from fungi through a horizontal gene transfer (HGT) event. Subsequently, positive selection with massive gene duplication and loss events contributed to the evolution of this subfamily in land plants. In Arabidopsis and rice, expression of GH5_11 genes are regulated by multiple abiotic stresses, the duplicated genes showing different patterns of expression. The Arabidopsis mutants atgh5_11a and atgh5_11c display low levels of cellulase and endoglucanase activities, with correspondingly high levels of cellulose, implying that the encoded proteins may function as endoglucanases. However, atgh5_11a and atgh5_11c also display an enlarged rosette leaf phenotype, and atgh5_11c is late-flowering under short photoperiods. These observations suggest that plant GH5_11s possess more functions beyond being endonucleases. To summarize, we demonstrate that the ancestor of land plants has acquired GH5_11 gene through HGT, which extends the cellulose degradation complexity. Our investigations illuminate features of part of the molecular framework underlying the origin of land plants and provide a focus on the cellulose degradation pathway | ||
| 650 | 4 | |a Journal Article | |
| 650 | 4 | |a Research Support, Non-U.S. Gov't | |
| 650 | 4 | |a Cellulase | |
| 650 | 4 | |a Glycoside hydrolase subfamily GH5_11 | |
| 650 | 4 | |a Horizontal gene transfer | |
| 650 | 4 | |a Land plants | |
| 650 | 7 | |a Cellulose |2 NLM | |
| 650 | 7 | |a 9004-34-6 |2 NLM | |
| 650 | 7 | |a Glycoside Hydrolases |2 NLM | |
| 650 | 7 | |a EC 3.2.1.- |2 NLM | |
| 700 | 1 | |a Yao, Youli |e verfasserin |4 aut | |
| 700 | 1 | |a Fang, Huimin |e verfasserin |4 aut | |
| 700 | 1 | |a Zhang, Enying |e verfasserin |4 aut | |
| 700 | 1 | |a Li, Pengcheng |e verfasserin |4 aut | |
| 700 | 1 | |a Xu, Yang |e verfasserin |4 aut | |
| 700 | 1 | |a Yin, Shuangyi |e verfasserin |4 aut | |
| 700 | 1 | |a Huangfu, Liexiang |e verfasserin |4 aut | |
| 700 | 1 | |a Sun, Guiling |e verfasserin |4 aut | |
| 700 | 1 | |a Xu, Chenwu |e verfasserin |4 aut | |
| 700 | 1 | |a Zhou, Yong |e verfasserin |4 aut | |
| 700 | 1 | |a Yang, Zefeng |e verfasserin |4 aut | |
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