Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants
The 1-aminocyclopropane-1-carboxylic acid (ACC) pathway that synthesizes ethylene is shared in seed plants, fungi and probably other organisms. However, the evolutionary relationship of the key enzyme ACC oxidase (ACO) in the pathway among organisms remains unknown. Herein, we cloned, expressed and...
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MDPI AG
2022-12-01
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| Series: | Journal of Fungi |
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| Online Access: | https://www.mdpi.com/2309-608X/9/1/55 |
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| author | Yanan Li Man Qi Qi Zhang Zhixu Xu Yan Zhang Yuqian Gao Yuancheng Qi Liyou Qiu Mingdao Wang |
| author_facet | Yanan Li Man Qi Qi Zhang Zhixu Xu Yan Zhang Yuqian Gao Yuancheng Qi Liyou Qiu Mingdao Wang |
| author_sort | Yanan Li |
| collection | DOAJ |
| description | The 1-aminocyclopropane-1-carboxylic acid (ACC) pathway that synthesizes ethylene is shared in seed plants, fungi and probably other organisms. However, the evolutionary relationship of the key enzyme ACC oxidase (ACO) in the pathway among organisms remains unknown. Herein, we cloned, expressed and characterized five ACOs from the straw mushroom (<i>Volvariella volvacea</i>) and the oyster mushroom (<i>Pleurotus ostreatus</i>): VvACO1-4 and PoACO. The five mushroom ACOs and the previously identified AbACO of the button mushroom contained all three conserved residues that bound to Fe(II) in plant ACOs. They also had variable residues that were conserved and bound to ascorbate and bicarbonate in plant ACOs and harbored only 1–2 of the five conserved ACO motifs in plant ACOs. Particularly, VvACO2 and AbACO had only one ACO motif 2. Additionally, VvACO4 shared 44.23% sequence identity with the cyanobacterium <i>Hapalosiphon</i> putative functional ACO. Phylogenetic analysis showed that the functional ACOs of monocotyledonous and dicotyledonous plants co-occurred in Type I, Type II and Type III, while putative functional gymnosperm ACOs also appeared in Type III. The putative functional bacterial ACO, functional fungi and slime mold ACOs were clustered in ancestral Type IV. These results indicate that ACO motif 2, ACC and Fe(II) are essential for ACO activity. The ACOs of the other organisms may come from the horizontal transfer of fungal ACOs, which were found ordinarily in basidiomycetes. It is mostly the first case for the horizontal gene transfers from fungi to seed plants. The horizontal transfer of ACOs from fungi to plants probably facilitates the fungal-plant symbioses, plant–land colonization and further evolution to form seeds. |
| first_indexed | 2024-03-09T12:04:25Z |
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| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-03-09T12:04:25Z |
| publishDate | 2022-12-01 |
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| spelling | doaj.art-1d0be1287c06411681845b876552bb2a2023-11-30T22:59:42ZengMDPI AGJournal of Fungi2309-608X2022-12-01915510.3390/jof9010055Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and PlantsYanan Li0Man Qi1Qi Zhang2Zhixu Xu3Yan Zhang4Yuqian Gao5Yuancheng Qi6Liyou Qiu7Mingdao Wang8Key Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaKey Laboratory of Enzyme Engineering of Agricultural Microbiology, Ministry of Agriculture and Rural Affairs, College of Life Sciences, Henan Agricultural University, Zhengzhou 450002, ChinaThe 1-aminocyclopropane-1-carboxylic acid (ACC) pathway that synthesizes ethylene is shared in seed plants, fungi and probably other organisms. However, the evolutionary relationship of the key enzyme ACC oxidase (ACO) in the pathway among organisms remains unknown. Herein, we cloned, expressed and characterized five ACOs from the straw mushroom (<i>Volvariella volvacea</i>) and the oyster mushroom (<i>Pleurotus ostreatus</i>): VvACO1-4 and PoACO. The five mushroom ACOs and the previously identified AbACO of the button mushroom contained all three conserved residues that bound to Fe(II) in plant ACOs. They also had variable residues that were conserved and bound to ascorbate and bicarbonate in plant ACOs and harbored only 1–2 of the five conserved ACO motifs in plant ACOs. Particularly, VvACO2 and AbACO had only one ACO motif 2. Additionally, VvACO4 shared 44.23% sequence identity with the cyanobacterium <i>Hapalosiphon</i> putative functional ACO. Phylogenetic analysis showed that the functional ACOs of monocotyledonous and dicotyledonous plants co-occurred in Type I, Type II and Type III, while putative functional gymnosperm ACOs also appeared in Type III. The putative functional bacterial ACO, functional fungi and slime mold ACOs were clustered in ancestral Type IV. These results indicate that ACO motif 2, ACC and Fe(II) are essential for ACO activity. The ACOs of the other organisms may come from the horizontal transfer of fungal ACOs, which were found ordinarily in basidiomycetes. It is mostly the first case for the horizontal gene transfers from fungi to seed plants. The horizontal transfer of ACOs from fungi to plants probably facilitates the fungal-plant symbioses, plant–land colonization and further evolution to form seeds.https://www.mdpi.com/2309-608X/9/1/551-aminocyclopropane-1-carboxylic acid oxidasebasidiomycetesequence motif analysishorizontal gene transfer |
| spellingShingle | Yanan Li Man Qi Qi Zhang Zhixu Xu Yan Zhang Yuqian Gao Yuancheng Qi Liyou Qiu Mingdao Wang Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants Journal of Fungi 1-aminocyclopropane-1-carboxylic acid oxidase basidiomycete sequence motif analysis horizontal gene transfer |
| title | Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants |
| title_full | Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants |
| title_fullStr | Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants |
| title_full_unstemmed | Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants |
| title_short | Phylogenesis of the Functional 1-Aminocyclopropane-1-Carboxylate Oxidase of Fungi and Plants |
| title_sort | phylogenesis of the functional 1 aminocyclopropane 1 carboxylate oxidase of fungi and plants |
| topic | 1-aminocyclopropane-1-carboxylic acid oxidase basidiomycete sequence motif analysis horizontal gene transfer |
| url | https://www.mdpi.com/2309-608X/9/1/55 |
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