Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i>
3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), as the rate-limiting enzyme in the mevalonate pathway, is essential for the biosynthesis of shikonin in <i>Lithospermum erythrorhizon</i>. However, in the absence of sufficient data, the principles of a genome-wide in-depth evolutionary ex...
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2023-08-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/15/12532 |
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| author | Xuan Wang Changyi Wang Minkai Yang Wencai Jie Aliya Fazal Jiangyan Fu Tongming Yin Jinfeng Cai Bao Liu Guihua Lu Hongyan Lin Hongwei Han Zhongling Wen Jinliang Qi Yonghua Yang |
| author_facet | Xuan Wang Changyi Wang Minkai Yang Wencai Jie Aliya Fazal Jiangyan Fu Tongming Yin Jinfeng Cai Bao Liu Guihua Lu Hongyan Lin Hongwei Han Zhongling Wen Jinliang Qi Yonghua Yang |
| author_sort | Xuan Wang |
| collection | DOAJ |
| description | 3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), as the rate-limiting enzyme in the mevalonate pathway, is essential for the biosynthesis of shikonin in <i>Lithospermum erythrorhizon</i>. However, in the absence of sufficient data, the principles of a genome-wide in-depth evolutionary exploration of <i>HMGR</i> family members in plants, as well as key members related to shikonin biosynthesis, remain unidentified. In this study, 124 <i>HMGR</i>s were identified and characterized from 36 representative plants, including <i>L. erythrorhizon</i>. Vascular plants were found to have more HMGR family genes than nonvascular plants. The phylogenetic tree revealed that during lineage and species diversification, the <i>HMGR</i>s evolved independently and intronless <i>LerHMGR</i>s emerged from multi-intron <i>HMGR</i> in land plants. Among them, <i>Pinus tabuliformis</i> and <i>L. erythrorhizon</i> had the most <i>HMGR</i> gene duplications, with 11 <i>LerHMGRs</i> most likely expanded through WGD/segmental and tandem duplications. In seedling roots and M9 cultured cells/hairy roots, where shikonin biosynthesis occurs, <i>LerHMGR1</i> and <i>LerHMGR2</i> were expressed significantly more than other genes. The enzymatic activities of LerHMGR1 and LerHMGR2 further supported their roles in catalyzing the conversion of HMG-CoA to mevalonate. Our findings provide insight into the molecular evolutionary properties and function of the <i>HMGR</i> family in plants and a basis for the genetic improvement of efficiently produced secondary metabolites in <i>L. erythrorhizon</i>. |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-11T00:24:40Z |
| publishDate | 2023-08-01 |
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| spelling | doaj.art-aac7ca11c6674864a084005576c821d62023-11-18T23:06:21ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-08-0124151253210.3390/ijms241512532Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i>Xuan Wang0Changyi Wang1Minkai Yang2Wencai Jie3Aliya Fazal4Jiangyan Fu5Tongming Yin6Jinfeng Cai7Bao Liu8Guihua Lu9Hongyan Lin10Hongwei Han11Zhongling Wen12Jinliang Qi13Yonghua Yang14State Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, ChinaCo-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, ChinaKey Laboratory of Molecular Epigenetics of the Ministry of Education (MOE), Northeast Normal University, Changchun 130024, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, ChinaState Key Laboratory of Pharmaceutical Biotechnology, Institute for Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210023, China3-hydroxy-3-methylglutaryl-CoA reductase (HMGR), as the rate-limiting enzyme in the mevalonate pathway, is essential for the biosynthesis of shikonin in <i>Lithospermum erythrorhizon</i>. However, in the absence of sufficient data, the principles of a genome-wide in-depth evolutionary exploration of <i>HMGR</i> family members in plants, as well as key members related to shikonin biosynthesis, remain unidentified. In this study, 124 <i>HMGR</i>s were identified and characterized from 36 representative plants, including <i>L. erythrorhizon</i>. Vascular plants were found to have more HMGR family genes than nonvascular plants. The phylogenetic tree revealed that during lineage and species diversification, the <i>HMGR</i>s evolved independently and intronless <i>LerHMGR</i>s emerged from multi-intron <i>HMGR</i> in land plants. Among them, <i>Pinus tabuliformis</i> and <i>L. erythrorhizon</i> had the most <i>HMGR</i> gene duplications, with 11 <i>LerHMGRs</i> most likely expanded through WGD/segmental and tandem duplications. In seedling roots and M9 cultured cells/hairy roots, where shikonin biosynthesis occurs, <i>LerHMGR1</i> and <i>LerHMGR2</i> were expressed significantly more than other genes. The enzymatic activities of LerHMGR1 and LerHMGR2 further supported their roles in catalyzing the conversion of HMG-CoA to mevalonate. Our findings provide insight into the molecular evolutionary properties and function of the <i>HMGR</i> family in plants and a basis for the genetic improvement of efficiently produced secondary metabolites in <i>L. erythrorhizon</i>.https://www.mdpi.com/1422-0067/24/15/12532duplication and lossevolutionaryenzymatic activitiesHMGR<i>Lithospermum erythrorhizon</i> |
| spellingShingle | Xuan Wang Changyi Wang Minkai Yang Wencai Jie Aliya Fazal Jiangyan Fu Tongming Yin Jinfeng Cai Bao Liu Guihua Lu Hongyan Lin Hongwei Han Zhongling Wen Jinliang Qi Yonghua Yang Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i> International Journal of Molecular Sciences duplication and loss evolutionary enzymatic activities HMGR <i>Lithospermum erythrorhizon</i> |
| title | Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i> |
| title_full | Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i> |
| title_fullStr | Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i> |
| title_full_unstemmed | Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i> |
| title_short | Genome-Wide Comparison and Functional Characterization of <i>HMGR</i> Gene Family Associated with Shikonin Biosynthesis in <i>Lithospermum erythrorhizon</i> |
| title_sort | genome wide comparison and functional characterization of i hmgr i gene family associated with shikonin biosynthesis in i lithospermum erythrorhizon i |
| topic | duplication and loss evolutionary enzymatic activities HMGR <i>Lithospermum erythrorhizon</i> |
| url | https://www.mdpi.com/1422-0067/24/15/12532 |
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