Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content
Sweet potato [Ipomoea batatas (L.) Lam.] is an important food and industrial crop. Its storage root is rich in starch, which is present in the form of granules and represents the principal storage carbohydrate in plants. Starch content is an important trait of sweet potato controlling the quality an...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-06-01
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| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1192417/full |
| _version_ | 1827915575108567040 |
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| author | Kai Zhang Kai Zhang Kai Zhang Zhengdan Wu Xuli Wu Xuli Wu Haohao Han Xisan Ju Xisan Ju Yonghai Fan Yonghai Fan Chaobin Yang Chaobin Yang Daobin Tang Daobin Tang Daobin Tang Qinghe Cao Jichun Wang Jichun Wang Jichun Wang Changwen Lv Changwen Lv Changwen Lv |
| author_facet | Kai Zhang Kai Zhang Kai Zhang Zhengdan Wu Xuli Wu Xuli Wu Haohao Han Xisan Ju Xisan Ju Yonghai Fan Yonghai Fan Chaobin Yang Chaobin Yang Daobin Tang Daobin Tang Daobin Tang Qinghe Cao Jichun Wang Jichun Wang Jichun Wang Changwen Lv Changwen Lv Changwen Lv |
| author_sort | Kai Zhang |
| collection | DOAJ |
| description | Sweet potato [Ipomoea batatas (L.) Lam.] is an important food and industrial crop. Its storage root is rich in starch, which is present in the form of granules and represents the principal storage carbohydrate in plants. Starch content is an important trait of sweet potato controlling the quality and yield of industrial products. Vacuolar invertase encoding gene Ibβfruct2 was supposed to be a key regulator of starch content in sweet potato, but its function and regulation were unclear. In this study, three Ibβfruct2 gene members were detected. Their promoters displayed differences in sequence, activity, and cis-regulatory elements and might interact with different transcription factors, indicating that the three Ibβfruct2 family members are governed by different regulatory mechanisms at the transcription level. Among them, we found that only Ibβfruct2-1 show a high expression level and promoter activity, and encodes a protein with invertase activity, and the conserved domains and three conserved motifs NDPNG, RDP, and WEC are critical to this activity. Only two and six amino acid residue variations were detected in sequences of proteins encoded by Ibβfruct2-2 and Ibβfruct2-3, respectively, compared with Ibβfruct2-1; although not within key motifs, these variations affected protein structure and affinities for the catalytic substrate, resulting in functional deficiency and low activity. Heterologous expression of Ibβfruct2-1 in Arabidopsis decreased starch content but increased glucose content in leaves, indicating Ibβfruct2-1 was a negative regulator of starch content. These findings represent an important advance in understanding the regulatory and functional divergence among duplicated genes in sweet potato, and provide critical information for functional studies and utilization of these genes in genetic improvement. |
| first_indexed | 2024-03-13T03:00:47Z |
| format | Article |
| id | doaj.art-9d871497da41487992bd846590ea468d |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-13T03:00:47Z |
| publishDate | 2023-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-9d871497da41487992bd846590ea468d2023-06-27T13:23:44ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-06-011410.3389/fpls.2023.11924171192417Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose contentKai Zhang0Kai Zhang1Kai Zhang2Zhengdan Wu3Xuli Wu4Xuli Wu5Haohao Han6Xisan Ju7Xisan Ju8Yonghai Fan9Yonghai Fan10Chaobin Yang11Chaobin Yang12Daobin Tang13Daobin Tang14Daobin Tang15Qinghe Cao16Jichun Wang17Jichun Wang18Jichun Wang19Changwen Lv20Changwen Lv21Changwen Lv22College of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaEngineering Research Center of South Upland Agriculture, Ministry of Education, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaEngineering Research Center of South Upland Agriculture, Ministry of Education, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaEngineering Research Center of South Upland Agriculture, Ministry of Education, Chongqing, ChinaXuzhou Institute of Agricultural Sciences in Jiangsu Xuhuai District/Sweet potato Research Institute, Chinese Academy of Agricultural Sciences, Xuzhou, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaEngineering Research Center of South Upland Agriculture, Ministry of Education, Chongqing, ChinaCollege of Agronomy and Biotechnology, Southwest University, Beibei, Chongqing, ChinaKey Laboratory of Biology and Genetic Breeding for Tuber and Root Crops in Chongqing, Beibei, Chongqing, ChinaEngineering Research Center of South Upland Agriculture, Ministry of Education, Chongqing, ChinaSweet potato [Ipomoea batatas (L.) Lam.] is an important food and industrial crop. Its storage root is rich in starch, which is present in the form of granules and represents the principal storage carbohydrate in plants. Starch content is an important trait of sweet potato controlling the quality and yield of industrial products. Vacuolar invertase encoding gene Ibβfruct2 was supposed to be a key regulator of starch content in sweet potato, but its function and regulation were unclear. In this study, three Ibβfruct2 gene members were detected. Their promoters displayed differences in sequence, activity, and cis-regulatory elements and might interact with different transcription factors, indicating that the three Ibβfruct2 family members are governed by different regulatory mechanisms at the transcription level. Among them, we found that only Ibβfruct2-1 show a high expression level and promoter activity, and encodes a protein with invertase activity, and the conserved domains and three conserved motifs NDPNG, RDP, and WEC are critical to this activity. Only two and six amino acid residue variations were detected in sequences of proteins encoded by Ibβfruct2-2 and Ibβfruct2-3, respectively, compared with Ibβfruct2-1; although not within key motifs, these variations affected protein structure and affinities for the catalytic substrate, resulting in functional deficiency and low activity. Heterologous expression of Ibβfruct2-1 in Arabidopsis decreased starch content but increased glucose content in leaves, indicating Ibβfruct2-1 was a negative regulator of starch content. These findings represent an important advance in understanding the regulatory and functional divergence among duplicated genes in sweet potato, and provide critical information for functional studies and utilization of these genes in genetic improvement.https://www.frontiersin.org/articles/10.3389/fpls.2023.1192417/fullsweet potatoinvertaseduplicated genesequence variationpromoter activity |
| spellingShingle | Kai Zhang Kai Zhang Kai Zhang Zhengdan Wu Xuli Wu Xuli Wu Haohao Han Xisan Ju Xisan Ju Yonghai Fan Yonghai Fan Chaobin Yang Chaobin Yang Daobin Tang Daobin Tang Daobin Tang Qinghe Cao Jichun Wang Jichun Wang Jichun Wang Changwen Lv Changwen Lv Changwen Lv Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content Frontiers in Plant Science sweet potato invertase duplicated gene sequence variation promoter activity |
| title | Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content |
| title_full | Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content |
| title_fullStr | Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content |
| title_full_unstemmed | Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content |
| title_short | Regulatory and functional divergence among members of Ibβfruct2, a sweet potato vacuolar invertase gene controlling starch and glucose content |
| title_sort | regulatory and functional divergence among members of ibβfruct2 a sweet potato vacuolar invertase gene controlling starch and glucose content |
| topic | sweet potato invertase duplicated gene sequence variation promoter activity |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1192417/full |
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