The genetic control of glabrous glume during African rice domestication
African cultivated rice, Oryza glaberrima, is characterized by its glabrous glumes. During domestication, the pubescent glumes of its wild ancestor, Oryza barthii, lost their trichomes, and in this study, we show that glabrous glume 5 (GLAG5), a WUSCHEL-like homeobox transcription factor gene on chr...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Journal Article |
| Language: | Inglés |
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Elsevier
2022
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| Subjects: | |
| Online Access: | https://hdl.handle.net/10568/126169 |
| _version_ | 1855533801500835840 |
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| author | Chang, L. Hu, M. Ning, J. He, W. Gao, J. Ndjiondjop, M.N. Fu, Y. Liu, F. Sun, H. Gu, P. Sunc, C. Zhu, Z. |
| author_browse | Chang, L. Fu, Y. Gao, J. Gu, P. He, W. Hu, M. Liu, F. Ndjiondjop, M.N. Ning, J. Sun, H. Sunc, C. Zhu, Z. |
| author_facet | Chang, L. Hu, M. Ning, J. He, W. Gao, J. Ndjiondjop, M.N. Fu, Y. Liu, F. Sun, H. Gu, P. Sunc, C. Zhu, Z. |
| author_sort | Chang, L. |
| collection | Repository of Agricultural Research Outputs (CGSpace) |
| description | African cultivated rice, Oryza glaberrima, is characterized by its glabrous glumes. During domestication, the pubescent glumes of its wild ancestor, Oryza barthii, lost their trichomes, and in this study, we show that glabrous glume 5 (GLAG5), a WUSCHEL-like homeobox transcription factor gene on chromosome 5, is required for trichome development. DNA methylation associated with an hAT transposable element inserted in the promoter region of GLAG5 is found to reduce its expression, leading to the formation of glabrous glumes and leaves in African cultivated rice. Among 82 African cultivated rice varieties investigated in this study, 59 (approximately 71%) lines exhibit glabrous glumes and harbor the hAT transposon; however, the other 23 varieties (approximately 29%), which exhibit pubescent glumes, lack the hAT transposon, indicating that glag5 had undergone strong artificial selection. The πw/πc ratios also show the hAT transposon insertions influence the genetic diversity of an approximately 150-kb interval encompassing the GLAG5 locus. The identification of the GLAG5 gene provides new insights into the domestication of cultivated rice in Africa. We speculate that the selection of varieties with mutations in their promoter regions is an important aspect of crop domestication.
Introduction
African cultivated rice (Oryza glaberrima) was domesticated from its wild progenitor Oryza barthii in Africa more than 3000 years ago (Purugganan, 2014). During domestication, farmers selected for morphological traits that facilitated cultivation and harvesting, which included reduced seed shattering, erect plant architecture and grains with short-awn or awnless glumes. African rice is a valuable genetic resource containing resistance genes to biotic and abiotic stresses, such as rice yellow mottle virus, high temperature, soil acidity, iron toxicity, and drought (Jones, 1997, Li et al., 2015, Linares, 2002, Thiémélé, 2010, Wambugu, 2013). Owing to its genetic importance, the origin and evolution of African rice has been studied extensively over several decades (Ammiraju et al., 2008; Van Andel, 2010; Molina et al., 2011; Sakai et al., 2011; Chen et al., 2013; Stein et al., 2018). Recent studies have identified the genes controlling the reduction of seed shattering and erect plant architecture characteristics in African cultivated rice (Wu et al., 2017; Hu et al., 2018; Lv et al., 2018), and this information has provided new insights into its domestication.
Oryza glaberrima is known as glabrous rice, and it is characterized by glabrous glumes and leaves. However, African wild rice is typically densely covered by hard (thorn-like) trichomes on the glumes and soft trichomes on the leaves, which aid seed dispersal and provide protection against seed predation by birds and other animals. The glabrous glumes of O. glaberrima are valued for hand-harvesting, because they decrease skin irritation during threshing, drying and milling, and reduce the amount of storage space required (Lim et al., 1984). The loss of trichomes is considered to be an important event during the domestication of wild rice. However, the molecular genetic mechanisms involved in the loss of trichomes remain largely unknown.
Transposable elements (TEs), or fragments of DNA that can move from one location in the genome to another, are major components of eukaryotic genomes (Feschotte et al., 2002). In rice, over 35% of the genomic content is composed of TEs, and generic sequences are embedded in these vast expanses of TEs (Ma et al., 2020). TEs can influence expressions of nearby genes either through cis-acting elements residing in their own sequences or by changing the DNA or chromatin methylation states of adjacent genes (Studer et al., 2011; Friedli and Trono, 2015; Li et al., 2017; Peng et al., 2019). To maintain genomic stability, TEs are usually silenced and inactive, owing to DNA and chromatin modifications.
In this study, we describe the isolation and characterization of glabrous glume 5 (GLAG5), which controls the formation of glabrous glumes and leaves in African rice. This gene was found to encode a homeobox domain transcription factor located on chromosome 5. Furthermore, we show that an hAT transposon insertion in the GLAG5 promoter during African cultivated rice domestication may have repressed gene expression through DNA methylation and led to the development of glabrous glumes. |
| format | Journal Article |
| id | CGSpace126169 |
| institution | CGIAR Consortium |
| language | Inglés |
| publishDate | 2022 |
| publishDateRange | 2022 |
| publishDateSort | 2022 |
| publisher | Elsevier |
| publisherStr | Elsevier |
| record_format | dspace |
| spelling | CGSpace1261692025-10-26T13:02:11Z The genetic control of glabrous glume during African rice domestication Chang, L. Hu, M. Ning, J. He, W. Gao, J. Ndjiondjop, M.N. Fu, Y. Liu, F. Sun, H. Gu, P. Sunc, C. Zhu, Z. rice plant genetics African cultivated rice, Oryza glaberrima, is characterized by its glabrous glumes. During domestication, the pubescent glumes of its wild ancestor, Oryza barthii, lost their trichomes, and in this study, we show that glabrous glume 5 (GLAG5), a WUSCHEL-like homeobox transcription factor gene on chromosome 5, is required for trichome development. DNA methylation associated with an hAT transposable element inserted in the promoter region of GLAG5 is found to reduce its expression, leading to the formation of glabrous glumes and leaves in African cultivated rice. Among 82 African cultivated rice varieties investigated in this study, 59 (approximately 71%) lines exhibit glabrous glumes and harbor the hAT transposon; however, the other 23 varieties (approximately 29%), which exhibit pubescent glumes, lack the hAT transposon, indicating that glag5 had undergone strong artificial selection. The πw/πc ratios also show the hAT transposon insertions influence the genetic diversity of an approximately 150-kb interval encompassing the GLAG5 locus. The identification of the GLAG5 gene provides new insights into the domestication of cultivated rice in Africa. We speculate that the selection of varieties with mutations in their promoter regions is an important aspect of crop domestication. Introduction African cultivated rice (Oryza glaberrima) was domesticated from its wild progenitor Oryza barthii in Africa more than 3000 years ago (Purugganan, 2014). During domestication, farmers selected for morphological traits that facilitated cultivation and harvesting, which included reduced seed shattering, erect plant architecture and grains with short-awn or awnless glumes. African rice is a valuable genetic resource containing resistance genes to biotic and abiotic stresses, such as rice yellow mottle virus, high temperature, soil acidity, iron toxicity, and drought (Jones, 1997, Li et al., 2015, Linares, 2002, Thiémélé, 2010, Wambugu, 2013). Owing to its genetic importance, the origin and evolution of African rice has been studied extensively over several decades (Ammiraju et al., 2008; Van Andel, 2010; Molina et al., 2011; Sakai et al., 2011; Chen et al., 2013; Stein et al., 2018). Recent studies have identified the genes controlling the reduction of seed shattering and erect plant architecture characteristics in African cultivated rice (Wu et al., 2017; Hu et al., 2018; Lv et al., 2018), and this information has provided new insights into its domestication. Oryza glaberrima is known as glabrous rice, and it is characterized by glabrous glumes and leaves. However, African wild rice is typically densely covered by hard (thorn-like) trichomes on the glumes and soft trichomes on the leaves, which aid seed dispersal and provide protection against seed predation by birds and other animals. The glabrous glumes of O. glaberrima are valued for hand-harvesting, because they decrease skin irritation during threshing, drying and milling, and reduce the amount of storage space required (Lim et al., 1984). The loss of trichomes is considered to be an important event during the domestication of wild rice. However, the molecular genetic mechanisms involved in the loss of trichomes remain largely unknown. Transposable elements (TEs), or fragments of DNA that can move from one location in the genome to another, are major components of eukaryotic genomes (Feschotte et al., 2002). In rice, over 35% of the genomic content is composed of TEs, and generic sequences are embedded in these vast expanses of TEs (Ma et al., 2020). TEs can influence expressions of nearby genes either through cis-acting elements residing in their own sequences or by changing the DNA or chromatin methylation states of adjacent genes (Studer et al., 2011; Friedli and Trono, 2015; Li et al., 2017; Peng et al., 2019). To maintain genomic stability, TEs are usually silenced and inactive, owing to DNA and chromatin modifications. In this study, we describe the isolation and characterization of glabrous glume 5 (GLAG5), which controls the formation of glabrous glumes and leaves in African rice. This gene was found to encode a homeobox domain transcription factor located on chromosome 5. Furthermore, we show that an hAT transposon insertion in the GLAG5 promoter during African cultivated rice domestication may have repressed gene expression through DNA methylation and led to the development of glabrous glumes. 2022-05 2022-12-21T08:59:37Z 2022-12-21T08:59:37Z Journal Article https://hdl.handle.net/10568/126169 en Limited Access Elsevier Chang, L., Hu, M., Ning, J., He, W., Gao, J., Ndjiondjop, M.N., Fu, Y., Liu, F., Sun, H., Gu, P., Sunc, C. and Zhu, Z. 2022. The genetic control of glabrous glume during African rice domestication. Journal of Genetics and Genomics 49(5):427-436. |
| spellingShingle | rice plant genetics Chang, L. Hu, M. Ning, J. He, W. Gao, J. Ndjiondjop, M.N. Fu, Y. Liu, F. Sun, H. Gu, P. Sunc, C. Zhu, Z. The genetic control of glabrous glume during African rice domestication |
| title | The genetic control of glabrous glume during African rice domestication |
| title_full | The genetic control of glabrous glume during African rice domestication |
| title_fullStr | The genetic control of glabrous glume during African rice domestication |
| title_full_unstemmed | The genetic control of glabrous glume during African rice domestication |
| title_short | The genetic control of glabrous glume during African rice domestication |
| title_sort | genetic control of glabrous glume during african rice domestication |
| topic | rice plant genetics |
| url | https://hdl.handle.net/10568/126169 |
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