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Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root
In various plant species, many transcription factors (TFs), such as MYB, bHLH, and WD40, have been identified as regulators of anthocyanin biosynthesis in underground organs. However, the regulatory elements of anthocyanin biosynthesis in the tuberous roots of sweet potato have not been elucidated y...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9393619/ https://www.ncbi.nlm.nih.gov/pubmed/36003808 http://dx.doi.org/10.3389/fpls.2022.924379 |
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author | Dong, Wen Tang, Linfei Peng, Yali Qin, Yuzhi Lin, Yuan Xiong, Xingyao Hu, Xinxi |
author_facet | Dong, Wen Tang, Linfei Peng, Yali Qin, Yuzhi Lin, Yuan Xiong, Xingyao Hu, Xinxi |
author_sort | Dong, Wen |
collection | PubMed |
description | In various plant species, many transcription factors (TFs), such as MYB, bHLH, and WD40, have been identified as regulators of anthocyanin biosynthesis in underground organs. However, the regulatory elements of anthocyanin biosynthesis in the tuberous roots of sweet potato have not been elucidated yet. Here, we selected the purple-fleshed sweet potato cultivar “Zhezi1” (ZZ(P)) and its spontaneous yellow-fleshed mutant “Xinli” (XL(Y)) to investigate the regulatory mechanism of the anthocyanin biosynthesis in the tuberous roots of sweet potato. By analyzing the IbMYB1 genotype in ZZ(P) and XL(Y), we found that the IbMYB1-2, a MYB TF involved in anthocyanin biosynthesis, was missing in the XL(Y) genome, which might lead to an extreme decrease in anthocyanins in XL(Y). A comparative transcriptome analysis of ZZ(P) and XL(Y) was conducted to find the TFs involved in anthocyanin biosynthesis in ZZ(P) and XL(Y). The anthocyanin structural genes were significantly enriched among the differentially expressed genes. Moreover, one MYB activator (IbMYB1), one bHLH (IbbHLH2), three WRKY activator candidates (IbWRKY21, IbWRKY24, and IbWRKY44), and two MYB repressors (IbMYB27 and IbMYBx-ZZ) were highly expressed in ZZ(P) accompanied with anthocyanin structural genes. We also tested the expression of these TFs in six purple- and two orange-fleshed sweet potato cultivars. Interestingly, most of these TFs were significantly positively correlated with anthocyanin contents in these cultivars. The function of the anthocyanin biosynthesis repression of IbMYB27 and IbMYBx-ZZ was verified through transient co-transformation with IbMYB1 into tobacco leaves. Further functional verification of the above TFs was conducted by Y2H, BiFC, and dual-luciferase assays. These tests showed that the MYB-bHLH-WD40/MYB-bHLH-WD40-WRKY complex activated the promoter of anthocyanin structural gene IbDFR and promoters for IbWRKY44, IbMYB27, and IbMYBx-ZZ, indicating reinforcement and feedback regulation to maintain the level of anthocyanin accumulation in the tuberous roots of purple-fleshed sweet potato. These results may provide new insights into the regulatory mechanism of anthocyanin biosynthesis and accumulation in underground organs of sweet potatoes. |
format | Online Article Text |
id | pubmed-9393619 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-93936192022-08-23 Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root Dong, Wen Tang, Linfei Peng, Yali Qin, Yuzhi Lin, Yuan Xiong, Xingyao Hu, Xinxi Front Plant Sci Plant Science In various plant species, many transcription factors (TFs), such as MYB, bHLH, and WD40, have been identified as regulators of anthocyanin biosynthesis in underground organs. However, the regulatory elements of anthocyanin biosynthesis in the tuberous roots of sweet potato have not been elucidated yet. Here, we selected the purple-fleshed sweet potato cultivar “Zhezi1” (ZZ(P)) and its spontaneous yellow-fleshed mutant “Xinli” (XL(Y)) to investigate the regulatory mechanism of the anthocyanin biosynthesis in the tuberous roots of sweet potato. By analyzing the IbMYB1 genotype in ZZ(P) and XL(Y), we found that the IbMYB1-2, a MYB TF involved in anthocyanin biosynthesis, was missing in the XL(Y) genome, which might lead to an extreme decrease in anthocyanins in XL(Y). A comparative transcriptome analysis of ZZ(P) and XL(Y) was conducted to find the TFs involved in anthocyanin biosynthesis in ZZ(P) and XL(Y). The anthocyanin structural genes were significantly enriched among the differentially expressed genes. Moreover, one MYB activator (IbMYB1), one bHLH (IbbHLH2), three WRKY activator candidates (IbWRKY21, IbWRKY24, and IbWRKY44), and two MYB repressors (IbMYB27 and IbMYBx-ZZ) were highly expressed in ZZ(P) accompanied with anthocyanin structural genes. We also tested the expression of these TFs in six purple- and two orange-fleshed sweet potato cultivars. Interestingly, most of these TFs were significantly positively correlated with anthocyanin contents in these cultivars. The function of the anthocyanin biosynthesis repression of IbMYB27 and IbMYBx-ZZ was verified through transient co-transformation with IbMYB1 into tobacco leaves. Further functional verification of the above TFs was conducted by Y2H, BiFC, and dual-luciferase assays. These tests showed that the MYB-bHLH-WD40/MYB-bHLH-WD40-WRKY complex activated the promoter of anthocyanin structural gene IbDFR and promoters for IbWRKY44, IbMYB27, and IbMYBx-ZZ, indicating reinforcement and feedback regulation to maintain the level of anthocyanin accumulation in the tuberous roots of purple-fleshed sweet potato. These results may provide new insights into the regulatory mechanism of anthocyanin biosynthesis and accumulation in underground organs of sweet potatoes. Frontiers Media S.A. 2022-08-08 /pmc/articles/PMC9393619/ /pubmed/36003808 http://dx.doi.org/10.3389/fpls.2022.924379 Text en Copyright © 2022 Dong, Tang, Peng, Qin, Lin, Xiong and Hu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Plant Science Dong, Wen Tang, Linfei Peng, Yali Qin, Yuzhi Lin, Yuan Xiong, Xingyao Hu, Xinxi Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
title | Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
title_full | Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
title_fullStr | Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
title_full_unstemmed | Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
title_short | Comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
title_sort | comparative transcriptome analysis of purple-fleshed sweet potato and its yellow-fleshed mutant provides insight into the transcription factors involved in anthocyanin biosynthesis in tuberous root |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9393619/ https://www.ncbi.nlm.nih.gov/pubmed/36003808 http://dx.doi.org/10.3389/fpls.2022.924379 |
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