Cargando…

The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter

To gain insight into how anthocyanin biosynthesis is controlled by light in fruit, transcriptome and metabolome analyses were performed in the Chinese sand pear cultivar “Mantianhong” (Pyrus pyrifolia) after bagging and bag removal. We investigated transcriptional and metabolic changes and gene-meta...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Hainan, Su, Jun, Zhu, Yangfan, Yao, Gaifang, Allan, Andrew C., Ampomah-Dwamena, Charles, Shu, Qun, Lin-Wang, Kui, Zhang, Shaoling, Wu, Jun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6885052/
https://www.ncbi.nlm.nih.gov/pubmed/31814987
http://dx.doi.org/10.1038/s41438-019-0217-4
_version_ 1783474672809017344
author Liu, Hainan
Su, Jun
Zhu, Yangfan
Yao, Gaifang
Allan, Andrew C.
Ampomah-Dwamena, Charles
Shu, Qun
Lin-Wang, Kui
Zhang, Shaoling
Wu, Jun
author_facet Liu, Hainan
Su, Jun
Zhu, Yangfan
Yao, Gaifang
Allan, Andrew C.
Ampomah-Dwamena, Charles
Shu, Qun
Lin-Wang, Kui
Zhang, Shaoling
Wu, Jun
author_sort Liu, Hainan
collection PubMed
description To gain insight into how anthocyanin biosynthesis is controlled by light in fruit, transcriptome and metabolome analyses were performed in the Chinese sand pear cultivar “Mantianhong” (Pyrus pyrifolia) after bagging and bag removal. We investigated transcriptional and metabolic changes and gene-metabolite correlation networks. Correlation tests of anthocyanin content and transcriptional changes revealed that 1,530 transcripts were strongly correlated with 15 anthocyanin derivatives (R(2) > 0.9, P-value < 0.05), with the top 130 transcripts categorized as being associated with flavonoid metabolism, transcriptional regulation, and light signaling. The connection network revealed a new photosensitive transcription factor, PybZIPa, that might play an important role during light-induced anthocyanin accumulation. The overexpression of PybZIPa promoted anthocyanin accumulation in pear and strawberry fruit as well as tobacco leaves. Dual luciferase and Y1H assays further verified that PybZIPa directly activated the expression of PyUFGT by binding to tandem G-box motifs in the promoter, which was key to differential anthocyanin accumulation in debagged pear skin, and the number of G-box motifs affected the transcriptional activation of PyUFGT by PybZIPa. The results indicate that the light-induced anthocyanin biosynthesis regulatory mechanism in pear differs from that described in previous reports suggesting that a bZIP family member co-regulates anthocyanin biosynthesis with other transcription factors in apple and Arabidopsis. It was found that, in response to light, PybZIPa promoted anthocyanin biosynthesis by regulating important transcription factors (PyMYB114, PyMYB10, and PyBBX22) as well as structural genes (PyUFGT) via binding to G-boxes within promoters. This activation was amplified by the self-binding of PybZIPa to activate its own promoter. Overall, we demonstrate the utility of a multiomics integrative approach for discovering new functional genes and pathways underlying light-induced anthocyanin biosynthesis.
format Online
Article
Text
id pubmed-6885052
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-68850522019-12-06 The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter Liu, Hainan Su, Jun Zhu, Yangfan Yao, Gaifang Allan, Andrew C. Ampomah-Dwamena, Charles Shu, Qun Lin-Wang, Kui Zhang, Shaoling Wu, Jun Hortic Res Article To gain insight into how anthocyanin biosynthesis is controlled by light in fruit, transcriptome and metabolome analyses were performed in the Chinese sand pear cultivar “Mantianhong” (Pyrus pyrifolia) after bagging and bag removal. We investigated transcriptional and metabolic changes and gene-metabolite correlation networks. Correlation tests of anthocyanin content and transcriptional changes revealed that 1,530 transcripts were strongly correlated with 15 anthocyanin derivatives (R(2) > 0.9, P-value < 0.05), with the top 130 transcripts categorized as being associated with flavonoid metabolism, transcriptional regulation, and light signaling. The connection network revealed a new photosensitive transcription factor, PybZIPa, that might play an important role during light-induced anthocyanin accumulation. The overexpression of PybZIPa promoted anthocyanin accumulation in pear and strawberry fruit as well as tobacco leaves. Dual luciferase and Y1H assays further verified that PybZIPa directly activated the expression of PyUFGT by binding to tandem G-box motifs in the promoter, which was key to differential anthocyanin accumulation in debagged pear skin, and the number of G-box motifs affected the transcriptional activation of PyUFGT by PybZIPa. The results indicate that the light-induced anthocyanin biosynthesis regulatory mechanism in pear differs from that described in previous reports suggesting that a bZIP family member co-regulates anthocyanin biosynthesis with other transcription factors in apple and Arabidopsis. It was found that, in response to light, PybZIPa promoted anthocyanin biosynthesis by regulating important transcription factors (PyMYB114, PyMYB10, and PyBBX22) as well as structural genes (PyUFGT) via binding to G-boxes within promoters. This activation was amplified by the self-binding of PybZIPa to activate its own promoter. Overall, we demonstrate the utility of a multiomics integrative approach for discovering new functional genes and pathways underlying light-induced anthocyanin biosynthesis. Nature Publishing Group UK 2019-12-01 /pmc/articles/PMC6885052/ /pubmed/31814987 http://dx.doi.org/10.1038/s41438-019-0217-4 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Liu, Hainan
Su, Jun
Zhu, Yangfan
Yao, Gaifang
Allan, Andrew C.
Ampomah-Dwamena, Charles
Shu, Qun
Lin-Wang, Kui
Zhang, Shaoling
Wu, Jun
The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter
title The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter
title_full The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter
title_fullStr The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter
title_full_unstemmed The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter
title_short The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter
title_sort involvement of pybzipa in light-induced anthocyanin accumulation via the activation of pyufgt through binding to tandem g-boxes in its promoter
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6885052/
https://www.ncbi.nlm.nih.gov/pubmed/31814987
http://dx.doi.org/10.1038/s41438-019-0217-4
work_keys_str_mv AT liuhainan theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT sujun theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT zhuyangfan theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT yaogaifang theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT allanandrewc theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT ampomahdwamenacharles theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT shuqun theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT linwangkui theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT zhangshaoling theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT wujun theinvolvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT liuhainan involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT sujun involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT zhuyangfan involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT yaogaifang involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT allanandrewc involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT ampomahdwamenacharles involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT shuqun involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT linwangkui involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT zhangshaoling involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter
AT wujun involvementofpybzipainlightinducedanthocyaninaccumulationviatheactivationofpyufgtthroughbindingtotandemgboxesinitspromoter