DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions
Gibberellin (GA) is frequently used in tree peony forcing culture, but inappropriate application often causes flower deformity. Here, 5-azacytidine (5-azaC), an efficient DNA demethylating reagent, induced tree peony flowering with a low deformity rate by rapidly inducing <i>PsFT</i> exp...
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2022-06-01
|
Series: | International Journal of Molecular Sciences |
Subjects: | |
Online Access: | https://www.mdpi.com/1422-0067/23/12/6632 |
_version_ | 1797486472205434880 |
---|---|
author | Kairong Sun Yuqian Xue Zeljana Prijic Shunli Wang Tatjana Markovic Caihuan Tian Yingying Wang Jingqi Xue Xiuxin Zhang |
author_facet | Kairong Sun Yuqian Xue Zeljana Prijic Shunli Wang Tatjana Markovic Caihuan Tian Yingying Wang Jingqi Xue Xiuxin Zhang |
author_sort | Kairong Sun |
collection | DOAJ |
description | Gibberellin (GA) is frequently used in tree peony forcing culture, but inappropriate application often causes flower deformity. Here, 5-azacytidine (5-azaC), an efficient DNA demethylating reagent, induced tree peony flowering with a low deformity rate by rapidly inducing <i>PsFT</i> expression, whereas GA treatment affected various flowering pathway genes with strong pleiotropy. The 5-azaC treatment, but not GA, significantly reduced the methylation level in the <i>PsFT</i> promoter with the demethylation of five CG contexts in a 369 bp CG-rich region, and eight light-responsive related <i>cis</i>-elements were also predicted in this region, accompanied by enhanced leaf photosynthetic efficiency. Through GO analysis, all methylation-closer differentially expressed genes (DEGs) were located in the <i>thylakoid</i>, the main site for photosynthesis, and were mainly involved in <i>response to stimulus</i> and <i>single-organism process</i>, whereas GA-closer DEGs had a wider distribution inside and outside of cells, associated with 12 categories of processes and regulations. We further mapped five candidate DEGs with potential flowering regulation, including three kinases (<i>SnRK1</i>, <i>WAK2,</i> and <i>5PTase7</i>) and two bioactive enzymes (<i>cytochrome P450</i> and <i>SBH1</i>). In summary, 5-azaC and GA may have individual roles in inducing tree peony flowering, and 5-azaC could be a preferable regulation approach; DNA demethylation is suggested to be more focused on flowering regulation with <i>PsFT</i> playing a core role through promoter demethylation. In addition, 5-azaC may partially undertake or replace the light-signal function, combined with other factors, such as <i>SnRK1</i>, in regulating flowering. This work provides new ideas for improving tree peony forcing culture technology. |
first_indexed | 2024-03-09T23:33:49Z |
format | Article |
id | doaj.art-1e69ce1811c7406db681cf964c8e556d |
institution | Directory Open Access Journal |
issn | 1661-6596 1422-0067 |
language | English |
last_indexed | 2024-03-09T23:33:49Z |
publishDate | 2022-06-01 |
publisher | MDPI AG |
record_format | Article |
series | International Journal of Molecular Sciences |
spelling | doaj.art-1e69ce1811c7406db681cf964c8e556d2023-11-23T17:04:18ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-06-012312663210.3390/ijms23126632DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture ConditionsKairong Sun0Yuqian Xue1Zeljana Prijic2Shunli Wang3Tatjana Markovic4Caihuan Tian5Yingying Wang6Jingqi Xue7Xiuxin Zhang8Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaInstitute for Medicinal Plants Research “Dr Josif Pančić”, 11000 Belgrade, SerbiaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaInstitute for Medicinal Plants Research “Dr Josif Pančić”, 11000 Belgrade, SerbiaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaKey Laboratory of Biology and Genetic Improvement of Horticultural Crops, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Beijing 100081, ChinaGibberellin (GA) is frequently used in tree peony forcing culture, but inappropriate application often causes flower deformity. Here, 5-azacytidine (5-azaC), an efficient DNA demethylating reagent, induced tree peony flowering with a low deformity rate by rapidly inducing <i>PsFT</i> expression, whereas GA treatment affected various flowering pathway genes with strong pleiotropy. The 5-azaC treatment, but not GA, significantly reduced the methylation level in the <i>PsFT</i> promoter with the demethylation of five CG contexts in a 369 bp CG-rich region, and eight light-responsive related <i>cis</i>-elements were also predicted in this region, accompanied by enhanced leaf photosynthetic efficiency. Through GO analysis, all methylation-closer differentially expressed genes (DEGs) were located in the <i>thylakoid</i>, the main site for photosynthesis, and were mainly involved in <i>response to stimulus</i> and <i>single-organism process</i>, whereas GA-closer DEGs had a wider distribution inside and outside of cells, associated with 12 categories of processes and regulations. We further mapped five candidate DEGs with potential flowering regulation, including three kinases (<i>SnRK1</i>, <i>WAK2,</i> and <i>5PTase7</i>) and two bioactive enzymes (<i>cytochrome P450</i> and <i>SBH1</i>). In summary, 5-azaC and GA may have individual roles in inducing tree peony flowering, and 5-azaC could be a preferable regulation approach; DNA demethylation is suggested to be more focused on flowering regulation with <i>PsFT</i> playing a core role through promoter demethylation. In addition, 5-azaC may partially undertake or replace the light-signal function, combined with other factors, such as <i>SnRK1</i>, in regulating flowering. This work provides new ideas for improving tree peony forcing culture technology.https://www.mdpi.com/1422-0067/23/12/6632<i>Paeonia suffruticosa</i>DNA methylationphotoperiod pathwayMcrBC PCRtranscriptomepromoter |
spellingShingle | Kairong Sun Yuqian Xue Zeljana Prijic Shunli Wang Tatjana Markovic Caihuan Tian Yingying Wang Jingqi Xue Xiuxin Zhang DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions International Journal of Molecular Sciences <i>Paeonia suffruticosa</i> DNA methylation photoperiod pathway McrBC PCR transcriptome promoter |
title | DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions |
title_full | DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions |
title_fullStr | DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions |
title_full_unstemmed | DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions |
title_short | DNA Demethylation Induces Tree Peony Flowering with a Low Deformity Rate Compared to Gibberellin by Inducing <i>PsFT</i> Expression under Forcing Culture Conditions |
title_sort | dna demethylation induces tree peony flowering with a low deformity rate compared to gibberellin by inducing i psft i expression under forcing culture conditions |
topic | <i>Paeonia suffruticosa</i> DNA methylation photoperiod pathway McrBC PCR transcriptome promoter |
url | https://www.mdpi.com/1422-0067/23/12/6632 |
work_keys_str_mv | AT kairongsun dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT yuqianxue dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT zeljanaprijic dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT shunliwang dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT tatjanamarkovic dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT caihuantian dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT yingyingwang dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT jingqixue dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions AT xiuxinzhang dnademethylationinducestreepeonyfloweringwithalowdeformityratecomparedtogibberellinbyinducingipsftiexpressionunderforcingcultureconditions |