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...

Full description

Bibliographic Details
Main Authors: Kairong Sun, Yuqian Xue, Zeljana Prijic, Shunli Wang, Tatjana Markovic, Caihuan Tian, Yingying Wang, Jingqi Xue, Xiuxin Zhang
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