Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation
The petals of <i>Paeonia lactiflora</i> ‘Coral Sunset’ change color from coral pink to pale yellow after flower opening. Pigment-targeted metabolomic analysis showed that the carotenoid and anthocyanin contents rapidly decreased after petal fading. SMART-sequencing and next-generation-se...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2023-11-01
|
Series: | Horticulturae |
Subjects: | |
Online Access: | https://www.mdpi.com/2311-7524/9/12/1295 |
_version_ | 1797380804310990848 |
---|---|
author | Hechen Zhang Xin Yuan Rui Wang Limin Wang Jie Gao Huijuan Wang Yanmin Li Zhenzhu Fu |
author_facet | Hechen Zhang Xin Yuan Rui Wang Limin Wang Jie Gao Huijuan Wang Yanmin Li Zhenzhu Fu |
author_sort | Hechen Zhang |
collection | DOAJ |
description | The petals of <i>Paeonia lactiflora</i> ‘Coral Sunset’ change color from coral pink to pale yellow after flower opening. Pigment-targeted metabolomic analysis showed that the carotenoid and anthocyanin contents rapidly decreased after petal fading. SMART-sequencing and next-generation-sequencing analyses were performed to identify differentially expressed transcripts to characterize the candidate genes involved in petal fading. The expression of certain genes associated with anthocyanin and carotenoid synthesis and degradation was correlated with the petal-fading phenotype. The anthocyanin synthesis (AS) structural genes, <i>CHS</i>, <i>F3H</i>, <i>F3′H</i>, <i>DFR</i>, and <i>ANS</i>, and the carotenoid synthesis genes, <i>LCYB</i> and <i>LCYE</i>, were strongly expressed before fading, but their expression significantly declined after fading. In contrast, the expression of certain genes associated with oxidase activity and light signaling significantly increased after fading. Therefore, inhibition of pigment synthesis and accelerated pigment degradation may be crucial for petal fading. A R2R3-MYB family member of subgroup 4 (<i>MYBs-SG4</i>) showed the same expression pattern as the AS structural genes and functioned in the positive regulation of anthocyanin synthesis by forming the MBW protein complex. This is the first report of a SG4 member with a positive regulatory function. This study provides a foundation for elucidation of the mechanisms of pigment synthesis and metabolism, and a theoretical basis for flower-color-directed breeding. |
first_indexed | 2024-03-08T20:42:22Z |
format | Article |
id | doaj.art-02128544943c48e4b85224c10d661ee3 |
institution | Directory Open Access Journal |
issn | 2311-7524 |
language | English |
last_indexed | 2024-03-08T20:42:22Z |
publishDate | 2023-11-01 |
publisher | MDPI AG |
record_format | Article |
series | Horticulturae |
spelling | doaj.art-02128544943c48e4b85224c10d661ee32023-12-22T14:12:31ZengMDPI AGHorticulturae2311-75242023-11-01912129510.3390/horticulturae9121295Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment DegradationHechen Zhang0Xin Yuan1Rui Wang2Limin Wang3Jie Gao4Huijuan Wang5Yanmin Li6Zhenzhu Fu7Horticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaHorticultural Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, ChinaThe petals of <i>Paeonia lactiflora</i> ‘Coral Sunset’ change color from coral pink to pale yellow after flower opening. Pigment-targeted metabolomic analysis showed that the carotenoid and anthocyanin contents rapidly decreased after petal fading. SMART-sequencing and next-generation-sequencing analyses were performed to identify differentially expressed transcripts to characterize the candidate genes involved in petal fading. The expression of certain genes associated with anthocyanin and carotenoid synthesis and degradation was correlated with the petal-fading phenotype. The anthocyanin synthesis (AS) structural genes, <i>CHS</i>, <i>F3H</i>, <i>F3′H</i>, <i>DFR</i>, and <i>ANS</i>, and the carotenoid synthesis genes, <i>LCYB</i> and <i>LCYE</i>, were strongly expressed before fading, but their expression significantly declined after fading. In contrast, the expression of certain genes associated with oxidase activity and light signaling significantly increased after fading. Therefore, inhibition of pigment synthesis and accelerated pigment degradation may be crucial for petal fading. A R2R3-MYB family member of subgroup 4 (<i>MYBs-SG4</i>) showed the same expression pattern as the AS structural genes and functioned in the positive regulation of anthocyanin synthesis by forming the MBW protein complex. This is the first report of a SG4 member with a positive regulatory function. This study provides a foundation for elucidation of the mechanisms of pigment synthesis and metabolism, and a theoretical basis for flower-color-directed breeding.https://www.mdpi.com/2311-7524/9/12/1295anthocyaninscarotenoidshigh-throughput sequencing<i>Paeonia lactiflora</i>pigment degradation |
spellingShingle | Hechen Zhang Xin Yuan Rui Wang Limin Wang Jie Gao Huijuan Wang Yanmin Li Zhenzhu Fu Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation Horticulturae anthocyanins carotenoids high-throughput sequencing <i>Paeonia lactiflora</i> pigment degradation |
title | Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation |
title_full | Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation |
title_fullStr | Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation |
title_full_unstemmed | Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation |
title_short | Comprehensive Transcriptome and Metabolome Characterization of Peony ‘Coral Sunset’ Petals Provides Insights into the Mechanism of Pigment Degradation |
title_sort | comprehensive transcriptome and metabolome characterization of peony coral sunset petals provides insights into the mechanism of pigment degradation |
topic | anthocyanins carotenoids high-throughput sequencing <i>Paeonia lactiflora</i> pigment degradation |
url | https://www.mdpi.com/2311-7524/9/12/1295 |
work_keys_str_mv | AT hechenzhang comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT xinyuan comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT ruiwang comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT liminwang comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT jiegao comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT huijuanwang comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT yanminli comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation AT zhenzhufu comprehensivetranscriptomeandmetabolomecharacterizationofpeonycoralsunsetpetalsprovidesinsightsintothemechanismofpigmentdegradation |